The Human Brain During the Late First Trimester (Atlas of Human Central Nervous System Development, Volume 4)

The

HUMAN BRAIN during the

LATE FIRST TRIMESTER

ATLAS OF HUMAN CENTRAL NERVOUS SYSTEM DEVELOPMENT SERIES Shirley A. Bayer and Joseph Altman

VOLUME 1

The Spinal Cord from Gestational Week 4 to the 4th Postnatal Month

VOLUME 2

The Human Brain During the Third Trimester

VOLUME 3

The Human Brain During the Second Trimester

VOLUME 4

The Human Brain During the Late First Trimester

VOLUME 5

The Human Brain During the Early First Trimester

The

HUMAN BRAIN during the

LATE FIRST TRIMESTER

Shirley A. Bayer and Joseph Altman

Boca Raton London New York

CRC is an imprint of the Taylor & Francis Group, an informa business

Published in 2006 by CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2006 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group No claim to original U.S. Government works Printed in the United States of America on acid-free paper 10 9 8 7 6 5 4 3 2 1 International Standard Book Number-10: 0-8493-1423-2 (Hardcover) International Standard Book Number-13: 978-0-8493-1423-0 (Hardcover) This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. No part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and recording, or in any information storage or retrieval system, without written permission from the publishers. For permission to photocopy or use material electronically from this work, please access www.copyright.com (http://www.copyright.com/) or contact the Copyright Clearance Center, Inc. (CCC) 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400. CCC is a not-for-profit organization that provides licenses and registration for a variety of users. For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged. Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. Library of Congress Cataloging-in-Publication Data Catalog record is available from the Library of Congress

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DEDICATION We dedicate this volume to the memory of Prof. Dr. Ferdinand Hochstetter (1861-1954) for his pioneering description of the development of the human brain during the first trimester. To this day, his publication that appeared in Vienna and Leipzig in 1919 is the best source for systematically showing the external features of the human brain at this stage, and the current work is built on the foundation he provided.

ACKNOWLEDGMENTS We thank Dr. William DeMyer, pediatric neurologist at Indiana University Medical Center, for access to his personal library on human central nervous system development. We also thank the staff of the National Museum of Health and Medicine at the Armed Forces Institute of Pathology, Walter Reed Hospital, Washington, D.C.: Dr. Adrianne Noe, Director; Archibald J. Fobbs, Curator of the Yakovlev Collection; Elizabeth C. Lockett; and William Discher. We are most grateful to Dr. James M. Petras at the Walter Reed Institute of Research who made his darkroom facilities available so that we could develop all the photomicrographs on location rather than in our laboratory in Indiana. Finally, we thank publisher Barbara Norwitz, project manager Jim McGovern, proofreader Samar Haddad, Randy Brehm, and Kari Budyk at CRC Press/Taylor and Francis for their personal attention to us and for expert help during production of the manuscript.

CONTENTS PART I. A. B. C. D. E. F. G. H.

INTRODUCTION -------------------------------------------------------------------------------------------1 Organization of the Atlas -----------------------------------------------------------------------------------1 Specimens ------------------------------------------------------------------------------------------------------2 Photography and Computer Processing -----------------------------------------------------------------2 Identification of Immature Brain Structures -----------------------------------------------------------3 Major Transitional Brain Structures in the Late First Trimester ----------------------------------4 A Note on Genetic Analyses of NEP Mosaicism --------------------------------------------------------7 A Note on Functional Maturation ------------------------------------------------------------------------8 References -----------------------------------------------------------------------------------------------------8

PART II. GW11 CORONAL ----------------------------------------------------------------------------------------- 14 Plates 1A, 1B (Level 1: Section 140) -----------------------------------------------------------------16, 17 Plates 2A, 2B (Level 2: Section 259) -----------------------------------------------------------------18, 19 Plates 3A, 3B (Level 3: Section 279) -----------------------------------------------------------------20, 21 Plates 4A, 4B (Level 4: Section 289) -----------------------------------------------------------------22, 23 Plates 5A, 5B (Level 5: Section 329) -----------------------------------------------------------------24, 25 Plates 6A, 6B (Level 6: Section 340) -----------------------------------------------------------------26, 27 Plates 7A, 7B (Level 7: Section 349) -----------------------------------------------------------------28, 29 Plates 8A, 8B (Level 8: Section 379) -----------------------------------------------------------------30, 31 Plates 9A, 9B (Level 9: Section 419) -----------------------------------------------------------------32, 33 Plates 10A, 10B (Level 10: Section 439) -------------------------------------------------------------34, 35 Plates 11A, 11B (Level 11: Section 459) -------------------------------------------------------------36, 37 Plates 12A, 12B (Level 12: Section 479) -------------------------------------------------------------38, 39 Plates 13A, 13B (Level 13: Section 500) -------------------------------------------------------------40, 41 Plates 14A, 14B (Level 14: Section 529) -------------------------------------------------------------42, 43 Plates 15A, 15B (Level 15: Section 569) -------------------------------------------------------------44, 45 Plates 16A, 16B (Level 16: Section 599) -------------------------------------------------------------46, 47 Plates 17A, 17B (Level 17: Section 629) -------------------------------------------------------------48, 49 Plates 18A, 18B (Level 18: Section 649) -------------------------------------------------------------50, 51 Plates 19A, 19B (Level 19: Section 659) -------------------------------------------------------------53, 53 Plates 20A, 20B (Level 20: Section 680) -------------------------------------------------------------54, 55 Plates 21A, 21B (Levels 21-22: Sections 709, 720) ------------------------------------------------56, 57 Plates 22A, 22B (Frontal Cortex, Section 269) ------------------------------------------------------58, 59 Plates 23A, 23B (Parietal Cortex, Section 519) -----------------------------------------------------60, 61 Plates 24A, 24B (Paracentral Cortex, Section 399) -------------------------------------------------62, 63 Plates 25A, 25B (Lateral Paracentral Cortex, Section 399) ----------------------------------------64, 65 Plates 26A, 26B (Brain Core, Section 389) ----------------------------------------------------------66, 67 Plates 27A, 27B (Brain Core, Section 419) ----------------------------------------------------------68, 69 Plates 28A, 28B (Diencephalon, Section 449) -------------------------------------------------------70, 71 Plates 29A, 29B (Diencephalon, Section 469) -------------------------------------------------------72, 73 Plates 30A, 30B (Diencephalon, Section 499) -------------------------------------------------------74, 75 Plates 31A, 31B (Midbrain and Pons, Section 529) ------------------------------------------------76, 77 Plates 32A, 32B (Midbrain and Pons, Section 549) ------------------------------------------------78, 79 Plates 33A, 33B (Midbrain and Pons, Section 569) ------------------------------------------------80, 81 Plates 34A, 34B (Midbrain, Pons, and Medulla, Section 589) ------------------------------------82, 83 Plates 35A, 35B (Midbrain, Pons, and Medulla, Section 599) ------------------------------------84, 85 PART III. GW11 HORIZONTAL ------------------------------------------------------------------------------------ 86 Plates 36A, 36B (Level 1: Section 108) --------------------------------------------------------------88, 89 Plates 37A, 37B (Level 2: Section 536) --------------------------------------------------------------90, 91 Plates 38A, 38B (Level 3: Section 696) --------------------------------------------------------------92, 93 Plates 39A, 39B (Level 4: Section 800) --------------------------------------------------------------94, 95 Plates 40A, 40B (Level 5: Section 962) --------------------------------------------------------------96, 97 Plates 41A, 41B (Level 6: Section 1023) -------------------------------------------------------------98, 99

CONTENTS Plates 42A, 42B (Level 7: Section 1143) ----------------------------------------------------------100, 101 Plates 43A, 43B (Level 8: Section 1256) ----------------------------------------------------------102, 103 Plates 44A, 44B (Level 9: Section 1351) ----------------------------------------------------------104, 105 Plates 45A, 45B (Level 10: Section 1414) --------------------------------------------------------106, 107 Plates 46A, 46B (Level 11: Section 1473) --------------------------------------------------------108, 109 Plates 47A, 47B (Level 12: Section 1566) --------------------------------------------------------110, 111 Plates 48A, 48B (Level 13: Section 1626) --------------------------------------------------------112, 113 Plates 49A, 49B (Level 14: Section 1716) --------------------------------------------------------114, 115 Plates 50A, 50B (Level 15: Section 1805) --------------------------------------------------------116, 117 Plates 51A, 51B (Level 16: Section 1866) --------------------------------------------------------118, 119 Plates 52A, 52B (Level 17: Section 1926) --------------------------------------------------------120, 121 Plates 53A, 53B (Level 18: Section 1962) --------------------------------------------------------122, 123 Plates 54A, 54B (Level 19: Section 2202) --------------------------------------------------------124, 125 Plates 55A, 55B (Level 20: Section 2322) --------------------------------------------------------126, 127 Plates 56A, 56B (Level 21: Section 2402) --------------------------------------------------------128, 129 PART IV. GW9 SAGITTAL ------------------------------------------------------------------------------------------130 Plates 57A-57D (Level 1: Slide 53, Section 1) ---------------------------------------------------- 132-135 Plates 58A-58D (Level 2: Slide 63, Section 1) --------------------------------------------------- 136-139 Plates 59A-59D (Level 3: Slide 67, Section 1) --------------------------------------------------- 140-143 Plates 60A-60D (Level 4: Slide 71, Section 2) --------------------------------------------------- 144-147 Plates 61A-61D (Level 5: Slide 75, Section 2) --------------------------------------------------- 148-151 Plates 62A-62D (Level 6: Slide 79, Section 2) --------------------------------------------------- 152-155 Plates 63A-63D (Level 7: Slide 83, Section 1) --------------------------------------------------- 156-159 Plates 64A-64D (Level 8: Slide 95, Section 1) --------------------------------------------------- 160-163 Plates 65A-65D (Level 9: Slide 99, Section 1) --------------------------------------------------- 164-167 Plates 66A-66D (Level 10: Slide 103, Section 1) ------------------------------------------------ 168-171 Plates 67A-67D (Level 11: Slide 105, Section 2) ------------------------------------------------ 172-175 Plates 68A, 68B (Dorsal Cortex, Slide 71, Section 2) -------------------------------------------176, 177 Plates 69A, 69B (Hippocampus, Slide 91, Section 1) -------------------------------------------178, 179 Plates 70A, 70B (Olfactory Bulb and Septum, Slide 67, Section 1) ---------------------------180, 181 Plates 71A, 71B (Hypothalamus, Slide 67, Section 1) ------------------------------------------182, 183 Plates 72A, 72B (Hippocampus and Thalamus, Slide 95, Section 1) --------------------------184, 185 Plates 73A, 73B (Lateral Forebrain, Slide 83, Section 1) ---------------------------------------186, 187 Plates 74A, 74B (Lateral Forebrain, Slide 87, Section 1) ---------------------------------------188, 189 Plates 75A, 75B (Lateral Forebrain, Slide 95, Section 1) ---------------------------------------190, 191 Plates 76A, 76B (Diencephalon and Midbrain, Slide 79, Section 2) --------------------------192, 193 Plates 77A, 77B (Midbrain, Slide 67, Section 1) -------------------------------------------------194, 195 Plates 78A, 78B (Midbrain Tectum, Slide 63, Section 1) ---------------------------------------196, 197 Plates 79A, 79B (Cerebellum, Slide 71, Section 2) ----------------------------------------------198, 199 Plates 80A, 80B (Pons and Medulla, Slide 75, Section 2) --------------------------------------200, 201 Plates 81A, 81B (Pons and Medulla, Slide 99, Section 1) --------------------------------------202, 203 Plates 82A, 82B (Pons, Medulla, and Sensory Ganglia, Slide 101, Section 1) --------------204, 205 Plates 83A, 83B (Pons and Sensory Ganglia, Slide 104, Section 1) ---------------------------206, 207 PART V. GW9 HORIZONTAL ------------------------------------------------------------------------------------208 Plates 84A, 84B (Levels 1-2: Sections 8, 33) -----------------------------------------------------210, 211 Plates 85A, 85B (Level 3: Section 42) -------------------------------------------------------------212, 213 Plates 86A-86D (Level 4: Section 53) ------------------------------------------------------------- 214-217 Plates 87A-87D (Level 5: Section 57) ------------------------------------------------------------- 218-221 Plates 88A-88D (Level 6: Section 63) ------------------------------------------------------------- 222-225 Plates 89A-89D (Level 7: Section 69) ------------------------------------------------------------- 226-229 Plates 90A-90D (Level 8: Section 75) ------------------------------------------------------------- 230-233

CONTENTS Plates 91A-91D (Level 9: Section 81) ------------------------------------------------------------- 234-237 Plates 92A-92D (Level 10: Section 86) ------------------------------------------------------------ 238-241 Plates 93A-93D (Level 11: Section 90) ------------------------------------------------------------ 242-245 Plates 94A, 95B (Level 12: Section 100) ----------------------------------------------------------246, 247 Plates 95A, 95B (Level 13: Section 105) ----------------------------------------------------------248, 249 Plates 96A, 96B (Level 14: Section 111) ----------------------------------------------------------250, 251 Plates 97A, 97B (Level 15: Section 117) ----------------------------------------------------------252, 253 Plates 98A, 98B (Level 16: Section 120) ----------------------------------------------------------254, 255 Plates 99A, 99B (Level 17: Section 124) ----------------------------------------------------------256, 257 Plates 100A, 100B (Level 18: Section 134) -------------------------------------------------------258, 259 Plates 101A, 101B (Level 19: Section 140) -------------------------------------------------------260, 261 PART VI. GW9 CORONAL ------------------------------------------------------------------------------------------262 Plates 102A, 102B (Levels 1-2: Sections 551, 480) ---------------------------------------------264, 265 Plates 103A, 103B (Levels 3-4: Sections 440, 410) ---------------------------------------------266, 267 Plates 104A, 104B (Level 5: Section 375) --------------------------------------------------------268, 269 Plates 105A, 105B (Level 6: Section 360) --------------------------------------------------------270, 271 Plates 106A, 106B (Level 7: Section 340) --------------------------------------------------------272, 273 Plates 107A, 107B (Level 8: Section 320) --------------------------------------------------------274, 275 Plates 108A, 108B (Level 9: Section 294) --------------------------------------------------------276, 277 Plates 109A, 109B (Level 10: Section 285) -------------------------------------------------------278, 279 Plates 110A, 110B (Level 11: Section 270) -------------------------------------------------------280, 281 Plates 111A, 111B (Level 12: Section 255) -------------------------------------------------------282, 283 Plates 112A, 112B (Level 13: Section 235) -------------------------------------------------------284, 285 Plates 113A, 113B (Level 14: Section 220) -------------------------------------------------------286, 287 Plates 114A, 114B (Level 15: Section 205) -------------------------------------------------------288, 289 Plates 115A, 115B (Level 16: Section 175) -------------------------------------------------------290, 291 Plates 116A, 116B (Level 17: Section 155) -------------------------------------------------------292, 293 Plates 117A, 117B (Level 18: Section 135) -------------------------------------------------------294, 295 Plates 118A, 118B (Level 19: Section 124) -------------------------------------------------------296, 297 Plates 119A, 119B (Level 20: Section 112) -------------------------------------------------------298, 299 Plates 120A, 120B (Level 21: Section 96) --------------------------------------------------------300, 301 Plates 121A, 121B (Level 22: Section 39) --------------------------------------------------------302, 303 PART VII. GW8 SAGITTAL ------------------------------------------------------------------------------------------304 Plates 122A-122D (Level 1: Slide 23, Section 2) ------------------------------------------------- 306-309 Plates 123A-123D (Level 2: Slide 22, Section 2) ------------------------------------------------ 310-313 Plates 124A-124D (Level 3: Slide 20, Section 2) ------------------------------------------------ 314-317 Plates 125A-125D (Level 4: Slide 19, Section 2) ------------------------------------------------ 318-321 Plates 126A-126D (Level 5: Slide 18, Section 2) ------------------------------------------------ 322-325 Plates 127A-127D (Level 6: Slide 16, Section 2) ------------------------------------------------ 326-329 Plates 128A-128D (Level 7: Slide 15, Section 1) ------------------------------------------------ 330-333 Plates 129A-129D (Level 8: Slide 13, Section 2) ------------------------------------------------ 334-337 Plates 130A-130D (Level 9: Slide 12, Section 4) ------------------------------------------------ 338-341 Plates 131A-131D (Level 10: Slide 11, Section 4) ----------------------------------------------- 342-345 Plates 132A, 132B (Lateral Telencephalon, Slide 15, Section 1) ------------------------------346, 347 Plates 133A, 133B (Hypothalamus, Slide 22, Section 2) ---------------------------------------348, 349 Plates 134A, 134B (Basal Telencephalon and Diencephalon, Slide 20, Section 2) ---------350, 351 Plates 135A, 135B (Basal Telencephalon and Diencephalon, Slide 19, Section 2) ---------352, 353 Plates 136A, 136B (Basal Telencephalon and Diencephalon, Slide 18, Section 2) ---------354, 355 Plates 137A, 137B (Basal Telencephalon and Diencephalon, Slide 17, Section 2) ---------356, 357 Plates 138A, 138B (Midbrain, Slide 24, Section 2) ----------------------------------------------358, 359 Plates 139A, 139B (Midbrain Tegmentum, Slide 23, Section 2) -------------------------------360, 361

CONTENTS Plates 140A, 140B (Cerebellum, Slide 20, Section 2) -------------------------------------------362, 363 Plates 141A, 141B (Cerebellum, Slide 12, Section 4) -------------------------------------------364, 365 Plates 142A, 142B (Pons and Medulla, Slide 23, Section 2) -----------------------------------366, 367 Plates 143A, 143B (Pons and Medulla, Slide 22, Section 2) -----------------------------------368, 369 Plates 144A, 144B (Brainstem, Slide 21, Section 2) --------------------------------------------370, 371 Plates 145A, 145B (Brainstem, Slide 20, Section 2) --------------------------------------------372, 373 Plates 146A, 146B (Lateral Pons, Medulla, and Sensory Ganglia, Slide 27, Section 3) ----374, 375 Plates 147A, 147B (Lateral Pons, Medulla, and Sensory Ganglia, Slide 27, Section 4) ----376, 377 PART VIII. GW8 CORONAL ------------------------------------------------------------------------------------------378 Plates 148A, 148B (Levels 1-3: Sections 820, 803, 791) ---------------------------------------380, 381 Plates 149A, 149B (Levels 4-5: Sections 755, 695) ---------------------------------------------382, 383 Plates 150A, 150B (Level 6: Section 653) --------------------------------------------------------384, 385 Plates 151A, 151B (Level 7: Section 635) --------------------------------------------------------386, 387 Plates 152A, 152B (Level 8: Section 605) --------------------------------------------------------388, 389 Plates 153A, 153B (Level 9: Section 587) --------------------------------------------------------390, 391 Plates 154A, 154B (Level 10: Section 546) -------------------------------------------------------392, 393 Plates 155A, 155B (Level 11: Section 531) -------------------------------------------------------394, 395 Plates 156A, 156B (Level 12: Section 504) -------------------------------------------------------396, 397 Plates 157A, 157B (Level 13: Section 468) -------------------------------------------------------398, 399 Plates 158A, 158B (Level 14: Section 438) -------------------------------------------------------400, 401 Plates 159A, 159B (Level 15: Section 402) -------------------------------------------------------402, 403 Plates 160A, 160B (Level 16: Section 390) -------------------------------------------------------404, 405 Plates 161A, 161B (Level 17: Section 324) -------------------------------------------------------406, 407 Plates 162A, 162B (Level 18: Section 276) -------------------------------------------------------408, 409 Plates 163A, 163B (Level 19: Section 252) -------------------------------------------------------410, 411 Plates 164A, 164B (Level 20: Section 234) -------------------------------------------------------412, 413 Plates 165A, 165B (Level 21: Section 206) -------------------------------------------------------414, 415 Plates 166A, 166B (Level 22: Section 170) -------------------------------------------------------416, 417 Plates 167A, 167B (Level 23: Section 158) -------------------------------------------------------418, 419 Plates 168A, 168B (Cerebral Cortex, Section 564) ----------------------------------------------420, 421 Plates 169A, 169B (Paracentral Cortex, Sections 564, 570) ------------------------------------422, 423 PART IX. GW8 HORIZONTAL ------------------------------------------------------------------------------------424 Plates 170A, 170B (Level 1: Section 160) --------------------------------------------------------426, 427 Plates 171A, 171B (Level 2: Section 139) --------------------------------------------------------428, 429 Plates 172A, 172B (Level 3: Section 128) --------------------------------------------------------430, 431 Plates 173A, 173B (Level 4: Section 109) --------------------------------------------------------432, 433 Plates 174A, 174B (Level 5: Section 97) ----------------------------------------------------------434, 435 Plates 175A, 175B (Level 6: Section 86) ----------------------------------------------------------436, 437 Plates 176A, 176B (Level 7: Section 74) ----------------------------------------------------------438, 439 Plates 177A, 177B (Level 8: Section 65) ----------------------------------------------------------440, 441 Plates 178A, 178B (Level 9: Section 45) ----------------------------------------------------------442, 443 Plates 179A, 179B (Level 10: Section 36) --------------------------------------------------------444, 445 Plates 180A, 180B (Diencephalon and Basal Ganglia, Section 97) ---------------------------446, 447 Plates 181A, 181B (Diencephalon, Section 91) --------------------------------------------------448, 449 Plates 182A, 182B (Diencephalon, Section 86) --------------------------------------------------450, 451 Plates 183A, 183B (Diencephalon and Midbrain Tegmentum, Section 66) ------------------452, 453 Plates 184A, 184B (Thalamus, Section 66) -------------------------------------------------------454, 455 Plates 185A, 185B (Hypothalamus and Subthalamus, Section 92) ----------------------------456, 457

CONTENTS PART X. GW7.5 CORONAL ---------------------------------------------------------------------------------------458 Plates 186A, 186B (Level 1: Section 10) ----------------------------------------------------------460, 461 Plates 187A, 187B (Level 2: Section 34) ----------------------------------------------------------462, 463 Plates 188A, 188B (Level 3: Section 40) ----------------------------------------------------------464, 465 Plates 189A, 189B (Level 4: Section 52) ----------------------------------------------------------466, 467 Plates 190A, 190B (Level 5: Section 58) ----------------------------------------------------------468, 469 Plates 191A, 191B (Level 6: Section 70) ----------------------------------------------------------470, 471 Plates 192A, 192B (Level 7: Section 76) ----------------------------------------------------------472, 473 Plates 193A, 193B (Level 8: Section 84) ----------------------------------------------------------474, 475 Plates 194A, 194B (Level 9: Section 92) ----------------------------------------------------------476, 477 Plates 195A, 195B (Level 10: Section 98) --------------------------------------------------------478, 479 Plates 196A, 196B (Level 11: Section 105) -------------------------------------------------------480, 481 Plates 197A, 197B (Level 12: Section 112) -------------------------------------------------------482, 483 Plates 198A, 198B (Level 13: Section 119) -------------------------------------------------------484, 485 Plates 199A, 199B (Level 14: Section 125) -------------------------------------------------------486, 487 Plates 200A, 200B (Level 15: Section 128) -------------------------------------------------------488, 489 Plates 201A, 201B (Level 16: Section 139) -------------------------------------------------------490, 491 Plates 202A, 202B (Level 17: Section 147) -------------------------------------------------------492, 493 Plates 203A, 203B (Level 18: Section 157) -------------------------------------------------------494, 495 Plates 204A, 204B (Level 19: Section 163) -------------------------------------------------------496, 497 Plates 205A, 205B (Level 20: Section 171) -------------------------------------------------------498, 499 Plates 206A, 206B (Level 21: Section 179) -------------------------------------------------------500, 501 Computer-Aided 3-D Reconstruction (Figures 10-11: Top View of Brain) -------------------502, 503 Computer-Aided 3-D Reconstruction (Figures 12-13: Bottom View of Brain) --------------504, 505 Computer-Aided 3-D Reconstruction (Figures 14-15: Side View of Brain) ------------------506, 507 Computer-Aided 3-D Reconstruction (Figure 16: Telencephalic Neuroepithelium) --------------508 Computer-Aided 3-D Reconstruction (Figure 17: Diencephalic Neuroepithelium) ---------------509 Computer-Aided 3-D Reconstruction (Figures 18-19: Rhombencephalic Neuroepithelium) -------------------------------------------510, 511 PART XI. GW7.5 SAGITTAL ---------------------------------------------------------------------------------------512 Plates 207A-207D (Level 1: Slide 30, Section 2) ------------------------------------------------- 514-517 Plates 208A-208D (Level 2: Slide 26, Section 2) ------------------------------------------------ 518-521 Plates 209A-209D (Level 3: Slide 24, Section 2) ------------------------------------------------ 522-525 Plates 210A-210D (Level 4: Slide 22, Section 2) ------------------------------------------------ 526-529 Plates 211A-211D (Level 5: Slide 21, Section 2) ------------------------------------------------ 530-533 Plates 212A-212D (Level 6: Slide 18, Section 2) ------------------------------------------------ 534-537 Plates 213A-213D (Level 7: Slide 17, Section 2) ------------------------------------------------ 538-541 Plates 214A, 214B (Cortex, Slide 32, Section 2/Slide 18, Section 2) -------------------------542, 543 Plates 215A, 215B (Basal Telencephalon, Slide 31, Section 2) --------------------------------544, 545 Plates 216A, 216B (Lateral Telencephalon, Slide 18, Section 2) ------------------------------546, 547 Plates 217A, 217B (Hypothalamus, Slide 28, Section 3) ---------------------------------------548, 549 Plates 218A, 218B (Midbrain Tegmentum, Slide 28, Section 3) -------------------------------550, 551 Plates 219A, 219B (Cerebellum, Slide 18, Section 2/Slide 29, Section 2) -------------------552, 553 Plates 220A, 220B (Pons and Peripheral Ganglia, Slide 18, Section 2) -----------------------554, 555 Plates 221A, 221B (Midline Raphe Glial Structure, Slide 31, Section 2/Slide 32, Section 2) --------------------556, 557 GLOSSARY

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1

PART PARTII

INTRODUCTION INTRODUCTION A. Organization of the Atlas This Atlas focuses on the development of the human brain during the late first trimester, and is Volume 4 in the Atlas of Human Central Nervous System Development series. Volume 1 (Bayer and Altman, 2002) provides a record of the development of the spinal cord from the 4th gestational week (GW4) to the 4th postnatal month. Volume 2 (Bayer and Altman, 2004a) records brain development during the third trimester, with the specimens ranging in age from GW37 to GW26. Volume 3 (Bayer and Altman, 2005) presents brain development during the second trimester, from GW24 to GW13.5. The specimens dealt with in the present volume cover the period from GW11 to GW7.5. The major theme of Volume 2 is the maturation of the brain’s settled and enduring neuron populations. The major theme of Volume 3 is the migration, sojourning, and settling of neuronal populations. Prominent migratory streams and sojourning structures are evident by GW13.5 and many of these are still present at GW24. The major theme of the present volume is late neurogenesis and early neuronal differentiation. The structures of central interest are the visually distinguishable divisions, or mosaics, of the germinal neuroepithelium that generate different populations of neurons and neuroglia. The major theme of the forthcoming Volume 5, which will deal with brain development during the early first trimester (GW3-GW7), will be neuroepithelial expansion along the expanding brain ventricles, and early neurogenesis. As in Volumes 2 and 3, the specimens are presented in a reverse, older-to-younger order. We do that for both heuristic and pedagogical reasons: proceeding from the familiar and better known to what is less familiar and often uncertain or hypothetical. The present volume contains grayscale photographs of nine sets of Nissl-stained, and one set of Bodian-stained sections, of normal brains ranging in age from early fetuses,

crown-rump (CR) length 57-60 mm and estimated age GW11, to late embryos, CR length 21-23 mm and estimated age GW7.5. As in the previous volumes, we sought to select for each age group, brains sectioned in the coronal, horizontal, and sagittal planes. However, this posed a problem as the terms “coronal” and “horizontal” (but not “sagittal”) become more and more ambiguous when applied to younger and younger fetal brains and then embryonic brains. The conventional neuroanatomical designation of “coronal” comes from the practice of placing the dissected brain on a horizontal surface, and with the base of the cerebral cortex and the cerebellar cortex lying flat on that surface, making transverse (left-to-right) cuts perpendicular to the supporting surface. In a similar manner, “horizontal” sections are made by making the cuts parallel to the surface. With this convention, there is little ambiguity, for instance, that the frontal lobe is situated anteriorly and the occipital lobe posteriorly. However, this practice has not been consistently followed by embryologists; indeed, it could not be followed when the brains are not shelled out and the embryo is sectioned de toto. Moreover, since the whole embryo, and more particularly the medulla, pons and brainstem (as described in this volume) undergo a series of flexures, a coronal cut made at one point becomes an oblique or horizontal cut at another point. The same applies to horizontal cuts. Indeed, perusal of embryological textbooks reveals little consistency in the positioning of an embryonic brain or series of brains in the illustrations. In order to produce consistency in presenting the human brains of different fetal and embryonic ages, and facilitate comparisons of the changes across all the ages, we have therefore adopted the following procedure. Each brain, irrespective whether it was designated in the original protocol as “coronal” or “horizontal,” has been placed into an X-Y coordinate frame as if it were a mature brain; i.e., the ventral surface of the cortex and the cerebellum lie flat on an imaginary line that we call the “cardinal horizontal

2 plane.” The line perpendicular to it, we call the “cardinal coronal plane.” Given this coordinate system we then indicate the deviation of a given brain from the cardinal coronal or cardinal horizontal. This method allows a consistent positioning of the telencephalon, diencephalon, mesencephalon, and cerebellum (but not of the pons, medulla and spinal cord) into an age-independent stereotactic framework, and designations like anterior and posterior, and dorsal and ventral pointing in the same direction for easy comparisons across ages. Each specimen is presented in a separate part of the Atlas: GW11 in the coronal plane in Part II; GW11 in the horizontal plane in Part III; GW9 in the sagittal plane in Part IV; GW9 in the horizontal plane in Part V; GW9 in the coronal plane in Part VI; GW8 in the sagittal plane in Part VII; GW8 in the coronal plane in Part VIII; GW8 in the horizontal plane in Part IX; GW7.5 in the coronal plane in Part X; and GW7.5 in the sagittal plane in Part XI. Selected “coronal” plates are presented from rostral to caudal in portrait orientation. The dorsal part of each section is toward the top of the page, the ventral part at the bottom, and the midline is in the vertical center of each section. Sagittal plates are presented from medial to lateral in portrait orientation. The anterior part of each section is facing left, posterior right, dorsal top, and ventral bottom. “Horizontal” plates are presented from rostral to caudal in landscape orientation. The anterior part of each section is facing to the left (bottom of page), posterior to the right (top of page), and the midline is in the horizontal center of each section. Each part contains companion plates, designated as A and B on facing pages; some of the plates are expanded into C and D parts. Parts A and C of each plate on the left page show the full contrast photograph without labels; parts B and D show low contrast copies of the same photograph on the right page with superimposed outlines of structures and unabbreviated labels. The low magnification plates show entire sections to identify the large structures of the brain, such as the various lobes and gyri of the cerebral cortex, and large subdivisions of the brain core, such as the basal ganglia, thalamus, hypothalamus, midbrain, pons, cerebellum, and medulla. The high magnification plates feature enlarged views of the brain core to identify smaller structures. For ease of interpretation in all plates, the ventricles are labeled in capitals, the neuroepithelium and other germinal zones in Helvetica bold, transient structures in Times bold italic, and permanent structures in Times Roman or Times bold. Fixation artifacts and processing damage are usually outlined with dashed lines in parts B or D of each plate. Finally, an alphabetized Glossary gives brief definitions of most labels used in the plates with expanded definitions of all transient developmental structures.

B. Specimens A total of 10 specimens are illustrated and annotated in this Volume. All of them are from the Collections of human embryos or fetal brains currently kept at the National Museum of Health and Medicine, Armed Forces Institute of Pathology, Washington, D.C. One brain, estimated age GW11, is from the Yakovlev Collection and is designated, using the prefix Y, as Y1-59. We give a brief description of the Yakovlev Collection in Volume 2 (Bayer and Altman, 2004a) and more detail is provided in Haleem (1990). Eight specimens are from the Carnegie Collection and are designated by their respective numbers with the added prefix C. The Carnegie Collection was started by Franklin P. Mall (1862-1917) and expanded at the Carnegie Institution of Washington under the direction of George L. Streeter (1873-1948) and George W. Corner (1889-1981). One specimen, estimated age GW9, is from the Minot Collection and is designated, using the prefix M, as M841. The Minot Collection is named after Charles S. Minot (1852-1914), who collected and prepared more than 1900 embryos of different animal species, and about 100 human embryos, close to a century ago. We made use of models of the embryonic and fetal brains prepared in the Carnegie Institution, and by Hochstetter (1919).

C. Photography and Computer Processing Selected sections of the Yakovlev specimen (Y1-59) were photographed at low magnification, using a macro lens (Vivitar, 55mm 1:2.8 auto macro) attached to a Nikkormat 35mm camera that was mounted on a stand over a fluorescent light board. The Carnegie and Minot specimens and all higher magnification views were photographed using either an Olympus photomicroscope or a Wild phototmakroskop. The magnification varied for each specimen according to the size of the dissected brain or entire fetal head: the section with the largest area that could be accommodated within the field of view set the magnification for all sections of a particular specimen. All photographs were taken with a green filter to increase the contrast of the black and white film (Kodak technical pan #TP442). The film was developed at 20°C for 6 to 7 minutes in Kodak HC110 developer (dilution F), followed by Kodak stop bath for 30 seconds, Kodak fixer for 5 minutes, Kodak hypo clearing agent for 1 minute, running water rinse for 10 minutes, and a brief rinse in Kodak photoflo before drying. The negatives were scanned at 2700 dots-per-inch (dpi) with a Nikon Coolscan-1000 35mm film scanner which was interfaced to a PowerPC G3 Macintosh computer running Adobe Photoshop (version 5.02) with a plug-in Nikon driver. To capture the subtle shades of gray, the negatives were scanned as color positives, inverted, and converted to grayscale. Using the enhancement features built into Adobe Photoshop and the additional features of Extensis

3 Intellihance, adjustments were made to increase contrast and sharpness. When the image resolution was set to 300 dpi, a full-size photographic file printed at approximately 12-10 inches. Images are shown at slightly reduced full size on separate pages. Adobe Illustrator was used to superimpose labels and outline structural details on low contrast copies of the Adobe Photoshop files. The Plates were placed into a book-form layout using Adobe InDesign. Finally, camera-ready files were provided to Taylor and Francis in Adobe portable document format. The entire brain and upper cervical spinal cord of C966 was three-dimensionally reconstructed to show the large superventricles and the surface features of the neuroepithelium in the telencephalon, diencephalon, and rhombencephalon (Figures 10-19, Part X). The brain reconstructions (Figures 10-15) involved five steps. First, photographs of serial sections were made throughout the entire brain; the negatives were scanned and converted to computer files as described in the preceding paragraph. Second, all the files of sections selected for the reconstruction were placed into one large Photoshop file that contained a separate photograph in each layer. By altering the visibility and transparency of these layers the sections were aligned to each other as they were before sectioning. Then each layer was saved as a separate file. Third, Adobe Illustrator was used to outline the brain surface and the edge of the ventricles, and the outlines of each section were saved in separate Adobe Illustrator eps (encapsulated postscript) files. Fourth, the eps files were imported into 3D space (x, y, and z coordinates) using Cinema 4DXL (C4D, Maxon Computer, Inc.), a modeling and animation software package. For each section, points on the outlines have unique x-y coordinates and the same z coordinate. By calculating the distance between sections, the entire array of outlines was stretched out in the z axis. The outlines were segregated into two groups, one for the brain surface, the other for the ventricular surface. The C4D loft tool builds a “skin” for each group of outlines by creating a spline mesh of polygons. The polygons start from the x-y points on the first outline with the most anterior z coordinate, to the x-y points on the next outline behind it, and finish with the x-y points on the last outline at the most posterior z coordinate. The spline meshes were rendered either as completely opaque or partly transparent surfaces using the C4D ray-tracing engine. Selected surfaces can be made either invisible or visible using the various options in C4D. The complex structure of the brain requires that the surface be built in several different lofts to avoid twisting the surface in the regions of the brain flexures. When these different loft segments are shown together, there are a few unavoidable artifacts, such as surface indentations and changes in the way light reflects from the surface; some of these are labeled in Figures 10-19. Fifth, the rendered images were converted to Adobe Photoshop files, and Adobe Illustrator was used to label the structures and to draw thin lines on some of the surfaces to make the images easier to under-

stand. The reconstruction of the parts of the neuroepithelium (Figures 16-19) followed the same five steps except that only the selected parts of the neuroepithelium in each section were outlined, and these were always rendered as completely opaque blocks of tissue.

D. Identification of Immature Brain Structures In contrast to the mature human brain, there are no comprehensive textbooks or atlases available on the entire course of the human brain development. The few publications that cover the late first trimester give overviews that identify the largest brain structures in chapters included in embryology textbooks (e.g., Patten, 1953; Hamilton et al., 1964) and atlases (Gasser, 1975; O’Rahilly and Müller, 1994). Some facets of human brain development during this period are part of an overview in an edited publication (Sidman and Rakic, 1982), and there are a few research papers available on the development of specific brain regions (e.g., Gilbert, 1935; Pearson, 1941; Kappers, 1958; Humphrey, 1960, 1968; Richter, 1965; Kahle, 1956; Hewitt, 1958; Shuangshoti and Netsky, 1966; Rakic and Sidman, 1970; Moore et al., 1999; Forutan et al., 2001; Koutcherov et al., 2002). There is no single publication that labels both large and small structures in the developing human brain in serially sectioned specimens at several different ages during the late first trimester. Many of the transient features of the early fetal/late embryonic human brain have never been studied. Therefore, we rely to a great extent on our experimental work in the developing rat brain to identify formative brain structures, migratory streams, and components of the germinal neuroepithelium. In those studies, we labeled proliferating cells in the germinal matrices of the brain with 3H-thymidine administered at daily intervals through the entire prenatal period, and every other day up to weaning. By varying survival times after 3 H-thymidine exposure from 1 hour, to days, we used the autoradiographic technique to establish quantitative timetables of neurogenesis, trace the speed and route of neuronal migrations, and document the settling patterns of neurons in the maturing brain. The results of these studies were published over a period of three decades in journal articles (see below) and reviewed in chapters contributed to edited books (Altman and Bayer, 1975, 1995, 2004; Altman, 1992; Bayer and Altman, 1995a, 1995b). We have also presented evidence for many parallels in the sequential order of brain development in rat and man (Bayer et al., 1993). Readers interested in details of those experimental results and the rationale of some of the anatomic and morphogenetic identifications made in this Atlas may consult the following publications. Amygdala: Bayer (1980c). Basal Ganglia: Bayer (1984, 1985b, 1987). Cerebellum: Altman and Bayer (1978a, 1982, 1985a, 1985b, 1985c, 1997).

4 Cerebral Cortex: Altman and Bayer (1990a, 1990b); Bayer and Altman (1990, 1991a, Bayer et al., 1991a). Cranial Nerve Nuclei: Altman and Bayer (1980a, 1980b, 1980c, 1982b). Hippocampus: Altman and Bayer (1975, 1990c, 1990d, 1990e); Bayer (1980a, 1980b). Hypothalamus: Altman and Bayer (1978c, 1978d, 1978e, 1986). Medulla: Altman and Bayer (1980a, 1980b, 1980c, 1982b). Midbrain: Altman and Bayer (1981a, 1981b, 1981c). Olfactory Bulb: Altman (1969); Bayer (1983). Pontine Area: Altman and Bayer (1978b, 1980d, 1987a, 1987b, 1987c, 1987d). Preoptic Area: Bayer and Altman (1987). Rhinencephalon: Bayer (1985a, 1986a, 1986b); Bayer and Altman (1991b). Septal Area: Bayer (1979a, 1979b). Spinal Cord: Altman and Bayer (1984, 2001). Thalamus: Altman and Bayer (1979a, 1979b, 1979c, 1988a, 1988b, 1988c, 1989a, 1989b, 1989c).

E. Major Transitional Brain Structures in the Late First Trimester Transitional brain structures in late first trimester fetuses include the following: (i) The neuroepithelium (NEP), the primary germinal matrix of neural stem cells that are the ultimate source of all the neurons and neuroglia of the central nervous system. (ii) The rhombencephalic, mesencephalic, diencephalic, and telencephalic superventricles that provide the greatly expanded cerebrospinal fluid (CSF) interface for the shuttling nuclei of the pseudostratified NEP cells that undergo mitotic division near the lumen. (iii) The expanding fetal choroid plexus (CP), and its later shrinkage and transformations, which appears to play a role in neurogenesis and neuronal differentiation. (iv) The spreading glioepithelia (GEP) along several fiber tracts, and the glioepithelia associated with the formative ependymal layer that lines the enduring portions of the brain ventricles (G/EP). (v) The secondary germinal matrices abutting the neuroepithelium, such as the subventricular zone (SVZ) of the cerebral cortex, and others situated some distance from the ventricles. (vi) Short-distance migratory routes, and long-distance migratory streams, such as the telencephalic rostral migratory and lateral migratory streams and several precerebellar migratory streams. (vii) The transient sojourn zones and stratified transitional fields, such as the cortical stratified transitional field (STF) and the cerebellar transitional field (CTF). The Neuroepithelium and its Mosaic Organization. The NEP is a cell-dense pseudostratified proliferative matrix that lines the extensive ventricular system of the developing brain and spinal cord. It used to be called the ependymal layer, but that term is no longer used because the ependyma is a highly specialized tissue that lines the

shrunken ventricles of the maturing and adult central nervous system. The NEP is composed of stem cells that either differentiate as specialized populations of neurons and neuroglia or give rise to secondary germinal matrices some distance from the ventricular system. The latter include the SVZ of the cerebral cortex, the external germinal layer of the cerebellar cortex, and the subgranular zone of the hippocampal dentate gyrus. At the outset of its development, the NEP stem cells are the sole constituents of the brain (to be described and illustrated in Volume 5). The bulk of NEP cells either keep proliferating or generate differentiating (postmitotic) neurons that, following a precise spatio-temporal order, migrate over a short or long distance to form various brain structures. While NEP cells all look alike in Nissl-stained preparations, discontinuous NEP “stretches” and “patches,” or mosaics, can be distinguished along the ventricles in terms of matrix thickness (pseudostratified cell depth), cell packing density, and as growing or shrinking ventricular protuberances, invaginations and evaginations. Using experimental techniques in rats (short-survival, sequential survival, and long-survival 3 H-thymidine autoradiography, respectively), we dated the changing proliferative dynamics of these NEP mosaics, tracked their migratory paths and settling patterns, and related that information to the time of origin of different neuronal populations in various brain regions and structures. On the assumption that the neurons that form discrete parenchymal regions and structures (different lobes, ganglia, nuclei, etc.) in the neighborhood of these NEP mosaics are progeny of those mosaics, we name the latter as putative NEPs of those structures. Examples of broader identifications of NEP “stretches” are frontal cortical NEP, hypothalamic NEP, thalamic NEP, and hippocampal NEP. An example of more specific identification of “patches” along the hippocampal NEP are subicular NEP (the mosaic that generates neurons of the subiculum), ammonic NEP (the mosaic that generates neurons the pyramidal cells of Ammon’s horn), and dentate NEP (the mosaic that generates the granule cells of the dentate gyrus). In cases where a germinal matrix abuts a fiber tract, we identify that as a putative glioepithelium (GEP), e.g, the fornical GEP. In addition to the cells that migrate short distances from their germinal sites of origin, there are others that migrate over long distances. Examples are the cells of the rostral migratory stream in the anterior telencephalon that migrate to the olfactory bulb (Altman, 1969), and the intramural (parenchymal) and extramural (subpial) migratory streams of the rhombencephalon that form the precerebellar nuclei in the medulla and pons (Altman and Bayer, 1987a-d). In such instances, we identify these NEP mosaics on the basis of the available experimental evidence of their ultimate destinations. Finally, there are many sites where we have no information at all on the destination of the neurons leaving particular NEP mosaics and indicate that uncertainty either by a question mark following a tentative identification or by omitting any identification.

5 Neurogenesis and its relation to the Expansion and Shrinkage of the Superventricles. The NEP originates as an open proliferative sheet, the neural plate, without its own fluid environment. As we shall illustrate in Volume 5, the ventricles begin to form at about GW3, after the closure of the neural tube (the future spinal cord) and the cephalic vesicles (the future brain) is completed. Following that momentous morphogenetic event, the ventricles expand enormously during the rest of the first trimester and, with differences among the different ventricles, then begin to shrink during the second or third trimester, and gradually assume their mature size and configuration. The first lumen to expand is the rhombencephalic ventricle. Beginning as a shallow invagination beneath a thin membrane (the medullary velum) at about GW4, it expands greatly as a cavernous cistern is formed by the flexures of the medulla, pons and brainstem, underneath the cover of the medullary velum. As illustrated in this Volume, the expansion of the rhombencephalic ventricle continues until about GW9, and then it starts to shrink and gradually assumes the form of the familiar 4th ventricle. Next, the mesencephalic ventricle (the future aqueduct) and the diencephalic ventricle (the future 3rd ventricle) start to expand and, after a shorter developmental period, begin to shrink. Finally, at about GW5.5, the lateral ventricles begin to form as symmetrical balloon-like fluid compartments of the midline diencephalic ventricle and expand enormously up to GW11; thereafter the lumen of the lateral ventricles begin to shrink as the basal ganglia and the cerebral cortex develop. We name these greatly expanded embryonic cisterns superventricles to distinguish them from the greatly diminished and transformed mature ventricles for the following reasons. (1) Unlike the shrunken mature ventricles, the cavernous embryonic ventricles are lined by proliferating NEP cells rather than differentiated ependymal cells. This raises the possibility that the embryonic and mature ventricles and the CSF they contain serve different functions. (2) We know since the pioneering studies of Sauer (1936) that the NEP is a pseudostratified epithelium and that the nuclei of NEP cells shuttle to the ventricular lumen before undergoing mitosis (Sauer called the process interkinetic nuclear migration). This shuttling to the lumen as a prerequisite for cell division means that the rate of NEP cell proliferation is limited by the length of the ventricular shoreline because the elongated cells straddling the depth of the pseudostratified NEP cannot divide unless there is room for them to move to the NEP/CSF interface. An interesting point in this context is the spatial orientation of the dividing cells near the lumen. It has been noted in the past (e.g., Bayer and Altman, 1991a) that the cleavage plane of these mitotic cells may be radial, or vertical (tangential to the ventricular lining) or horizontal (parallel to the ventricular lining). Vertically cleaving cells occupy double of the NEP/CSF interface when compared with hor-

izontally cleaving cells. It has been hypothesized recently that vertical cleavage results in symmetrical cell division, and horizontal cleavage in asymmetric cell division (e.g., Chenn and McConnell, 1995; Kornack and Rakic, 1995). Symmetric cell division is assumed to produce two proliferative NEP cells lying next to one another along the ventricle; collectively that should result in an expansion of the ventricular shoreline. Asymmetric cell division is assumed to produce a postmitotic daughter cell, presumably the one farther from the ventricle, a differentiating cell that is ready to leave the NEP. Some evidence has been presented recently of an increase in asymmetric division in the cortical NEP of mice as a function of increasing fetal age (Estivill-Torrus et al., 2002). Asymmetric division should not affect the length of NEP/CSF interface. The shrinkage of the NEP during fetal development would take place if more and more NEP cells lost their mitotic potency and their nuclei no longer returned to the ventricular lumen. (3) Why is it obligatory for NEP cell nuclei to move to the ventricular lumen to divide when the stem cells of secondary germinal matrices, like the subpial external germinal layer of the cerebellum or the subgranular zone of the hippocampus, divide some distance from the ventricles? One possibility is that the embryonic CSF contains some factor or factors necessary for primary (pluripotent) NEP cell division. This is supported by reports that embryonic CSF promotes NEP cell survival, proliferation, and neurogenesis in experimental animals (Mashayekhi et al., 2002; Gato et al., 2005). (4) The distinctiveness of the two ventricular systems is suggested by a different functional relationship between the superventricles and the fetal CP, and the enduring ventricles and the mature CP. To begin with, the initial expansion of the rhombencephalic and the telencephalic superventricles starts before the CP forms (this will be documented in Volume 5 of this series). Hence, unlike the CSF of the mature ventricular system, the CSF of the embryonic superventricles must originate from some other source than CP secretion. (5) Moreover, the fetal CP that forms later and rapidly expands to fill the rhombencephalic and telencephalic superventricles (as illustrated in this Volume) has a different cellular organization than the mature CP (Kappers, 1958; Tennyson and Pappas, 1964; Shuangshoti and Netsky, 1966; Dohrmann, 1970; Dziegielewska et al., 2001; Johansson et al., 2005). The adult choroid plexus is a distinctive frond-like tissue composed of a monolayer of differentiated cuboidal cells that surround a capillary core. The exposed surface of these cuboidal cells is covered by a rich meshwork of microvilli and some cilia, and the cell interior is filled with mitochondria. These features, and added evidence, is the basis of the widely held view that the mature CP is a secretory tissue involved in CSF production. In contrast, the fetal CP is a smooth, multilayered

6 (pseudostratified) epithelium composed of spindle-shaped cells that have a simple exposed surface and contain few mitochondria. Unlike the mature CP cells, these fetal CP cells are filled with glycogen. Hence, it has been suggested that the principal function of the embryonic CP is the glycolytic (anaerobic) support of NEP cell proliferation and neurogenesis rather than the production of CSF. (6) Finally, and most importantly, the chronological differences in the expansion, configurational transformations, and persistence of the different superventricles can be related to regional differences in the kinetics, date of origin, and time span of cell proliferation in stretches and patches of the NEP lining that produce neurons and neuroglia for different brain structures. For instance, the dorsal roof and lateral wall of the telencephalic superventricle is formed by an extensive, continuous dome-like stretch of NEP that generates an immense number and homogeneous set of cortical neurons in a precise sequential order (infragranular layer cells first, granular layer cells next, and supragranular layer cells last) through its entire extent and over an extended period of time. These neurogenetic features account for the smooth, spherical configuration of the NEP lining of the telencephalic superventricle over an extended period during embryonic and fetal development. In contrast, the ventral and medial shores of the telencephalic superventricles are much less regular because discrete NEP stretches or patches generate neurons here for diverse brain structures – septum, basal ganglia, nucleus accumbens, basal telencephalon, amygdala, hippocampus, etc. – each with different neurogenetic timetables, cell compositions, and population sizes. At these sites, the expanding and shrinking NEP mosaics (and the differentiating parenchymal structures associated with them) produce variably shaped ventricular pools, recesses, and narrows. Still more complex are the configurational changes over time in the diencephalic, mesencephalic, and rhombencephalic superventricles. This is so because at these locations short NEP patches give rise to a multitude of structurally and functionally different brain nuclei, many of which are composed of a relatively small number of neurons generated over a short time span. For instance, we can distinguish along the diencephalic superventricle not only NEP stretches that give rise to the thalamus, epithalamus, subthalamus and hypothalamus, but also patches – temporary evaginations and invaginations – that generate neurons, for instance, for the distinct thalamic nuclei. These expanded and short-lived shorelines create an expanded NEP/CSF interface for the optimal generation of neural stem cells of a particular type. Glioepithelia and the Ependymal Linings of the Enduring Ventricles. Glioepithelia (GEP) are fate-restricted tissues of proliferative cells that produce neuroglia. On the basis of experimental studies in rats, in which proliferative cells are tagged with 3H-thymidine, we distinguish four types of GEP. The first is difficult to distinguish from the

primary NEP lining the ventricles except that these patches tend to be thin and display proliferative activity for some time after local neurogenesis has ended. These patches begin to appear caudally in the older fetuses of the age group covered in this Volume, and because at most of these sites an ependymal lining will be forming around the enduring ventricles, they are designated uncertainly as glioepithelium/ependyma (G/EP). Examples are the medullary, pontine, hypothalamic, and thalamic G/EP. The second type lines fiber tracts that are devoid of neuronal cell bodies. In the older fetuses of this age group this type is exemplified by the fornical GEP, a continuation of the hippocampal NEP. The fornical GEP probably contains precursors of oligodendrocytes. The third type is the perifascicular GEP that surrounds and penetrates large fiber tracts. In the older specimens of this age group these are seen around the olfactory tract and the optic nerve, chiasm and tract. The fourth type, the subpial GEP, is found as a covering of the telencephalon, known as the subpial granular layer (Brun, 1965). The perifascicular and subpial GEPs may be continuous and of placodal rather than neuroepithelial origin. Secondary Germinal Matrices, Migratory Streams, and Sojourn Zones. Prominent transitional structures of the developing brain during the second trimester, as illustrated in Volume 3 of this series, are the secondary germinal matrices, the prominent sojourn zones, and the large migratory streams. The principal secondary germinal matrices are the subventricular zone (SVZ) abutting the cortical NEP, the SVZ of the basal ganglionic (anterolateral, anteromedial and posterior) eminences, the subgranular zone of the hippocampal dentate gyrus, and the external germinal layer of the cerebellar cortex. All of these secondary matrices are late-generated, fate-restricted stem cells that divide some distance from the ventricles and produce microneurons (neurons with small cell bodies and locally ramifying axons); many of which are known as “granule cells.” In the specimens we use, the time of emergence of the cortical SVZ could not be determined because of the difficulty of distinguishing it from the NEP, but it is clearly present by GW11. The basal ganglionic SVZ begins to form as early as GW7.5 and is prominent between the NEP and the parenchyma by GW8. The external germinal layer that originates in the germinal trigone of the cerebellar NEP is not recognizable until GW9. The hippocampal dentate NEP, which is the source of the dentate migration (and which will later form the subgranular zone) is present by GW9; however, the dentate gyrus is only a miniscule structure at GW11. In general, there is no evidence for the onset of microneuron production during this period. There are long and short migratory streams that carry neural stem cells and/or immature neurons from the NEP to their destination. A prominent long-distance migration during the second trimester is the rostral migratory stream of the telencephalon which, among others, contains cells

7 that differentiate as olfactory bulb granule cells. The rostral migratory stream is not clearly distinguishable at GW9 from the olfactory NEP, which generates the output neurons (mitral cells) of the olfactory bulb; it becomes recognizable as a distinct entity by GW11, and expands greatly during the second trimester (Volume 3). Among the long-distance precerebellar migratory streams, the posterior intramural migratory stream, which contains the neurons that migrate to form the prominent inferior olive, is evident by GW7.5, and remains so throughout the late first trimester. Also present in these specimens are the posterior extramural migratory stream that contains neurons of the lateral reticular and external cuneate nuclei, and the anterior extramural migratory stream that contains pontine gray neurons. However, the pontine gray nucleus is not evident until GW11 when the earliest corticofugal fibers begin to traverse it and the earliest fibers of the middle cerebellar peduncle begin to form. In Volume 3 during the second trimester, we have illustrated the prominence of the cortical stratified transitional field (STF) sandwiched between the NEP and the cortical plate, the future gray matter. We have identified six distinct cellular and fibrous layers within the STF, where cortical neurons sojourn for some time and mingle with afferent, efferent, and commissural fibers before they resume their migration and settle in the cortical plate. We postulated that the STF is a staging area where connections are formed between unspecified cortical neurons and the functionally and topographically specified thalamocortical fiber systems that provide input to them. As seen in the present Volume, the cortical STF is developing during the late first trimester. STF1 and STF5 are first evident at GW8 in the earlier-maturing anterolateral cortical region spreading into the later-maturing dorsomedial cortical region. The formation of STF5 appears to coincide with the growth of thalamocortical fibers through the diencephalic-telencephalic junction and their penetration into the formative cerebral cortex. Between GW9 and GW11 an additional layer, STF4, begins to emerge slowly and uncertainly in the earlier maturing regions of the cortex (i.e., the lateral aspect of the anterior hemisphere). The emergence of STF4 may be associated with the onset of the descent of corticofugal fibers. The other STF layers (STF3, STF2, and STF6) do not start to form until the beginning of the second trimester (Volume 3). Several other transitional fields are seen in the developing brain during this period. In the GW7.5-GW8 specimens, large cell aggregates surround the thalamic NEP that we interpret to be sojourning neuronal populations of the anterior, dorsal and ventral thalamic complexes. And, based on observations in rats, we assume that the posterior thalamic complex that will produce neurons for the lateral geniculate body and the pulvinar is initially in a dorsomedial position and then migrates gradually ventrolaterally toward the growing optic tract. The morphogenetic sig-

nificance of the transitional cell columns and fiber bands seen in the GW9 thalamus, before the thalamic neurons assume their “nuclear” configuration, remains to be elucidated. Another region with alternating bands of sojourning cells and growing fibers is the cerebellar transitional field (CTF). Six layers are distinguished in the formative cerebellum in GW7.5 specimens from the surface toward the NEP: the fibrous CTF1, the cellular CTF2, CTF3 with cells and fibers, the cellular CTF4, CTF5 with cells and fibers, and the cellular CTF6. On the basis of experimental evidence in rats, we interpret the upper cellular layers (CTF2-4) as the earlier generated deep neurons that sojourn for a while superficially, and the lower cellular layers (CTF5-6) as consisting mainly of the later generated Purkinje cells. This stratification becomes blurred by GW8 and GW9 as the Purkinje cells migrate toward the surface and the deep neurons move back toward the core of the cerebellum. The upward migration of Purkinje cells is associated with the spreading of the external germinal layer over the surface of the formative cerebellar cortex. By GW11 most of the Purkinje cells are in a superficial position, where they form parasagittal bands beneath the continuous canopy of the external germinal layer.

F. A Note on Genetic Analyses of NEP Mosaicism As we noted earlier, the NEP cells that line the banks of the superventricles look alike in Nissl-stained preparations. The idea of NEP mosaicism is based on the siteand age-dependent distinctiveness of stretches and patches of the NEP in terms of their thickness, the temporary formation of larger protuberances and smaller evaginations and invaginations into the ventricle, and their differential proliferative dynamics, as ascertained with 3H-thymidine autoradiography. These spatiotemporal differences in the regional appearance and proliferative dynamics of NEP mosaics, and the fact that they give rise to different brain structures and cell types, raise the possibility that the stem cells composing them are different genetically before they start to differentiate. There is, indeed, emerging experimental evidence in embryonic and fetal mammals (mostly mice) for the genetic distinctiveness of some of the stretches and patches of NEP that are homologous with those we describe here in the first trimester human brain. The experiments are based mostly on in situ hybridization of homeodomain-containing transcription factors that are visualized in the developing brain of normal and mutant mice with immunohistochemical markers. Several laboratories, for instance, have reported a pronounced expression of Pax6, in combination with other transcription factors, in the dorsal neocortical NEP (e.g., Walther and Gruss, 1991; Stoykova and Gruss, 1994; Warren et al., 1999; EstivillTorrus et al., 2002; Kimura et al., 2005). At the embryonic age when Pax6 expression is limited to the dorsal telencephalon, Nkx2.1 and Gsh2 are expressed in the ventral telencephalon and the medial telencephalon (Corbin et al.

8 2003). Some differences were noted in the expression of these factors in the lateral, medial and posterior components of the ganglionic ventral telencephalon. According to another study, different markers highlight different components of the medial telencephalon and the diencephalon in 12.5 day-old mouse embryos (Kimura et al., 2005). Using a different terminology from that used by the authors, Wnt8b appears to demarcate the entire hippocampal primordium in the medial cortex, and the epithalamus and the mammillary body in the diencephalon. Within the domain of the medial telencephalon, Ephb1 demarcates the Ammonic NEP, Wnt3a the dentate NEP, and TTR the primordium of the telencephalic choroid plexus. Although as yet this genetic approach is limited to a single species in mammals, it is expected that it will shed considerable light on NEP cell heterogeneity and the regional differentiation of the embryonic and fetal brain in other animals and man.

G. A Note on Functional Maturation There is currently considerable scientific interest in the physiological maturation of the prenatal human brain, and the correlated issue of the mental status of the embryo and fetus is receiving much public attention. Studies in the first half of the twentieth century with aborted fetuses have indicated that embryos of about 20-21 mm CR length (corresponding to the GW7.5 specimens in the present volume) begin to reliably respond to tactile stimulation with holokinetic (“total pattern”) body movements (Fitzgerald and Windle, 1942; Hooker, 1942). In GW10 fetuses (CR 48.5 mm) ideokinetic or isolated movements are also elicited, such as partial closure of the fingers (though not effective grasping), when the palm of the hand was stimulated (Humphrey, 1964). The more recent introduction of ultrasonic recording techniques has permitted the observation of the emergence of “spontaneous” fetal behavior in normal embryos and fetuses in utero. A pioneering study showed that the holokinetic “startle” response emerges as early as GW6, isolated arm and leg movements by GW7, and head rotation and hand and face contact beginning at about GW8 (de Vries, 1982, 1985). According to a more recent study with improved ultrasonic recording methods, isolated arm movements are more frequent than isolated leg movements during the first trimester, and head turning and hand to head contact do not occur with high frequency until the second trimester (Kurjak et al., 2005). Are the late-embryonic and early-fetal movements reflex reactions mediated by lower-level spinal cord and brain stem mechanisms, or are they emerging voluntary activities carried out under higher-level cortical guidance, reflecting sentience? We have raised this question earlier in the context of our study of the development of the reflex circuitry of the human spinal cord (Altman and Bayer, 2001). Because the spinal cord substrate of the sensorimotor reflex arc begins to form between GW7 and GW8 – the collateral branches of dorsal root sensory nerves sprout and then

reach the ventral horn motor neurons during this period – we proposed that the isolated limb movements displayed by embryos of that age are reflex reactions. The morphogenetic evidence presented in this Volume extends that inference by showing that the first trimester embryonic movements cannot be cortically mediated voluntary activities. First, the higher-level sensory channel, the medial lemniscal system relayed in the thalamus, does not reach the cortical plate (the future cortical gray matter) during this period. The internal capsule that contains the thalamocortical fibers is not yet evident at GW7.5 either in the lateral border of the thalamus or the narrow parenchymal bridge that links the diencephalon and the telencephalon. A large collection of thalamocortical fibers “funnel” through the internal capsule by GW8, passing through the basal ganglia and approaching the base of the formative cerebral cortex. These fibers begin to penetrate STF4 of the paracentral lobule by GW9 and that process continues through GW11. It is probable, but this needs to be experimentally verified, that the neurons of layer IV of the cortex, the principal target of thalamocortical fibers, are either still being generated or are still in the STF5 sojourn zone. Thus, there is as yet no functional connection between the thalamus and cells of the cortical plate. The second consideration concerns corticofugal output to the brain stem and spinal cord, which is a prerequisite for cortically mediated motor control. The pontine gray, through which the corticospinal tract descends to the spinal cord, is not evident at GW9; it begins to form about GW11. In one such specimen illustrated (Y1-59; CR 60 mm), but not in the other (C1500; CR 57 mm), a bundle of corticofugal fibers traverses the pons. Although the earliest contact between thalamocortical fibers and differentiating cortical neurons may be established during this period, we have shown earlier that the lateral and ventral corticospinal tracts do not penetrate the spinal cord until the second trimester (Altman and Bayer, 2001: Figs. 7-23, 7-24, 7-35) and are still unmyelinated at birth (Altman and Bayer, 2001: Fig. 8-14).

H. References Altman, J. (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. Journal of Comparative Neurology, 137:433-458. Altman, J. (1992) The early stages of nervous system development: Neurogenesis and neuronal migration. In: A. Björklund, T. Hökfelt and M. Tohyama (eds.) Handbook of Chemical Neuroanatomy. Volume 10. Ontogeny of Transmitters and Peptides in the CNS, pp. 1-31. Amsterdam: Elsevier.

9 Altman, J. and S. A. Bayer. (1975) Postnatal development of the hippocampal dentate gyrus under normal and experimental conditions. In: R. L. Isaacson and K. H. Pribram (eds.), The Hippocampus. Vol. 1. Structure and Development, pp. 95-122. New York: Plenum Press. Altman, J. and S. A. Bayer (1978a) Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum. Journal of Comparative Neurology, 179:23-48. Altman, J. and S. A. Bayer (1978b) Prenatal development of the cerebellar system in the rat. II. Cytogenesis and histogenesis of the inferior olive, pontine gray, and the precerebellar reticular nuclei. Journal of Comparative Neurology, 179:49-76. Altman, J. and S. A. Bayer (1978c) Development of the diencephalon in the rat. I. Autoradiographic study of the time of origin and settling patterns of neurons of the hypothalamus. Journal of Comparative Neurology, 182:945-972. Altman, J. and S. A. Bayer (1978d) Development of the diencephalon in the rat. II. Correlation of the embryonic development of the hypothalamus with the time of origin of its neurons. Journal of Comparative Neurology, 182:973-994.

of the time of origin of neurons of the lower medulla. Journal of Comparative Neurology, 194:1-35. Altman, J. and S. A. Bayer (1980b) Development of the brain stem in the rat. II. Thymidine-radiographic study of the time of origin of neurons of the upper medulla, excluding the vestibular and auditory nuclei. Journal of Comparative Neurology, 194:37-56. Altman, J. and S. A. Bayer (1980c) Development of the brain stem in the rat. III. Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla. Journal of Comparative Neurology, 194:877-904. Altman, J. and S. A. Bayer (1980d) Development of the brain stem in the rat. IV. Thymidine-radiographic study of the time of origin of neurons in the pontine region. Journal of Comparative Neurology, 194:905-929. Altman, J. and S. A. Bayer (1981a) Time of origin of neurons of the rat inferior colliculus and the relations between cytogenesis and tonotopic order in the auditory pathway. Experimental Brain Research, 42:411-423. Altman, J. and S. A. Bayer (1981b) Time of origin of neurons of the rat superior colliculus in relation to other components of the visual and visuomotor pathways. Experimental Brain Research, 42:424-434.

Altman, J. and S. A. Bayer (1978e) Development of the diencephalon in the rat. III. Ontogeny of the specialized ventricular linings of the hypothalamic third ventricle. Journal of Comparative Neurology, 182:995-1016.

Altman, J. and S. A. Bayer (1981c) Development of the brain stem in the rat. V. Thymidine-radiographic study of the time of origin of neurons of the midbrain tegmentum. Journal of Comparative Neurology, 198:677-716.

Altman, J. and S. A. Bayer (1979a) Development of the diencephalon in the rat. IV. Quantitative study of the time of origin of neurons and the internuclear chronological gradients in the thalamus. Journal of Comparative Neurology, 188:455-472.

Altman, J. and S. A. Bayer (1982a) Morphological development of the rat cerebellum and some of its mechanisms. In: S. L. Palay and V. Chan-Palay (eds.). The Cerebellum: New Vistas, pp. 8-49. Berlin: SpringerVerlag.

Altman, J. and S. A. Bayer (1979b) Development of the diencephalon in the rat. V. Thymidine-radiographic observations on internuclear and intranuclear gradients in the thalamus. Journal of Comparative Neurology, 188:473-500.

Altman, J. and S. A. Bayer (1982b) Development of the Cranial Nerve Ganglia and Related Nuclei in the Rat. (Advances in Anatomy, Embryology and Cell Biology, Vol. 74). Berlin: Springer-Verlag.

Altman, J. and S. A. Bayer (1979c) Development of the diencephalon in the rat. VI. Re-evaluation of the embryonic development of the thalamus on the basis of thymidine-radiographic datings. Journal of Comparative Neurology, 188:501-524. Altman, J. and S. A. Bayer (1980a) Development of the brain stem in the rat. I. Thymidine-radiographic study

Altman, J. and S. A. Bayer (1984) The Development of the Rat Spinal Cord. (Advances in Anatomy, Embryology and Cell Biology, Vol. 85). Berlin: Springer-Verlag. Altman, J. and S. A. Bayer (1985a) Embryonic development of the rat cerebellum. I. Delineation of the rat cerebellum and early cell movements. Journal of Comparative Neurology, 231:1-26.

10 Altman, J. and S. A. Bayer (1985b) Embryonic development of the rat cerebellum. II. Translocation and regional distribution of the deep neurons. Journal of Comparative Neurology, 231:27-41. Altman, J. and S. A. Bayer (1985c) Embryonic development of the rat cerebellum. III. Regional differences in the time of origin, migration and settling of Purkinje cells. Journal of Comparative Neurology, 231:42-65. Altman, J. and S. A. Bayer (1986) The Development of the Rat Hypothalamus. (Advances in Anatomy, Embryology and Cell Biology, Vol.100). Berlin: SpringerVerlag. Altman, J. and S. A. Bayer (1987a) Development of the precerebellar nuclei in the rat. I. The precerebellar neuroepithelium of the rhombencephalon. Journal of Comparative Neurology, 257:477-489. Altman, J. and S. A. Bayer (1987b) Development of the precerebellar nuclei in the rat. II. The intramural olivary migratory stream and the neurogenetic organization of the inferior olive. Journal of Comparative Neurology, 257:490-512. Altman, J. and S. A. Bayer (1987c) Development of the precerebellar nuclei in the rat. III. The posterior precerebellar extramural migratory stream and the lateral reticular and external cuneate nuclei. Journal of Comparative Neurology, 257:513-528. Altman, J. and S. A. Bayer (1987d) Development of the precerebellar nuclei in the rat. IV. The anterior precerebellar extramural migratory stream and the nucleus tegmenti pontis and the basal pontine gray. Journal of Comparative Neurology, 257:529-552. Altman, J. and S. A. Bayer (1988a) Development of the rat thalamus. I. Mosaic organization of the thalamic neuroepithelium. Journal of Comparative Neurology, 275:346-377. Altman, J. and S. A. Bayer (1988b) Development of the rat thalamus. II. Time and site of origin and settling pattern of neurons derived from the anterior lobule of the thalamic neuroepithelium. Journal of Comparative Neurology, 275:378-405. Altman, J. and S. A. Bayer (1988c) Development of the rat thalamus. III. Time and site of origin and settling pattern of neurons of the reticular nucleus. Journal of Comparative Neurology, 275:406-428. Altman, J. and S. A. Bayer (1989a) Development of the rat thalamus. IV. The intermediate lobule of the thalamic neuroepithelium, and the time and site of origin and

settling pattern of neurons of the ventral nuclear complex. Journal of Comparative Neurology, 284:534-566. Altman, J. and S. A. Bayer (1989b) Development of the rat thalamus. V. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the medial geniculate body. Journal of Comparative Neurology, 284:567-580. Altman, J. and S. A. Bayer (1989c) Development of the rat thalamus. VI. The posterior lobule of the thalamic neuroepithelium and the time and site of origin and settling pattern of neurons of the lateral geniculate and lateral posterior nuclei. Journal of Comparative Neurology, 284:581-601. Altman, J. and S. A. Bayer (1990a) Vertical compartmentation and cellular transformations in the germinal matrices of the embryonic rat cerebral cortex. Experimental Neurology, 107:23-35. Altman, J. and S. A. Bayer (1990b) Horizontal compartmentation in the germinal matrices and intermediate zone of the embryonic rat cerebral cortex. Experimental Neurology, 107:36-47. Altman, J. and S. A. Bayer (1990c) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. Journal of Comparative Neurology, 301:325-342. Altman, J. and S. A. Bayer (1990d) The prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. Journal of Comparative Neurology, 301:343-364. Altman, J. and S. A. Bayer (1990e) The migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. Journal of Comparative Neurology, 301:365-381. Altman, J. and S. A. Bayer (1990f) Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cells. Journal of Comparative Neurology, 301:325-342. Altman, J. and S. A. Bayer (1995) Atlas of Prenatal Rat Brain Development. Boca Raton, FL: CRC Press Altman, J. and S. A. Bayer (1997) Development of the Cerebellar System in Relation to Its Evolution, Structure, and Functions. Boca Raton, FL: CRC Press. Altman, J. and S. A. Bayer (2001) Development of the Human Spinal Cord: An Interpretation Based

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Bayer, S. A. and J. Altman (1987) Development of the preoptic area: Time and site of origin, migratory routes, and settling patterns of its neurons. Journal of Comparative Neurology, 265:65-95. Bayer, S. A. and J. Altman (1990) Development of layer I and the subplate in the rat neocortex. Experimental Neurology, 107:48-62. Bayer, S. A. and J. Altman (1991a) Neocortical Development. New York, NY: Raven Press. Bayer, S. A. and J. Altman (1991b) Development of the endopiriform nucleus and the claustrum in the rat brain. Neuroscience, 45:391-412. Bayer, S. A and J. Altman (1995a) Neurogenesis and neuronal migration. In: G. Paxinos (ed.) The Rat Nervous System (Second edition), pp. 1041-1078. San Diego, CA: Academic Press. Bayer, S. A and J. Altman (1995b) Principles of neurogenesis, neuronal migration, and neural circuit formation. In: G. Paxinos (ed.) The Rat Nervous System (Second edition), pp. 1079-1098. San Diego, CA: Academic Press. Bayer, S. A. and J. Altman (2002) Atlas of Human Central Nervous System Development. Volume 1: The Spinal Cord from Gestational Week 4 to the 4th Postnatal Month. Boca Raton, FL: CRC Press. th

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Bayer, S. A., J. Altman, X. Dai and L. Humphreys (1991b) Planar differences in nuclear area and orientation in the subventricular and intermediate zones of the rat embryonic neocortex. Journal of Comparative Neurology, 307:487-498.

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14

PART PARTII: II: GW11 GW11 CORONAL CORONAL This specimen is a stillborn female fetus with a crownrump length (CR) of 60 mm estimated to be at gestational week (GW) 11 (Yakovlev case number RPSL-WX-1-59, referred to here as Y1-59). The brain was cut in the coronal (frontal) plane in 35-µm thick sections and is classified as a Normative Control in the Yakovlev Collection (Haleem, 1990). Since there is no photograph of this brain before it was embedded and cut, a specimen from Hochstetter (1919) that is comparable in age to Y1-59 is used to show the approximate section plane and external features of a GW11 brain (Figure 1). Photographs of 22 Nisslstained sections (Levels 1-22) are shown at low magnification in Plates 1-21. Plates 22-35 show high-magnification views of various parts of the brain from the cerebral cortex (Plates 22-23) to the midbrain, pons, and medulla (Plates 33-35). Several high-magnification plates are rotated 90˚ (landscape orientation) to more efficiently use page space. Y1-59 has more mature brain structures in the diencephalon, midbrain, pons, and medulla than any other specimen in this Volume. Immature brain structures predominate in the telencephalon and the cerebellum. Throughout the cerebral cortex, the neuroepithelium and subventricular zone are prominent. The stratified transitional field (STF) contains mainly STF1 and STF5 throughout; with STF4 only in lateral areas and a questionable STF2 in a few areas; STF6 and STF3 are not present. The STF is filled with migrating and sojourning neurons and, unlike any specimen in Volume 3, has no regional heterogeneity. The cerebral cortex is completely smooth except for a questionable calcarine sulcus in the left cerebral hemisphere (Plate 15); “lobes” are identified as future lobes. The most prominent developmental feature of the cerebral cortex is that both the STF layers and the cortical plate have a pronounced lateral (thicker) to medial (thinner) maturation gradient. There is no corpus callosum. The olfactory bulb is beneath the anterior septum and striatum; it contains the rostral migratory stream in its core. In anterolateral parts of the cerebral cortex, streams of neurons and glia appear to leave STF4 and enter the lateral migratory stream. The hippocampus is in an immature position dorsal to the thalamus and medial to the temporal lobe. Cells are entering Ammon’s horn pyramidal layer in the ammonic migration, and granule cells and their precursors are migrating to the hilus of the presumptive dentate gyrus in the dentate migration; there is no granular layer. A massive neuroepithelium/subventricular zone overlies the amygdala, nucleus accumbens, and striatum (caudate

and putamen) where neurons (and glia) are being generated. The caudate, the putamen, and basolateral parts of the amygdala are smaller than in the GW13.5 specimen in Volume 3, but are similar to that specimen because the striatal neuroepithelium and subventricular zone have indistinct subdivisions. The strionuclear glioepithelium forms definite continuities with the fornical glioepithelium in the telencephalon. Unlike the GW13.5 specimen, the septum in Y1-59 has a neuroepithelium at the ventriclar surface instead of a glioepithelium/ependyma. The cerebellum is a thick, smooth plate overlying the posterior pons and medulla. However, there is only a thin glioepithelium/ependyma at the ventricular surface, indicating that all deep neurons and Purkinje cells have been generated. The deep neurons are in place beneath the cortex, but have indefinite nuclear subdivisions. The cortical surface is covered by an external germinal layer (egl) that is actively producing neuronal stem cells, granule, stellate, and basket cells of the cerebellar cortex. Lamination in the cortex is nearly absent, except for a thin molecular layer beneath the egl. Nearly all Purkinje cells are migrating, some in discrete clumps. Lobulation has barely begun in the vermis and is nearly absent in the hemispheres. The germinal trigone is prominent in the dorsal rhombic lip. The third ventricle, aqueduct, and fourth ventricle are lined by a thin glioepithelium/ependyma indicating that neurogenesis in the primary neuroepithelium is complete. In the medulla, there are two active germinal sites in anterior and posterior parts of the ventral rhombic lip. 1) The auditory neuroepithelium generates cochlear nucleus neurons. 2) A large precerebellar neuroepithelium generates precerebellar (mainly pontine gray) neurons. Neurons throughout the diencephalon are settling in fairly well-defined nuclear divisions; the major exceptions are the immature appearance of the lateral and medial geniculate bodies in the posterior thalamus and the hypothalamic medial mammillary body. Neurons are settled in the midbrain tegmentum, pons, and medulla. But the pontine gray is nearly absent, and neurons are still migrating into it from the large anterior extramural migratory stream. Posterior extramural and intramural migratory streams contain lateral reticular neurons, external cuneate nucleus neurons, and inferior olive neurons. The corticospinal tract forms a small cerebral peduncle in the midbrain, but has not grown into the pons.

15

GW11 CORONAL SECTION PLANES LEVEL SECTION

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 140 259 279 289 329 340 349 379 419 439 459 479 500 529 569 599 629 649 659 680 709 720

CORONAL PLANE (90˚)

Y1-59's cutting angle rotates 7˚ clockwise from the true coronal plane (90˚). The dorsal part of each section is slightly posterior to the ventral part.

E

T

MIDBRAIN

SUL

INFERIOR COLLICULUS

M

FRON

Optic nerve

E

Olfactory bulb

O

B

L

IN

CE T R

PHAL NCEHEMISPON E HER L E EL BRA

TE

A

PARIETAL LOBE

A

BE LO

EN

E BUL LO AL R T

IPITAL LOBE CC

PA RA C

HORIZONTAL PLANE (0˚)

PO

R AL

PONS

HYPOTHALAMUS

DIENCEPHALON

LO

CEREBELLUM

MEDULLA SPINAL CORD

Figure 1. The lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 68 mm (modified from Figure 47, Table VIII, Hochstetter, 1919) serves to show the approximate locations and cutting angles of the illustrated sections of Y1-59 in the following pages. The small inset identifies the major structural features. The cut beneath the cerebellum is the edge of the medullary velum.

16

PLATE 1A GW11 Coronal CR 60 mm, Y1-59 Level 1: Section 140

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

17

PLATE 1B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: NEP - Neuroepithelium SVZ - Subventricular zone

Interhemispheric fissure

FUTURE FRONTAL LOBE

Layer I Cortical plate

Cortical (frontal) NEP

anterio

halic telencep tricle superven

ntricle) teral ve (future la r pool

Cortical (frontal) SVZ

STF1 t1 STF5/4 Frontal STF

Cortical (orbitofrontal) NEP and SVZ

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

18

PLATE 2A GW11 Coronal CR 60 mm, Y1-59 Level 2: Section 259

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the frontal cortex from section 269 in Plates 22A and B.

19

PLATE 2B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (frontal) NEP and SVZ

Interhemispheric fissure

Layer I Cortical plate STF2? STF1 t1 STF5/4

Frontal STF

anterodorsal pool

FUTURE FRONTAL LOBE

Future cingulate gyrus Cortical (cingulate) NEP and SVZ

telencephalic superventricle

(future lateral ventricle)

anteroventral pool

Subpial GEP

Olfactory bulb Olfactory NEP

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Dashed lines indicate staining and/or sectioning artifacts.

n am e

TU RIA ST

Anterolateral ganglionic NEP and SVZ

Internal capsule (early corticofugal fibers?)

Put

Septal NEP

BASAL GANGLIA dat e

Corticoganglionic NEP and SVZ

C au

Cortical (orbitofrontal) NEP and SVZ

Tenia tecta

M

Accumbent NEP and SVZ Anterior commissure? olfactory recess

Rostral migratory stream

20

PLATE 3A GW11 Coronal CR 60 mm, Y1-59 Level 3: Section 279

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the frontal cortex from section 269 in Plates 22A and B.

PLATE 3B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (frontal) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate

anterodorsal pool Future cingulate gyrus

telencephalic superventricle

(future lateral ventricle) FUTURE HIPPOCAMPUS?

Septal NEP Anteromedial ganglionic NEP and SVZ

Olfactory NEP

Accumbent NEP and SVZ olfactory recess

Subpial GEP

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Dashed lines indicate staining and/or sectioning artifacts.

Fornix

Tenia tecta

anteroventral pool

SEPTUM

Lateral septal nucleus

Diagonal band of Broca (vertical limb)?

Nucleus accumbens

Olfactory tubercle

Rostral migratory stream (contributing cells to vertical limb of diagonal band and olfactory tubercle)

STRIATUM Pu tam en

Corticoganglionic NEP and SVZ

BASAL GANGLIA

Frontal STF

Telencephalic choroid plexus

dat e

Cortical (cingulate) NEP and SVZ

Cortical (hippocampal?) NEP and SVZ

Anterolateral ganglionic NEP and SVZ

STF1 t1 STF5/4

STF2?

Cingulate STF

Cau

FUTURE FRONTAL LOBE

Internal capsule (early corticofugal fibers?) Future insular gyrus

Anterior commissure?

External capsule

Future primary olfactory cortex

21

22

PLATE 4A GW11 Coronal CR 60 mm, Y1-59 Level 4: Section 289

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

PLATE 4B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (frontal) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate

Cingulate STF

anterodorsal pool

Cortical (cingulate) NEP and SVZ

Cortical (hippocampal?) NEP and SVZ

anteroventral pool

Glial migration (fornix and hippocampal commissure)

Hippocampal commissure?

Septal NEP

SEPTUM

Lateral septal nucleus

Medial septal nucleus Diagonal band of Broca (vertical limb)

Accumbent NEP and SVZ Subpial GEP

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Dashed lines indicate staining and/or sectioning artifacts.

STRIAT

UM

BASAL GANGLIA

Anteromedial ganglionic NEP and SVZ

(future lateral ventricle)

Fornix

Anterolateral ganglionic NEP and SVZ

Frontal STF

telencephalic superventricle

FUTURE HIPPOCAMPUS?

Fornical GEP

Corticoganglionic NEP and SVZ

STF1 t1 STF5/4

Telencephalic Future choroid cingulate plexus gyrus

Cau dat Int e ern al ca Pu tam psul e en

FUTURE FRONTAL LOBE

ac Nu cu cle m us be ns Olfactory tubercle

Anterior commissure?

Future insular gyrus Internal capsule (early corticofugal fibers?) External capsule Endopiriform nucleus (infiltrated by lateral migratory stream) Future primary olfactory cortex Lateral olfactory tract

Lateral migratory stream

23

24

PLATE 5A GW11 Coronal CR 60 mm, Y1-59 Level 5: Section 329

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

PLATE 5B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (frontal) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate

Cingulate STF

anterodorsal pool Future cingulate gyrus Telencephalic choroid plexus

Cortical (cingulate) NEP and SVZ Cortical (hippocampal) NEP and SVZ

FUTURE HIPPOCAMPUS

Ammonic migration Dentate migration Fornical GEP

Accumbent NEP and SVZ

SEPTUM Medial septal nucleus

Anterior commissure

inata tia innom Substan

Subpial GEP

Medial forebrain bundle

Preoptic G/EP

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Dashed lines indicate staining and/or sectioning artifacts.

Diagonal band of Broca (vertical limb) Preoptic area

en m

te

STRIATUM

ac Nu cu cle m us be ns

ta

Septal NEP

Internal capsule (early corticofugal fibers?)

Pu

Hippocampal commissure? L a te r nucall septa eu s l

Anteromedial ganglionic NEP and SVZ

Fornix

BASAL GANGLIA

Lateral migratory stream?

(future lateral ventricle)

anteroventral pool Diencephalic choroid plexus

Anterolateral ganglionic NEP and SVZ

Frontal STF

telencephalic superventricle

In

Corticoganglionic NEP and SVZ

STF1 t1 STF4? STF5/4

Ca ud at rn e al ca ps ul e

FUTURE FRONTAL LOBE

External capsule Future insular gyrus Claustrum Lateral migratory stream Endopiriform nucleus Lateral olfactory tract Future primary olfactory cortex

25

26

PLATE 6A GW11 Coronal CR 60 mm, Y1-59 Level 6: Section 340

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

PLATE 6B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (frontal) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate

FUTURE FRONTAL LOBE

Cingulate STF

dorsal pool

Cortical (cingulate) NEP and SVZ

STF1 t1 STF4? STF5/4

Future cingulate gyrus

Telencephalic choroid plexus

Cortical (hippocampal) NEP and SVZ Ammonic migration Dentate migration Fornical GEP

Corticoganglionic NEP and SVZ

Frontal STF

telencephalic superventricle

Lateral migratory stream?

(future lateral ventricle) Diencephalic HIPPOCAMPUS choroid plexus ventral

pool

Fornix

Strionuclear NEP Subpial GEP

Preoptic G/EP

third ventricle

Lateral preoptic area Medial preoptic area

en

inata nom tia in n a t s Sub

Medial forebrain bundle

Optic nerve GEP Nerve II (optic)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Dashed lines indicate staining and/or sectioning artifacts.

External capsule Claustrum

Bed nucleus of the stria terminalis

issure

PREOPTIC AREA

m

Pu

STRIATUM Anterior comm

Endopiriform nucleus

Ca ud ter at na e lc ap su le

foramen of monro

Future insular gyrus

ta

BASAL GANGLIA

Choroid plexus stem cells

In

s ow rr na

Anteromedial ganglionic NEP and SVZ

Fornix

al iat str

Anterolateral ganglionic NEP and SVZ

Early corticofugal fibers?

Lateral migratory stream Lateral olfactory tract Future primary olfactory cortex

27

28

PLATE 7A GW11 Coronal CR 60 mm, Y1-59 Level 7: Section 349

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

PLATE 7B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (frontal) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate

FUTURE FRONTAL LOBE

Cingulate STF Cortical (cingulate) NEP and SVZ

dorsal pool Future cingulate gyrus

Telencephalic choroid plexus

Cortical (hippocampal) NEP and SVZ

Frontal STF

telencephalic superventricle

(future lateral ventricle)

Ammonic migration Dentate migration

Diencephalic choroid plexus

Fornical GEP

Future Ammon's horn

Lateral migratory stream?

ventral pool

HIPPOCAMPUS

st

Fornix

Corticoganglionic NEP and SVZ

STF1 t1 STF4? STF5/4

r ia ar

STRIATUM

en

ws

foramen of monro

Bed nucleus of the stria terminalis

Fornix

Strionuclear NEP

Lateral preoptic area

PREOPTIC AREA

Endopiriform nucleus Subpial GEP

Preoptic G/EP

Medial preoptic area

Suprachiasmatic G/EP?

Pu

ta

Anteromedial ganglionic NEP and SVZ

Choroid plexus stem cells

m

ro

BASAL GANGLIA

In

ln

Anterolateral ganglionic NEP and SVZ

Ca ud te at rn e al ca ps ul e

ta

Early corticofugal fibers?

Anterior commissure

Substantia innominata

Nerve II (optic) preoptic recess

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Dashed lines indicate staining and/or sectioning artifacts.

External capsule Claustrum Lateral migratory stream Future primary olfactory cortex

Lateral olfactory tract Medial forebrain bundle Suprachiasmatic nucleus?

Optic (nerve and chiasm) GEP

optic recess

Future insular gyrus

third ventricle

29

30

PLATE 8A GW11 Coronal CR 60 mm, Y1-59 Level 8: Section 379

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See high-magnification views of the right paracentral cortex, thalamus, and basal ganglia from section 399 in Plates 24A and B to 25A and B. See a high-magnification view of the diencephalon and basal telencephalon from section 389 in Plates 26A and B.

PLATE 8B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

PA F R RO TRACE NT AN NT AL SI RA LO TI L B O N LO E/ AR BU EA LE

Cortical (frontal/paracentral) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate dorsal pool

Cingulate STF

STF1 t1 STF4? STF5

Future cingulate gyrus

Cortical (cingulate) NEP and SVZ

Telencephalic choroid plexus

telencephalic superventricle

Cortical (hippocampal) NEP and SVZ Ammonic and dentate migrations

Frontal/ paracentral STF

(future lateral ventricle)

Future Ammon's horn

Diencephalic choroid plexus

Fornical GEP Corticoganglionic NEP and SVZ

Lateral migratory stream?

Choroid plexus stem cells

HIPPOCAMPUS

ix rn Fo

Claustrum

R

et

Stria terminalis

i cu

Thalamic G/EP n

la r

ucle

us

Bed nucleus of the stria terminalis Subthalamic G/EP SUBTHALAMUS

BASAL GANGLIA

Endopiriform nucleus

Subpial GEP

Medial forebrain bundle

Forel's fields Paraventricular nucleus

e

l ca rly rti Ea oco s? m er ala ib th f

Optic chiasm GEP

External capsule Putamen

Lateral migratory stream Future primary olfactory cortex

Suprachiasmatic nucleus?

Optic chiasm

Future insular gyrus

Putamen

Globus Sub pallidus stan Anterior t i a Lateral inn commissure om hypothalamic ina ta area Basal nucleus of Meynert

Supraoptic nucleus Suprachiasmatic G/EP?

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

STRIATUM

l na t e r le In ap su c

Anterior nucleus?

(lateral olfactory tract)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

at

Periventricular complex

HYPOTHALAMUS

Hypothalamic G/EP

Early corticofugal fibers?

ud

third ventricle

Anterior complex

Anteromedial ganglionic NEP and SVZ Strionuclear GEP

Stria medullaris

THALAMUS

Ca

Anterolateral ganglionic NEP and SVZ

Lateral olfactory tract

31

32

PLATE 9A GW11 Coronal CR 60 mm, Y1-59 Level 9: Section 419

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the diencephalon and basal telencephalon from level 9 in Plates 27A and B.

PLATE 9B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (paracentral) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate dorsal pool

Cingulate STF

STF2?

Telencephalic choroid plexus

telencephalic superventricle

Cortical (hippocampal) NEP and SVZ Ammonic and dentate migrations

Future Ammon's horn

rs al m pl ex

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Dashed lines indicate staining and/or sectioning artifacts.

TH HYP AL OAM US

a ert na Zo

External capsule

en

Perifascicular GEP

Future insular gyrus

tam

Hypothalamic G/EP

Dorsomedial nucleus

l ra reb cle Ce dun pe

Lateral tuberal nucleus? Ventromedial nucleus Arcuate nucleus

le x

p

Endipiriform nucleus

ct

Globus pallidus

om

AMYGDALA

tr a

Forel's fields

ate

l ra nt um Ve iat str l ra al nt us er C e u c le la t x s o p le n B a com

Subpial GEP

Medial forebrain bundle

Internal capsule

r ti c o medial c

tic

Ventral complex

Co

Op

C aud

Pu

SUBTHALAMUS

Subthalamic G/EP

Early thalamocortical fibers?

Stria medullaris

Periventricular complex

third ventricle

Thalamic G/EP

Lateral migratory stream?

UM IAT STR

BASAL GANGLIA

co

s cleu R e t i cu l a r n u

Stria terminalis

Central complex

Dorsomedial nucleus

Choroid plexus stem cells

nix For

Dorsolateral nucleus

Do

THALAMUS

Strionuclear GEP

FUTURE TEMPORAL LOBE

HIPPOCAMPUS

Diencephalic choroid plexus

Posterior ganglionic NEP and SVZ

Paracentral STF

(future lateral ventricle)

Fornical GEP

Corticoganglionic NEP and SVZ

STF1 t1 STF4? STF5/4

Future cingulate gyrus

Cortical (cingulate) NEP and SVZ

in c

FUTURE PARACENTRAL LOBULE

Median eminence/ posterior pituitary gland (neurohypophysis) Anterior pituitary gland (adenohypophysis, distal part)

Lateral migratory stream? Future primary olfactory cortex Lateral olfactory tract

33

34

PLATE 10A GW11 Coronal CR 60 mm, Y1-59 Level 10: Section 439

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the diencephalon from section 449 in Plates 28A and B.

35

PLATE 10B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (paracentral) NEP and SVZ

Interhemispheric fissure

dorsal pool

Cingulate STF

Future cingulate gyrus

Cortical (cingulate) NEP and SVZ

STF2?

telencephalic superventricle

Cortical (hippocampal) NEP and SVZ

al co m ex

Mammillothalamic tract

Thalamic G/EP

Internal capsule

Periventricular complex

ate Caud

Ventral complex

t ic tr a

Premammillary area

Lateral tuberal nucleus Arcuate nucleus

Pu

ta

C nu ent cle ra us l

Basolateral complex

m

en

Early thalamocortical fibers?

Temporal STF

Anterior commissure

pl x

e

Hypothalamic G/EP

HYPOTHALAMUS

m e d i al co m

ct

Medial forebrain bundle

Co rti co

Op

SUBForel's fields THALAMUS

Trigeminal ganglion (V)

Nerve V (trigeminal proximal branch)

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

External capsule

third ventricle

Subthalamic G/EP

Perifascicular GEP Subpial GEP

THALAMUS

Medial lemniscus?

AMYGDALA

Lateral migratory stream?

Medial habenular Lateral nucleus geniculatebody Stria Dorsomedial medullaris nucleus

Ce re br Z al pe ona du nc ince le rt a

Central complex

Dorsolateral nucleus

Choroid plexus stem cells

UM IAT STR

Stria terminalis

pl

Strionuclear GEP BASAL GANGLIA

FUTURE TEMPORAL LOBE

rs Reticular nucleus

Posterior ganglionic NEP and SVZ

HIPPOCAMPUS

Epithalamic G/EP

ix rn Fo

Dentate migration r r io x s t e le Po omp c

Future Ammon's horn

Diencephalic choroid plexus

Do

Corticoganglionic NEP and SVZ

Paracentral STF

(future lateral ventricle)

Ammonic migration Fornical GEP

STF1 t1 STF4? STF5/4

Telencephalic choroid plexus

Str term ia inalis

FUTURE PARACENTRAL LOBULE

Layer I Cortical plate

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Future temporal cortex Future entorhinal cortex Lateral olfactory tract

Dashed lines indicate staining and/or sectioning artifacts.

36

PLATE 11A GW11 Coronal CR 60 mm, Y1-59 Level 11: Section 459

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the diencephalon from section 449 in Plates 28A and B, from section 469 in Plates 29A and B.

PLATE 11B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (paracentral) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate dorsal pool Future cingulate gyrus

Cingulate FUTURE STF PARACENTRAL LOBULE Cortical (cingulate)

STF2?

NEP and SVZ

Stria medullaris

Epithalamic

Pulvinar Medial habenular nucleus

a ct

na Zo rta

e SUBinc THALAMUS c i m

a la s b t h le u Su nuc al p VENTRAL HIPPObr C e re CAMPUS

Fornix

HYPOTHALAMUS Mammillary body

Mammillothalamic tract

Lateral tuberal nucleus?

ventral pool Future parahippocampal gyrus

third ventricle (mammillary recess)

Nerve V (trigeminal distal branch)

Subpial GEP

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Future temporal cortex

un

Hypothalamic G/EP Medial forebrain bundle

Amygdaloid NEP and SVZ

Ventral complex

ed

NEP and SVZ

Forel's fields

Subthalamic G/EP

Cortical

(ventral hippocampal)

third ventricle Centromedian nucleus

Ventral medial nucleus

Ventral lateral geniculate body

O

Ventral lateral nucleus

Central complex

Periventricular complex

c le

Ret nucicular leu s

Po st

FUTURE TEMPORAL LOBE

Thalamic G/EP

Ventral anterior nucleus

l era d y L a t a te b o l icu

Dorsomedial nucleus

c tr

plex com r io er THALAMUS Dorsal complex

Choroid plexus stem cells

gen

Posterior ganglionic NEP and SVZ

DORSAL HIPPOCAMPUS

G/EP

n ix For

Corticoganglionic NEP and SVZ

Future Ammon's horn

p ti

NEP and SVZ

Fornical GEP

(future lateral ventricle)

Diencephalic choroid plexus

(dorsal hippocampal)

Dentate migration

Paracentral STF

telencephalic superventricle

Telencephalic choroid plexus Cortical

Ammonic migration

STF1 t1 STF5/4

Cortical (parahippocampal) NEP

Trigeminal ganglion (V) Nerve V (trigeminal proximal branch)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Future entorhinal cortex

STF1 t1 STF5/4 Temporal STF

Dashed lines indicate staining and/or sectioning artifacts.

37

38

PLATE 12A GW11 Coronal CR 60 mm, Y1-59 Level 12: Section 479

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the diencephalon from section 469 in Plates 29A and B.

39

PLATE 12B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (paracentral) NEP and SVZ

Interhemispheric fissure

dorsal pool

Cingulate STF Cortical (cingulate) NEP and SVZ

Epithalamic G/EP

NEP and SVZ

rio rc

Centromedian nucleus

Ventral complex a

e

t

bs

Su

Cortical

(ventral hippocampal)

NEP and SVZ

Future temporal cortex

pt

ic

a Forel's SUBTHALAMUS ince r t i g r O n Zona fields tia Medial foren a brain bundle ed MIDBRAIN Ventral lp TEGMENTUM tegmental area ra b e Cer Interpeduncular nucleus

Subthalamic G/EP

cl

Pos te ular nuc l eus

ic Ret

Ventral medial nucleus

THALAMUS third ventricle

alic ceph cle elen

FUTURE TEMPORAL LOBE

Ventral lateral nucleus

Central complex

Periventricular complex

t tri ricle) rven t supe ateral ven re l (futu

Posterior ganglionic NEP and SVZ

Ventral anterior nucleus

Choroid plexus stem cells

Fornix

Fornical GEP

Pulvinar

Lateral habenular nucleus Dorsomedial Medial habenular nucleus nucleus

al Later body ulate genic

Dentate migration

I- US EP AM AL TH

x ple om Dorsal complex Thalamic G/EP

Ammonic migration

DORSAL HIPPOCAMPUS

ct

Cortical

Paracentral/ parietal STF

Future Ammon's horn

Stria medullaris

tr a

Diencephalic choroid plexus

Subicular migration (dorsal hippocampal)

STF1 t1 STF5/4

Future cingulate gyrus Telencephalic choroid STF2? plexus

un

FUTURE PARACENTRAL/ PARIETAL LOBULE

Layer I Cortical plate

VENTRAL HIPPOCAMPUS

ventral pool

Subpial GEP Cortical (parahippocampal) NEP and SVZ Parahippocampal STF Cortical (temporal) NEP and SVZ

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Nerve V (trigeminal distal branch)

STF5/4 STF1 t1

Trigeminal ganglion

Temporal STF

Dashed lines indicate staining and/or sectioning artifacts.

40

PLATE 13A GW11 Coronal CR 60 mm, Y1-59 Level 13: Section 500

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the midbrain and thalamus from section 499 in Plates 30A and B.

41

PLATE 13B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (parietal) NEP and SVZ

Interhemispheric fissure Layer I Cortical plate dorsal pool

FUTURE PARIETAL LOBE

Future cingulate gyrus

Cortical (cingulate) NEP and SVZ

Diencephalic choroid plexus

Subpial GEP

Ventral tegmental area?

C

b ere

ra

le a

r

Optic tract

nc

tia

g ni

du

an

t

Interpeduncular nucleus? Red nucleus bs

rio rc s

Pos te r nucleu

icula

Ret

MIDBRAIN TEGMENTUM

Ventral complex

alic ceph cle elen

Mesencephalic G/EP

Central complex

US

Ventral posteromedial nucleus

THALAMUS Periventricular complex

CAM P

Centromedian nucleus

Medial habenular nucleus

Fimbri a/fornix

Ventral posterolateral nucleus

Thalamic G/EP

Lateral habenular nucleus Pulvinar

H IP P O

FUTURE TEMPORAL LOBE

third ventricle

Ventral lateral nucleus

Future Ammon's horn

al Later body ulate genic

Dentate migration

tract

Stria medullaris

t tri ricle) rven t supe ateral ven re l (futu

I- US EP AM AL TH

x ple Habenuloom interpeduncular

Telencephalic choroid plexus

Su

Epithalamic G/EP

Subicular migration

Cortical (hippocampal) NEP and SVZ

Parietal STF

STF2? Cingulate STF

Ammonic migration

STF1 t1 STF5/4

Future temporal cortex

Future Ammon's horn ventral pool

e lp

aqueduct Parahippocampal STF

Cortical (parahippocampal) NEP and SVZ Cortical (temporal) NEP and SVZ

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Temporal STF STF5/4 STF1 t1

Dashed lines indicate staining and/or sectioning artifacts.

42

PLATE 14A GW11 Coronal CR 60 mm, Y1-59 Level 14: Section 529

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the parietal cortex from section 519 in Plates 23A and B, and of the thalamus and midbrain from this section in Plates 31A and B.

43

PLATE 14B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Cortical (parietal) NEP and SVZ

Interhemispheric fissure

Layer I Cortical plate STF2? STF1 t1 STF5/4

dorsal pool

FUTURE PARIETAL LOBE

Parietal STF

Telencephalic choroid plexus Future cingulate gyrus

Posterior commissure

FUTURE TEMPORAL LOBE

ody

i c u l a te b ge n al

Red nucleus

L

ventral pool

ni tia tan e s b lp Su ra eb Cer

du

Subpial GEP

Cortical (parahippocampal) NEP and SVZ

Parahippocampal STF

Ponti n gray e

PONS

Temporal STF

Dashed lines indicate staining and/or sectioning artifacts.

STF5/4 STF1 t1

Anterior extramural migratory stream (pontine gray and pontine reticular neurons)

Pontocerebellar fibers (decussation)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Future temporal cortex

er

Oculomotor nuclear complex (III)

nucleus

Cortical (temporal) NEP and SVZ

Medial geniculate body

Central gray

MIDBRAIN InterTEGMENTUMpeduncular

Perifascicular GEP (lines fiber tracts)

Pulvinar

aqueduct

at

Mesencephalic G/EP

THALAMUS

gr nc a le

rio rc

Pos te

Medial geniculate body

Pretectal G/EP

b ic

Pulvinar

Su

x ple om

Subcommissural organ

lic ha cle le) i ep c nc ntr entri le te rve l v a pe er su lat m u lu

Diencephalic choroid plexus

EPR TUM C TE

Subicular migration Cortical (subiculum) NEP and SVZ

re tu (fu

Cortical (cingulate) NEP and SVZ Cingulate STF

44

PLATE 15A GW11 Coronal CR 60 mm, Y1-59 Level 15: Section 569

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the midbrain and pons from section 549 in Plates 32A and B, and from this section in Plates 33A and B.

45

PLATE 15B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Layer I Cortical plate Cortical (parietal) NEP and SVZ

Interhemispheric fissure

FUTURE PARIETAL LOBE

telencephalic superventricle

STF1 t1 STF2? STF5

Parietal STF

(future lateral ventricle)

Telencephalic choroid plexus Cortical (occipital) NEP and SVZ

FUTURE TEMPORAL LOBE

FUTURE OCCIPITAL LOBE

Cortical (temporal) NEP and SVZ

Subpial GEP

posterior pool Calcarine sulcus? Posterior commissure

SUPERIOR COLLICULUS Central gray

Subcommissural organ

MIDBRAIN TECTUM

Occipital STF

aqueduct

Mesencephalic G/EP Reticular formation

MIDBRAIN TEGMENTUM

Oculomotor nuclear complex (III)

Temporal STF

Superior cerebellar peduncle (decussation)

Reticular formation

PONS

Lateral lemniscus

Nucleus of the lateral lemniscus (ventral)

Raphe dorsalis

Middle cerebellar peduncle Raphe nuclear complex

Anterior extramural migratory stream (pontine gray and

pontine reticular neurons) Pontine gray

Posterior intramural migratory stream (inferior olive neurons)

Medial lemniscus and trapezoid body

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Dashed lines indicate staining and/or sectioning artifacts.

STF5/4 STF2? STF1 t1

Raphe migration?

46

PLATE 16A GW11 Coronal CR 60 mm, Y1-59 Level 16: Section 599

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

See a high-magnification view of the midbrain and pons from section 589 in Plates 34A and B and from this section in Plates 35A and B.

PLATE 16B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Layer I Cortical plate Interhemispheric fissure Cortical (parietal) NEP and SVZ

STF1 t1 STF5/4 FUTURE PARIETAL LOBE

Parietal STF

telencephalic superventricle

(future lateral ventricle)

posterior pool

Cortical (occipital) NEP and SVZ

FUTURE OCCIPITAL LOBE

FUTURE TEMPORAL LOBE

Calcarine sulcus? Posterior commissure

SUPERIOR COLLICULUS Central gray

Subpial GEP

Mesencephalic G/EP

Dorsal rhombic lip (cerebellar germinal trigone)

Reticular formation

Cerebellar G/EP

Ventral rhombic lip

Raphe nuclear complex

Pontine G/EP

Dashed lines indicate staining and/or sectioning artifacts.

aqueduct Temporal STF

STF5/4 STF1 t1

Trigeminal motor nucleus (V)

PONS Raphe nuclear complex

Lateral lemniscus Migrating and settling hemispheric Purkinje cells

Medial longitudinal fasciculus

Reticular formation

MEDULLA

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Subcommissural organ

Parabigeminal nuclei

MIDBRAIN TEGMENTUM External germinal layer

Occipital STF

MIDBRAIN TECTUM

Facial motor nucleus (VII)

(V) P r i n cipal sensory n cleus u

Cortical (temporal) NEP and SVZ

Superior, middle and inferior cerebellar peduncles

CEREBELLUM (HEMISPHERE)

fourth ventricle (lateral recess)

Anterior extramural migratory stream (pontine gray and pontine reticular neurons)

Inferior olivary complex Medial lemniscus Raphe migration?

Posterior intramural migratory stream (inferior olive neurons)

47

48

PLATE 17A GW11 Coronal CR 60 mm, Y1-59 Level 17: Section 629

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

49

PLATE 17B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Layer I Cortical plate

Interhemispheric fissure

Cortical (occipital) NEP and SVZ

telencephalic superventricle

(future lateral ventricle)

posterior pool

FUTURE OCCIPITAL LOBE

STF1 t1 STF5/4

Posterior commissure SUPERIOR COLLICULUS

Subpial GEP

Occipital STF

MIDBRAIN TECTUM Subcommissural organ

Mesencephalic G/EP Nucleus of the lateral lemniscus (dorsal)

Central nucleus

INFERIOR COLLICULUS

aqueduct

Lateral lemniscus

ISTHMUS Mesencephalic nucleus (V)

External germinal layer

Mesencephalic nucleus (V)

Dorsal rhombic lip

(cerebellar germinal trigone)

isthmal canal

Isthmal G/EP Cerebellar G/EP

Ventral rhombic lip

rhombencephalic superventricle

(future fourth ventricle) Vestibular nuclear s ositu complex Prep cleus nu

Medullary G/EP

Inferior cerebellar peduncle Spinal tract (V) Spinal nucleus (V)

Reticular formation

MEDULLA

Spinocerebellar tracts?

Medial lemniscus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

e dl id e s m ncl nd du r a pe r io la r pe el Su ereb c

Locus coeruleus?

Central gray

Solitary nucleus? Raphe nuclear complex

Inferior olivary complex

Dentate nucleus

Migrating and settling hemispheric Purkinje cells

CEREBELLUM (HEMISPHERE)

Rhombencephalic choroid plexus fourth ventricle (lateral recess)

Anterior extramural migratory stream (pontine gray and pontine reticular neurons)

Posterior intramural migratory stream (inferior olive neurons)

Posterior extramural migratory stream

(lateral reticular and external cuneate neurons cross midline)

Dashed lines indicate staining and/or sectioning artifacts.

50

PLATE 18A GW11 Coronal CR 60 mm, Y1-59 Level 18: Section 649

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

51

PLATE 18B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Layer I Cortical plate Interhemispheric fissure FUTURE OCCIPITAL LOBE

Cortical (occipital) NEP and SVZ

telencephalic superventricle

(future lateral ventricle)

posterior pool

STF1 t1 STF5/4 Occipital STF

MIDBRAIN TECTUM

Subpial GEP SUPERIOR COLLICULUS

Subcommissural organ

aqueduct Central gray

Mesencephalic G/EP INFERIOR COLLICULUS

Nucleus of the lateral lemniscus (dorsal) Isthmal NEP

External germinal layer

isthmal canal

ISTHMUS

Hypoglossal nucleus (XII)

MEDULLA

Lateral reticular nucleus Medial lemniscus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Dashed lines indicate staining and/or sectioning artifacts.

Solitary nucleus and tract

fourth ventricle (lateral recess)

Anterior extramural migratory stream (pontine gray and

Reticular formation

Spinal tract (V)

Spinocerebellar tracts?

Rhombencephalic choroid plexus

D nu orsa cle l s us en D (X sor nu orsa ) y cle l m us o (X tor )

Inferior cerebellar peduncle

Spinal nucleus (V)

CEREBELLUM (HEMISPHERE)

(future fourth ventricle)

Medullary G/EP Vestibular nuclear complex

Interpositus nucleus

ta te D e n le u s nuc

Fastigial nucleus?

rhombencephalic superventricle

Cerebellar G/EP

Ventral rhombic lip

Migrating and settling hemispheric Purkinje cells

Trochlear nucleus (IV)

Isthmal G/EP Dorsal rhombic lip (cerebellar germinal trigone)

Lateral lemniscus

Central nucleus

Raphe nuclear complex

Inferior olivary complex

pontine reticular neurons)

Posterior intramural migratory stream (inferior olive neurons)

Posterior extramural migratory stream (lateral reticular and external cuneate neurons cross midline)

52

PLATE 19A GW11 Coronal CR 60 mm, Y1-59 Level 19: Section 659

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons.

STF2 Upper cellular layer, the most superficial sojourn zone where cells translocate to the cortical plate.

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

STF3 Honeycomb trilaminar matrix (3a, 3b, 3c) of cells and fibers that is not present during the first trimester and is found in granular (sensory) cortices.

STF6 Late-forming deep layer of callosal fibers outside the germinal matrix that is not present during the first trimester.

53

PLATE 19B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

telencephalic superventricle

(future lateral ventricle, posterior pool)

Interhemispheric fissure Layer I Cortical plate

STF1 t1 STF5/4

FUTURE OCCIPITAL LOBE

Cortical (occipital) NEP and SVZ

Subpial GEP

Central gray

Subcommissural organ

aqueduct

Mesencephalic G/EP

Central nucleus

INFERIOR COLLICULUS

Inferior colliculus NEP Isthmal NEP

External germinal layer

isthmal canal

ISTHMUS

Nucleus of the lateral lemniscus (dorsal) Lateral lemniscus Migrating and settling hemispheric Purkinje cells ta te D e n le u s nuc

Interpositus nucleus

CEREBELLUM (FUSING VERMIS)

Cerebellar G/EP

Occipital STF

MIDBRAIN TECTUM

SUPERIOR COLLICULUS

Dorsal rhombic lip (cerebellar germinal trigone)

STF1 t1 STF5/4

CEREBELLUM (HEMISPHERE)

rhombencephalic superventricle

(future fourth ventricle)

Rhombencephalic choroid plexus

Anterior precerebellar NEP (source of pontine gray neurons)

Ventral rhombic lip

fourth ventricle

(lateral recess) Vestibular nuclear complex

Medullary G/EP

Solitary nucleus and tract

Anterior extramural migratory stream (pontine gray and pontine reticular neurons)

Hypoglossal nucleus (XII)

Spinal nucleus (V) Spinocerebellar tracts?

MEDULLA

Dorsal motor nucleus (X) Reticular formation

Raphe nuclear complex

Posterior intramural migratory stream (inferior olive neurons) Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

SPINAL CORD Ventral gray

Dashed lines indicate staining and/or sectioning artifacts.

54

PLATE 20A GW11 Coronal CR 60 mm, Y1-59 Level 20: Section 680

55

PLATE 20B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: G/EP - Glioepithelium/ependyma NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. MIDBRAIN TECTUM SUPERIOR COLLICULUS

INFERIOR COLLICULUS

External germinal layer

aqueduct

Central gray

Mesencephalic G/EP Inferior colliculus NEP

Central nucleus

Migrating and settling Purkinje cells

Isthmal NEP

Dorsal rhombic lip (cerebellar germinal trigone)

CEREBELLUM (VERMIS)

Migrating Purkinje cells

CEREBELLUM (HEMISPHERE)

Cerebellar G/EP rhombencephalic superventricle

Rhombencephalic choroid plexus

(future fourth ventricle)

Ventral rhombic lip

fourth ventricle

Anterior precerebellar NEP (source of pontine gray neurons)

(lateral recess)

Posterior precerebellar NEP (source of lateral reticular and external cuneate neurons)

Medullary G/EP

Solitary nucleus?

Reticular formation

Spinocerebellar tracts?

MEDULLA

SPINAL CORD Dorsal gray

Spinal nucleus (V)

Raphe nuclear complex

56

PLATE 21A GW11 Coronal CR 60 mm, Y1-59

Level 21: Section 709

Level 22: Section 720

57

PLATE 21B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Gioepithelium/ependyma - G/EP

Level 21: Section 709

Discrete groups of migrating and settling Purkinje cells

External germinal layer Primitive molecular layer

E

F

Migrating and settling Purkinje cells

CEREBELLUM (VERMIS)

DC B A

Migrating Purkinje cells

Dorsal rhombic lip (with cerebellar germinal trigone)

V

A B

CEREBELLUM (HEMISPHERE)

1. External germinal layer

rhombencephalic superventricle

2. Cerebellar G/EP

(future fourth ventricle)

3. Choroid plexus stem cells Rhombencephalic choroid plexus

Discrete groups of migrating and settling Purkinje cells

Level 22: Section 720 External germinal layer

Migrating and settling Purkinje cells

Circumferential cerebellar germinal trigone

H

E GC F

CEREBELLUM (VERMIS)

D B

A

D A C B F

CEREBELLUM (HEMISPHERE)

E

H G

Cerebellar germinal trigone

(in dorsal rhombic lip) 1. External germinal layer 2. Cerebellar G/EP

rhombencephalic superventricle

3. Choroid plexus stem cells

(future fourth ventricle)

Rhombencephalic choroid plexus Cerebellar G/EP

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Cerebellar germinal trigone

(in dorsal rhombic lip)

Cerebellar G/EP

Primitive molecular layer

F

E C D

58

PLATE 22A

See level 2 in Plates 2A and B, level 3 in Plates 3A and B.

GW11 Coronal CR 60 mm, Y1-59 Between levels 2 and 3: Section 269 FRONTAL CORTEX

PLATE 22B FRONTAL CORTEX

Layer I

Frontal stratified transitional field (STF)

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Cortical plate

Cajal-Retzius cells

STF1 t1 STF2? STF5/4

Cortical (frontal) neuroepithelium (NEP) Cortical (frontal) subventricular zone (SVZ) Although this part of the cerebral cortex will be an agranular (motor) area where layer IV is indistinct, the stratified transitional field does not show any differences from the parietal cortex (granular, somatosensory) in Section 519 (see Plates 23A and B). Thus, at the end of the first trimester, motor and sensory areas are indistinguishable. This is in sharp contrast to the differences observed in the second (Volume 3) and third (Volume 2) trimesters. That difference indicates that at GW11 the superficial cortical layers (II, III, and IV) have either not yet been generated or are still sequestered in the cortical neuroepithelium and subventricular zone.

telencephalic superventricle (future lateral ventricle)

anterodorsal pool

59

60

PLATE 23A

See level 14 in Plates 14A and B.

GW11 Coronal CR 60 mm, Y1-59 Near level 14: Section 519 PARIETAL CORTEX

PLATE 23B PARIETAL CORTEX

Layer I

Cajal-Retzius cells

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Cortical plate

Parietal stratified transitional field (STF)

STF1 t1

STF5/4

Cortical (parietal) neuroepithelium (NEP)

Cortical (parietal) subventricular zone (SVZ)

Although this part of the cerebral cortex will be a granular (somatosensory) area where layer IV is prominent, the stratified transitional field does not show any differences from the frontal cortex (agranular, motor) in Section 269 (see Plates 22A and B). Thus, at the end of the first trimester, motor and sensory areas are indistinguishable. This is in sharp contrast to the differences observed in the second (Volume 3) and third (Volume 2) trimesters. That difference indicates that at GW11 the superficial cortical layers (II, III, and IV) have either not yet been generated or are still sequestered in the cortical neuroepithelium and subventricular zone.

telencephalic superventricle (future lateral ventricle)

dorsal pool

61

62

PLATE 24A

GW11 Coronal CR 60 mm, Y1-59 Between levels 8 and 9: Section 399 PARACENTRAL CORTEX See levels 8 and 9 in Plates 8 to 9A and B. Enlarged in Plates 25A and B.

63 Interhemispheric fissure

PLATE 24B

Cortical (paracentral) neuroepithelium (NEP) and subventricular zone (SVZ)

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

FUTURE PARACENTRAL LOBULE

dorsal pool

Layer I Cortical plate Layer VII (subplate) STF1 t1 STF4? STF5/4

Cingulate STF

Telencephalic choroid plexus

STF2? Future cingulate gyrus

Subpial glioepithelium

Presumed direction of neuron migration from neuroepithelial sources.

Cortical (cingulate) NEP and SVZ

Presumed direction of axon growth in brain fiber tracts.

telencephalic superventricle

(future lateral ventricle)

Cortical (hippocampal) NEP and SVZ

HIPPOCAMPUS

Ammonicmigration

Future Ammon's horn Diencephalic choroid plexus

Dentate migration

Ve nt r nu al a c l nt e u er s io r

x

ple com Periventricular

ti

SUBTHALAMUS Forel's fields

Dorsomedial nucleus

HYPOTHALAMUS

c

eu

Thalamocortical fibers funnel into cortex via the internal capsule

ter na lc ap su le

r

a ul

u Ca

da

te

Stria terminalis

cl nu

Ventral complex

Strionuclear glioepithelium

s

THALAMUS

Posterior ganglionic NEP and SVZ Lateral migratory stream percolates through STF4

In

Thalamic glioepithelium/ ependyma (G/EP)

Dorsomedial nucleus

Re Subthalamic G/EP

third ventricle

Hypothalamic G/EP

ex

pl

om Dorsolateral nucleus

lc

Do

Choroid plexus stem cells

nix For

Stria medullaris

Pioneer corticofugal fibers enter internal capsule in STF4

Corticoganglionic NEP and SVZ

Fornical glioepithelium

a rs

Paracentral stratified transitional field (STF)

Putamen Pioneer corticofugal fibers

Future insular gyrus

BASAL GANGLIA

s du i l l pa External s segment u ob l G

Lateral migratory stream infiltrates external capsule?

Internal segment

Ventral striatum

Putamen

FUTURE TEMPORAL LOBE External capsule

64

PLATE 25A GW11 Coronal CR 60 mm, Y1-59 Between levels 8 and 9: Section 399 ENTRY/EXIT ZONE IN LATERAL PARACENTRAL CORTEX

See levels 8 and 9 in Plates 8 to 9A and B.

65

PLATE 25B

FUTURE PARACENTRAL LOBULE

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Arrows indicate the Cortical (paracentral) presumed direction of neuroepithelium (NEP) and neuron migration from neuroepithelial sources. subventricular zone (SVZ)

Layer I Cortical plate (dense superficial part) Cortical plate (less dense deep part)

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

STF1 t1 STF4 STF5/4

telencephalic superventricle

Cajal-Retzius cells

(future lateral ventricle)

dorsal pool

Paracentral stratified transitional field (STF)

Corticoganglionic NEP and SVZ

Pioneer corticofugal fibers enter internal capsule in STF4

Posterior ganglionic NEP and SVZ

Lateral migratory stream percolates through STF4

Strionuclear glioepithelium

C

d au

a te

Future insular gyrus

Stria terminalis

Pioneer corticofugal fibers

Thalamocortical fibers funnel into cortex STF4 via the internal capsule

Subpial granular layer (glioepithelium)

Internal capsule

Putamen

Cajal-Retzius cells

Globus pallidus External segment

Putamen

BASAL GANGLIA

Lateral migratory stream infiltrates external capsule?

External capsule

66

PLATE 26A GW11 Coronal, CR 60 mm, Y1-59, Near level 8: Section 389

See level 8 in Plates 8A and B.

DIENCEPHALON, BASAL GANGLIA, and BASAL TELENCEPHALON

PLATE 26B

Dentate migration Corticostriatal Fornical glioepithelium NEP and SVZ Choroid plexus stem cells

Diencephalic choroid plexus

(future lateral ventricle)

l ra nt e s ov u ter cle An nu

Anterodorsal nucleus?

Ventral complex

Anteromedial ganglionic NEP and SVZ

ul

tic

Stria terminalis

Re

Strionuclear glioepithelium

In

ar

Anterior complex

THALAMUS Thalamic G/EP

nu

ter na lc ap su le

cle u

s

Anteromedial nucleus

Co

third ventricle

Forel's fields

Paraventricular nucleus

HYPOTHALAMUS

Perifascicular glioepithelium

(lateral olfactory tract)

n ma

lf ga u of tic

ibe

y)

r

few s(

)

dus alli External p bus segment Glo Medullary

Internal segment

lamina

External capsule

Anterior commissure

Substantia innominata

Ansa lenticularis?

Basal nucleus of Meynert Endopiriform nucleus?

(infiltrated by lateral migratory stream stream))

Neurons migrating between paraventricular and supraoptic nuclei? Anterior nucleus

Supraoptic nucleus Lateral olfactory tract

Periventricular nucleus

glioepithelium

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

ea ar ic m la ha ot yp lh

n halo ata) p e c len min al te ia inno s a B ant st Optic chiasm (sub

Hypothalamic glioepithelium/ ependyma (G/EP)

r

ib

te

Putamen

ra

Medial forebrain bundle

al f

( ers

da

te

(percolates through external capsule)

Medial forebrain bundle

T h ala m

ti c o c or

La

Lateral migratory stream

(extends to primary olfactory cortex)

er nt l a leus a r nt uc Ve n

Internal capsule

Subthalamic G/EP

Lateral migratory stream

u Ca

ior

Periventricular complex

SUBTHALAMUS

BASAL GANGLIA

Primary olfactory cortex

third ventricle

Stria medullaris

ix rn Fo

Anterolateral ganglionic neuroepithelium (NEP) and subventricular zone (SVZ)

telencephalic superventricle

Anterobasal nucleus?

Optic chiasm

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

67

68

PLATE 27A, GW11 Coronal, CR 60 mm, Y1-59, Level 9: Section 419

See level 9 in Plates 9A and B.

DIENCEPHALON, BASAL GANGLIA AMYGDALA, AND BASAL TELENCEPHALON

telencephalic superventricle

Ve n

t

la

a

t

w)

( fe rs

External capsule

t ac tr c ti p O

Lateral tuberal nucleus? Ventromedial nucleus Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Anterior commissure

x

e

Arcuate nucleus

l ra nt us Ce ucle n

Medial forebrain bundle

e

Putamen

al er at ex ol pl as m B co

third ventricle

Internal segment

Cerebral peduncle Dorsomedial nucleus

fi b

pl

Median eminence/ posterior pituitary gland (neurohypophysis) Anterior Pituitary gland (adenohypophysis, distal part)

Forel's fields

com

(surrounds fiber tracts)

al fu g

s? ulari tic en l Lateral migratory stream a (percolates through external capsule) ns A

al om e di

Perifascicular glioepithelium

y)

lamina

rtic

AMYGDALA

HYPOTHALAMUS

an

tico Cor

Co

Hypothalamic glioepithelium/ ependyma (G/EP)

a l fib ers ( m

l ra nt um Ve riat st

BASAL GANGLIA

rt i c

dus alli p External bus segment Glo Medullary

Medial lemniscus?

SUBTHALAMUS Subthalamic G/EP

moc o

a te

in c

o

Mammillothalamic tract

l ra

a la

ud Ca

Internal capsule

na

x

lc

Thalamic G/EP

Ve n t r a l complex

P

Zo

le ra

THALAMUS

Th

a ar

cleus

p nt

pl ex

Periventricular complex

er

m

Ce

r nucleus ticula Re

Strionuclear glioepithelium

Stria terminalis

m

Dorsomedial nucleus

nu

c

nt ral nu ra cle l nu a us cl nt eu er s io r

l

ce

a

nt

rs

o

Posterior ganglionic neuroepithelium (NEP) and subventricular zone (SVZ)

Dorsolateral nucleus

Ve

Do

m e S tr i du a lla r is

al

HIPPOCAMPUS

nix For

Choroid plexus stem cells

(future lateral ventricle)

Diencephalic choroid plexus

ert

Dentate migration

Fornical glioepithelium

third ventricle

PLATE 27B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

La

te

ra

l o lf

P ri m a r

acto

y o l fa c t o r y c o

rtex

ry tr act

69

70

PLATE 28A GW11 Coronal, CR 60 mm, Y1-59, Between levels 10 and 11: Section 449

See levels 10 and 11 in Plates 10A and B to 11A and B.

DIENCEPHALON

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Habenula

Lateral habenular nucleus Medial habenular nucleus Stria medullaris

Diencephalic choroid plexus

Epithalamic G/EP r

s

eu

Medial forebrain bundle

l uc

rn

od eb

la t

tr

en

Supramammillary area

e Cer

t tr

l la

pt

le

ic

tra

O

ic m la s a u h e bt cl Su nu

nc

na

Ve n

Zo

ce

du

SUBTHALAMUS

in

ac

rt

a

ter al ge nic u

V

pe

Forel's fields

te

y?

lat

al

Vent Ve n t r al medial n u c l e us

al c a p s ule ic tr act

Reticular nucleus In

era

Ve

l nucl eus

nt

ral

nu

cle

us

anterior n

cular complex

Par

a

l

Subthalamic G/EP Hypothalamic G/EP

third ventricle

x

Perifascicular GEP

Mammillothalamic tract

Periventri

co r

ter

io

Medial lemniscus?

Medial lemniscus?

(surrounds fiber tracts)

third ventricle

lex

ody te b ula

mp

al

n ic

e pl c o m

co

tr

ge

al

n ace

al

Thalamic G/EP

In transient dorsal position

er

tr

la t

en

Dorsomedial n u c l e us

al

ex pl

C

rs

m co

r belt

THALAMUS

Do

m

pl

l sa

icula

Ve n t r a l

Ret

Po s

Dorsolateral nucleus

D

Pulvinar?

o

ex

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium

Opt

PLATE 28B

br

HYPOTHALAMUS Lateral tuberal nucleus?

Hypothalamic (mammillary) NEP

Lateral mammillary nucleus? Medial mammillary nucleus? third ventricle (mammillary recess)

71

72

PLATE 29A GW11 Coronal, CR 60 mm, Y1-59, Between levels 11 and 12: Section 469

See levels 11 and 12 in Plates 11A and B to 12A and B.

DIENCEPHALON

PLATE 29B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Diencephalic choroid plexus

Habenula

Epithalamic G/EP

cular complex

tr a nu l lat eral cle us

Hypothalamic G/EP

ct a?

ic a ms l ha eu bt ucl u S n al

Supramammillary area

Ce

HYPOTHALAMUS Medial forebrain bundle

ert

e

nc a i n Zo

cl

SUBTHALAMUS

un

(lines fiber tracts)

p

Subthalamic G/EP

Op

tic

tra

Ventral Ve n t r al medial medial nucleus n u c l e us

Ventral lateral geniculate body

ed

x

st Po

V

Forel's fields Perifascicular GEP

e

en

Medial lemniscus?

Dorsomedial D orsomedial nucleus n u c l e us

Periventri

Thalamic G/EP

third ventricle

r belt

e pl c o m

icula

r complex

THALAMUS

R

cu

Dorsal complex

In transient dorsal position

Ventral anterior nucleus

ti

Ve n t r a l

Ret

erio

Pulvinar

mplex r co

Po

te

o ri

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium

l tera l la ody rsa te b Do ula nic ucleus ge r n la

s

Lateral habenular nucleus Medial habenular nucleus Stria medullaris

re

br

Mammillary body

Fornix

Mammillothalamic tract

Hypothalamic (mammillary) NEP

Medial mammillary nucleus? third ventricle (mammillary recess)

73

74

PLATE 30A GW11 Coronal, CR 60 mm, Y1-59, Adjacent to level 13: Section 499

See level 13 in Plates 13A and B.

DIENCEPHALON

PLATE 30B Epithalamic G/EP

Habenula

Lateral habenular nucleus Medial habenular nucleus Stria medullaris Habenulo-interpeduncular tract

Mesencephalic G/EP MIDBRAIN TEGMENTUM

Interpeduncular nucleus

V

Medial lemniscus?

Red nucleus

Su

Ventral tegmental area?

Ce

Medial forebrain bundle

nig ia t tan bs

ra

t

trac

tic Op

lp os nuc terolate ral le u s

tra

postVentral er nuc omedia leus ? l

en

c o m p l e x aqueduct

Ventral lateral geniculate body?

le

(lines fiber tracts)

l

nc

Perifascicular GEP

a

du

e

tr

Centromedian nucleus

In transient dorsal position

pe

le

mp r c o

V

r belt

Posterio

icula

C e n t r al c o m p l e x

ral y ate ll bod sa ate l nucleus or D i c u ticular n Re ge

Ret

THALAMUS

Parafascicular nucleus

Pulvinar

Thalamic G/EP

n

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma

Diencephalic choroid plexus

complex

third ventricle

rior

x

P

te os

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

r

r eb

al

Habenulo-interpeduncular tract

75

76

PLATE 31A GW11 Coronal, CR 60 mm, Y1-59, Level 14: Section 529

See level 14 in Plates 14A and B.

DIENCEPHALON AND MIDBRAIN TEGMENTUM

PLATE 31B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Diencephalic choroid plexus

Posterior commissure Glia migrating into posterior commissure?

GEP (posterior commissure)

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma

ex

Visual radiation to occipital cortex?

Pretectal G/EP

Mesencephalic G/EP

Central gray

MIDBRAIN TEGMENTUM

Oculomotor nuclear complex (III)

Medial lemniscus?

Perifascicular GEP (lines fiber tracts)

Ventral lateral geniculate body?

Medial longitudinal fasciculus

Interpeduncular nucleus

Medial forebrain bundle Capsule of red nucleus (superior cerebellar peduncle) Habenulo-interpeduncular tract

Red nucleus

Ventral tegmental area

Optic tract

ra

i

ig

er

Medial geniculate body

S

s ub

C ere

ta

bra

l

i nt

a

d pe

n

e

P

t os

aqueduct

cl

co

THALAMUS

m

pl

m

or

er

Post

r

co

Pretectum

x ple

eral sal lat Dor late body icu gen

io

Auditory radiation to temporal cortex?

un

77

78

PLATE 32A GW11 Coronal CR 60 mm, Y1-59 Near level 15: Section 549

See Level 15 in Plates 15A and B.

MIDBRAIN AND PONS

79 FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

PLATE 32B

Pineal gland

Optic tract intermingled with the auditory radiation to temporal cortex?

Posterior commissure

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ ependyma

PRETECTUM Pretectal olivary nucleus

Pretectal G/EP

Mesencephalic nucleus (V)?

aqueduct

Reticular formation

Central gray

Medial longitudinal fasciculus

Perifascicular GEP

nt

ia

(lines fiber tracts)

c l e

nig

ra

Medial lemniscus?

Habenulo-interpeduncular tract?

Reticular tegmental nucleus

PONS

u d

p

l

r a

cular Interpedun fossa

Middle cerebellar peduncle

C

Capsule of red nucleus (superior cerebellar peduncle)

S

e r e b

Ventral tegmental area

e

ub

sta

InterRed peduncular nucleus? nucleus

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Bra chiu mo f the

Oculomotor nuclear complex (III)

MIDBRAIN TEGMENTUM

Medial forebrain bundle?

infe rior colli culu s

Mesencephalic G/EP

n

THALAMUS (remnant of the posterior complex)

Medial geniculate body (remnant)

Pontine gray Pontocerebellar fibers Transpontine corticofugal tract

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Pontocerebellar fibers (decussation)

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

80

PLATE 33A GW11 Coronal CR 60 mm, Y1-59 Level 15: Section 569

See Level 15 in Plates 15A and B.

MIDBRAIN AND PONS

81

PLATE 33B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma

Posterior commissure Subcommissural organ Optic tract

SUPERIOR COLLICULUS

MIDBRAIN TECTUM aqueduct

Migrating superior colliculus neurons sorting into various gray layers

Central gray

Mesencephalic G/EP

Brachium of the inferior colliculus

Mesencephalic nucleus (V)?

Reticular formation

Oculomotor nuclear complex (III)

MIDBRAIN TEGMENTUM Perifascicular GEP

Medial longitudinal fasciculus

Superior cerebellar peduncle (decussation) i s c u s

(lines fiber tracts)

a l e r t L a

l e m

n

Reticular formation Raphe nuclear complex

PONS

Nerve VIII (vestibulocochlear)?

Middle cerebellar peduncle Pontine gray

Medial lemniscus and trapezoid body

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Nucleus of the lateral lemniscus (ventral)

Dashed lines indicate staining and/or sectioning artifacts.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

82

PLATE 34A GW11 Coronal CR 60 mm, Y1-59 Near level 16: Section 589

See Level 16 in Plates 16A and B.

MIDBRAIN, PONS, AND MEDULLA

83

PLATE 34B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Posterior commissure

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma

Subcommissural organ Optic tract

MIDBRAIN TECTUM

SUPERIOR COLLICULUS Future gray layers

Future white layers

Central gray

Mesencephalic G/EP

Central gray

Brachium of the inferior colliculus

Reticular formation

Perifascicular GEP

r e r io S u p b e lla r cere uncle p ed

Middle cerebellar peduncle

MIDBRAIN TEGMENTUM

Trochlear nucleus (IV) Medial longitudinal fasciculus

Reticular formation

Principal sensory nucleus (V) Trigeminal motor nucleus (V)

Raphe nuclear complex

Reticular formation

Facial motor nucleus (VII)

Superior olivary complex?

Medial lem niscus

PONS cer e b In f e ll e r i ar or pe du nc le

Migrating and settling Purkinje cells

Super cerebe ior pedun llar cle

ce re I be nf lla er r p ior ed un cl e

External germinal layer

Raphe nuclear complex

us lemnisc Lateral

Later al lem niscus

(lines fiber tracts)

Mesencephalic nucleus (V)?

CE (HE REBE MIS LLU PHE M RE)

aqueduct

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Trapezoid body Posterior intramural migratory stream? (inferior olive neurons)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

84

PLATE 35A GW11 Coronal CR 60 mm, Y1-59 Level 16: Section 599

See Level 16 in Plates 16A and B.

MIDBRAIN, PONS, AND MEDULLA

85

PLATE 35B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium

Posterior commissure Subcommissural organ

MIDBRAIN TECTUM

Optic tract

SUPERIOR COLLICULUS

Sorting future white and gray layers

Mesencephalic G/EP

Central gray

INFERIOR COLLICULUS

aqueduct

r e r io S u p b e lla r cere uncle p ed

Reticular formation

Medial longitudinal fasciculus Super cerebe ior pedun llar cle

Principal sensory nucleus (V)

Middle cerebellar peduncle Cochlear nucleus

cer eb In f e ll e r i ar or pe du nc le

Migrating and settling Purkinje cells

Pontine G/EP Trigeminal motor nucleus (V)

PONS Spinal nucleus (V) Facial motor nucleus (VII)

MEDULLA Ventral rhombic lip (auditory NEP)

Raphe nuclear complex

Inferior olive

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Posterior intramural migratory stream (inferior olive neurons) Capsule Principal nucleus

fourth ventricle (lateral recess) Medial lemniscus

Dorsal rhombic lip (cerebellar germinal trigone)

Reticular formation

cer In e b e fe r lla r io r ped unc le

External germinal layer

Raphe nuclear complex

Mesencephalic nucleus (V)?

CE (HE REBE MIS LLU PHE M RE)

Later al lem niscus

(lines fiber tracts)

us lemnisc Lateral

MIDBRAIN TEGMENTUM

Perifascicular GEP

Nucleus of the lateral lemniscus (dorsal)?

Intramural migratory stream enters inferior olive

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

86

PART PARTIII: III: GW11 GW11 HORIZONTAL HORIZONTAL

This is specimen number 1500 in the Carnegie Collection, designated here as C1500. A normal fetus with a crown-rump length (CR) of 56 mm was collected in 1916. The fetus is estimated to be early in gestational week (GW) 11. The entire fetus was fixed in formalin and was cut in the horizontal plane. The records are not clear regarding section thickness, but the brain is present in 2,400 sections, more than three times the number of 35 µm sections in the GW17 horizontally sectioned brain in the Yakovlev Collection (Bayer and Altman, 2005, Volume 3, Part IX). We estimate that the sections are between 8-10 µm thick. All sections were stained with Bodian’s method to show developing fiber tracts. Since there is no photograph of C1500’s brain before it was embedded and cut, a specimen from Hochstetter (1919) that is comparable in age is used to show the approximate section plane and external features in early GW11 (Figure 2). Levels 1-10, large sections containg the cerebral hemispheres, are shown at low magnification in Plates 36-45. Levels 11-21, small sections containing only the brainstem, are shown at a higher magnification in Plates 46-56. To maximize image size within page space, C1500’s sections are rotated 90˚ (landscape orientation). The anterior part of each section is on the left (page bottom), and the posterior part of each section is on the right (page top). C1500 has many of the same features as Y1-59, except that it is slightly less mature. Throughout the cerebral cortex, the neuroepithelium and subventricular zone are prominent. The stratified transitional field (STF) contains STF1 and STF5 throughout; with STF4 only in lateral areas. The most prominent developmental feature of the cerebral cortex is that both the STF layers and the cortical plate have a pronounced lateral (thicker) to medial (thinner) maturation gradient. The olfactory bulb beneath the anterior septum and striatum contains a small rostral migratory stream in its core. In anterolateral parts of the cerebral cortex, streams of neurons and glia appear to leave STF4 and enter the lateral migratory stream. The hippocampus is in an immature position dorsal to the thalamus and medial to the temporal lobe. Cells are entering Ammon’s horn pyramidal layer in the ammonic migration, and granule cells and their precursors are migrating to the hilus of the presumptive dentate gyrus in the den-

tate migration; there is no granular layer. A massive neuroepithelium/subventricular zone overlies the amygdala, nucleus accumbens, and striatum (caudate and putamen) where neurons (and glia) are being generated. The cerebellum is a thick, smooth plate overlying the posterior pons and medulla. However, there is only a thin glioepithelium/ependyma at the ventricular surface, indicating that all deep neurons and Purkinje cells have been generated. The deep neurons are in place beneath the cortex, but have indefinite nuclear subdivisions. The cortical surface is covered by an external germinal layer (egl) that is actively producing neuronal stem cells, granule, stellate, and basket cells of the cerebellar cortex. Lamination in the cortex is nearly absent, except for a thin molecular layer beneath the egl. Nearly all Purkinje cells are migrating, and settling. In contrast to Y1-59, there is no evidence of lobulation in the cerebellar cortex. The third ventricle, aqueduct, and fourth ventricle are lined by a thin glioepithelium/ependyma indicating that neurogenesis in the primary neuroepithelium is complete. In the medulla there are two active germinal sites in anterior and posterior parts of the ventral rhombic lip. 1) The auditory neuroepithelium generates cochlear nucleus neurons. 2) A large precerebellar neuroepithelium generates precerebellar (mainly pontine gray) neurons. Neurons throughout the diencephalon, midbrain tegmentum, pons, and medulla are settling. Because C1500 is not Nissl-stained, nuclear divisions are very indistinct. The large anterior extramural, posterior extramural, and intramural migratory streams are prominent in the medulla and pons. The Bodian stain clearly shows several fiber tracts and nerves throughout the brainstem. The optic nerve and tract are well defined, along with the medial forebrain bundle. Unlike Y1-59, there is no sure evidence of a cerebral peduncle in the midbrain tegmentum or pontine gray. However, pontine gray fibers cross the midline and a distinct middle cerebellar peduncle is present. There is also a distinct superior and inferior cerebellar peduncle. There is definite staining in the trigeminal nerve and tract, the facial nerve, the abducens nerve, and the glossopharyngeal nerve.

87

GW11 HORIZONTAL SECTION PLANES C1500's cutting angle rotates 3.9˚ counterclockwise from the true horizontal plane (0˚). The anterior part of each section is slightly ventral to the posterior part.

LEVEL:SECTION 1:108

2:536 3:696 4:800

CORONAL PLANE (90˚)

5:962 6:1023 7:1143

HORIZONTAL PLANE (0˚)

SUL

E

TE

M

B

IN

E

A

FRONTAL LOBE

PARIETAL LOBE

CEPHALON EN L HEMISPHE L A RE E BR

CE T R

PARACENTRAL LOBULE

8:1256 9:1351 10:1414 11:1473 12:1566 13:1626 14:1716 15:1805 16:1866 17:1926 18:1962

PO

R AL

Olfactory bulb Optic nerve

DIENCEPHALON (HYPOTHALAMUS)

Trigeminal nerve

LO

OCCIPITAL LOBE

19:2202

MIDBRAIN PONS

20:2322 21:2402

CEREBELLUM MEDULLA SPINAL CORD

Figure 2. The lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 53 mm (modified from Figure 46, Table VIII, Hochstetter, 1919) serves to show the approximate locations and cutting angles of the illustrated sections of C1500 in the following pages. The small inset identifies the major structural features. The cut beneath the cerebellum is the edge of the medullary velum.

88

PLATE 36A GW11 Horizontal CR 57 mm C1500 Level 1: Section 108 LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 36B FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

NEP - Neuroepithelium

FUTURE PARACENTRAL LOBULE Layer I Cortical plate Subplate (layer VII) Channel 2 STF1 t1 Paracentral STF STF5

Interhemispheric fissure

Cortical (paracentral) NEP

telencephalic superventricle

(future lateral ventricle)

Cortical (paracentral) NEP

mid-dorsal pool

89

90

PLATE 37A GW11 Horizontal CR 57 mm, C1500 Level 2: Section 536

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 37B

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

FUTURE PARIETAL LOBE

FUTURE PARACENTRAL LOBULE

NEP - Neuroepithelium

Thick cortical plate

FUTURE FRONTAL LOBE

Paracentral STF

STF1 t1 STF5 Frontal STF

Lateral (more mature) to medial (less mature) morphogenetic gradient

Dorsal telencephalic choroid plexus Cingulate STF

Future anterior cingulate gyrus

Interhemispheric fissure

Layer I Cortical plate Subplate (layer VII) Channel 2 STF1 t1 STF5 Parietal STF

Thin cortical plate

Future posterior cingulate gyrus

Cortical (cingulate) NEP

Cortical (medial frontal) NEP and SVZ anterodorsal pool

Cortical (medial parietal) NEP and SVZ

telencephalic superventricle (future lateral ventricle)

posterodorsal pool

mid-dorsal pool

Cortical (lateral frontal) NEP Cortical (lateral paracentral) NEP

Dashed lines indicate staining and/or sectioning artifacts.

Cortical (lateral parietal) NEP

91

92

PLATE 38A GW11 Horizontal CR 57 mm, C1500 Level 3: Section 696

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 38B ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Paracentral STF

Frontal STF

Parietal STF

FUTURE PARACENTRAL LOBULE

STF1 t1 STF5

BASAL GANGLIA (STRIATUM)

FUTURE FRONTAL Future anteroventral cingulate gyrus LOBE

Anterior telencephalic choroid plexus

Cingulate STF

Interhemispheric fissure

anterior pool

Cortical (cingulate) NEP

Fimbria/fornix GEP

telencephalic superventricle (future lateral ventricle)

ix orn a/f i r b Fim

Dorsal hippocampus

third ventricle Dorsal thalamic complex

ga ng lio nic na rr ow s

Layer I Cortical plate Subplate (layer VII) Channel 2 STF1 t1 STF5

Posterior telencephalic choroid plexus

THALAMUS

FUTURE PARIETAL LOBE

Future retrosplenial area Diencephalic choroid plexus

Interhemispheric fissure

Cortical (medial parietal) NEP Cortical (hippocampal) NEP posterior pool

telencephalic superventricle (future lateral ventricle)

Cortical (frontal) NEP Cortical (lateral paracentral) NEP

Dashed lines indicate staining and/or sectioning artifacts.

Posterior ganglionic NEP and SVZ Corticoganglionic NEP and SVZ Anteromedial ganglionic NEP and SVZ

Cortical (lateral parietal) NEP

93

94

PLATE 39A GW11 Horizontal CR 57 mm, C1500 Level 4: Section 800

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 39B ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Paracentral STF Frontal STF

Channel 2

Parietal STF

FUTURE PARACENTRAL LOBULE

Internal capsule (thick bundled corticofugal and corticopetal fibers intermingle?)

BASAL GANGLIA

Ca ud ate

Anterior telencephalic choroid plexus

(STRIATUM)

Dorsal complex

mp

Fornix

Interhemispheric fissure

Cortical (frontal) NEP

Cortical (cingulate) NEP

An te r io r

Cingulate STF

Posterior complex

THALAMUS

co

Future anteroventral cingulate gyrus

Fornix

Dorsal hippocampus lex

FUTURE FRONTAL LOBE

Posterior telencephalic choroid plexus

Dentate migration? Future Ammon's horn

men Puta

STF1 t1 STF5

Periventricular complex

plex al com Centr EPITHALAMUS Habenu lar com plex

Diencephalic choroid plexus

third ventricle (thalamic/epithalamic)

Fornical GEP

Thalamic G/EP

Choroid plexus stem cells

anterior pool

telencephalic superventricle (future lateral ventricle)

Layer I Cortical plate Subplate (layer VII) Channel 2 STF1 t1 STF5

FUTURE PARIETAL LOBE

ga

ng

l io

ni

cn

ar

ro

w

s

FUTURE OCCIPITAL LOBE

Occipital STF

Interhemispheric fissure Cortical (occipital) NEP

Epithalamic (habenular) G/EP

Choroid plexus stem cells Fornical GEP posterior pool Cortical (hippocampal) NEP

telencephalic superventricle (future lateral ventricle)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Cortical (lateral paracentral) NEP

Dashed lines indicate staining and/or sectioning artifacts.

Corticoganglionic NEP and SVZ Posterior ganglionic NEP and SVZ Anteromedial ganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ Corticoganglionic NEP and SVZ

Cortical (lateral parietal) NEP

95

96

PLATE 40A GW11 Horizontal CR 57 mm, C1500 Level 5: Section 962

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 40B ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Frontal STF

Visual radiation (Meyer's loop) and auditory radiation?

Internal capsule (thin bundled corticopetal fibers?)

Putamen

Cingulate STF

Ca

ud

ate

Interhemispheric fissure

Cortical (cingulate) NEP

r erio A n t p le x ? com

Diencephalic choroid plexus

Pretectal G/EP

Mesencephalic G/EP aqueduct

limb rior Ante

Fornical GEP

i o r li m b

Cortical (hippocampal) NEP Corticoganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ Anteromedial ganglionic NEP and SVZ

Dashed lines indicate staining and/or sectioning artifacts.

SUPERIOR COLLICULUS

Strionuclear GEP

Cortical (paracentral) NEP

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Central gray

Thalamic G/EP

Internal capsule

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Posterior commissure

(thalamic)

ter

anterior pool

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex.

MIDBRAIN TECTUM

third ventricle

os

(future lateral ventricle)

um tect Pre

Periventricular complex

Fornical GEP

telencephalic superventricle

Ventral complex

Central complex?

FUTURE OCCIPITAL LOBE Occipital STF

lic

Dorsal hippocampus

Posterior complex

THALAMUS

Bed nucleus of the stria terminalis

Fornix

Cortical (frontal) NEP

Posterior complex

(STRIATUM)

pha

Layer I Cortical plate Channel 2 STF1 t1 Subplate (layer VII) STF5

Future Ammon's horn Dentate migration?

Fornix

BASAL GANGLIA

P

FUTURE FRONTAL LOBE

An teri cho or tele roid nce ple phal xus ic Future anteroventral cingulate gyrus

ce e le n or t us t e r i d p le x s o P roi ch o

Cauda te

FUTURE INSULAR GYRUS

STF1 t1 STF5

FUTURE TEMPORAL LOBE

Temporal STF

Posterior ganglionic NEP and SVZ Corticoganglionic NEP and SVZ

Cortical (occipital) NEP

telencephalic superventricle (future lateral ventricle)

posterior pool

Cortical (temporal) NEP

97

98

PLATE 41A GW11 Horizontal CR 57 mm, C1500 Level 6: Section 1023

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 41B

STF4

Lateral migratory stream

Lateral migratory stream STF4

Frontal STF

Claustrum Internal capsule (thin bundled corticopetal fibers?)

Ca An

FUTURE FRONTAL LOBE Cingulate STF

ter c h io r t o r e le o id n p le c e p h x u a li s c

ate

BASAL GANGLIA (STRIATUM)

Stria terminalis Bed nucleus of the stria terminalis

Future anteroventral cingulate gyrus

SEPTUM

Interhemispheric fissure

Cortical (cingulate) NEP

Lateral septal nucleus Medial septal nucleus

Fornix

Septal NEP

Posterior complex (lateral geniculate body) Posterior complex (medial geniculate body) Auditory and somatosensory radiations?

Habenulo-interpeduncular tract?

SUPERIOR

Future oculomotor complex? COLLICULUS (Nerve III) Central gray

(thalamic)

aqueduct

Mesencephalic G/EP

Strionuclear NEP

Fornical GEP

i o r li m b

limb rior Ante

Strionuclear GEP

Internal capsule

Cortical (hippocampal) NEP

Cortical (frontal) NEP

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

TECTUM

MIDBRAIN

Thalamic G/EP Strionuclear GEP

anterior pool

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Reticular formation

Periventricular complex

third ventricle

Dorsal hippocampus

TEGMENTUM

ter

(future lateral ventricle)

Anterior complex? Stria medullaris

Ventral complex

Occipital STF

Future Ammon's horn Dentate migration?

os

telencephalic superventricle

THALAMUS

Fornical GEP

Fornix

Visual radiation (Meyer's loop)

Putamen

ud

FUTURE OCCIPITAL LOBE

Cauda te

FUTURE INSULAR GYRUS

STF1 t1 STF5

Layer I Cortical plate Channel 2 STF1 t1 Subplate (layer VII) STF5

FUTURE TEMPORAL LOBE

Temporal STF

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

P

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Corticoganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ Anteromedial ganglionic NEP and SVZ

Dashed lines indicate staining and/or sectioning artifacts.

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex.

telencephalic superventricle

Posterior ganglionic NEP and SVZ

Cortical (occipital) NEP

(future lateral ventricle)

Corticoganglionic NEP and SVZ

posterior pool

Cortical (temporal) NEP

99

GW11 Horizontal CR 57 mm, C1500 Level 7: Section 1143

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

100

PLATE 42A

PLATE 42B ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

FUTURE Temporal STF TEMPORAL LOBE

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Layer I Cortical plate Channel 2 STF1 t1 STF5

STF4

Lateral migratory stream

Frontal/orbitofrontal STF

Interhemispheric fis

Cortical (cingulate) NEP

Medial septal nucleus?

SEPTUM

third ventricle Fornical GEP

? bt ha Fu la m tu ic re nu c le us ?

zon F u t a i ure nc ert a

Reticular formation

BASAL GANGLIA

(future lateral ventricle)

aqueduct

(superior pool)

Thalamic G/EP Mesencephalic tegmental G/EP

Strionuclear GEP Fornical GEP

anterior pool Cortical (hippocampal) NEP Cortical (frontal) NEP Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Cortical (orbitofrontal) NEP

Posterior ganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ

ray ral g Cent

(thalamic/subthalamic)

Strionuclear GEP Strionuclear NEP

TECTUM

TEGMENTUM

Subthalamic G/EP

Septal NEP

telencephalic superventricle

MIDBRAIN

su

Fo rni x

sure

SUBTHALAMUS

Hippocampus

R S IO U R UL P E IC SU L L O C

Tenia tecta

Future Ammon's horn Dentate migration?

(po

Future anteroventral cingulate gyrus

Occipital STF

cap sul e

Cingulate STF

Claustrum and n Endopiriform nucleus Putame Inte UM r IAT st ud nal caps R e ri T ule ate S bus or l (an i m b) G lo lid u s teri or l l a imb M p U ) D I Bed LL n PA T stria ucleus H term of the (Ve ALA inal Fornix n tr M U is al c S om Stria terminalis p le x) Lateral septal nucleus

Ca

STF4

ter nal

Future primary olfactory cortex

Cau date

In

FUTURE FRONTAL LOBE STF1 t1 STF5

FUTURE OCCIPITAL LOBE?

Lateral migratory stream

telencephalic superventricle (future lateral ventricle)

posterior pool

Mesencephalic tectal G/EP

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex. Cortical (occipital) NEP

Corticoganglionic NEP and SVZ

Dashed lines indicate staining and/or sectioning artifacts.

Cortical (temporal) NEP

101

GW11 Horizontal CR 57 mm, C1500 Level 8: Section 1256

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

102

PLATE 43A

PLATE 43B

Temporal STF

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Layer I Cortical plate Channel 2 STF1 t1 STF5

STF4

Lateral migratory stream

Future primary olfactory cortex

vent ral s en/ tria tum

Bed nucleus of the stria terminalis

Future anteroventral cingulate gyrus Late ra nuclel septal us

Tenia tecta

Medial septal nucleus

ure Interhemispheric fiss

SEPTUM Cortical (cingulate) NEP

Septal NEP

telencephalic superventricle (future lateral ventricle)

Lateral hypothalamic area

Strionuclear NEP

HYPOTHALAMUS third ventricle

Future Ammon's horn Dentate migration?

Fornix

bundle

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Cortical (orbitofrontal) NEP

aqueduct

Mesencephalic tegmental G/EP

Fornical GEP Cortical (hippocampal) NEP

Amygdaloid NEP and SVZ Anterolateral ganglionic NEP and SVZ Corticoganglionic NEP and SVZ

ray ral g Cent

(superior pool)

Hypothalamic G/EP

BASAL TELENCEPHALON

TECTUM

INFERIOR COLLICULUS?

(hypothalamic)

anterior pool

Cortical (frontal) NEP

Hippocampus

MIDBRAIN

Fu ve tur nt e s TEGMENTUM ra ub l t e st gm a n t Reticular en ia n formation tal ig ar r a / e Future red a? Nerve III? nucleus?

Optic tract

Medial fo rebrain

Anterior commissure

STF4

AMYGDALA Medial BASAL nucleus? TELENCEPHALON

R S IO U R UL P E IC SU L L O C

FUTURE FRONTAL LOBE Cingulate STF

A n te r (antioer comm r Puta ior limbis)sure m

La

?

Central nucleus?

ra

te

STF1 t1 STF5

us

cle

u ln

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex.

FUTURE TEMPORAL LOBE

Lateral migratory stream

Frontal STF

Mesencephalic tectal G/EP

telencephalic superventricle (future lateral ventricle)

posterior pool

Cortical (temporal) NEP

103

GW11 Horizontal CR 57 mm, C1500 Level 9: Section 1351

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

104

PLATE 44A

PLATE 44B ABBREVIATIONS: G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Temporal (granular) STF

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Layer I Cortical plate Channel 2 STF1 t1 STF5

FUTURE TEMPORAL LOBE

Lateral migratory stream

STF4

Frontal STF

nu cle i?

FUTURE FRONTAL LOBE STF1 t1 STF4 STF5

Co rti cal

Future primary olfactory cortex

N AL BAS PHALO E ENC

Me nucledial us?

Lateral hypothalamic area

Brachium of the inferior colliculus?

MIDBRAIN

Optic tract

Lateral preoptic Medial fo area rebrain b undle PREOPTIC AREA HYPOTHALAMUS Medial preoptic area third ventricle Diagonal band (preoptic/hypothalamic) of Broca

TEGMENTUM F u tu vent re subs t ral t e g m a n tia n i g e n ta l are ra/ a? Future interpeduncular nucleus?

Reticular formation

ay Trochlear nucleus? l gr tra (nerve IV) Cen isthmal canal

Preoptic NEP Hypothalamic G/EP Cortical (cingulate) NEP telencephalic superventricle

Cortical (parahippocampal) NEP

AMYGDALA Cortical (orbitofrontal) NEP

Amygdaloid NEP and SVZ

te le n (f ce ut p ur ha e li la c

te su ra p l er ve v nt en ri t po cl ri st e) cl

er io r

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

aqueduct (superior pool)

Mesencephalic tectal G/EP

BASAL TELENCEPHALON

anterior pool

Cortical (frontal) NEP

Central nucleus?

Mesencephalic tegmental G/EP

Accumbent NEP and SVZ?

(future lateral ventricle)

TECTUM INFERIOR COLLICULUS R RIO S? PE LU SU LICU L CO

ure Interhemispheric fiss

ac Nu cu cle m us be ns ?

Tenia tecta

TEL

Central Basal nucleus? nucleus?

AMYGDALA

Anterior commissure (anterior limb)

Future anteroventral cingulate gyrus

Cingulate STF

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex.

Lateral migratory stream

Dashed lines indicate staining and/or sectioning artifacts.

e

po ol

Cortical (temporal) NEP

Cortical (temporal) NEP

105

GW11 Horizontal CR 57 mm, C1500 Level 10: Section 1414

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

106

PLATE 45A

ABBREVIATIONS: G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Temporal STF STF4

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Lateral migratory stream

al Bas us? le nuc

FUTURE FRONTAL LOBE

Future primary olfactory cortex

Lateral migratory stream

M nu edi cle al us ?

FUTURE TEMPORAL LOBE

Subthalamic nucleus?

Nucleus accumbens (remnant)?

STF4

Layer I Cortical plate STF1 t1 STF5

Supraoptic nucleus? Lateral hypothalamic area

Optic tract

third ventricle (hypothalamic)

Hypothalamic G/EP

MIDBRAIN

Interpeduncular nucleus Reticular

Interpeduncular fossa

formation

Central tegmental tract?

TECTUM Trochlear nucleus? (nerve IV)

ray al g ntr Ce isthmal

(future lateral ventricle)

anteroventral pool

olfactory recess

Cortical (orbitofrontal) NEP

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Accumbent NEP and SVZ?

AMYGDALA Amygdaloid NEP and SVZ

Dashed lines indicate staining and/or sectioning artifacts.

te le n (f ce ut p ur ha e li la c

aqueduct (superior pool)

canal

Mesencephalic tegmental G/EP

telencephalic superventricle

R S IO U R UL F E IC IN L L O C

Olfactory tubercle

Supramammillary area?

Paraventricular nucleus?

Fossa created by the downward curve of the inferior colliculus

TEGMENTUM

HYPOTHALAMUS Medial forebrain bundle Tenia tecta

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex.

AMYGDALA

(Orbitofrontal area)

STF1 t1 STF5

Central nucleus?

Frontal (orbitofrontal) STF

Cor tica l nu clei ?

PLATE 45B

Mesencephalic tectal G/EP

Cortical (parahippocampal) NEP

te su ra p po l er st ve v er nt en ri t io cl ri r e) cl po e ol

Cortical (temporal) NEP

Cortical (temporal) NEP

107

GW11 Horizontal CR 57 mm, C1500 Level 11: Section 1473

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

108

PLATE 46A

PLATE 46B ABBREVIATIONS: G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Note the lateral (more mature) to medial (less mature) morphogenetic gradient in the cerebral cortex.

Temporal STF STF4

Layer I Cortical plate STF1 t1 STF5

Lateral migratory stream

n

(Orbitofrontal area) Rostral migratory stream

Tenia tecta

uc

al Bas us? le nuc

l

Primary olfactory cortex

STF1 t1 STF5

Ce nuc ntral leu s ?

Lateral migratory stream

ic a

FUTURE FRONTAL LOBE

lei

(HEMISPHERE)

Lateral lemniscus? Lateral tuberal nucleus?

MIDBRAIN

Mammillary body

Dentate nucleus

Parabrachial nucleus

Interpositus nucleus

TEGMENTUM Central gray

isthmal canal

Superior cerebellar peduncle (decussation)

Medial longitudinal fasciculus

Fastigial nucleus

CEREBELLUM (VERMIS)

Cortical (parahippocampal) NEP

Hypothalamic G/EP

anteroventral pool

AMYGDALA

Olfactory NEP

Cortical (orbitofrontal) NEP

Medial vermis

CEREBELLUM

Optic tract

HYPOTHALAMUS (future lateral ventricle)

Hemisphere Lateral vermis

olfactory recess telencephalic superventricle

Migrating Purkinje cells

?

Medial forebrain bundle Ventromedial nucleus third ventricle (hypothalamic)

Anterior olfactory nucleus

External germinal layer

FUTURE TEMPORAL LOBE

rt

STF4

Co

Frontal (orbitofrontal) STF

te le n (f ce ut p ur ha e li la c

Nerve IV decussation

Mesencephalic tegmental G/EP

te su ra p po l er ve v st nt en er ri t io cl ri r e) cl po e ol

Amygdaloid NEP and SVZ

Cortical (temporal) NEP Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Dashed lines indicate staining and/or sectioning artifacts. 109

110

PLATE 47A GW11 Horizontal CR 57 mm, C1500 Level 12: Section 1566

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 47B ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold Layer I Cortical plate

Frontal (orbitofrontal) STF

BASE OF FUTURE TEMPORAL LOBE

STF1 t1

External germinal layer Settling Purkinje cells Hemisphere

Entorhinal cortex

FUTURE FRONTAL LOBE

STF1 t1 STF5

(Orbitofrontal area)

Lateral vermis Medial vermis

CEREBELLUM Olfactory bulb

Rostral migratory stream

Suprachiasmatic nucleus Supraoptic nucleus Optic tract Ventromedial nucleus

(HEMISPHERE)

TEGMENTUM

(optic recess)

Olfactory NEP

rior

Central gray

Medial longitudinal fasciculus Dorsal tegmental nucleus?

isthmal canal

third ventricle

olfactory recess

Supe

Superior cerebellar peduncle (decussation)

Arcuate nucleus

Optic nerve HYPOTHALAMUS and tract Hypothalamic GEP G/EP

C er ebel lar p Interpositus edu nucleus ncle Middle s

MIDBRAIN

Mi ddl e Inf eri or Fastigial nucleus

CEREBELLUM (VERMIS)

third ventricle

(infundibular recess)

Cortical (orbitofrontal) NEP Layer I Cortical plate

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Mesencephalic tegmental G/EP

Cerebellar G/EP

STF1 t1 STF5

Dashed lines indicate staining and/or sectioning artifacts. 111

GW11 Horizontal CR 57 mm, C1500 Level 13: Section 1626

112

PLATE 48A

PLATE 48B FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

G/EP - Glioepithelium/ependyma

External germinal layer Settling Purkinje cells Hemisphere Lateral vermis

Note that corticofugal fibers are absent in the pontine gray.

BASE OF FUTURE FRONTAL LOBE (Orbitofrontal area)

Medial vermis

CEREBELLUM Lateral lemniscus

Optic nerve (II)

BASE OF HYPOTHALAMUS

(HEMISPHERE) Inf eri or cer ebe llar

Pontocerebellar fibers MIDBRAIN/PONS INTERFACE Reticular formation Pontine gray Raphe nuclear com plex

Optic chiasm

Mesencephalic/ pontine G/EP

third ventricle

ped unc le

Central gray

isthmal canal CEREBELLUM (VERMIS)

(infundibular recess)

Hypothalamic G/EP

Olivo-cerebellar fibers?

Layer I

Cortical plate

Cortical plate Layer I

Cerebellar G/EP

BASE OF FUTURE TEMPORAL LOBE Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Dashed lines indicate staining and/or sectioning artifacts. 113

GW11 Horizontal CR 57 mm, C1500 Level 14: Section 1716

Levels 14 to 21 are only shown at high magnification.

114

PLATE 49A

PLATE 49B

Auditory germinal trigone

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold External germinal layer (cochlear nuclei)

Middle cerebellar peduncle

Pontine gray

Trigem inal mo tor

nucleus (V)

Reticular formation Decussation of reticular formation fibers

Pontocerebellar fibers (decussation)

Raphe nucle

Medial vermis

CEREBELLUM

Trigeminal nerve fibers (V)

(HEMISPHERE)

Genu of facial nerve fibers (VII) Central gray

rhombencephalic superventricle

(future fourth ventricle)

(VERMIS)

Pontocerebellar fibers

Principal sensory nucleus (V)

Lateral vermis

lateral pool

CEREBELLUM

Medial lemniscus and trapezoid body

Hemisphere

Co ch l (d ear or nu sa cl l) eu s Lateral le mniscus

Proximal nerve V (trigeminal)

Cerebellar germinal trigone

Settling Purkinje cells

Rhombencephalic choroid plexus Co ch l (v ear en nu tra cl l) eus

ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium

3. Stem cells of choroid plexus 2. External germinal layer 1. Auditory NEP

3. Stem cells of choroid plexus 2. External germinal layer 1. Cerebellar NEP

medial pool ar complex

Pontine (midline) G/EP

Reticular tegmental nucleus Anterior extramural migratory stream (pontine gray neurons intermingled with pioneer fibers of the middle cerebellar peduncle)

PONS

Pontine (facial) G/EP Sprouting fibers of hook bundle? Pontine (trigeminal) G/EP

Note that corticofugal fibers are absent in the pontine gray.

Cerebellar G/EP

Trigeminal ganglion (V) Pontine (vestibulocochlear) G/EP

Dashed lines indicate staining and/or sectioning artifacts.

Arrows indicate the presumed direction of axon growth in nerves and fiber tracts.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Ventral rhombic lip (auditory germinal trigone)

Dorsal rhombic lip (cerebellar germinal trigone)

115

GW11 Horizontal CR 57 mm, C1500 Level 15: Section 1805

Levels 14 to 21 are only shown at high magnification.

116

PLATE 50A

PLATE 50B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

G/EP - Glioepithelium/ependyma

Stem cells of choroid plexus

lateral pool leus (dor sal ) lear nuc Coch

Nuclei of the lateral lemniscus Middle cerebellar peduncle

Medial lemniscus Pontocerebellar fibers

fibers (V)? Principal sensory nucleus (V)?

Superior olive complex

Reticular formation Abducens nucleus (VI) Decussation of reticular formation fibers

Genu of facial nerve fibers (VII)

rhombencephalic superventricle

(future fourth ventricle) Premigratory facial motor nucleus (VII) neurons?

Pontocerebellar fibers (decussation)

Reticular tegmental nucleus

Raphe nuclear complex

PONS

Anterior extramural migratory stream (pontine gray neurons intermingled with pioneer fibers of the middle cerebellar peduncle)

Arrows indicate the presumed direction of axon growth in nerves and fiber tracts.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Pontine (midline) G/EP

medial pool

Pontine (facial) G/EP

(BASE OF VERMIS)

Pontine gray

Superior vestibular nucleus

CEREBELLUM

Note that corticofugal fibers are absent in the pontine gray.

te

La

s iscu Trigeminal ner ve

mn

le ral

Inferior cerebellar peduncle

)

Trapezoid body

M RE LUPHE EL IS EBHEM EROF

External germinal layer (cochlear nuclei)

C E AS (B

Rhombencephalic choroid plexus

Pontine (trigeminal) G/EP?

Pontine (vestibular) G/EP

Pontine (cochlear) G/EP

Trigeminal ganglion (V)

Dashed lines indicate staining and/or sectioning artifacts.

Ventral rhombic lip (auditory germinal trigone)

Cerebellar G/EP?

Dorsal rhombic lip? (cerebellar germinal trigone)

117

GW11 Horizontal CR 57 mm, C1500 Level 16: Section 1866

Levels 14 to 21 are only shown at high magnification.

118

PLATE 51A

PLATE 51B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: G/EP - Glioepithelium/ependyma NEP - Neuroepithelium Rhombencephalic choroid plexus

Cochlear nucleus (dorsal)?

lateral pool

Proximal nerve VIII (vestibulocochlear)

Medullary velum

Nerve VII (facial) Spinal tract (V)

Lateral lemniscus Trapezoid body Medial lemniscus

Spinal nucleus (V)

r rio pe ive ex u S ol pl m Reticular formation co

Medial vestibular nucleus Abducens nucleus (VI)

Raphe nuclear complex

Pontocerebellar fibers (decussation)

Pr e nu posit cle us us

Decussation of reticular formation fibers

Pontine gray/arcuate nucleus Pontocerebellar fibers

Genu of facial nerve fibers (VII)

PONS

Facial motor nucleus (VII)

Rhombencephalic choroid plexus

medial pool

Upper medullary (midline) G/EP Upper medullary (prepositus/ vagal/solitary) G/EP

UPPER MEDULLA Nerve VI (abducens)

rhombencephalic superventricle

(future fourth ventricle)

Medullary velum

Upper medullary (vestibular) G/EP Upper medullary (cochlear) G/EP Posterior precerebellar G/EP (source of external cuneate and lateral reticular neurons)

Arrows indicate the presumed direction of axon growth in nerves and fiber tracts.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Anterior precerebellar NEP (source of pontine gray and reticular tegmental neurons) Anterior extramural migratory stream (pontine gray neurons)

Dashed lines indicate staining and/or sectioning artifacts. 119

GW11 Horizontal CR 57 mm, C1500 Level 17: Section 1926

Levels 14 to 21 are only shown at high magnification.

120

PLATE 52A

PLATE 52B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

G/EP - Glioepithelium/ependyma

Spinocerebellar tract fibers Spinal tract (V) Spinal nucleus (V)

Facial motor nucleus (VII)

Decussation of reticular formation fibers

Pr e nu posit cle us us

Nerve VI (abducens)

Reticular formation

L ves ater a nu tibula l cle r us Medial vestibular nucleus

Medial lemniscus Raphe nuclear complex

rhombencephalic superventricle

(future fourth ventricle)

medial pool Medullary velum

Upper medullary (midline) G/EP Upper medullary (prepositus/ vagal/solitary) G/EP

UPPER MEDULLA

Upper medullary (vestibular) G/EP

Posterior precerebellar G/EP (source of external cuneate and lateral reticular neurons)

Premigratory external cuneate and lateral reticular neurons

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Arrows indicate the presumed direction of axon growth in nerves and fiber tracts.

121

GW11 Horizontal CR 57 mm, C1500 Level 18: Section 1962

Levels 14 to 21 are only shown at high magnification.

122

PLATE 53A

PLATE 53B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

G/EP - Glioepithelium/ependyma

Nerve IX (glossopharyngeal) Spinocerebellar tract fibers Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Spinal tract (V) Spinal nucleus (V)

ct ra s y t eu ar cl lit nu So nd a

F nu acia Reticular formation cle l m us ot (V or II)

Medial lemniscus Raphe nuclear complex

MEDULLA

Do r n sa u cle l sen us sor (X y )

Decussation of reticular formation fibers

Inf ves erior nu tibula (?) cle r us

rhombencephalic superventricle

(future fourth ventricle)

medial pool Medullary velum

Medullary (midline) G/EP Medullary (prepositus/ vagal/solitary) G/EP Medullary (vestibular) G/EP

Posterior precerebellar G/EP (source of external cuneate and lateral reticular neurons)

Premigratory external cuneate and lateral reticular neurons

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in nerves and fiber tracts.

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Dashed lines indicate staining and/or sectioning artifacts. 123

GW11 Horizontal CR 57 mm, C1500 Level 19: Section 2202

Levels 14 to 21 are only shown at high magnification.

124

PLATE 54A

PLATE 54B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

G/EP - Glioepithelium/ependyma

Spinal tract (V) Spinocerebellar tract fibers Inferior olive capsule Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Spinal nucleus (V)

Cuneate nucleus Cuneate fasciculus

Solitary tract and nucleus

Reticular formation Decussation of reticular formation fibers

Gracile nucleus

Dorsal motor nucleus (X)

Raphe nuclear complex

Medial lemniscus

Gracile fasciculus

Dorsal sensory nucleus (X) Transition to spinal canal

Hypoglossal nucleus (XII)

Inferior olive complex

Superior ganglion (nerves IX and X)?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

LOWER MEDULLA

Spinomedullary G/EP

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Dashed lines indicate staining and/or sectioning artifacts. 125

GW11 Horizontal CR 57 mm, C1500 Level 20: Section 2322

Levels 14 to 21 are only shown at high magnification.

126

PLATE 55A

PLATE 55B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

G/EP - Glioepithelium/ependyma

Spinal tract (V) Spinocerebellar tract fibers Lateral reticular nucleus Inferior olive capsule

Spinal nucleus (V)

Reticular formation Decussation of medial lemniscus fibers

Posterior extramural migratory stream (external cuneate and lateral reticular neurons cross midline)

Raphe nuclear complex

Cuneate nucleus

External cuneate nucleus Cuneate fasciculus

So a n lita r dn yt u c rac le u t s?

Gracile fasciculus Gracile nucleus

Arcuate fibers

Transition to spinal canal

Medial lemniscus Hypoglossal nucleus (XII)?

Inferior olive complex

LOWER MEDULLA Spinomedullary G/EP

Superior ganglion (nerves IX and X)?

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Inferior ganglion (nerves IX and X)? Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

127

GW11 Horizontal CR 57 mm, C1500 Level 21: Section 2402

Levels 14 to 21 are only shown at high magnification.

128

PLATE 56A

PLATE 56B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

G/EP - Glioepithelium/ependyma

Spinal tract (V) Central and lateral cervical nuclei? Spinocerebellar tract fibers

Raphe nuclear complex

Reticular formation

Spinal nucleus (V)

External cuneate nucleus Cuneate fasciculus

Cuneate nucleus

Decussation of medial lemniscus fibers

Gracile fasciculus Gracile nucleus

Arcuate fibers

Posterior extramural migratory stream (external cuneate neurons cross midline)

Transition to spinal canal

Accessory nucleus (XI) Hypoglossal nucleus (XII)?

Spinomedullary G/EP

LOWER MEDULLA Superior ganglion (nerves IX and X)?

Posterior extramural migratory stream (external cuneate neurons)

Inferior ganglion (nerves IX and X)?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

129

130

PART PARTIV: IV: GW9 GW9 SAGITTAL SAGITTAL

This is specimen number 6658 in the Carnegie Collection, designated here as C6658, a female with a crownrump length (CR) of 40 mm estimated to be at gestational week (GW) 9. The entire fetus was cut in the sagittal plane in 40 µm sections and stained with hematoxylin and eosin. Information on the date of specimen collection, fixative, and embedding medium (appears to be celloidin) was not available to us. The histology is excellent, and this is one of the best preserved specimens in any of the Collections at the National Museum of Health and Medicine. Since there is no photograph of this specimen’s brain before histological processing, a specimen from Hochstetter (1919) that is comparable in age to C6658 is used to show external brain features at GW9 (A, Figure 3). C6658’s brain structures are more difficult to understand because the sections are not cut parallel to the midline; Figure 3 shows the approximate rotations in horizontal (B) and vertical (C) dimensions. Photographs of 11 sections (Levels 1-11) are illustrated at low magnification in four-parts (Plates 57A-D through 67A-D). The A/B parts show the brain in place in the skull; the C/D parts show only the brain (and some peripheral ganglia) at slightly higher magnification. Plates 68-83 show high-magnification views of various parts of the brain at different levels from the cerebral cortex (Plate 68) to the pons and sensory ganglia (Plates 82-83). All of the high-magnification plates are rotated 90˚ (landscape orientation) to more efficiently use page space. C6658 is considerably less mature than the GW11 specimens. Throughout the cerebral cortex, the neuroepithelium is prominent and appears to be without a subventricular zone. The stratified transitional field (STF) contains STF1 and STF5 throughout; with STF4 only in lateral areas. The most prominent developmental feature of the cerebral cortex is that both the STF layers and the cortical plate have a pronounced anterolateral (thicker) to dorsomedial (thinner) maturation gradient. The olfactory bulb is just beginning to evaginate in front of the basal telencephalic neuroepithelium. In anterolateral parts of the cerebral cortex, streams of neurons and glia appear to leave STF4 and enter the lateral migratory stream. The hip-

pocampus contains ammonic and dentate migrations, but there is no evidence of a pyramidal in Ammon’s horn or a dentate gyrus. A massive neuroepithelium/subventricular zone overlies the amygdala, nucleus accumbens, and striatum (caudate and putamen) where neurons (and glia) are being generated. The cerebellum is a thick, smooth plate overlying the posterior pons and medulla, and a definite neuroepithelium at the ventricular surface, indicating some Purkinje cells are still being generated. Many Purkinje cells are sojourning in a dense layer outside the neuroepithelium, and others are migrating upward. Many of the deep neurons are superificial in the cerebellum, but some are migrating downward to intermingle with upwardly migrating Purkinje cells. The cortical surface is partially covered by an external germinal layer (egl) that is actively producing neuronal stem cells, as it grows over the surface of the cerebellar cortex. The third ventricle, aqueduct, and fourth ventricle are lined by thin neuroepithelia. The midbrain tegmentum, pons, and medulla have the thinnest neuroepithelia indicating that only the latest generated neurons are being produced at this time. The thick precerebellar neuroepithelium is an exception in the medulla. Thicker neuroepithelia are in the cerebellum (see above) and midbrain tectum, indicating many neurons are still being generated, although the majority of the neurons in these sites are already postmitotic. The neuroepithelium is still thicker in the hypothalamus and thalamus, in accordance with the later maturation of the diencephalon compared to the rest of the brainstem. Neurons throughout the diencephalon, midbrain tegmentum, pons, and medulla are migrating and settling. Nuclear divisions are very indistinct throughout the diencephalon. More definition is seen in the midbrain tegmentum, pons, and medulla. The large anterior extramural, posterior extramural, and intramural migratory streams are prominent in the medulla and pons.

131

GW9 SAGITTAL

T

C

RA PA

RE

T

E

C

T

R O

f

EL M E B u l l a rLy U v me

elu

d

Trigeminal nerve (V)

S

M E D U

m

Medullary velum

e

N

dge o

CE

NTAL AR EA

RO

AL

LO

BE

E

R

O

Optic nerve (II)

R

Cut

E

HYPOTHALAMUS

rhombencephalic superventricle

L

L

A

Left side

Right side

SP I CO NAL RD

C BACK VIEW B

INFERIOR COLLICULUS

P

P

B

PHAL O N

M

M

LO

PREOPTIC AREA

E TURE T

U

L

DIENC E

FU

T

TA

Sections of C6658's brain are not parallel to the midline either horizontally (-11.71˚, FU top view) or vertically OF T U R E O RBIT (-6.64˚, back view). In each of the illustrated Olfactory bulb sections on the following pages, the anterior edge of the cortex (top right) is tilted away from the observer, while the medulla and upper spinal cord (bottom) are tilted toward the observer.

C

LON HA EP

TE G

LA

ENTUM M

I

U NS

E

MES EN C

E

B

L

R

LOBE

TU

I TA L

E

SUPERIOR COLLICULUS

CIP

L

O N

R

A

M I S P H E H

E

FU

H A L E P

C

N

E

F

OC

EN

B

RE

A

LO

E

E UL

TU

R

L

R E P A R I E TA L L OB

U

A

FUTURE FRON

A perfect sagittal cut through the brain bisects the cerebral cortex into two separate hemispheres by passing through the interhemispheric fissure, and does the same in the brainstem by passing through the midline of the ventricles.

FUTU

Right side

Level

1 (cere bral c ortex) -11.71˚

-6.64˚ Level 6 (br ainstem)

TOP VIEW

Left side

Figure 3. A, Lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 38 mm (modified from Figure 43, Table VII, Hochstetter, 1919) identifies external features of a brain similar to C6658 (CR 40 mm). B, Top view of the brain in A (modified from Figure 45, Table VIII, Hochstetter, 1919) shows how C6658’s sections rotate from a line parallel to the horizontal midline in the interhemispheric fissure. C, Back view of the brain in A (modified from Figure 44, Table VIII, Hochstetter, 1919) shows how C6658’s sections rotate from a line parallel to the vertical midline in the brainstem and upper cervical spinal cord.

132

PLATE 57A

GW9 Sagittal CR 40 mm, C6658 Level 1: Slide 53, Section 1 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

133

PLATE 57B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line) CEREBRAL CORTEX (right hemisphere)

T E L E N

telencephalic superventricle

(future lateral ventricle)

C

E

P

F

H

u

A

t

u

Telencephalic choroid plexus

r

N TEX O COR re) L AL sphe i S B R em MU RE f t h LA HA CE ( l e IT

PONS

Spiral ganglion (VIII) Salivary gland

Superior and inferior ganglia (IX and X)

M ECTU PRET

ha l

ic ur et s hi up rd v

c ep

(f u t

dien

N LO

RHOMBENCE PH C AL (H ERE E

Petrous temporal bone

M BEL IS PH LU ER M E)

N O

ble

TE

UM CT

di

MES EN TE GM

HYPOTHALAMUS

d

Eustachian tube?

Tongue

an

oi

LAMUS

PHA CE

a

IC PT EOREA R P A preoptic recess

TUM EN

M

l

pro cess l ca vity

n

e

O ra

Nasal cavity

Sph

M a x i Pal a ta l l

N LO A H EP C EN SUB DI THA

n e b o

Olfactory epithelium

THALAMUS

l t a i e a r

UM N PT O SE L

E NC EPH A

p

Frontal bone

e

TE

L

E

e

P

Diencephalic choroid plexus

Nerve I (olfactory)

Frontonasal process

le r ic nt ) ve icle r e ntr

Rhombencephalic choroid plexus

Squa

mou

s occip

bo it al

ne

rhombencephalic superventricle

(future fourth ventricle)

Atlas spinal process?

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

134

PLATE 57C

GW9 Sagittal CR 40 mm, C6658 Level 1: Slide 53, Section 1

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

M id lin e

e sid t e gh id Ri tf s Le

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

135

PLATE 57D

Cortical (paracentral) NEP Cortical (parietal) NEP Layer I Cortical plate STF1 t1 STF5

Cortical (posterior cingulate) NEP

Interhemispheric fissure

Cortical layers less prominent

ing an d thala mic ne ur

rs

Cortical (occipital) NEP Habenulo-interpeduncular tract?

Settling thalamic neurons

Strionuclear

M

Anterior complex

Medial septal nucleus

ECTU

Cortical (anterior cingulate) NEP

Dorsal complex?

Ventral complex?

Bed nucleus of the NEP stria terminalis

PR ET

Cortical (frontal) NEP

Sojo u rn

Do

Septal NEP

Cortical plate absent plex com

Anterior thalamic NEP

Tenia tecta

H ab

ar ul

Cortical layers more prominent

EP i c N ng a m igrati l a m s th on al

en

Fo rn ix

Epithalamic NEP

Superior colliculus

Forel's fields

Migrating preoptic neurons

Medial forebrain bundle

Preoptic NEP

Settling hypothalamic neurons

Optic chiasm Subpial GEP (optic chiasm)

Mammillary body

Su bs n ig ta n t r a ia

Optic tract Lateral lemniscus Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) sory nucleus (V) en ular Vestib omplex rc nuclea

Spiral ganglion (VIII)

Inferior cerebellar peduncle

Inferior colliculus

Lateral lemniscus

Superior cerebellar peduncle Premigratory deep neurons

Migrating Purkinje cells External germinal layer Sojourning Purkinje cells

Temporal bone labyrinth

Cerebellar germinal trigone (in dorsal rhombic lip)

Superior and inferior ganglia (IX and X)

Cerebellar NEP Choroid plexus stem cells

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Reticular formation

Nucleus of the lateral lemniscus

Princip al s

Temporal bone labyrinth

Central gray

Precerebellar NEP (in ventral rhombic lip)

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

136

PLATE 58A

GW9 Sagittal CR 40 mm, C6658 Level 2: Slide 63, Section 1 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

137

PLATE 58B Skull and skin Meninges (dura and arachnoid)

R

R

C

e

A

H

ECTUM

T

P

PR

MESE NC TEG

LAMUS SUBTHA

C U M

O

T

HALON EP

ENCEP MB HA P O N S

E

DIE NC E

T

ET

L SA LT

Pineal gland

n e b o

e tur (fu

R HO

N E

E

BA

l t a i e a r

pineal recess

L

n um col l a r teb ver l ic a erv

N

p

tal bone C E

u

r

Fron

F

ic hal e cep tricrlicle) n e di rven vent d e sup thir

ER UPP LLA U MED

? one id b Hyo

e? vicl Cla

Squa

C

(future lateral ventricle)

NTUM ME

le

occipital

ib

O

Pituitary gland (anterior part)

B a s al

d

O

HYPOTHALAMUS

Sella turcica

Tongue

n

telencephalic superventricle

u

t ic op cess re

d oi

a

X

t

N IC PT EO EA PR AR

Olfactory nerve (I)

a

ro

LO

M

l

on men of m

E EL

SE PT UM

Sphe n

pro cess l ca v ity

E

L

US M A AL L TH

fora

HA

O ra

A

Brain surface (pia, heavier line)

"Blooming" telencephalic choroid plexus*

Nasal cavity

M a x i Pal a ta l l

T

DORSAL HIPPOCAMPUS

EP NC

OLFACTORY BULB olfactory recess Frontonasal Olfactory epithelium process

R

N

E

(future lateral ventricle)

H

P

E

B

telencephalic superventricle

L

A

O

C

N

CEREBELLUM

bo mou s occipit al

(HEMISPHERE)

ne

rhombencephalic superventricle

(future fourth ventricle)

"Budding" rhombencephalic choroid plexus*

Atlas spinal process?

Axis spinal process?

*The sagittal plane of sectioning is ideal to show the difference between the growth dynamics of the telencephalic and rhombencephalic choroid plexuses. At GW9, the telencephalic choroid plexus is greatly expanded ("blooming") but the rhombencephalic choroid plexus is still small ("budding"). The rhombencephalic choroid plexus "blooms" during the second and third trimesters (see Volumes 3 and 2). FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

138

PLATE 58C

GW9 Sagittal CR 40 mm, C6658 Level 2: Slide 63, Section 1

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES See a high magnification view of the midbrain tectum in Plates 78A and B.

de t si h g Ri ft Le

ine

dl Mi

s id

e

BRAINSTEM FLEXURES

4

2

2. Pontine 3. Mesencephalic 4. Diencephalic

3

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

139

PLATE 58D

Cortical (paracentral) NEP

Cortical (parietal) NEP

Layer I Cortical plate STF1 t1 STF5 DORSAL HIPPOCAMPUS

Cortical layers less prominent

Fornical GEP Cortical (dentate) NEP

Ammonic migration

Cortical (hippocampal) NEP

Cortical (occipital) NEP Fornix

Cortical layers more prominent

Cortical plate absent Habenular complex Habenulo-interpeduncular tract

Settling thalamic neurons

ting igras m nd uron ga nin mic ne r u o Soj thala ic lam tha l a r t P Ven NE Anterior thalamic NEP

Olfactory nerve (I)

Pr

Subpial migration in basal telencephalon

eo

Optic tract Subpial GEP (optic tract)

p

tic

Hy p

NE

o

P

Subthalamic

ic N lam tha

Fornix Interpeduncular nucleus?

Reticular formation

P ECTU Central gray

Central gray

Substantia nigra

Central gray

Reticular formation

Superior colliculus

Superior colliculus

Reticular formation

Parabrachial nucleus? Pontine NEP

Superior cerebellar peduncle

Inferior colliculus

Superior cerebellar peduncle

er P Upp r y N E ulla m ed

Spinal nucleus (V)?

M

l NE ecta Red nucleus

Superior olive? Facial motor nucleus (VII)?

Posterior commissure

Mesencephalic NEP

Mammillary body

Hypothalamic NEP

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

NEP

EP

ng r a ti mig ns nd neuro a g nin mic our ala Soj ypoth h

Pituitary gland (anterior part)

Pret

EA AR

Pineal gland

PR ET

IC PT EO PR

Epithalamic NEP

Anterior complex

Lateral septal nucleus

Olfactory bulb NEP

Dorsal complex?

Stria medullaris

Strionuclear NEP Cortical Bed nucleus of the (frontal) stria terminalis NEP Septal NEP

Mesencephalic NEP

Descending deep neurons

Sprouting fibers of hook bundle?

External germinal layer Migrating Purkinje cells Sojourning Purkinje cells Cerebellar NEP

Cerebellar germinal trigone (in dorsal rhombic lip) Choroid plexus stem cells

Inferior cerebellar peduncle

Precerebellar NEP (in ventral rhombic lip)

Posterior extramural migratory stream (external cuneate and lateral reticular neurons) FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

140

PLATE 59A

GW9 Sagittal CR 40 mm, C6658 Level 3: Slide 67, Section 1 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

141

PLATE 59B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

R

B

A

L

O

N

R

H

P

E

t

L

u

al bone

F

N

E

C

DORSAL HIPPOCAMPUS "Blooming" telencephalic choroid plexus

E

HAL N O

R HO

Sella turcica

MB E N C E P P O N S

rhombencephalic superventricle

(future fourth ventricle)

UPPER MEDULLA

Inferior ganglia (X)?

S qu

Foramen magnum

us a mo

HA

b o n e

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

mammillary recess

LO

CER

N

cal rvi

n lu m o c ral te b ver

LO HA N EP

a g li an g t roo al ors

Basal occipital

? one id b Hyo

Pharynx

C

UM

Pituitary gland

Epiglottis

Ce

infundibular recess

Anterior part Intraglandular cleft Intermediate part

a

Tongue

D

d lic hir haure t p ME ce fut en ( i T E G M SEN d

NT

Sphenoid

(future aqueduct)

E

l

C

HYPOTHALAMUS

Nasal cavity

ta l pro cess O ra l ca v ity

D

IE

N

mesencephalic superventricle

le ic tr n ) ve cle erntri p e su v

T E C T U M

IC PT EO PR AREA

optic recess

M a x i l Pal a

A H

P E

ont Fr

T BA

CE P

t a l i e a r

L TEL EN SA

N

p

SEPTUM

L

O

e

BASAL GANGLIA

Olfactory nerve (I)

Frontonasal process

THALAMUS

r

olfactory recess

u

foramen of monro

OLFACTORY BULB

Clavicle?

telencephalic superventricle (future lateral ventricle)

C

E

(future lateral ventricle)

Mandible

A

E

telencephalic superventricle

T E X C O R

L

aqueduct

(HE EBEL MIS PHELUM RE)

o cc

ip

lb it a

on

e

"Budding" rhombencephalic choroid plexus

142

PLATE 59C

GW9 Sagittal CR 40 mm, C6658, Level 3: Slide 67, Section 1 NEUROEPITHELIAL/ GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

ine idl M

See a high-magnification view of the hypothalamus and basal telencephalon in Plates 70A and B to 71A and B. e sid t gh e Ri sid t ef ine L idl M

BRAINSTEM FLEXURES

4

2

See a high-magnification view of the midbrain in Plates 77A and B. 3

2. Pontine 3. Mesencephalic 4. Diencephalic

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

143

PLATE 59D Cortical (paracentral) NEP Cortical (parietal) NEP Layer I Cortical plate STF1 t1 STF5 DORSAL HIPPOCAMPUS Cortical layers less prominent

Fornical GEP Cortical (dentate) NEP

Ammonic migration

Cortical (hippocampal) NEP

Choroid plexus stem cells

Cortical layers more prominent

Cortical (occipital) NEP

Anteromedial ganglionic NEP and SVZ

Dorsal complex?

Fornix

Cortical plate absent Habenular complex Habenulo-interpeduncular tract

Th ala mo Stria cor medullaris tica l fi ber Anterior complex s

ng ati gr s i d m ron an neu g in ic rn am jou thal o S

Cortical (frontal) NEP

Epithalamic NEP

Reticular nucleus?

Septal NEP Lateral septal nucleus

Olfactory bulb NEP

Posterior commissure Subcommissural organ

Ventral thalamic NEP

M

in g

sup erior col

licul us

ne uro

ns

ns

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

uro

P NE

Spinal nucleus (V)?

ne

y llar du Me

Solitary nucleus and tract

Sprouting fibers of hook bundle?

tl r colliculu s

Inferior colliculus

Superior cerebellar peduncle

Vestibular complex

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ior colliculus) NE P

Pontine NEP

Reticular formation

et

p er

Reticular formation

perio

l Superior cerebellar peduncle

al hi s ac eu br cl ra nu Pa

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Reticular formation

su

(s u

Mammillary body

Oculomotor nuclear complex (III)

Centra gray

Pituitary gland

Substantia nigra

EP N l) l t a e n tr a C ray g

Optic tract

Subpial GEP (optic tract)

Posterior Intermediate

g

li c ha

n

Interpeduncular nucleus

Anterior

d s R e le u c nu

Hypothalamic NEP

Preoptic NEP

S

at

Thalamic c (tegm (reticular) NEP? ali e ph Strionuclear NEP ce n e s e M

Olfactory nerve (I) Subpial migration in basal telencephalon Migrating preoptic neurons

i

g Mes e nc r ep

Anterior thalamic NEP

in

Anterior commissure Bed nucleus of the stria terminalis

Olfactory bulb

Pineal gland

GEP (posterior commissure)

Mesencephalic (inferior colliculus) NEP

Premigratory deep neurons Descending deep neurons External germinal layer

Migrating Purkinje cells Sojourning Purkinje cells Cerebellar NEP

Cerebellar germinal trigone (in dorsal rhombic lip) Choroid plexus stem cells

Vestibular complex

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Precerebellar NEP (in ventral rhombic lip)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

144

PLATE 60A

GW9 Sagittal, CR 40 mm, C6658 Level 4: Slide 71, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

145

PLATE 60B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

B

A

R

(future lateral ventricle)

R

H

P

E

E

C"Blooming" telencephalic

O

ri

N

E

DORSAL HIPPOCAMPUS

et al

L

diencephalic superventricle

E

EPITHALAMUS

mesencephalic superventricle

la

m

ic

T

THALAMUS

H

O

RH

m

ic po /ep o l it ) ha

L

O

Foramen magnum Atlas

LON

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

ISTH MUS

INFERIOR COLLICULUS

N

E

PH L L U M ER E)

(future fourth ventricle)

a g li an C3 g ot l ro rsa n C4 o D um col C5 l ra Axis te b ver C6 l a C3 c rvi C4 Ce C5

A

rhombencephalic superventricle

Axis

C6

P O N S

PH

UPPER MEDULLA

Cricoid cartilage Thyroid gland

BENCE

HA

Pituitary gland

M

EP

(fut

N

C

Larynx

Pha ryn x

s lotti Epig

Hyoid bone

a lic cep h ic l e dienrvenvterntricle) e d thir su p ure

Intermediate part Intraglandular cleft Anterior part

SE

(

Mandible

mi ala oth hyp pool

tal l occipi Basa

Oropharynx

T E G M

EB C E R MIS HE

Tongue

ME

U M N T

cavity

US LAM HA T O YP c

Sella turcica

y

O ra l

ess

v it ca al

a x Na i l l a s Palata l proc

MUS

SUPERIOR COLLICULUS

E

optic recess

(future aqueduct)

C T U T E M

Sphenoid

LA

la

L

PREOPTIC AREA

HA

ha

BT

(t

SU

BASAL T E ON OLFACTORY AL E BULB N C E PH

ne

olfactory recess

BASAL GANGLIA

bo

al bone ont r F

N

pa

C

L

choroid plexus

Nasal conchae

Clavicle?

A

(future third ventricle)

Frontonasal process

M

telencephalic superventricle

re

(future lateral ventricle)

X

tu

telencephalic superventricle

E

Fu

E

L

T

R

O

C

LOWER MEDULLA

S qu

am

o

o us

c ci

p

o lb it a

ne

"Budding" rhombencephalic choroid plexus

146

PLATE 60C

GW9 Sagittal, CR 40 mm, C6658 Level 4: Slide 71, Section 2 NEUROEPITHELIAL/ GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

ine idl M

ide ts h g e Ri sid t ef ine L idl M

BRAINSTEM FLEXURES

4

2

See a high-magnification view of the cerebellum in Plates 79A and B. 3

2. Pontine 3. Mesencephalic 4. Diencephalic

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

147

PLATE 60D Cortical (paracentral) NEP

Cortical (parietal) NEP

Layer I Cortical plate STF1 t1 STF5

DORSAL HIPPOCAMPUS

Cortical layers less prominent

Fornical GEP Cortical (dentate) NEP

Ammonic migration

Cortical (hippocampal) NEP

Cortical (occipital) NEP Strionuclear NEP

Fornix

Basal telencephalic NEP

So

M

id

dl

ic N E P e hy thalam po

Abducens nucleus (VI)?

Inferior olive

P ary NE Medull

Reticular formation

Trochlear nucleus (IV)

Pontine NEP

Superior cerebellar peduncle

Sprouting fibers of hook bundle?

Inferior colliculus Premigratory deep neurons Descending deep neurons External germinal layer

Migrating Purkinje cells Sojourning Purkinje cells Cerebellar NEP

Vestibular nuclear complex

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

ha lic

Reticular formation

Reticular formation

Medial lemniscus?

Cerebellar germinal trigone (in dorsal rhombic lip)

Choroid plexus stem cells

Solitary nucleus and tract

Spinal tract (V) Spinal nucleus (V)

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

mammillary recess

PONS

Incipient pontine gray Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Raphe nuclear complex?

tal) NEP

Optic tract Arcuate nucleus Pituitary gland

Mesence p

Interpeduncular nucleus Ventral tegmental area

Posterior hypothalamic NEP

Supbial GEP (optic tract)

Posterior commissure

Epithalamic NEP

NEP ntal) gme (te Central gray

P NE ic m a al bth Su

Preoptic NEP

GEP (posterior commissure)

uperior collic g s u l us in neu ttl ron g supe r i or colli Se s cu atin l u s cephalic igr M sen ( t e neuro n s e c

Olfactory nerve (I) Subpial migration in basal telencephalon Migrating preoptic neurons

Habenular complex Habenulo-interpeduncular tract

M

Bed nucleus of the stria terminalis

Olfactory bulb NEP

Cortical plate absent

EP

Cortical (frontal) NEP

jo u th r n in al g am a ic n d Th ne m i al ur gr am o n a ti ic s ng N

Stria medullaris Th al am Dorsal oc Anterior or complex? tic complex al fib er s Mammillothalamic Central tract? complex?

r r io ? ste ex Po mpl co

Cortical layers more prominent

Anteromedial ganglionic NEP and SVZ

Precerebellar NEP (in ventral rhombic lip)

Cuneate nucleus Cuneate fasciculus

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

148

PLATE 61A

GW9 Sagittal, CR 40 mm, C6658 Level 5: Slide 75, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

149

PLATE 61B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

O

C L

A

R B E

E L E

L A

EPITHALAMUS

AL

TH

N

C N

S U B T ALAMU H

S

ME

T E

N

G

I

n lum co l ra C5 eb ert v l ica rv Ce

F

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

UPPER MEDULLA

CE

Inferior colliculus

CEREBELLUM

(LATERAL VERMIS)

rhombencephalic superventricle

(future fourth ventricle)

LOWER MEDULLA

S q ua

C3

C4

C6

N MBE

L ON PHA

Foramen magnum

M

yn x

n lum Axis co l ra b rte C3 ve al c i v r C4 Ce RD C5 O C C6 L Axis NA

LON

Atlas

HO

R

l occipita

Ph ar

Larynx

B a s al

Oropharynx

Clavicle?

HA

x ryn

o tti s Epigl

SP

P O N S

ha

Mandible

EP

rc i c a

C

ll a

tu

op

Tongue

N T U M

Se

s Na

Palatal process O ral cavity

E

HYPOTHALAMUS

Pituitary gland M a x i l (anterior part) l a

(future aqueduct)

SE

M

E D I

mesencephalic superventricle

PRETECTUM

E

PH

(future third ventricle)

AM

o r c o lli c u l u s peri Su T E C T U

LO

T

bone tal n ro

diencephalic superventricle

ne

A

IC PT O EA E R PR A

bo

C EPH

al

EN

ie t

TE L

US

ar

BA SA L

OLFACTORY BULB?

Frontonasal process

Hyoid bone

p re

BASAL GANGLIA

N

tu

O

N

DORSAL HIPPOCAMPUS

Sphenoid

Trachea

O

"Blooming" telencephalic choroid plexus

(future lateral ventricle)

Thyroid gland

A Fu

R

H

L

C E

(future lateral ventricle)

P

E

C

N

telencephalic superventricle

telencephalic superventricle

E X R T

m

c so u o

ne bo l ita cip

"Budding" rhombencephalic choroid plexus

150

PLATE 61C

GW9 Sagittal, CR 40 mm, C6658 Level 5: Slide 75, Section 2 NEUROEPITHELIAL/ GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

ine idl M

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages. ide ts h g e Ri sid t f e ine L idl M

BRAINSTEM FLEXURES

See a highmagnification view of the brainstem in Plates 80A and B.

4 2 1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

1

3

151 Cortical (paracentral) NEP

PLATE 61D

Cortical (parietal) NEP

Layer I Cortical plate STF1 t1 STF5 DORSAL HIPPOCAMPUS Cortical layers less prominent

Fornical GEP Cortical (dentate) NEP

Ammonic migration

Anteromedial ganglionic NEP and SVZ Cortical layers more prominent

Cortical (hippocampal) NEP

Strionuclear NEP

Thalamocortical fibers Dorsal complex?

GEP (posterior commissure)

Posterior commissure

Migrating pretectal neurons Central complex?

enc

Medial forebrain bundle?

ha

Dorsomedial nucleus?

Incipient pontine gray Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Reticular formation Medial longitudinal fasciculus

Central gray

Reticular tegmental nucleus

tine N E P on

Medial lemniscus?

Reticular formation

Prepositus nucleus

Cerebellar NEP

Reticular formation

P

Solitary nucleus and tract

External germinal layer Migrating Purkinje cells

NE

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Descending deep neurons Sprouting fibers of hook bundle?

y

Inferior olive Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Premigratory deep neurons

Medulla r

Inferior olive fibrous capsule

Inferior colliculus

Superior cerebellar peduncle

P

Pontomedullary trench

l) NE P

Pituitary gland

Central gray

cta

Ventral Mammillary tegmental area body Ventromedial Middle Oculomotor nuclear nucleus? Hypothalamic complex (III)? NEP

t e g m e n t a l ) NE l ic ( P

Optic tract

ep

Interpeduncular nucleus

e ri o r c o lli c u l u s n e u g su p ro ns t l in S et s u p e r i o r c o l l i c u l u s ne ur tin g o ns

Subpial migration in basal telencephalon Migrating preoptic neurons

Pretectal NEP

sen c e p halic ( t e

Forel's fields

P NE

Me

ic m la a Th

g ra Mi

Olfactory bulb?

Stria terminalis Reticular nucleus

Habenulo-interpeduncular tract Habenular complex

Me s

S in ubs no ta m nt in ia at a

Be st d n ri uc a le te u rm s in of t al he is

Basal telencephalic NEP

Cortical (occipital) NEP

Cortical plate absent r r io ? ste ex Po mpl co

Cortical (frontal) NEP

Olfactory NEP

Lateral geniculate/ pulvinar migration

Fornix

Sojourning Purkinje cells Cerebellar germinal trigone (in dorsal rhombic lip)

Choroid plexus stem cells

Ventral rhombic lip

Cuneate fasciculus Cuneate nucleus

White matter (lateral funiculus)

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

152

PLATE 62A

GW9 Sagittal, CR 40 mm, C6658 Level 6: Slide 79, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

153

PLATE 62B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line) C

A

L

"Blooming" telencephalic choroid plexus

R

E

E

H

p re tu

C

L

Fu

O

E

(future lateral ventricle)

P

E

C

N

B

R

L

A

telencephalic superventricle

T E X O R

E

H

BTH

ALAMUS

IT

M

E

S N

CE

Fr on

M

ch ea

s gu ha

Tr a

l na ca l

LON

n

al

co

m lu

RD O C AL N I

CEREBELLUM

"Budding" rhombencephalic choroid plexus

O H LOWER MEDULLA

N

(LATERAL VERMIS)

M

B

N

HA CEP

O

ior

SP

a

l co

op

e lv

UPPER MEDULLA

l Basal occipita

nx /es

ca

E

m

R

P ha ry

Ce

i rv

rt

r eb

h ist

L Infelriculus

d

Larynx

Cricoid cartilage

P O N S

A

i Orophar ynx

tis Epiglot

PH

o

e Hyoid bone?

Thyroid cartilage

Thyroid gland

r y nx

u

s ty vi ca

av ic l e

g

es

Cl

d ib u la rp roc ess

n

oc

M

an

Or al

p ha Naso

pr

T o

ISTHMUS

Superio r c o T E C llicu lu TU M s

E

n

M a x i l l a Palatal

Sup T E C erior TU c M o

lus

DI

EP

U

bon e ?

e

a ti c

SU

MEN HYPOTEG T THALAMUS

h

gom

(future aqueduct)

cu

p

Zy

E THALAMUS

lli

S

C

N C EPHA

EN

LE

N LO

PTIC PREOEA AR

Eyelid Neural layer of retina Intraretinal space Pigment layer of retina Sclera

TE

mesencephalic superventricle

AL AM US PRETE CT UM

T e bon l ta

BASAL

LON

e

EYE

A PH

n bo

BASAL GANGLIA

al iet

DORSAL HIPPOCAMPUS

ar

(future lateral ventricle)

N

telencephalic superventricle

Sq

u

so ou am

cc

ip

e on lb a it

rhombencephalic superventricle

(future fourth ventricle)

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

154

PLATE 62C

GW9 Sagittal, CR 40 mm, C6658 Level 6: Slide 79, Section 2 NEUROEPITHELIAL/ GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a highmagnification view of the diencephalon and midbrain in Plates 76A and B. ine idl M

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

R ine idl M

t igh

sid

e

e sid t f Le

BRAINSTEM FLEXURES 4 2 1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

1

3

155

PLATE 62D

Cortical (parietal) NEP Layer I Cortical plate STF1 t1 STF5

Cortical (paracentral) NEP DORSAL HIPPOCAMPUS Fornical GEP Cortical (dentate) NEP

Choroid plexus stem cells

Cortical (hippocampal) NEP

Anterolateral ganglionic NEP and SVZ Cortical layers more prominent

Cortical (occipital) NEP

Lateral geniculate/ pulvinar migration

Fornix

Cortical plate absent

GEP (internal capsule) Strionuclear NEP

Internal capsule

Stria medullaris

Reticular nucleus

Habenular complex

Ventral complex?

M

rs? b e Be d l fi s a tr i o n u c fug a t f t h le co er e us rti o m c in Anterior rly a li Ea s commissure

Cortical layers less prominent

Ammonic migration

TU

ET

EC

Mi

PR

Cortical (frontal) NEP

Se

at

Pretectal NEP

tt li ng in s g su p

u collic lus neuro ns or ri or colliculus n eur pe ri ons

P

i n P o n t

e

Midline raphe glial system

N E P

Cerebellar NEP Dorsal rhombic lip Choroid plexus stem cells

NE

Inferior olive

Migrating Purkinje cells Sojourning Purkinje cells

ary

Vestibular nuclear complex

Premigratory deep neurons External germinal layer

Medull

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Inferior olive fibrous capsule

l) NE

Reticular formation

r erio s Inf iculu l col

Medial lemniscus?

)N EP

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

en c ep

Raphe nuclear complex

Midline raphe GEP?

hali c (te cta

Mammillary Substantia body nigra/ ventral tegmental area

e

M es

Ventromedial nucleus

phalic (tegmen Mesence t al

gray Central

Lateral olfactory tract

gr

u

Basal P NE Su telencephalon ic Central inn bsta om ntia complex? lam ina a ta Th Primary HabenuloLa Forel's fields ter interpeduncular olfactory al p tract reo cortex pti c/h ypo Intertha Red peduncular lam nucleus? ic a nucleus? Optic tract rea s

P

Posterior extramural migratory stream (external cuneate and lateral reticular neurons) Reticular formation

Ventral rhombic lip

Cuneate fasciculus

Ventral gray Ventral white matter

Cuneate nucleus

Dorsal white columns Dorsal gray (substantia gelatinosa) Intermediate gray

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

156

PLATE 63A

GW9 Sagittal, CR 40 mm, C6658 Level 7: Slide 83, Section 1 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

157

PLATE 63B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line) T E X O R

C

L

A

R

B

H

A

L

"Blooming" telencephalic choroid plexus

R

E

E

(future lateral ventricle)

P

E

C

N

telencephalic superventricle

p re tu

L

C

E

Fu

O

E

C

N

PRETE CT UM

HA

T

l na ca

l

a

n Ph ar yn

x

s gu ha op /es

Ce

r

c vi

SP

al

ve

rt

r eb

AL IN

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

al

c

u ol

R CO

D

HO

M

BE

ON

"Budding" rhombencephalic choroid plexus

LOWER MEDULLA

it

e on lb

a

R

m

Cricoid cartilage

EP

L HA

LO

Larynx

NC

hm

ior fer lus In icu l M l co LLU EBEMIS) CER(VER

Oropharynx

Thyroid cartilage

ist

N

Superio T r co E C T llicu U M lus

T

EP

Hyoid bone?

UPPER MEDULLA

l Basal occipita

M

av ic l e

TEGMEN

UM

en o i d sph Eustachian tube

Oral cavity

Cl

M

AMUS

P O N S

Palatal process

d ib u la rp roc ess

HAL

ISTHMUS

x i l l a M a

an

BT

Sup er T E C ior T U co M

lus

DI

SU

H THA YPOLAM US

Nerve II (optic)

(future aqueduct)

THALAMUS

cu

bito-

EN

O

ENCEPH

mesencephalic superventricle

lli

Or

EL

E

LON

C EN ES

Vitreous body Lens Eyelid Neural layer of retina Intraretinal space Pigment layer of retina Sclera

AL

A PH

e

bone tal n o Fr

n bo

BASAL GANGLIA BASAL T

al iet

EYE

DORSAL HIPPOCAMPUS

ar

(future lateral ventricle)

N

telencephalic superventricle

Sq

u

so ou am

cc

ip

rhombencephalic superventricle

(future fourth ventricle)

158

PLATE 63C

GW9 Sagittal, CR 40 mm, C6658 Level 7: Slide 83, Section 1 NEUROEPITHELIAL/ GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the lateral forebrain in Plates 73A and B.

M

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages. R id M

e lin

t igh

id

lin

e

BRAINSTEM FLEXURES

de

si

L

e ft

sid

e

4 2

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

1

3

159 Cortical (paracentral) NEP

PLATE 63D

Cortical (parietal) NEP

Layer I Cortical plate STF1 t1 STF5 DORSAL HIPPOCAMPUS

Choroid plexus stem cells

Cortical layers less prominent

Fornical GEP Fornix Cortical (dentate) NEP

Anterolateral ganglionic NEP and SVZ

Ammonic migration

Cortical (occipital) NEP

Cortical (hippocampal) NEP

Cortical layers more prominent Cortical plate absent

ers? gal fib ofu tic or c Stria r ly terminalis Ea

Su inn bstan om tia ina ta

thalamic neurons

Reticular nucleus

ling ett s on

Ventral complex?

For e l's fiel ds

Medial forebrain bundle

Optic tract

or

Mesencephalic (tectal) NEP

t t li n

Isthmal NEP

Superior

co colliculus lli cu ri o lu (right) rc s oll icu lu sn eu

d se

ntin

E e N

Reticular formation

u pe

e ri

Superior colliculus (left)

P

External germinal layer

Inferior olive (right) Raphe nuclear complex

Migrating Purkinje cells Sojourning Purkinje cells

Cerebellar germinal trigone (in dorsal rhombic lip) Choroid plexus stem cells

N E P

Inferior olive fibrous capsule Dorsal motor nucleus (X) Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Cerebellar NEP

Medu l l a ry

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

up

g su p. c o l l. n eur ons

Medial longitudinal fasciculus

Abducens nucleus (VI)

Pretectal NEP

ng s

ior s fer lu In llicu co

Medial lemniscus?

d Re eus? cl nu

/ nigra tantia ental Subtsral tegm area ven

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Migrat i

Migrating an

Ventromedial nucleus Mammillary body

Set tlin gs

Migrating an ds pretecta ln eu r

(mainly thalamocortical fibers)

Central gray

Cortical (frontal) NEP

Internal capsule

Mesencephalic (tegmen t a l) N EP

Primary olfactory cortex

Strionuclear GEP Migrating and settling

s s on ron ur ne

Lateral olfactory tract

Globus pallidus

Stria medullaris

Po

Anterior commissure

GEP (internal capsule)

Medullary velum

Inferior olive (left)

Ventral rhombic lip Reticular formation

Gracile fasciculus Gracile nucleus

Ventral gray

Cuneate nucleus Cuneate fasciculus

Ventral white matter Dorsal white columns Dorsal gray (substantia gelatinosa) Intermediate gray

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

160

PLATE 64A

GW9 Sagittal, CR 40 mm, C6658 Level 8: Slide 95, Section 1 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

161

PLATE 64B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

L

A

(future lateral ventricle)

H

A

E

L

E

pa

N

ure Fut

L

"Blooming" telencephalic choroid plexus

O

C E

P

E

R

E

C

N

B

R

telencephalic superventricle

R T E X C O

rie

T

bone tal n o

THALAMUS

L

E

NC

E P H ALON

DIENCEPHALON

Fr

BE

EP

L NA I P

RD O C

ON

HO

M

NC

L HA

n m

S

br

N

rv

l

te

lu

M

Ce

a ic

r ve

co al

ulus U

CEREBELLUM

(LATERAL VERMIS)

R

Clavic le

llic r co T

Spiral ganglion (VIII, bordering temporal bone labyrinth)

C

Basal occipital

d ib u la rp roc ess

rio

Eustachian tube?

L O feriorlus In llicu co

Petrous temporal bone

UPPER MEDULLA

M

an

ISTHMUS

P O N S

Facial ganglion (VII)?

Meckel's cartilage

HA

Orbito-sphenoid

E

EP

TUM

Proximal

Distal

T

N C

E

SE

N

Nerve V (trigeminal) Trigeminal ganglion (V)

ME

pe

TE GM

PRETECTUM

Su

AMYGDALA

Vitreous body Lens Eyelid Neural layer of retina Intraretinal space Pigment layer of retina Sclera

e

TE

on

L

lb

BA S A

ta

EYE

L RSA US DO CAMP O P HIP

B A S A L G A N G L I A

LOWER MEDULLA

Sq

u

so ou am

ip cc

mesencephalic superventricle (future aqueduct)

? ne bo l it a

"Budding" rhombencephalic choroid plexus

rhombencephalic superventricle

(future fourth ventricle)

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

162

PLATE 64C

GW9 Sagittal, CR 40 mm, C6658 Level 8: Slide 95, Section 1 NEUROEPITHELIAL/ GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the hippocampus and thalamus in Plates 72A and B.

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

BRAINSTEM FLEXURES 4 3 2

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

1

163 Layer I Cortical plate STF1 t1 STF4? STF5

PLATE 64D

Cortical (parietal) NEP

Cortical (paracentral) NEP Choroid plexus stem cells

Cortical layers more prominent

DORSAL HIPPOCAMPUS

Ganglionic NEP and SVZ

Corticoganglionic NEP and SVZ Anterolateral

Ammonic migration

Posterior

Cortical (dorsal hippocampal) NEP

Migrating and setling striatal neurons

Cortical (frontal) NEP

Ca

External capsule

Primary olfactory cortex

Fornical GEP Cortical (dentate) NEP Fimbria/fornix

ud

Cortical layers less prominent a te

Lateral geniculate body/pulvinar

Putamen

Lateral olfactory tract

Reticular nucleus

Globus pallidus Substantia innominata

Thin-bundled corticopetal fibers Thick-bundled corticopetal fibers

Posterior complex

Migrating amygdaloid neurons

lli c u

ur lus ne

Trigeminal ganglion (V)

Trochlea nucleus (I r V)

Distal trigeminal nerve (V)

Reticular formation

tine NE P

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Medial lemniscus? Inferior olive fibrous capsule

Mesencephalic

Inferior (tectal) NEP colliculus

Sprouting fibers of hook bundle?

Medullary

) us (V ucle al n Spin

Spiral ganglion (VIII, bordering temporal bone labyrinth)

Superior cerebellar peduncle

Pon

Petrous temporal bone

Facial ganglion (VII)?

u s n e u r o n sons

Proximal trigeminal nerve (V)

Central gray

Superior colliculus

licul

Trigeminal motor nucleus (V) intermingled with principal sensory nucleus (V)

Mesencephalic (tegmental) NEP

gs u

col

Cortical (ventral hippocampal) NEP

Subs ta

a nigra nti

Amygdalo-hippocampal area?

tlin

r co rior rio upe pe gs tin ra ig M

Amygdaloid NEP and SVZ

Internal capsule

Set

Setling pretectal neurons

Setling thalamic neurons Optic tract

Vestibular nuclear complex

Cerebellar NEP

Premigratory deep neurons Descending deep neurons External germinal layer Migrating Purkinje cells Sojourning Purkinje cells Cerebellar germinal trigone (in dorsal rhombic lip)

Choroid plexus stem cells

NEP

Inferior olive Solitary nucleus?

Medullary velum

Posterior extramural migratory stream (external cuneate and lateral reticular neurons) Reticular formation

Ventral rhombic lip

Vestibular nuclear complex Ventral gray

Spinal nucleus (V)?

Ventral white matter SP

AL IN

RD CO

Dorsal white columns Intermediate gray Dorsal gray (substantia gelatinosa)

Lateral white matter

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

164

PLATE 65A

GW9 Sagittal, CR 40 mm, C6658 Level 9: Slide 99, Section 1 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

165

PLATE 65B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

R

T E

L

PU

S

pa

AL

OC

AM

DIENCEPHALON

PP HI

THALAMUS

Sup

M

LO

US

Fr o

n

HO

Basal occipital m

R

u

l

c

LOWER MEDULLA

P

(future aqueduct)

"Budding" rhombencephalic choroid plexus

rhombencephalic superventricle

(future fourth ventricle)

li a

l

t

l

mesencephalic superventricle

g

v

a

er

a

E

Inferior colliculus

n

er

ic

v

eb

r

o

NC

CEREBELLUM

(LATERAL VERMIS)

M

BE

Petrous temporal bone

H

AL

N

ON

ulus

U

M

Eustachian tube?

UPPER MEDULLA

Vestibular ganglion (VIII)

Meckel's cartilage

C

T

M

TH

HA

TU

IS

P O N S

Spiral ganglion (VIII, bordering temporal bone labyrinth)

llic

EN

Orbito-sphenoid

EP

M

Nerve V (trigeminal, proximal)

or

E

C

G

Trigeminal ganglion (V)

N

eri

C

TE

SE

T

co

ME

e

AMYGDALA

on

P H ALON

lb

CE

ta

N

rie

LE

bone? al nt

ure Fut

B A S A L G A N G L I A TE

EYE

Vitreous body Eyelid Neural layer of retina Intraretinal space Pigment layer of retina Sclera

N

BA S

L

"Blooming" telencephalic choroid plexus

O

C E R

E

(future lateral ventricle)

C E P H A

N

E

B

C O R T E X

L

A

telencephalic superventricle

o

t

g

a

ro al br e al t s er D o r l v ica v r Ce

l co

um

n

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

166

PLATE 65C

GW9 Sagittal, CR 40 mm, C6658 Level 9: Slide 99, Section 1

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the pons and medulla in Plates 81A and B. See high-magnification views of the pons, medulla, and sensory ganglia from the opposite side of the brain in Plates 82A and B to 83A and B.

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

167

PLATE 65D Layer I Cortical plate STF1 t1 STF4? STF5

Cortical (paracentral) NEP Cortical (parietal) NEP

Cortical layers more prominent Corticostriatal NEP and SVZ

Lateral migratory stream (flows out of STF4?)

Cortical layers less prominent Posterior ganglionic NEP and SVZ

Insular gyrus

ate ud Ca

Primary olfactory cortex

Putamen

DORSAL HIPPOCAMPUS Cortical (dorsal hippocampal) NEP

Lateral olfactory tract

Thick-bundled corticopetal fibers

Ammonic migration Fimbria/fornix

Globus pallidus?

ia nt ta ta a bs in Su nom in

Thin-bundled corticopetal fibers

Cortical (temporal) NEP

Migrating and setling striatal neurons

External capsule

Internal capsule

Fornical GEP

Settling

THALAMUS

VENTRAL HIPPOCAMPUS

Migrating amygdaloid neurons

Mi

g ra

r

c

Superior colliculus

ul us

l.

neu

s on ur ne

Central gray

io

lic

supe rior co l

us

Mesencephalic (tegmental/isthmal) NEP

rons

cle nu lic ha cep ? eus ru l coe

)? (V

Trigeminal ganglion (V)

Parabrachial nucleus

Vestibular ganglion (VIII)

Reticular formation

Po

Inferior colliculus

P ntine NE

n

u cl

eu s

Premigratory deep neurons Descending deep neurons External germinal layer Migrating Purkinje cells Sojourning Purkinje cells Cerebellar germinal trigone (in dorsal rhombic lip)

Sprouting fibers of hook bundle?

Cerebellar NEP

Choroid plexus stem cells

(V

u l l a r y e d

al

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Mesencephalic (tectal) NEP

Superior cerebellar peduncle

M

lar tibu r Ves uclea x n ple com

in Sp

Petrous temporal bone

Spiral ganglion (VIII, bordering temporal bone labyrinth)

sen

Proximal trigeminal nerve (V)

cus

Principal sensory nucleus (V)

Me

Entorhinal cortex

Trigeminal nerve (V) boundary cap

Lo

Cortical (ventral hippocampal) NEP

er

ol

Amygdaloid NEP and SVZ

ging

sup

) Solitary nucleus and tract

N E P

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Medullary velum Ventral rhombic lip

Reticular formation

External cuneate nucleus Cuneate nucleus Cuneate fasciculus Spinal nucleus (V) FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

168

PLATE 66A

GW9 Sagittal, CR 40 mm, C6658 Level 10: Slide 103, Section 1 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

169

PLATE 66B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

R

E P H A L N C O E

C E R

E

B

C O R T E X

L

A

(future lateral ventricle)

N

BASAL GANGLIA

rie

M

P PO CA M

HI

T

er

io

a ot

g

ro b l rte sa r ve l Do ica rv Ce

a

n

g

o lc ra

lu

ON AL

H

P

(HEMISPHERE)

(future aqueduct)

Inferior colliculus

Rhombencephalic choroid plexus

M

BE

CEREBELLUM

mesencephalic superventricle

Squamous temporal bone?

R

rhombencephalic superventricle

(future fourth ventricle)

li

a

a

NC

E

HO

n m

l

u

e

ic

er

r

o

M LOW E D ULER LA

C

rv

l

v

b te

l

c

S U

Basal occipital

Inferior ganglia (X)?

? M

Superior and inferior ganglia (IX)?

M

R PE LA UP DUL ME

Nerve IX (glossopharyngeal)?

Middle ear ossicles?

TU

TH

Facial ganglion (VII)?

Eustachian tube?

EN

IS

P O N S

Meckel's cartilage

T

M

Nerve VIII (vestibulocochlear)

li

G

Vestibular ganglion (VIII)

Spiral ganglion (VIII, bordering temporal bone labyrinth)

C

TE

Petrous temporal bone

Trigeminal ganglion (V)

ol

E

c

N ALO P Hc u l u s U M

r

E

AMYGDALA

Vitreous body Eyelid Neural layer of retina Intraretinal space Pigment layer of retina Sclera

E E SSu p N C

e

P H ALON

S PU

on

LE

Orbito-sphenoid

CE

lb

TE

EYE

N

ta

AL

pa

BA S

ure Fut

T

E

L

telencephalic superventricle

m

n Superior ganglion (X)?

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

170

PLATE 66C

GW9 Sagittal, CR 40 mm, C6658 Level 10: Slide 103, Section 1

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See high-magnification views of the pons, medulla, and sensory ganglia from the opposite side of the brain in Plates 82A and B to 83A and B.

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

171

PLATE 66D Cortical (paracentral) NEP

Layer I Cortical plate STF1 t1 STF4? STF5

Cortical layers more prominent Cortical (parietal) NEP

Cortical layers less prominent Lateral migratory stream?

Insular gyrus Primary olfactory cortex

External capsule

Caudate

Cortical (hippocampal) NEP Migrating amygdaloid neurons

Superior colliculus

Me sen cep

Internal capsule

Putamen

tia tan ta bs ina Su nom in

Thick-bundled corticopetal fibers

Posterior ganglionic NEP and SVZ

Migrating and setling striatal neurons

Lateral olfactory tract

Thin-bundled corticopetal fibers

Cortical (temporal) NEP

ha

Amygdaloid NEP and SVZ

nu cle

Cochlear nuclei?

Vestibular ganglion (VIII)

Central gray Inferior colliculus

l l

Reticular formation

Mesencephalic (tectal) NEP

Sprouting fibers of hook bundle?

(V)

Nerve IX (glossopharyngeal)?

Reticular formation

Precerebellar NEP Medullary NEP

Superior and inferior ganglia (IX)?

us cle l nu ina Sp

Petrous temporal bone

Migrating and settling inferior colliculus neurons

Superior cerebellar peduncle?

Pontine NEP

Spiral ganglion (VIII, bordering temporal bone labyrinth)

Inferior ganglia (X)?

tera

)? (V

La

us

Cortical (parahippocampal) NEP Nerve V (trigeminal) Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Nucleus of the lateral lemniscus? Nerve VIII (vestibulocochlear) emniscus Trigeminal ganglion (V) Distal trigeminal nerve (V)

Migrating and settling superior colliculus neurons

lic

Entorhinal cortex

Cerebellar NEP

Premigratory deep neurons Descending deep neurons External germinal layer Migrating Purkinje cells Sojourning Purkinje cells Cerebellar germinal trigone (in dorsal rhombic lip) Choroid plexus stem cells

Medullary velum Ventral rhombic lip

Posterior extramural migratory stream? (external cuneate and lateral reticular neurons) Superior ganglion (X)?

Area postrema? Posterior intramural migratory stream? (inferior olive neurons)

Spinal nucleus (V)?

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

172

PLATE 67A

GW9 Sagittal, CR 40 mm, C6658 Level 11: Slide 105, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

173

PLATE 67B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

E

C E P H A L E N

C

E

R

L

O

bo

telencephalic superventricle

ne

E P H L ON A

(future lateral ventricle)

er

LON HA us EPr collicul

ESEN M Sup C

AMYGDALA

Vitreous body Eyelid Neural layer of retina Intraretinal space Pigment layer of retina Sclera

al

TE

NC

iet

AL

BASAL GANGLIA

ar

S BA

C TU S U

BE

Eustachian tube?

n m

l

u

C

v er

ic

a

e

AL Rhombencephalic choroid plexus

r

a

l

c

o

Squamous temporal bone?

M LOW ED E U LLR A

Basal occipital

mesencephalic superventricle

(HEMISPHERE)

RH

Superior and inferior ganglia (IX)?

b

N

CE

Inferior colliculus

CEREBELLUM (future aqueduct)

OM

Meckel's cartilage

PH

R PE LA UP DUL ME

Menckel's cartilage

v

M

M

P O N S

Facial ganglion (VII)?

l

TH

Spiral ganglion (VIII, bordering temporal bone labyrinth)

e rt

io

TE

IS

Petrous temporal bone

Vestibular ganglion (VIII) Nerve VIII (vestibulocochlear)

ON

EYE

LE

Orbito-sphenoid

ep tur Fu

T

N

E

C O R T E X

L R A

B

rhombencephalic superventricle

(future fourth ventricle)

Superior ganglion (X)? Dorsal root ganglion

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

174

PLATE 67C

GW9 Sagittal, CR 40 mm, C6658 Level 11: Slide 105, Section 2

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See high-magnification views of the pons, medulla, and sensory ganglia from the opposite side of the brain in Plates 82A and B to 83A and B.

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

175

PLATE 67D Cortical (paracentral) NEP

Layer I Cortical plate STF1 t1 STF4? STF5

Cortical layers more prominent Cortical (parietal) NEP

Cortical layers less prominent Lateral migratory stream (exits from STF4?)

Corticostriatal NEP and SVZ

External capsule

Internal capsule (thin-bundled corticopetal fibers)

ate?

Putamen

Lateral olfactory tract

Posterior ganglionic NEP and SVZ

C aud

Primary olfactory cortex

Cortical (temporal) NEP

Migrating and settling striatal neurons Migrating amygdaloid neurons

Amygdaloid NEP and SVZ

Entorhinal cortex Migrating and settling superior colliculus neurons

Cortical (parahippocampal) NEP Nuclei of the lateral lemniscus

Superior colliculus Migrating and settling inferior colliculus neurons

Inferior cerebellar peduncle Cochlear nuclei? Nerve VIII (vestibulocochlear)

Facial ganglion (VII)?

PONS Petrous temporal bone

Sprouting fibers of hook bundle?

x mple ar co nucle ular Vestib n matio lar for

Superior and inferior ganglia (IX)? Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Posterior intramural migratory stream? (inferior olive neurons) Posterior extramural migratory stream? (external cuneate and lateral reticular neurons)

Reticular formation

Pontine NEP

Reticu

Spiral ganglion (VIII, bordering temporal bone labyrinth)

al s ter scu La m ni le

Vestibular nuclear complex

Vestibular ganglion (VIII)

Cerebellar NEP

Inferior colliculus

Mesencephalic (tectal) NEP

Premigratory deep neurons Descending deep neurons External germinal layer Migrating Purkinje cells Sojourning Purkinje cells Cerebellar germinal trigone (in dorsal rhombic lip) Choroid plexus stem cells

Medullary velum Anterior Posterior

Precerebellar NEP

(in ventral rhombic lip)

Dorsal root ganglion

Spinal nucleus (V)

Superior ganglion (X)?

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

GW9 Sagittal CR 40 mm, C6658 Level 4: Slide 71, Section 2 DORSAL CORTEX

See the entire section in Plates 60A-D.

176

PLATE 68A

Pia

PLATE 68B

Layer I contains Cajal-Retzius cells settled near the pia.

The cortical plate contains settling neurons, mainly those in future layer VI and some in layer VII that have not yet migrated downward into the subplate. The subplate contains neurons that originally resided in the cortical plate. Stratified transitional field (STF) 1 contains migrating neurons, mainly those that will settle in cortical layer VI. STF1 is in the early t1 stage when cells are plentiful among the fibers.

STF 5 contains sojourning neurons, mainly those that will settle in cortical layers V and VI.

Pia meninx cells

Layer I

Cajal Retzius cells

Cortical plate

Settling neurons

Layer VII (subplate)

Delaminating subplate neurons

STF1 t1

Migrating neurons

Sojourning neurons

STF5 Blood vessel

The cortical neuroepithelium (NEP) is a pseudostratified layer of neural stem cells. Arrows indicate mitotic figures. The majority are at the ventricular surface, where nuclei migrate to divide within the tall and thin columnar cytoplasm. At this stage of development, large numbers of cortical neurons are being generated.

Blood vessel Proliferating neural stem cells

Cortical NEP

Mitotic zone Neural stem cells in mitotic division at the border of the telencephalic superventricle

177

GW9 Sagittal CR 40 mm, C6658 Between Levels 7 and 8: Slide 91, Section 1 DORSAL HIPPOCAMPUS

See a low-magnification view of Level 7 in Plates 63A-D, Level 8 in Plates 64A-D.

178

PLATE 69A

PLATE 69B

Cortical (hippocampal ammonic) neuroepithelium (NEP)

telencephalic superventricle (future lateral ventricle)

Periventricular mitotic cells Periventricular mitotic cells

Ammonic migration (pyramidal cells)

Cortical (hippocampal dentate) NEP

Cortical (subiculum) NEP

Dentate migration (mainly early-generated granule cells?) Fornix

Early-generated neurons in the stratum oriens and stratum radiatum of future Ammon's horn

Future subiculum

Pia membrane

Fornical glioepithelium

Stratified transitional field (STF) 5

Mitotic cells Dentate migration (mainly granule cell precursors?) Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

179

GW9 Sagittal CR 40 mm, C6658 Level 3: Slide 67, Section 1 OLFACTORY BULB AND SEPTUM

See the entire section in Plates 59A-D.

180

PLATE 70A

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Trajectory of successive waves of migrating septal neurons

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field

La ter -g en e

ra

Septal NEP

telencephalic superventricle

te d

d an

al sep g later n i l t t e s rla t e

tal

n

l uc

s eu

ro n neu

s

SEPTUM

Early-generated and early-settling lateral septal nucleus neurons

BASAL TELENCEPHALON

(anterior pool, future lateral ventricle)

Basal telencephalic NEP (presumptive source of mitral cells)

Diagonal band of Broca (vertical limb)?

olfactory recess

Presumptive trajectory of subpial migrating neurons from olfactory areas toward hypothalamus

Cortical (olfactory) NEP

PREOPTIC AREA

PLATE 70B

Cortical (orbitofrontal) NEP

ORBITOFRONTAL CORTEX STF 5 STF1 t1 Cortical plate Layer I

Presumptive trajectory of migrating mitral cells into the olfactory bulb Olfactory nerve (1)

OLFACTORY BULB

Subpial GEP?

Trajectory of successive waves of migrating olfactory bulb interneurons

181

182

PLATE 71A

GW9 Sagittal CR 40 mm, C6658 Level 3: Slide 67, Section 1 PREOPTIC AREA AND ANTERIOR HYPOTHALAMUS

See the entire section in Plates 59A-D.

PLATE 71B MEDIAL PREOPTIC AREA

Anterior hypothalamic area

Anterior hypothalamic NEP

diencephalic superventricle

Settling medial preoptic area neurons

Trajectories of migrating medial preoptic neurons

(future third ventricle, hypothalamic part)

Settling anterior hypothalamic area neurons

Trajectory of migrating hypothalamic neurons Middle hypothalamic NEP

Settling medial preoptic area neurons Trajectory of migrating hypothalamic neurons

ANTERIOR HYPOTHALAMUS Preoptic NEP

infundibular recess optic recess

Optic tract

MEDIAL us BASAL e l uc HYPOTHALAMUS n ate cu r A

Subpial GEP? ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Subpial GEP? (optic tract)

Anterior part (pars distalis)

PITUITARY GLAND

Intraglandular cleft Intermediate part

183

184

PLATE 72A

GW9 Sagittal CR 40 mm, C6658 Level 8: Slide 95, Section 1 HIPPOCAMPUS AND THALAMUS

See the entire section in Plates 64A-D.

185

PLATE 72B

Ammonic migration

Cortical (hippocampal ammonic) NEP

Early-generated neurons in the stratum oriens and stratum radiatum of future Ammon's horn

Expanded telencephalic choroid plexus

DORSAL HIPPOCAMPUS a

s

?

Reticular nucleus

m

e

d

Fornix

Cortical (hippocampal dentate) NEP

l

i

u

l

r

Lateral geniculate/pulvinar

r

i

a

Dentate migration

S

t

Choroid plexus stem cells

Reticular nucleus

Fornical GEP

LATERAL THALAMUS Subpial GEP

Lateral geniculate/pulvinar

Migrating amygdaloid neurons Settling amygdaloid neurons

Reticular nucleus

x rni Fo

Dentate migration

nix For

Fornical GEP

Cortical (hippocampal dentate) NEP

VENTRAL HIPPOCAMPUS

s de ) va body n i t ( te racicula t c ti en O p ral g e la t Subpial GEP (optic tract)

Cortical (hippocampal ammonic) NEP

Amygdaloid NEP

AMYGDALA Ammonic migration Amygdalohippocampal area?

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

telencephalic superventricle (future lateral ventricle, amygdalo-hippocampal narrows)

GW9 Sagittal CR 40 mm, C6658 Level 7: Slide 83, Section 1 LATERAL FOREBRAIN

See the entire section in Plates 63A-D.

186

PLATE 73A

PLATE 73B Expanded telencephalic choroid plexus

telencephalic superventricle (future lateral ventricle)

Dorsal hippocampus

Lateral geniculate/pulvinar migration Stria medullaris

Anterolateral ganglionic NEP and SVZ

al

er

s?

ha

rt Ea

rly

co

Internal capsule

lam

ocort cal rad i

BASAL GANGLIA

io

Thalamic axons enter internal capsule

Reticular nucleus

Internal capsule

Globus pallidus

Ventral complex? Habenulointerpeduncular tract

SUBTHALAMUS (Forel's fields)

Ventral striatum La

M

Primary olfactory cortex

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Ventral complex?

(compact region of fused bundles in "cortical funnel")

Putamen

Substantia innominata Lateral olfactory tract

t ia

(diffuse region)

Anterior commissure Anterior commissure

THALAMUS

Reticular nucleus

Stria terminalis

n

ug

b fi

Strionuclear GEP

ic

of

GEP (internal capsule)

T

Cortical (orbitofrontal) NEP

Dorsal complex?

Caudate?

PRETECTUM

Migrating ganglionic neurons

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Optic tract

ter

ed

al hyp otha ia lamic area l f or eb ra in bu ndl e

HYPOTHALAMUS Ventromedial nucleus?

Mammillary body

di Me

al

for

e

bu in a br

nd

le

r ula nc u d s Substantia nigra/ pe leu ter uc ventral tegmental area In n

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

187

GW9 Sagittal CR 40 mm, C6658 Between Levels 7 and 8: Slide 87, Section 1 LATERAL FOREBRAIN

See a low-magnification view of Level 7 in Plates 63A-D, Level 8 in Plates 64A-D.

188

PLATE 74A

PLATE 74B

DORSAL HIPPOCAMPUS

Fornical GEP Expanded telencephalic choroid plexus

telencephalic superventricle (future lateral ventricle)

Cortical (hippocampal dentate) NEP Cortical (hippocampal ammonic) NEP Ammonic migration Dentate migration Lateral geniculate/pulvinar migration

Anterolateral ganglionic NEP and SVZ

Migrating ganglionic neurons

Caudate

Cortical (orbitofrontal) NEP

Th

Internal capsule (diffuse region)

Early

Putamen

BASAL GANGLIA

ala

moc

ortical radia

tio

Thalamic axons enter internal capsule

n

(com Inte pact r bund nal ca les in p cortic "cor sule ofuga tical funn l fibe el") rs

Ventral complex?

Reticular nucleus

Globus pallidus Exte r

na

lc

Lateral olfactory tract

PRETECTUM

e ns ul xo aps a l lc ica a rt tern o C in r te n e

GEP (internal capsule) Strionuclear GEP Stria terminalis

THALAMUS

Central complex?

Central complex?

Ventral striatum ap

s u le

Anterior commissure

Subs

Basal nucleus of Meynert?

tan

tia

BASAL TELENCEPHALON

inno

minata

Primary olfactory cortex Arrows indicate the ABBREVIATIONS: presumed direction of GEP - Glioepithelium neuron migration from NEP - Neuroepithelium SVZ - Subventricular zone neuroepithelial sources.

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

SUBTHALAMUS

Lateral hypothalamus?

Optic

Incipient cerebral peduncle

tract

Substantia nigra

Subthalamic nucleus

189

190

PLATE 75A

GW9 Sagittal CR 40 mm, C6658 Level 8: Slide 95, Section 1 LATERAL FOREBRAIN

See a low-magnification view of Level 8 in Plates 64A-D.

PLATE 75B

Layer I Cortical plate STF1 t1 STF4 t1 STF5

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

telencephalic superventricle (future lateral ventricle)

DORSAL HIPPOCAMPUS

Expanded telencephalic choroid plexus

Cortical (hippocampal ammonic) NEP

Ammonic migration Dentate migration Cortical (hippocampal dentate) NEP

Posterior ganglionic NEP and SVZ

Fornical GEP Fo rn ix

Migrating ganglionic neurons Cortical (frontal) NEP

Posterior complex

Caudate

THALAMUS

Internal capsule (diffuse region)

BASAL GANGLIA Putamen

Optic tract

Anterior Amygdaloid NEP and SVZ amygdaloid AMYGarea

te rn

al

Ventral striatum ca psu le

Substantia ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Globus pallidus

Migrating amygdaloid neurons

Reticular nucleus

Ex

Lateral olfactory tract

(compact bundles in "cortical funnel")

rnix ria/fo Fimb

Diffuse bundles of early corticofugal axons enter internal capsule

Primary olfactory cortex

Internal capsule

Thalamocortical radiation

Choroid plexus stem cells

BASAL TELENCEPHALON

innom

DALA

inat a telencephalic superventricle

(future lateral ventricle, amygdalo-hippocampal narrows)

VENTRAL HIPPOCAMPUS Amygdalohippocampal area?

191

GW9 Sagittal CR 40 mm C6658 Level 5: Slide 79, Section 2 DIENCEPHALON AND MIDBRAIN

See a low-magnification view of Level 5 in Plates 61A-D.

192

PLATE 76A

telencephalic superventricle

ix rn Fo

(future lateral ventricle)

Stria medullaris

Fornical GEP

Late

pu late/ enicu r al g

lvin a

ia tio n

THALAMUS

ad

Strionuclear NEP and GEP

MIDBRAIN TECTUM

Habenular complex

Posterior complex

Choroid plexus stem cells

Superior colliculus

n r migratio

UM

Expanded telencephalic choroid plexus

r

Ventral Thalamic axons enter internal capsule complex?

Thalamic NEP

(compact bundles in "cortical funnel")

Supra m

Raphe nuclear complex

Anterior extramural migratory stream

(contains pontine gray and reticular tegmental neurons)

PONS Reticular formation

Raphe nuclear complex

a l fasciculus?

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Ventromedial nucleus

Midline raphe glial system

e

udin

Optic tract

Ventral tegmental area

Raphe nuclear complex

git

HYPOTHALAMUS

Mammillary body

ular unc d e p s r Inte nucleu

on l l

l nd

ia

as

m bu ala oth in p a y br L a t e r al p re o ptic a n d h ore f l ia Med illary a r e a m am PREOPTIC

AREA

Pontine NEP

193

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

e ar

ed

ic

Substantia innominata

MIDBRAIN TEGMENTUM

t

BASAL TELENCEPHALON

Red nucleus

trac

SUBTHALAMUS (Forel's fields)

ular

Red nucleus

ay gr

Central complex?

M

Reticular nucleus

Mesencephalic (tegmental) NEP

Oculomotor nuclear complex (III)

edunc

Bed nucleus of the stria terminalis

mesencephalic superventricle

al ntr Ce

Internal capsule

Pretectal NEP (future cerebral aqueduct)

ul o - i n t e r p

Stria terminalis

a

o

al

ben

l T ha

c mo

c r ti

Ha

GEP (internal capsule)

Mesencephalic (tectal) NEP

PRETEC T

PLATE 76B

GW9 Sagittal CR 40 mm, C6658 Level 3: Slide 67, Section 1 MIDBRAIN

See a low-magnification view of Level 3 in Plates 59A-D.

194

PLATE 77A

PLATE 77B c o l l i c u l u s

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Successive waves of migrating and settling superior colliculus neurons

MIDBRAIN TECTUM

Subcommissural organ Posterior commissure Pineal gland

(future cerebral aqueduct)

In

Migrating and settling inferior colliculus neurons

External germinal layer Premigratory deep neurons

i

Central gray

lus

ray

Parabrachial nucleus

g ral

nt

Ce

gi

tudinal f a s c ic

ulu

CEREBELLUM

s

(future third ventricle)

ed

Oculomotor nuclear complex (III)

M

diencephalic superventricle

ia

l

lo

n

GEP (posterior commissure)

r coll

(future cerebral aqueduct)

rio

mesencephalic superventricle

fe

Mesencephalic (superior colliculus) NEP

pineal recess

Epithalamic NEP

mesencephalic superventricle

MIDBRAIN TECTUM

Mesencephalic (posterior tegmental) NEP

(third ventricle)

Mesencephalic (inferior colluculus) NEP

cu

r r i o e p S u

MIDBRAIN TEGMENTUM

Superior cerebellar peduncle

Descending deep neurons

Superior cerebellar peduncle

THALAMUS

ral g

Mesencephalic (anterior tegmental) NEP

C en t

Thalamic NEP

ray

Reticular formation

ain br e r l fo le? dia und e M b Ventral tegmental area/ Substantia nigra

Reticular formation

PONS

Pontine NEP Migrating Purkinje cells Sojourning Purkinje cells Sprouting fibers of hook bundle?

195

Cerebellar NEP

MIDBRAIN TECTUM

See a low-magnification view of Level 2 in Plates 58A-D.

196

PLATE 78A GW9 Sagittal CR 40 mm, C6658 Level 2: Slide 63, Section 1

PLATE 78B Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Pineal gland

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

i o r r p e u S Posterior commissure

Optic nerve layer? Superficial gray layers Middle gray layers Deep white layers Deep gray layers?

c o l l i c u l u s

Successive waves of migrating and settling superior colliculus neurons

MIDBRAIN TECTUM

pineal recess (third ventricle)

Migrating glial cells? GEP (posterior commissure)

Central gray Mesencephalic (superior colluculus) NEP

P

diencephalic superventricle

R

(future third ventricle)

E T

Central gray

C

U

T

Migrating pretectal neurons?

E

Pretectal NEP

M

197

GW9 Sagittal CR 40 mm, C6658 Level 4: Slide 71, Section 2 CEREBELLUM

See a low-magnification view of Level 4 in Plates 60A-D.

198

PLATE 79A

PLATE 79B

Mesencephalic (inferior colliculus) NEP

Inferior colliculus

Nerve IV (trochlear)? S

Mesencephalic (tegmental) NEP

u

p

er i p or ed u cer n e cl b e el

2. External germinal layer Cerebellar germinal trigone (in

la

2

r

1

Superior cerebellar peduncle

M

e

ng s di n en ro sc neu De ep de

Several trajectories of migrating Purkinje cells

d

ia l ng

i n j e

lo

it

3

3. Choroid plexus stem cells

ciculus l fas

r u

P

ina

k

1. Cerebellar NEP

g n i n l u r o j nd S o u b k

e

ud

CEREBELLUM (HEMISPHERE)

rhombencephalic superventricle

(future fourth ventricle)

of Sprouting fi bers

ho

o

rhombencephalic superventricle

(future fourth ventricle)

Rhombencephalic choroid plexus

199

Pontine NEP

dorsal rhombic lip)

Premigratory deep neurons

c e l l s

Trochlear nucleus (IV)

Migrating and proliferating external germinal layer cells

NEP - neuroepithelium Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

GW9 Sagittal, CR 40 mm, C6658 Level 5: Slide 75, Section 2 PONS/MEDULLA

See a low-magnification view of Level 5 in Plates 61A-D.

200

PLATE 80A

PLATE 80B

NEP - neuroepithelium

E N

la

ry

rhombencephalic superventricle

l

N

ul

)

(future fourth ventricle)

a

er

r

m

EP

y NE

Pontomedullary trench

P

p Up

Raphe nuclear complex

Po

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

in

er eti

Raphe nuclear complex cu

la r

Incipient pontine gray

te g m

e n ta

d

itu pos Pre

Posterior intramural migratory stream (inferior olive neurons) Reticular formation

UPPER MEDULLA

l nucl

eu s

Reticular formation

li

or

o

Medial longitudinal fasciculus

PONS nt

e

ll

P N E ucleus sn

ri

Midline raphe glial system (provides structural support for brainstem flexures)

er

m

u

y ar

fe

ne nti Po us ul ic sc

Area of mesencephalic flexure

LOWER MEDULLA

L

fa

Reticular formation

Solitary nucleus and tract

ed

ta

l o n g l git ial ud d e in M a l

MIDBRAIN TEGMENTUM

Cune ate fa scicu lus Cun eate nucl eus

w

C e n t r a

en

o

cephalic (teg m

ve

fi

br

a s c ou

Reticular formation psu

le

Inferior olive Area of medullary flexure

In

Me

n se

P

Ventral rhombic lip

Medial lemniscus?

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Area of pontine flexure

201

GW9 Sagittal CR 40 mm, C6658 Level 9: Slide 99, Section 1 PONS/MEDULLA

See a low-magnification view of Level 9 in Plates 65A-D.

202

PLATE 81A

Locus coeruleus?

ISTHMUS

Reticular formation

NEP - neuroepithelium

Sojourning Purkinje cells Sprouting fibers of hook bundle

Superior cerebellar peduncle

CEREBELLUM

Cerebellar NEP

Rh o ch mbe oro nc id eph ple ali xu c s

PLATE 81B

Cerebellar notch Isthmal NEP

Medullary velum

rhombencephalic superventricle

(future fourth ventricle)

Pontine NEP Pontomedullary trench

PONS

Trigeminal ganglion (V)

Pro xim a ner l trige ve ( min V) al

MEDULLA

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Posterior intramural migratory stream (inferior olive neurons) Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Cuneate nucleus Cuneate fasciculus? External cuneate nucleus

us

Trigeminal nerve (V) boundary cap

Reticular formation

Solitary nuc Solitary t leus rac t

ventral rhombic lip

cle nu al ) ud (V

Central trigeminal nerve (V) fibers

Oral nucleus (V)

ted ola p r e Int

) s (V u e l nuc

Lower medullary NEP

Ca

Pri nci nuc pal se leus nsor (V) y

r ibula Vest clear nu plex com

Upper medullary NEP

Spinal nucleus (V)

203

204

PLATE 82A

GW9 Sagittal CR 40 mm, C6658 Between Levels 9 and 10: Slide 101, Section 1 PONS, MEDULLA, AND SENSORY GANGLIA

See low-magnification views of Level 9 in Plates 65A-D, Level 10 in Plates 66A-D.

205 rhombencephalic superventricle

PLATE 82B

(future fourth ventricle)

Reticular formation

Pontine neuroepithelium (NEP)

Vestibular nuclear complex

Pontomedullary trench

Vestibular nuclear complex

UPPER MEDULLA

Reticular formation

PONS

Principal sensory nucleus (V) Sparse interspersed glia

Upper medullary NEP

Oral nucleus (V)

Nucleus of the lateral lemniscus Central trigeminal nerve (V) fibers Trigeminal nerve (V) boundary cap

Lateral lemniscus Trajectory of vestibular and auditory fiber growth Proximal trigeminal ner nervvee (V)

Trajectory of trigeminal fiber growth

Dense interspersed glia (Schwann cells)

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Spiral ganglion (VIII)

Petrous temporal bone

Future Organ of Corti

Trigeminal ganglion (V)

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Future vestibular part of the temporal bone labyrinth?

Distal trigeminal nerve (V)

Dense interspersed glia

GW9 Sagittal CR 40 mm, C6658 Between Levels 10 and 11: Slide 104, Section 1 PONS AND SENSORY GANGLIA

See low-magnification views of Level 10 in Plates 66A-D, Level 11 in Plates 67A-D.

206

PLATE 83A

PLATE 83B Inferior cerebellar peduncle

PONS

Central glossopharyngeal nerve (IX) fibers (sparse glia) Central vestibulocochlear nerve (VIII) fibers (sparse glia) Glossopharyngeal nerve (IX) boundary cap

L

a

te

ra

l

le

mn

isc

Cochlear nucleus?

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Nerve (IX, dense interspersed glia)

us

Superior ganglion (IX)

Vestibulocochlear nerve (VIII) boundary cap Vestibulocochlear nerve (VIII, dense interspersed glia, Schwann cells)

Petrous temporal bone Vestibular ganglion (VIII)

Basal occipital bone

Auditory branch (nerve VIII) Spiral ganglion (VIII)

Trigeminal ganglion (V)

Future vestibular part of the temporal bone labyrinth?

Future Organ of Corti

Inferior ganglion (IX)

Vagal ganglion (X)?

207

208

PART PARTV: V: GW9 GW9 HORIZONTAL HORIZONTAL This is specimen number 886 in the Carnegie Collection, designated here as C886. A normal fetus with a crownrump length (CR) of 43 mm was collected in 1914 after a hysterectomy due to pelvic inflammation. The fetus is estimated to be at gestational week (GW) 9. The entire fetus was fixed in Bouin’s, embedded in celloidin, and 100 µm sections were cut in a plane midway between the horizontal and coronal planes (Figure 4). Because many of the sections do not contain the cerebral cortex and the brainstem is cut in a crosswise direction, it more closely resembles a horizontally sectioned brain. All sections were stained with hematoxylin and eosin. Since there is no photograph of C886’s brain before it was embedded and cut, a specimen from Hochstetter (1919) is used to show the external features of the brain at GW9 (Figure 4). Levels 1-11, generally larger sections containing the cerebral hemispheres, are shown at low magnification in Plates 84A/B93A/B. The core parts of the sections in Levels 3-11 are also shown at high magnification in Plates 85C/D-93C/D. Levels 12-19, generally smaller sections containing only the brainstem, are shown at a high magnification in Plates 94A/B-101A/B. To more efficiently use page space, all plates are in landscape orientation (anterior/ventral: left side of photograph, bottom of page; posterior/dorsal: right side of photograph, top of page). C886 is similar to C6658 in the level of brain maturation. The chief reason for including this specimen is to provide a different perspective for viewing brain structure at GW9. In the cerebral cortex, the neuroepithelium is prominent as the sole germinal matrix; the stratified transitional field (STF) consists of STF1, STF5, and STF4 only in lateral areas. The anterolateral (thicker) to dorsomedial (thinner) maturation gradient in the cortical plate and STF layers are evident. In anterolateral parts of the cerebral cortex, streams of neurons and glia appear to leave STF4 and enter the lateral migratory stream. The hippocampus contains ammonic and dentate migrations, but there is no evidence of a pyramidal in Ammon’s horn or a dentate gyrus. A massive neuroepithelium/subventricular zone overlies the amygdala, nucleus accumbens, and stria-

tum (caudate and putamen) where neurons (and glia) are being generated. The cerebellum is a thick, smooth plate overlying the posterior pons and medulla, and a definite neuroepithelium at the ventricular surface, indicating some Purkinje cells are still being generated. Many Purkinje cells are sojourning in a dense layer outside the neuroepithelium, and others are migrating upward. Many of the deep neurons are superificial in the cerebellum, but some are migrating downward to intermingle with upwardly migrating Purkinje cells. The cortical surface is partially covered by an external germinal layer (egl) that is actively producing neuronal stem cells, as it grows over the surface of the cerebellar cortex. The third ventricle, aqueduct, and fourth ventricle are lined by thin neuroepithelia. The midbrain tegmentum, pons, and medulla have the thinnest neuroepithelia indicating that only the latest generated neurons are being produced at this time. The thick precerebellar neuroepithelium is an exception in the medulla. Thicker neuroepithelia are in the cerebellum (see above) and midbrain tectum, indicating many neurons are still being generated, although the majority of the neurons in these sites are already postmitotic. The neuroepithelium is still more thick in the hypothalamus and thalamus, in accordance with the later maturation of the diencephalon compared to the rest of the brainstem. Neurons throughout the diencephalon, midbrain tegmentum, pons, and medulla are migrating and settling. This specimen shows a very prominent migration of subthalamic nucleus neurons from the posterior hypothalamic neuroepithelium. Except for the subthalamic nucleus, nuclear divisions are very indistinct throughout the diencephalon. More definition is seen in the midbrain tegmentum, pons, and medulla. The anterior extramural and posterior extramural migratory streams are dense subpial accumulations in the medulla and pons.

209

GW9 "HORIZONTAL" SECTION PLANES LEVEL:SECTION

1:8

2:32 3:42 4:53 5:57 6:63

C886's cutting angle rotates 50˚ counterclockwise from the true horizontal plane (0˚), slightly over midway between true horizontal and true coronal. The anterior part of each section is considerably ventral to the posterior part.

7:69 8:75 9:81 10:86

11:90 12:100 13:105 14:111

CORONAL PLANE (90˚)

15:117 16:120 17:124

18:134 19:140

HORIZONTAL PLANE (0˚) PARIETAL LOBE OCCIPITAL LOBE

TE

BE

TECTUM

LO

L

IN

FRONTAL LOBE

SUL

MESENCEPHALON

M P O RA

Olfactory bulb Optic nerve

DIENCEPHALON (HYPOTHALAMUS) Trigeminal nerve Trigeminal nerve

TEGMENTUM

PONS CEREBELLUM MEDULLA

RHOMBENCEPHALON

CERE BR

EPHALON NCAL HEMISPHERE A

TEL E

PARACENTRAL LOBULE

SPINAL CORD

Figure 4. The lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 38 mm (modified from Figure 43, Table VII, Hochstetter, 1919) serves to show the approximate locations and cutting angles of the illustrated sections of C886 in the following pages. The small inset identifies the major structural features. The line in the cerebellum and dorsal edges of the pons and medulla is the cut edge of the medullary velum.

210

PLATE 84A GW9 Horizontal CR 43 mm, C886 Level 1: Section 8

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

Level 2: Section 33

PLATE 84B FUTURE PARACENTRAL LOBULE

Paracentral STF Layer I Cortical plate Subplate (layer VII)? STF1 t1 Paracentral STF STF5

Parietal STF

Layer I Cortical plate

FUTURE PARACENTRAL LOBULE

FUTURE PARIETAL LOBE

Subplate (layer VII)?

STF1 t1 STF5

FUTURE FRONTAL LOBE

Future dorsal hippocampus

Future anterior cingulate gyrus

Frontal STF

Interhemispheric fissure

middorsal pool

Cortical (frontal) NEP

Cortical (anterior cingulate) NEP

al

rs do ro ol te po

(future lateral ventricle)

Future posterior cingulate gyrus

Interhemispheric fissure

an

telencephalic superventricle

Dorsal telencephalic choroid plexus

Cortical (posterior cingulate) NEP

Cortical (dorsal hippocampal) NEP

posterodorsal pool

telencephalic superventricle (future lateral ventricle)

middorsal pool

Cortical (paracentral) NEP

Neuroepithelium - NEP Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Cortical (paracentral) NEP

Cortical (parietal) NEP

211

GW9 Horizontal CR 43 mm, C886 Level 3: Section 42

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

212

PLATE 85A

PLATE 85B Lateral migratory stream?

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

FUTURE PARACENTRAL LOBULE

Paracentral STF

Cortical layers more prominent

Parietal STF Dorsal telencephalic choroid plexus

FUTURE BASAL GANGLIA

FUTURE FRONTAL LOBE

Future dorsal hippocampus

Future anterior cingulate gyrus

Frontal STF

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF4 STF5

Ammonic migration Future posterior cingulate gyrus

Fornix

Cortical (anterior cingulate) NEP

Cortical (paracentral) NEP

FUTURE PARIETAL LOBE

Dentate migration

Diencephalic choroid plexus

Interhemispheric fissure

Cortical (frontal) NEP

Cortical layers less prominent

anterodorsal pool

diencephalic superventricle (future third ventricle)

Dorsal thalamic NEP

Fornical GEP Cortical (dorsal hippocampal) NEP

Cortical (posterior cingulate) NEP

telencephalic superventricle (future lateral ventricle) middorsal pool

posterodorsal pool

Cortical (parietal) NEP

Corticoganglionic NEP and SVZ Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Anterolateral ganglionic NEP and SVZ

213

GW9 Horizontal CR 43 mm, C886 Level 4: Section 53

See the brain core enlarged in parts C and D of this plate on the following pages.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

214

PLATE 86A

PLATE 86B

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF4 STF5

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Parietal STF

FUTURE PARIETAL LOBE

Future insular gyrus

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Lateral migratory stream?

(future lateral ventricle) Putamen

(future lateral ventricle)

Cortical layers more prominent

Ca ud ate

Frontal STF

BASAL GANGLIA

Dentate migration Ammonic migration

An comterio p le r x

SE

Fornix

foramen of monro

Cortical (anterior cingulate) NEP

Cortical (orbitofrontal) NEP

Occipital (granular) STF FUTURE OCCIPITAL LOBE

Posterior Dorsal complex complex US LAM THA Migrating an thalamic ned settling urons

Habenula

Cortical plate absent diencephalic superventricle

(future third ventricle) Diencephalic choroid plexus

Epithalamic NEP Posterior thalamic NEP Dorsal thalamic NEP Anterior thalamic NEP

GEP (internal capsule)

Septal NEP

Cortical (occipital) NEP

Cortical (hippocampal) NEP

External capsule

Corticoganglionic NEP and SVZ

Fornical GEP Choroid plexus stem cells Internal capsule

Anterolateral ganglionic NEP and SVZ

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Cortical layers less prominent

Internal capsule

For PT nix U M

Interhemispheric fissure

posterior pool

HIPPOCAMPUS Fimbria/fornix

(STRIATUM)

anterior pool

Future anterior cingulate gyrus

Telencephalic choroid plexus

Caudate

telencephalic superventricle

FUTURE FRONTAL LOBE

telencephalic superventricle

Anteromedial ganglionic NEP and SVZ Cortical (parietal) NEP

215

Posterior ganglionic NEP and SVZ

GW9 Horizontal CR 43 mm C886 Level 4: Section 53

See the entire section in parts A and B of this plate on the preceding pages.

216

PLATE 86C

PLATE 86D

To cortex

Internal capsule (thin bundles of many corticopetal and few corticofugal fibers) External capsule

Putamen

Ca uda STRIATUM te

telencephalic superventricle

From cortex St

ri

La

al

nu

a g ic

n

a

r r

o w

s

cle

UM

s

PT

n

us

on

SE

o

ur

al Fo sep rn ta l ix nu

Tenia tecta

n

cle

li

ne

ter

ng

r

ga

io

l a t e r a l se ting pt

ra

Mi g

r

er

io

st

er

po

(future lateral ventricle)

us

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Interhemispheric Transient structure - Times bold italic fissure Permanent structure - Times Roman or Bold

Fornix

An comterio ple r x

ant

g

anterior pool

er at

o li

n

m

ic

in

a li

r na

s?

ro

Telencephalic choroid plexus

ws

Ammonic migration (p

Internal capsule

(funnel for thalamocortical fibers)

Dorsal complex

M ig

r a ti n

foramen of monro

HIPPOCAMPUS Dentate migration

ul P Fim v o br b o i n a r st er ia/ d y a n io for in d l r c nix d o a t om rs era p a l l le po gen x sit ic ion ul ) a te

THALAMUS

g and

s e ttlin g

thalamic neurons

Dorsal thalamic NEP Anterior thalamic NEP

GE ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone Arrows indicate the presumed direction of axon growth in brain fiber tracts. Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Corticoganglionic NEP and SVZ

Anteromedial ganglionic NEP and SVZ

posterior pool

diencephalic superventricle

a al c te rn n i ( P

ps u

le )

Habenula Diencephalic choroid plexus

Epithalamic NEP Posterior thalamic NEP Cortical (occipital) NEP

s c e ll em t s us plex o id r o Ch G EP ic a l n r Fo

Posterior ganglionic NEP and SVZ

Cortical (ammonic) NEP Cortical (dentate) NEP

217

Anterolateral ganglionic NEP and SVZ

(future lateral ventricle)

(future third ventricle)

Subpial GEP

Septal NEP

telencephalic superventricle

218

PLATE 87A GW9 Horizontal CR 43 mm, C886 Level 5: Section 57

See the brain core enlarged in parts C and D of this plate on the following pages.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 87B

Cortical layers more prominent

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF4 STF5

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Parietal/temporal STF

FUTURE PARIETAL/ TEMPORAL LOBE

Future insular gyrus

Pu

(future lateral ventricle, anteroventral pool)

Anterior olfactory nucleus?

Caudate

le

c a psu

telencephalic superventricle

le su ap lc BASAL a rn en te m GANGLIA Ex a t

s bu s lo lidu n G al Int e r p

Bed nucleus of the stria terminalis

Rostral migratory stream? olfactory recess

Subpial migration toward basal telencephalon?

SE Fo PTU rn M ix

Septal NEP

Caudate

Future primary olfactory cortex

(future lateral ventricle)

Telencephalic choroid plexus

Anterior complex

foramen of monro

Cortical (olfactory) NEP

Cortical layers less prominent

HIPPOCAMPUS Fimbria/fornix

Dentate migration Ammonic migration

al

Lateral migratory stream?

telencephalic superventricle

posterior pool

FUTURE OCCIPITAL LOBE

Stria terminalis Po Internal c o ste r capsule Ce m p io r co n le x m tr pl al e Dorsal x

US LAM THA Migrating and settling thalamic neurons complex

Cortical plate absent ula Haben

diencephalic superventricle (future third ventricle)

Diencephalic choroid plexus Epithalamic NEP Posterior thalamic NEP Dorsal/central thalamic NEP Anterior thalamic NEP Strionuclear NEP and GEP

Cortical (occipital) NEP

Cortical (hippocampal) NEP

Anterolateral ganglionic NEP and SVZ

Fornical GEP Choroid plexus stem cells

Anteromedial ganglionic NEP and SVZ

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Posterior ganglionic NEP and SVZ Cortical (parietal/temporal) NEP

219

GW9 Horizontal CR 43 mm, C886 Level 5: Section 57

See the entire section in parts A and B of this plate on the preceding pages.

220

PLATE 87C

Internal capsule (thin bundles of many corticopetal and few corticofugal fibers) M

s bu s lo lidu G al p

STR

IA

TU Pu tam en

le su ap lc a n ter Ex

BASAL GANGLIA

Caudate telencephalic superventricle

From cortex

ra

pt

ep

cl

uc

ea

SEPTUM

s

eu

leu

n

ln

nu

r

ta

al

s ow rr ns na ro

ls

se

i

x

ra

ga ng l ic

te

ng

Bed nucleus of the stria terminalis

n io

rn F o

La

ti

or

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium Medial septal nucleus NEP - Neuroepithelium SVZ - Subventricular zone

Septal NEP

at

er

m

in

a li

s

(pu P lvi os bo nar terio dy an r in d la co do te mp Ce rsa ral le ntr l p ge x osi nic al tio ula co n) te

(funnel for thalamocortical fibers)

Anterior complex

foramen of monro

Fo rn ix

Internal capsule

Dorsal complex

mp lex

T HA

LAM US

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Habenula

Lateral geniculate migration

Migrating and settling thalamic neurons rventricle diencephalic supe

Dorsal/central thalamic NEP

tricle) (future third ven

Posterior thalamic NEP

Habenulointerpeduncular tract Lateral nucleus Medial nucleus Diencephalic choroid plexus

Epithalamic NEP

Anterior thalamic NEP

Strionuclear NEP and GEP

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

HIPPOCAMPUS Dentate migration Ammonic migration

Meyer's loop

po st

an te ri

M

ig

Telencephalic choroid plexus

Stria terminalis

ri St

(future lateral ventricle, anteroventral pool)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

To cortex

anglionic n rg ar io ro ws er

PLATE 87D

telencephalic superventricle

(future lateral ventricle, posterior pool)

Choroid plexus stem cells Fornical GEP

Anterolateral ganglionic NEP and SVZ Anteromedial ganglionic NEP and SVZ Posterior ganglionic NEP and SVZ

Cortical (ammonic) NEP Cortical (dentate) NEP

221

GW9 Horizontal CR 43 mm, C886 Level 6: Section 63

See the brain core enlarged in parts C and D of this plate on the following pages.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

222

PLATE 88A

PLATE 88B FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

(future lateral ventricle, posterior pool)

ta Pu

Basal telencephalon

us Globdus palli

Medial forebrain bundle?

Reti enicu cul lat ar e nu cle m Ventral us complex

THALAMUS

Cortical plate absent

Centr complealx

Posterior complex

Hab enul a

Migrating and settling thalamic neurons

pineal recess

Pineal gland

Subthalamic NEP

Epithalamic NEP Posterior thalamic NEP Dorsal/ventral/central thalamic NEP

Preoptic NEP

Inte

Lateral migratory stream? Future insular gyrus

rnal c a psule

BASAL GANGLIA

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

FUTURE OCCIPITAL LOBE?

n tio ra ig

PREOPTIC AREA

Cortical layers less prominent

Lateral g

Dorsal complex

(future third ventricle)

Cortical (olfactory) NEP

Forel's fields diencephalic superventricle

Medial preoptic area

? Anterior c o m m i s s u re

Nerve I (olfactory)

Dentate migration Ammonic migration

Stria terminalis

SUBTHALAMUS Lateral preoptic area

HIPPOCAMPUS Fornix

Zona incerta

Rostral migratory stream? olfactory recess

Temporal STF

telencephalic superventricle

e ul ps ca l na ter n Ex me

OLFACTORY BULB

Cortical layers more prominent

FUTURE TEMPORAL LOBE

date Cau al Intern le cap su

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF4 STF5

Strionuclear GEP

Cortical (occipital?) NEP Cortical (hippocampal) NEP Telencephalic choroid plexus

Fornical GEP Choroid plexus stem cells

Posterior ganglionic NEP and SVZ Cortical (temporal) NEP

223

GW9 Horizontal CR 43 mm, C886 Level 6: Section 63 See the entire section in parts A and B of this plate on the preceding pages.

224

PLATE 88C

PLATE 88D FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Fornical GEP

OLFACTORY BULB

Stria terminalis

Globus pallidus

telencephalic superventricle

e ul psr ers) a l c l fo fib na ne cal er (funcorti t In amo Zona al incerta th

Medial forebrain bundle?

Diagonal band of Broca (horizontal limb)?

Medial preoptic area

Preoptic NEP

Migrating subthalamic neurons

Dorsal complex

Cortical (occipital?) NEP

Habenula

THALAMUS Centra complexl

Po co steri mp or lex

Habenulointerpeduncular tract Lateral nucleus Medial nucleus

Migrating and settling thal amic neurons

pineal recess

ventricle) diencephalic superventricle (future third

Subthalamic NEP

Dorsal/ventral/central thalamic NEP

Staining artifact Cortical (olfactory) NEP

Latera l gen Fo icu rni lat cu x em la r i g nu r Ventral cl a e complex

Reti

s

Nerve I (olfactory)

r commissure?

PREOPTIC AREA

Migrating preoptic area neurons Forel's fields

Anterio

Lateral preoptic area

(future lateral ventricle, posterior pool)

u

SUBTHALAMUS

olfactory recess

Cortical (ammonic) NEP

n tio

Rostral migratory stream?

Ammonic migration

Strionuclear GEP

Basal telencephalon

HIPPOCAMPUS

Cortical (dentate) NEP

Posterior ganglionic NEP and SVZ

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Dentate migration

Choroid plexus stem cells

BASAL GANGLIA

Internal capsule

Epithalamic NEP

Pineal gland

Posterior thalamic NEP

Arrows indicate the presumed direction of axon growth in brain fiber tracts. Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

225

GW9 Horizontal CR 43 mm, C886 Level 7: Section 69

See the brain core enlarged in parts C and D of this plate on the following pages.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

226

PLATE 89A

PLATE 89B FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF4 STF5

FUTURE TEMPORAL LOBE

telencephalic superventricle

C o r ti c o m

l ra ate x sol le Ba comp

e

d ia

HIPPOCAMPUS Fornix Dentate migration Ammonic migration

AMYGDALA

l c o m ple x Stria terminalis

Optic tract? Zona incerta Ventral complex

Dorsomedial nucleus

Forel's fields

Fornix?

PREOPTIC AREA

Central complex

al Intern le capsu

Basal telencephalon Medial forebrain bundle?

Temporal STF

(future lateral ventricle, posteroventral pool)

Internal capsule?

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Cortical layers more prominent

diencephalic superventricle

Reti cul ar nu cle us Posterior complex

THALAMUS

Centr complealx

Migrating and settling thalamic neurons

Cortical layers less prominent

Cortical plate absent

Habenulo-interpeduncular tract

Habenula Posterior commissure GEP (posterior commissure)

(future third ventricle)

Preoptic NEP Subthalamic Hypothalamic NEP NEP TH S HYPOAL UB THALAMUS AM Internal US capsule

Epithalamic NEP Posterior thalamic NEP Ventral/central thalamic NEP

Lateral geniculate migration

Optic tract

Optic tract Strionuclear GEP

AMYGDALA

Amygdaloid NEP and SVZ

Future insular gyrus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Cortical (hippocampal) NEP Fornical GEP Telencephalic choroid plexus Choroid plexus stem cells

Cortical (temporal) NEP

227

228

PLATE 89C GW9 Horizontal CR 43 mm, C886 Level 7: Section 69

See the entire section in parts A and B of this plate on the preceding pages.

PLATE 89D

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

HIPPOCAMPUS Dentate migration

Fornical GEP

Choroid plexus stem cells Amygdaloid NEP and SVZ

Cortical (dentate) NEP Cortical (ammonic) NEP

Ammonic migration

Corticomedial amygdaloid complex Basal Stria t ermin telencephalon alis Optic tr act

Strionuclear GEP

Medial preoptic area

Zon a in cert a

Lateral preoptic area

Internal capsule

(funnel for thalamocortical fibers)

Medial forebrain bundle

Dorsomedial nucleus

Hypothalamic migration Preoptic migration

Ret i c u l a r n u cle us Ventral lateral geniculate body?

Ventral complex

Forel's fields

Fornix?

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Po co steri mp or lex

Centra complexl

e Migrating and settlin g thalamic n

Subthalamic migration

diencephalic superventricle

Lateral geniculate migration

Habenulointerpeduncular tract Lateral nucleus

Medial nucleus

ns u ro

(future third ventricle)

Habenula

Habenular neuron migration

Posterior commissure

GEP (posterior commissure)

Preoptic NEP

HYPOTHALAMUS

Subthalamic NEP

SUBTHALAMUS

Posterior thalamic NEP

Epithalamic NEP

EPITHALAMUS

THALAMUS Lateral geniculate migration

a

c

t

PREOPTIC AREA

Hypothalamic NEP

Ventral/central thalamic NEP

t

r

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Op

rac tic t

t

c t i O p

Lateral geniculate migration

229

GW9 Horizontal CR 43 mm, C886 Level 8: Section 75

See the brain core enlarged in parts C and D of this plate on the following pages.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

230

PLATE 90A

telencephalic superventricle

Fornix Dentate migration HIPPOCAMPUS Ammonic migration

l ra ate x sol ple a B com Central complex

AMYGDALA co m

ple x

Re t i c u l a r

Zo ince na rta

leus

ed

i al

Optic tract

Paraventricular nucleus?

cl

Ventral complex

eu

s

ul tic

Lateral hypothalamic area

Lateral geniculate migration nu

ar

Medial forebrain bundle PREOPTIC AREA

Temporal STF

(future lateral ventricle, posteroventral pool)

C o r ti c o m

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

FUTURE TEMPORAL LOBE

nuc

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF4 STF5

Forel's fields

Central complex

g ettlin and s rons g n i t u a Migr alamic ne th

Re

PLATE 90B

Habenulo-interpeduncular tract PRETECTUM

Posterior commissure

diencephalic superventricle (future third ventricle)

GEP (posterior commissure) Subthalamic Hypothalamic mesencephalic superventricle NEP EPIPreoptic NEP (future aqueduct) NEP US THALAMUS M A L Pretectal NEP Ventral/central THA HYPO Subthalamic T thalamic NEP Epithalamic NEP S nucleus? H AL UB AM THALAMUS Optic tract US Lateral geniculate migration Strionuclear GEP?

Optic tract

AMYGDALA

Amygdaloid NEP and SVZ

Cortical (hippocampal) NEP Fornical GEP

Future insular gyrus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Cortical (temporal) NEP

231

GW9 Horizontal CR 43 mm, C886 Level 8: Section 75

See the entire section in parts A and B of this plate on the preceding pages.

232

PLATE 90C

PLATE 90D

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Re

Zona incerta

PREOPTIC AREA

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

N

C

(future aqueduct)

Posterior commissure

leu

(future third ventricle)

Damaged area in pretectum

SUBTHALAMUS

Ventral/central thalamic NEP

n

E

P

H

A

L

Pretectal NEP

PRETECTUM

THALAMUS

L ater al g e n

GEP (posterior commissure)

Epithalamic NEP

ti o

E

m

mesencephalic superventricle

ra

I

and settl

a la in g th

e ic n

Medial habenular nucleus?

s on r u

EPITHALAMUS

HYPOTHALAMUS

D

Habenulo-interpeduncular tract

Centra complexl

Subthalamic NEP

Sub thal cere Incip nucleu amic bra ient s? l pe dun cle?

Optic tract

lc

r

la

diencephalic superventricle

Hypothalamic NEP

Preoptic NEP

icu Mi g r a ti ng

Paraventricular nucleus?

Hypothalamic migration

nu

Ret

Forel's fields

Lateral geniculate migration

us

Ventral complex

s

Subthalamic nucleus? (originates in the hypothalamic NEP)

Lateral hypothalamic area

Medial preoptic area

u l ar nucle

icu

e lat

m

M

ES

C EN

N

ient ? Incippeduncle l a r b cere

Medial forebrain bundle

Preoptic migration

tic

O

Optic tract

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

E

A PH

L

ig

N

O 233

GW9 Horizontal CR 43 mm, C886 Level 9: Section 81

See the brain core enlarged in parts C and D of this plate on the following pages.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

234

PLATE 91A

PLATE 91B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Future entorhinal cortex

telencephalic superventricle

(future lateral ventricle, posteroventral pool)

HIPPOCAMPUS Dentate migration Ammonic migration Fimbria/fornix

Reticular n u cl

Optic tract

Future suprachiasmatic nucleus? Preoptic NEP GEP (optic nerve and tract)

La

te r

Central complex om ntr e Ce

Habenulo-interpeduncular tract Medial longitudinal fasciculus?

diencephalic superventricle (future third ventricle)

Hypothalamic Subthalamic NEP NEP Ventral/central HYPOTHALAMUS thalamic NEP SUBTHALAMUS Subthalamic nucleus

Amygdaloid NEP and SVZ

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Forel's fields

eu s

n nu c . dia

PREOPTIC AREA optic recess (third ventricle)

ea e ar dl i c d ia l u n m e nb la a M ai th br po re hy fo al

Ventral complex

Zona incerta

Nerve II (optic)

Temporal STF

YG AMALA D

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

FUTURE TEMPORAL LOBE

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF4 STF5

Superior colliculus

mesencephalic superventricle

(future aqueduct)

Posterior commissure GEP (posterior commissure)

Tectal NEP Pretectal/ mesencephalic MIDBRAIN tegmental NEP TECTUM PRETECTUM/ MIDBRAIN THALAMUS TEGMENTUM

GEP (fimbria/fornix) Cortical (hippocampal) NEP

Cortical (temporal) NEP

235

GW9 Horizontal CR 43 mm, C886 Level 9: Section 81

See the entire section in parts A and B of this plate on the preceding pages.

236

PLATE 91C

PLATE 91D

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Optic tract

Incipient cerebral peduncle? ic m la s a u h e bt cl Su nu

Optic tract

te r

a

fo

Hypothalamic migration

Subthalamic migration

Preoptic migration

Future suprachiasmatic nucleus?

Central complex

Habenulo-interpeduncular tract

omedia ntr Ce

Medial longitudinal fasciculus?

s

optic recess (third ventricle)

La

e l dl ia n ed n bu M ai br re

Successive waves of migrating superior colliculus neurons

u ucle nn

PREOPTIC AREA

Zona incerta

Nerve II (optic)

ea ar ic m a al o th yp lh

R e t i cul a r n ucl eu s Ventral complex

Forel's Thalamic fields migration

Superior colliculus

Pretectal/ tegmental migration

diencephalic superventricle (future third ventricle)

mesencephalic superventricle (future aqueduct)

Preoptic NEP GEP (optic nerve and tract)

Hypothalamic NEP

Posterior commissure

Subthalamic Ventral/central NEP thalamic NEP

HYPOTHALAMUS

Tectal NEP Pretectal/ mesencephalic MIDBRAIN tegmental NEP

TECTUM

SUBTHALAMUS

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

I

E

N

C

ic la m ha us b t le Su nuc

D

E

P

THALAMUS

H

GEP (posterior commissure)

A

L

O

PRETECTUM/ MIDBRAIN TEGMENTUM

N

ME

N SE

C

H EP

A

LO

N

237

GW9 Horizontal CR 43 mm, C886 Level 10: Section 86

See the brain core enlarged in parts C and D of this plate on the following pages.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

238

PLATE 92A

PLATE 92B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

FUTURE TEMPORAL LOBE

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF4 STF5

NEP - Neuroepithelium

Temporal STF

telencephalic superventricle Auditory radiation?

Optic tract ic la m th a u s Subnucle

diencephalic superventricle

(future third ventricle)

Lateral hypothalamic area Sup Ventromedial nucleus?

Medial forebrain bundle

ram a aremmilla a r

(future lateral ventricle, ventral pool)

Nucleus of the optic tract

Medial geniculate body Mammillo thalamic tract?

Habenulo-interpeduncular tract Medial longitudinal fasciculus? Superior colliculus

y

mesencephalic superventricle (future aqueduct)

Posterior commissure

Optic chiasm Hypothalamic NEP HYPOTHALAMUS

SUBTHALAMUS

Oculomotor nuclear complex (III)?

MIDBRAIN TEGMENTUM

THALAMUS

Mesencephalic tectal NEP MIDBRAIN TECTUM Mesencephalic tegmental NEP

Cortical (temporal) NEP Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

239

240

PLATE 92C GW9 Horizontal CR 43 mm, C886 Level 10: Section 86

See the entire section in parts A and B of this plate on the preceding pages.

PLATE 92D

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

NEP - Neuroepithelium Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Optic tract

Nucleus of the optic tract

Auditory radiation?

Medial geniculate body?

Subthalamic nucleus

Migrating and settling tegmental neurons

Habenulo-interpeduncular tract

Medial le? forebrain bund Lateral hypo t h a la m i c a re a Hypothalamic

Medial longitudinal fasciculus?

Reticular formation

migration

Supramammillary area

C

(future third ventricle)

HYPOTHALAMUS D I

E

Posterior

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

E

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

P

H

A

Posterior commissure?

MIDBRAIN TEGMENTUM

Hypothalamic SUBNEP THALAMUS

C

(future aqueduct)

otor nuclear complex (III)? ulom Oc

Subthalamic nucleus

N

Superior colliculus

y gra

mesencephalic superventricle

diencephalic superventricle

Middle

al entr

THALAMUS

M L

E

O

S

Mesencephalic tegmental NEP

MIDBRAIN TEGMENTUM

E

N

C

N

Optic chiasm

Ventromedial nucleus?

Successive waves of migrating superior colliculus neurons

Mesencephalic tectal NEP

MIDBRAIN TECTUM

O

Optic tract

L

A

E

P

H

N 241

GW9 Horizontal CR 43 mm, C886 Level 11: Section 90

See the brain core enlarged in parts C and D of this plate on the following pages.

242

PLATE 93A

PLATE 93B FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

NEP - Neuroepithelium FUTURE TEMPORAL LOBE

HYPOTHALAMUS Mammillary body

Subthalamic nucleus

Optic tract? Substantia nigra?

Nucleus of the optic tract

Medial longitudinal fasciculus?

Ventromedial nucleus

Oculomotor nuclear complex (III)?

Arcuate nucleus Pituitary gland

Superior colliculus mesencephalic superventricle (future aqueduct)

Posterior commissure

diencephalic superventricle

(future third ventricle)

Middle hypothalamic NEP Posterior hypothalamic NEP

DIENCEPHALON

MIDBRAIN TEGMENTUM Subthalamic (Luysian) nucleus migration

MIDBRAIN TECTUM Mesencephalic tectal NEP Mesencephalic tegmental NEP

MESENCEPHALON

Layer I Cortical plate

BASE OF TELENCEPHALON Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

243

GW9 Horizontal CR 43 mm, C886 Level 11: Section 90

See the entire section in parts A and B of this plate on the preceding pages.

244

PLATE 93C

PLATE 93D

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

NEP - Neuroepithelium Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Incipient cerebral peduncle?

Nucleus of the optic tract

Optic tract? Substantia nigra?

Subthalamic nucleus Subthalamic (Luysian) nucleus neuron migration

Pituitary gland

Medial longitudinal fasciculus?

Migrating and settling tegmental neurons Reticular formation

Superior colliculus

Ce

Hypothalamic migration diencephalic superventricle

mi

cn

e u r o e p it

h

(NEP) um eli

MIDBRAIN TEGMENTUM

Arcuate nucleus Ventromedial nucleus

HYPOTHALAMUS

r nt

al

ay

(future cerebral aqueduct)

Posterior commissure? Reticular formation

MIDBRAIN TECTUM

Mammillary body Mesencephalic tegmental NEP

D I E N C E P H A L O N

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

gr

mesencephalic superventricle

otor nuclear complex (III)? ulom Oc

(future third ventricle)

Hypoth a la

Successive waves of migrating superior colliculus neurons

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

M

E

S

E

N

C

E

P

H

Mesencephalic tectal NEP

A

L

O

N

245

GW9 Horizontal CR 43 mm, C886 Level 12: Section 100

Levels 12 to 19 are shown only at higher magnification.

246

PLATE 94A

PLATE 94B ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Optic tract?

Subpial GEP

Nucleus of the optic tract

Incipient cerebral peduncle?

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Migrating red nucleus neurons?

gr

a

Successive waves of migrating superior colliculus neurons

Ventral tegmental area

Me dial f bun orebra dle in

Su

bs

ta

nt

ia

ni

Migrating and settling tegmental neurons

Medial longitudinal fasciculus?

C Interpeduncular nucleus

e

r nt

Raphe nuclear complex

al

Superior colliculus gr

ay

mesencephalic superventricle (future aqueduct)

Reticular formation

MIDBRAIN TEGMENTUM

Commissure of the superior colliculus?

MIDBRAIN TECTUM

Red nucleus?

Mesencephalic tectal NEP Rubral NEP?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Mesencephalic tegmental NEP

247

GW9 Horizontal CR 43 mm, C886 Level 13: Section 105

Levels 12 to 19 are shown only at higher magnification.

248

PLATE 95A

PLATE 95B

Evaginations and invaginations ABBREVIATIONS: of the neuroepithelium are mosaic GEP - Glioepithelium compartments that give rise to NEP - Neuroepithelium different brain structures.

Nerve V root (trigeminal) Trigeminal boundary cap

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Spinal tract (V) Trigeminal motor nucleus (V)? Subpial GEP

Optic tract? Nucleus of the optic tract

Principal sensory nucleus (V)

Migrating red nucleus neurons? Successive waves of migrating superior colliculus neurons

Substantia nigra?

Reticular formation Superior olive complex? Incipient pontine gray

Migrating and settling tegmental neurons

Medial longitudinal fasciculus?

Reticular tegmental nucleus

I

edu erp ncula nt r

Interpeduncular fossa

C uc

n

Raphe nuclear complex

Superior colliculus

Migrating and settling tegmental neurons

le u

s

e

r nt

Raphe nuclear complex

al

a gr

y

mesencephalic superventricle (future aqueduct)

Midline raphe glial system (provides structural support for brainstem and spinal flexures)

PONS

Reticular formation

MIDBRAIN TEGMENTUM

Red nucleus?

Rubral NEP?

Commissure of the superior colliculus?

MIDBRAIN TECTUM

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Mesencephalic tectal NEP Mesencephalic tegmental NEP

249

GW9 Horizontal CR 43 mm, C886 Level 14: Section 111

Levels 12 to 19 are shown only at higher magnification.

250

PLATE 96A

PLATE 96B

Cerebellar (hemispheric Purkinje cell) NEP Choroid plexus stem cells

lateral recess

NEP - Neuroepithelium

Sojourning and migrating hemispheric Purkinje cells

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

External germinal layer

(fourth ventricle)

Superior cerebellar peduncle? Evaginations and invaginations Nuclei of the lateral lemniscus (ventral and dorsal) of the neuroepithelium are mosaic compartments that give rise to Lateral lemniscus different brain structures. Parabigeminal Optic tract? nucleus? Nucleus of the optic tract

Inferior cerebellar peduncle Lateral lemniscus?

Trigeminal motor nucleus (V)?

sor en ) s al (V cip leus n i c Pr nu

al Spin s (V) u e nucl

y

Inferior colliculus

Superior olive complex Reticular formation Trapezoid body and medial lemniscus

Migrating red nucleus neurons?

Migrating and settling tegmental neurons Medial longitudinal fasciculus?

Raphe nuclear complex

Red nucleus?

n Ce

Migrating inferior colliculus neurons Successive waves of migrating superior colliculus neurons

Superior colliculus

ay gr l a tr

mesencephalic superventricle (future aqueduct)

Midline raphe glial system (provides structural support for brainstem flexures)

PONS

Reticular formation

MIDBRAIN TEGMENTUM

MIDBRAIN TECTUM

Spinal tract (V)? Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Commissure of the superior colliculus?

Mesencephalic tectal NEP

Mesencephalic tegmental NEP Rubral NEP? CEREBELLUM (HEMISPHERE)

251

252

PLATE 97A GW9 Horizontal CR 43 mm, C886 Level 15: Section 117

Levels 12 to 19 are shown only at higher magnification.

PLATE 97B

lateral recess

Rhombencephalic choroid plexus

Cochlear nucleus (dorsal) Inferior cerebellar peduncle Cochlear nucleus (ventral) Nerve VIII (boundary cap)

Superior cerebellar peduncle? Lateral lemniscus Brachium of the inferior colliculus

Cerebellar deep nucleus (dentate?)

Spinal tract (V) Vestibular nuclear complex Pontine/isthmal NEP

Spinal nucleus (V) Pontine NEP

Facial motor nucleus (VII)

Reticular formation

Superior olive complex

Medial longitudinal fasciculus?

Premigratory facial motor neurons? intermingled with abducens nucleus (VI)

Raphe nuclear complex

Midline raphe glial system (provides structural support for brainstem flexures)

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

External germinal layer

Nerve VIII (vestibulocochlear)

Trapezoid body and medial lemniscus

NEP - Neuroepithelium

Sojourning and migrating hemispheric Purkinje cells

(fourth ventricle)

PONS

Migrating inferior colliculus neurons

Superior colliculus

Migrating isthmal neurons

mesencephalic superventricle (future aqueduct)

Pontine/ isthmal NEP rhombencephalic superventricle

(future fourth ventricle)

Pontomedullary trench

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Successive waves of migrating superior colliculus neurons

Trochlear nucleus (IV)?

Raphe nuclear complex

Reticular formation

Locus coeruleus?

Inferior colliculus

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ISTHMUS

MIDBRAIN TECTUM

Mesencephalic tectal NEP

Isthmal NEP

Auditory NEP Ventral rhombic lip Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

CEREBELLUM (HEMISPHERE) Dorsal rhombic lip (contains cerebellar germinal trigone)

253

Cerebellar (hemispheric Purkinje cell) NEP

GW9 Horizontal CR 43 mm, C886 Level 16: Section 120

Levels 12 to 19 are shown only at higher magnification.

254

PLATE 98A

PLATE 98B

lateral recess

Sojourning and migrating hemispheric Purkinje cells

(fourth ventricle)

Rhombencephalic choroid plexus

Cochlear nucleus (dorsal) Inferior cerebellar peduncle

Vestibular nuclear complex

Raphe nuclear complex

rhombencephalic superventricle

Trapezoid body and medial lemniscus

Abducens nucleus (VI) Premigratory facial motor neurons?

Lateral lemniscus

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Inferior colliculus

Migrating inferior colliculus neurons

Central nucleus Brachium of the inferior colliculus

Migrating deep neurons? (future fourth ventricle)

Facial motor nucleus (VII) Superior olive complex?

Superior cerebellar peduncle?

Cerebellar deep nucleus (dentate?)

Spinal tract (V) Spinal nucleus (V)

NEP - Neuroepithelium

Successive waves of migrating superior colliculus neurons

Migrating isthmal neurons Trochlear nucleus (IV)

Superior colliculus

mesencephalic superventricle

isthmal canal

(future aqueduct)

Reticular formation

LOWER PONS/ UPPER MEDULLA Pontine/medullary NEP

ISTHMUS

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Auditory NEP Ventral rhombic lip Cerebellar (deep neurons) NEP?

Cerebellar (hemispheric Purkinje cell) NEP

MIDBRAIN TECTUM

Reticular formation

Isthmal NEP

Mesencephalic (superior colliculus) NEP

Mesencephalic (inferior colliculus) NEP

CEREBELLUM (HEMISPHERE) External germinal layer Dorsal rhombic lip (contains cerebellar germinal trigone)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

255

GW9 Horizontal CR 43 mm, C886 Level 17: Section 124

Levels 12 to 19 are shown only at higher magnification.

256

PLATE 99A

PLATE 99B

lateral recess

Sojourning and migrating hemispheric Purkinje cells

(fourth ventricle)

Rhombencephalic choroid plexus Cochlear nucleus (dorsal)?

NEP - Neuroepithelium

Migrating and proliferating external germinal layer cells

Inferior cerebellar peduncle Superior cerebellar peduncle?

Nerve IX (boundary cap) Nerve IX (glossopharyngeal)?

Inferior colliculus

Sojourning and migrating vermal Purkinje cells

Prepositus nucleus

rhombencephalic superventricle

(future fourth ventricle)

Cerebellar (vermal Purkinje cell?) NEP

MEDULLA

Cerebellar (deep neurons) NEP?

CEREBELLUM (FUSING VERMIS)

Ventral rhombic lip

Migrating superior colliculus neurons

MIDBRAIN TECTUM

Upper medullary NEP

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Superior colliculus

(future aqueduct)

Raphe nuclear complex

Migrating inferior colliculus neurons

mesencephalic superventricle

Midline raphe glial system (provides structural support for brainstem flexures)

uclear complex

Ve s ular n tib

Reticular formation

Medial lemniscus

Migrating deep neurons?

p ?) ee tus r d osi lla rp be te re (in Ce eus cl

nu

Spinal tract (V) Spinal nucleus (V)

Inferior olive complex

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Mesencephalic (superior colliculus) NEP

CEREBELLUM (HEMISPHERE)

Mesencephalic (inferior colliculus) NEP

External germinal layer Cerebellar (hemispheric Purkinje cell) NEP

Dorsal rhombic lip (contains cerebellar germinal trigone)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures. Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

257

GW9 Horizontal CR 43 mm, C886 Level 18: Section 134

Levels 12 to 19 are shown only at higher magnification.

258

PLATE 100A

PLATE 100B

lateral recess

Sojourning and migrating hemispheric Purkinje cells

(fourth ventricle)

Rhombencephalic choroid plexus Migrating lateral cuneate and lateral reticular neurons

NEP - Neuroepithelium FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Inferior cerebellar peduncle Spinal tract (V) Vestibular nuclear complex

Spinal nucleus (V) Reticular formation

Inferior olive complex Medial lemniscus

Raphe nuclear complex

Posterior extramural migratory stream crosses midline

Lower medullary NEP

Medial accessory nucleus Capsule Principal nucleus

Solitary nucleus rhombencephalic superventricle

(future fourth ventricle)

MEDULLA

Premigratory precerebellar neurons

Precerebellar NEP (in ventral rhombic lip)

Fastigial nucleus?

Sojourning and migrating vermal Purkinje cells

Cerebellar (vermal Purkinje cell?) NEP

CEREBELLUM (HEMISPHERE)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Migrating deep neurons?

Reticular formation

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Solitary tract

CEREBELLUM (FUSING VERMIS)

Dorsal motor nucleus (X)? Hypoglossal nucleus (XII)

Sprouting fibers of hook bundle?

For a detailed description of the development of the hook bundle, see Altman and Bayer (1996) pp.71-73, 202-204.

External germinal layer

Cerebellar (hemispheric Purkinje cell) NEP

Dorsal rhombic lip (contains cerebellar germinal trigone)

259

GW9 Horizontal CR 43 mm, C886 Level 19: Section 140

Levels 12 to 19 are shown only at higher magnification.

260

PLATE 101A

PLATE 101B

Inferior cerebellar peduncle

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

lateral recess

(fourth ventricle)

Rhombencephalic choroid plexus Migrating lateral cuneate and lateral reticular neurons

Sojourning and migrating hemispheric Purkinje cells

NEP - Neuroepithelium Spinal tract (V) Spinal nucleus (V)

Vestibular nuclear complex

Reticular formation

Inferior olive complex Medial lemniscus

Raphe nuclear complex

Solitary nucleus Dorsal sensory nucleus (X) rhombencephalic superventricle (future fourth ventricle)

Midline raphe glial system

(provides structural support for brainstem and spinal flexures)

Solitary tract

Medial accessory nucleus Fibrous capsule

Lower medullary NEP

cerebellar pool medullary pool

LOWER MEDULLA Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

CEREBELLUM (HEMISPHERE)

Principal nucleus

Reticular formation

CEREBELLUM (FUSING VERMIS)

Dorsal motor nucleus (X)? Hypoglossal nucleus (XII)

Sojourning and migrating vermal Purkinje cells

Cerebellar (vermal Purkinje cell?) NEP

External germinal layer Cerebellar (hemispheric Purkinje cell) NEP

Precerebellar NEP (in ventral rhombic lip)

Dorsal rhombic lip (contains cerebellar germinal trigone)

261

262

PART PARTVI: VI: GW9 GW9 CORONAL CORONAL

This specimen is human fetus number 282 with a crownrump length (CR) of 42 mm estimated to be at gestational week (GW) 9 (Minot Collection histological record number 841, referred to here as M841). The fetus was embedded in paraffin, cut in 10-µm thick sections, and stained with borax carmine and Lyon’s blue. No information is available on date of collection (sometime between 1900 and 1910) and the kind of fixative. Since there is no photograph of this brain before it was embedded and cut, a specimen from Hochstetter (1919) that is comparable to M841 has been modified to show the approximate section plane and external features of the brain at GW9 (inset, Figure 5). Like most of the specimens in this Volume, the sections are not cut exactly in one plane; M841 is midway between coronal and horizontal. Since the cerebral cortex is in every section and the brainstem is cut in a more horizontal orientation, the brain more closely resembles a coronally sectioned brain. Photographs of 22 sections (Levels 1-22) are illustrated at low magnification in Plates 102-121. Excellent tissue detail is preserved at low magnification, but there is a fine granular precipitate visible at high magnification. M841 is similar to the other GW9 specimens in the level of brain maturation. The chief reason for including this specimen is to provide a third perspective for viewing brain structure at GW9. In the cerebral cortex, the neuroepithelium is prominent as the sole germinal matrix; the stratified transitional field (STF) consists of STF1, STF5, and STF4 only in lateral areas. The anterolateral (thicker) to dorsomedial (thinner) maturation gradient in the cortical plate and STF layers are evident. In this specimen, the olfactory evagination is most evident coming from the basal telencephalic rather than from the cerebral cortical neuroepithelium. In anterolateral parts of the cerebral cortex, streams of neurons and glia appear to leave STF4 and enter the lateral migratory stream. A massive neuroepithelium/subventricular zone overlies the amyg-

dala, nucleus accumbens, and striatum (caudate and putamen) where neurons (and glia) are being generated. The cerebellum has a definite neuroepithelium at the ventricular surface. Most of the Purkinje cells are sojourning in a thick dense layer outside the neuroepithelium, and others are migrating upward. Many of the deep neurons are superificial in the cerebellum, but some are migrating downward to intermingle with upwardly migrating Purkinje cells. The cortical surface is partially covered by an external germinal layer (egl) that is actively producing neuronal stem cells, as it grows over the surface of the cerebellar cortex. The third ventricle, aqueduct, and fourth ventricle are lined by thin neuroepithelia. The midbrain tegmentum, pons, and medulla have the thinnest neuroepithelia indicating that only the latest generated neurons are being produced at this time. The thick precerebellar neuroepithelium is an exception in the medulla. Thicker neuroepithelia are in the cerebellum (see above) and midbrain tectum, indicating many neurons are still being generated, although the majority of the neurons in these sites are already postmitotic. The neuroepithelium is still thicker in the hypothalamus and thalamus, in accordance with the later maturation of the diencephalon compared to the rest of the brainstem. Neurons throughout the diencephalon, midbrain tegmentum, pons, and medulla are migrating and settling. Nuclear divisions are very indistinct throughout the diencephalon because more neurons are migrating and have not yet settled permanently. More definition is seen in the midbrain tegmentum, pons, and medulla where cell migration is waning. As with the other GW9 speciments, the anterior extramural and posterior extramural migratory streams are dense subpial accumulations in the medulla and pons.

263

GW9 "CORONAL" SECTION PLANES

S 15 EL 14

16 17

18 19 20

21

M841's cutting angle rotates 48˚ counterclockwise from the true coronal plane (90˚) and is between true horizontal and true coronal. The dorsal (top) part of each section is considerably anterior to the ventral (bottom) part.

22

V 13 LE 11 12

5

6

7

8

10 9

4:510

CORONAL PLANE (90˚)

3:440 2:480 22:39 20:112 1:551

21:96 19:124 18:135 17:155 16:175

HORIZONTAL PLANE (0˚)

15:205 14:220

PARIETAL LOBE

TE

MP O RA

Olfactory bulb Optic nerve

DIENCEPHALON (HYPOTHALAMUS)

12:255

OCCIPITAL LOBE

MESENCEPHALON TECTUM

TEGMENTUM

PONS CEREBELLUM MEDULLA

Trigeminal nerve

11:278 10:285 9:294

BE

LO L

IN

FRONTAL LOBE

SUL

13:235

RHOMBENCEPHALON

CERE BR

EPHALON NCAL HEMISPHERE A

TEL E

PARACENTRAL LOBULE

8:320 7:340 6:360 5:375

LEVEL:SECTION

SPINAL CORD

Figure 5. The lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 38 mm (modified from Figure 43, Table VII, Hochstetter, 1919) serves to show the approximate locations and cutting angles of the illustrated sections of M841 in the following pages. The small inset identifies the major structural features. The line in the cerebellum and dorsal edges of the pons and medulla is the cut edge of the medullary velum.

264

PLATE 102A GW9 Coronal CR 42 mm M841

Level 1: Section 551

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

Level 2: Section 480

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

265

PLATE 102B

NEP - Neuroepithelium

Level 1: Section 551 Interhemispheric fissure Layer I Cortical plate Subplate (layer VII)? STF1 t1 Frontal STF STF5

FUTURE FRONTAL LOBE

Cortical (frontal) NEP

telencephalic superventricle (future lateral ventricle)

anterior pool

Level 2: Section 480 Interhemispheric fissure

Layer I Cortical plate Subplate (layer VII)? STF1 t1 Frontal STF STF5

Cortical (frontal) NEP

FUTURE FRONTAL Telencephalic choroid plexus LOBE Cortical (cingulate) NEP

Cingulate STF telencephalic superventricle (future lateral ventricle)

anterior pool

Tenia tecta Cortical (orbitofrontal) NEP Orbitofrontal STF

Cortical (olfactory) NEP

Anterior olfactory nucleus? olfactory recess

Nerve I (olfactory)

Cortical folding in the midline is a shrinkage artifact.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

266

PLATE 103A

Level 3: Section 440

GW9 Coronal CR 42 mm M841

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1-Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5-Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal

Level 4: Section 410

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

267

PLATE 103B

Level 3: Section 440

ABBREVIATIONS: NEP - Neuroepithelium SVZ - Subventricular zone

Interhemispheric fissure

Cortical (frontal) NEP

Cortical (cingulate) NEP

FUTURE FRONTAL LOBE

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Frontal STF

telencephalic superventricle (future lateral ventricle)

anterior pool

Telencephalic choroid plexus

Cingulate STF

Tenia tecta Septal NEP

Corticoganglionic NEP and SVZ

Migrating neurons Septal Septal Ganglionic

Lateral septal nucleus

Ca ud ate

Lateral migratory stream?

SEPTUM

BASAL GANGLIA Ba s al te l e n c e p h a l o n

Anterolateral ganglionic NEP and SVZ

Future insular gyrus Future primary olfactory cortex

Horizontal limb? Vertical limb Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Level 4: Section 410 Interhemispheric fissure

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Frontal STF

Cortical (frontal) NEP Cortical (cingulate) NEP FUTURE FRONTAL LOBE

Telencephalic choroid plexus

Corticoganglionic NEP and SVZ

telencephalic superventricle (future lateral ventricle)

anterior pool

Cingulate STF Tenia tecta Migrating neurons Septal

Septal NEP

Ganglionic

Medial septal nucleus

lo n

Anteromedial ganglionic NEP and SVZ diencephalic superventricle

PREOPTIC AREA

Preoptic NEP

Future insular gyrus Future primary olfactory cortex

Migrating preoptic neurons

(future third ventricle)

Cortical folding in the midline is a shrinkage artifact.

Lateral migratory stream?

M

nce pha

Lateral septal nucleus

U PT

Caudate G BAS Ba ANG AL sa LI l te A le

SE

Anterolateral ganglionic NEP and SVZ

Diagonal band of Broca

Optic chiasm

Diagonal band of Broca (horizontal limb?) Medial preoptic area Suprachiasmatic nucleus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

268

PLATE 104A GW9 Coronal CR 42 mm M841 Level 5: Section 375

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

269

Cortical (frontal) NEP

telencephalic superventricle

(future lateral ventricle)

Interhemispheric fissure PLATE 104B Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Frontal STF Cingulate STF

FUTURE FRONTAL LOBE

Cortical folding in the midline is a shrinkage artifact.

Cortical (cingulate) NEP Telencephalic choroid plexus

Future cingulate gyrus

Hippocampal NEP

anterior pool

Dorsal hippocampus

Fornical GEP

Septal NEP

BASAL Anterolateral ganglionic GANGLIA NEP and SVZ Gl

Anteromedial ganglionic NEP and SVZ Strionuclear NEP Paraventricular nucleus?

Lateral SEPTUM septal nucleus Medial septal nucleus Anterior commissure

M

c ni lio g an s gg n it n euro ra ig n

Bed nucleus of the stria terminalis

Migrating hypothalamic neurons

T HA LA M

External capsule

Putamen p ob all us idu s Ba sa l te len cep hal on

Lateral migratory stream?

Migrating septal neurons

US

Future insular gyrus Future primary olfactory cortex

diencephalic superventricle

(hypothalamic part, future third ventricle)

Lateral hypothalamic area Optic tract

PO

Ca ud ate

x rni Fo

Corticoganglionic NEP and SVZ

GEP (optic tract)

H

Hypothalamic NEP

Y

Trigeminal ganglion (V)

Arcuate nucleus

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures. ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

SPINAL CORD

Subpial GEP

Midline raphe glial system (provides structural support for brainstem and spinal flexures) Spinal cord G/EP central canal

Ventral funiculus Ventral gray Lateral funiculus Intermediate gray Central autonomic area Dorsal gray (substantia gelatinosa) Dorsal funiculus (gracile and cuneate fasciculi)

270

PLATE 105A GW9 Coronal CR 42 mm M841 Level 6: Section 360

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

271 Interhemispheric fissure

FUTURE FRONTAL LOBE

Cortical (frontal) NEP

Cortical (cingulate) NEP

Cingulate STF

Telencephalic choroid plexus telencephalic superventricle

PLATE 105B

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Frontal STF

Future cingulate gyrus

Hippocampal NEP

(future lateral ventricle)

anterior pool

Septal NEP

septal nucleus

Putamen

Ba

Globus pallidus

s al

t e len

Migrating hypothalamic neurons

GEP(optic tract)

Future primary olfactory cortex

Medial forebrain bundle

cephal on

Anteromedial ganglionic NEP and SVZ Strionuclear NEP

Future insular gyrus

Bed nucleus of the stria terminalis

T HALAM U

External capsule

ud

BASAL ate GANGLIA

S

Lateral hypothalamic area Optic tract

PO

Anterolateral ganglionic NEP and SVZ

Lateral migratory stream?

HY

Internal capsule

Ca

Migrating septal neurons Migrating ganglionic neurons Triangular

nix For

Corticoganglionic NEP and SVZ

Dorsal hippocampus

Fornical GEP

Hypothalamic NEP Arcuate nucleus

diencephalic superventricle

(hypothalamic part, future third ventricle)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures. ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

MEDULLA Posterior extramural migratory stream (contains external cuneate and lateral reticular neurons) Medial lemniscus

Raphe nuclear complex intermingled with midline glial fibers (provide structural support for brainstem and spinal flexures)

Medial accessory nucleus Principal nucleus Fibrous capsule

Inferior olive complex

Subpial GEP Spinal cord G/EP central canal

Cortical folding in the midline is a shrinkage artifact.

SPINAL CORD

Intermediate gray Central autonomic area Dorsal gray (substantia gelatinosa) Dorsal funiculus (gracile and cuneate fasciculi)

272

PLATE 106A GW9 Coronal CR 42 mm M841 Level 7: Section 340

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

273

Cortical (frontal) NEP

Cortical (cingulate) NEP

(future lateral ventricle)

Future cingulate gyrus Dorsal hippocampus

Fornical GEP

anterior pool

Dentate migration

Ca Internal capsule

ud

at

t e len

cephal on

PO US HYLAM A TH

Anteromedial ganglionic NEP and SVZ

FUTURE TEMPORAL LOBE

Hypothalamic NEP

Future insular gyrus

BASAL GANGLIA

diencephalic superventricle

Globus pallidus

s al

Migrating ganglionic neurons

foramen of monro

e

Putamen

Ba

Lateral migratory stream?

(hypothalamic part, future third ventricle)

Anterolateral ganglionic NEP and SVZ External capsule

Ammonic migration

nix For

Corticoganglionic NEP and SVZ

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 STF4 Frontal STF

Cingulate STF

Telencephalic choroid plexus Hippocampal NEP

telencephalic superventricle

PLATE 106B

Interhemispheric fissure

FUTURE FRONTAL LOBE

Future primary olfactory cortex

Lateral hypothalamic area Optic tract GEP (optic tract)

Migrating hypothalamic neurons

Arcuate nucleus Superior olivary complex Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Trapezoid body?

Inferior cerebellar peduncle

Lateral lemniscus?

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Reticular formation

Raphe nuclear complex intermingled with midline raphe glial fibers (provide structural support for brainstem and spinal flexures)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures. ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Spinal cord G/EP

LOWER MEDULLA Medial lemniscus Principal nucleus Fibrous capsule

SPINAL CORD

Inferior olive complex

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Central autonomic area central canal

Dorsal gray (substantia gelatinosa) Dorsal funiculus (gracile and cuneate fasciculi)

274

PLATE 107A GW9 Coronal CR 42 mm M841 Level 8: Section 320

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

275

Cortical (cingulate) NEP

Cortical (frontal/ paracentral) NEP

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 STF4

Cingulate STF

Telencephalic choroid plexus

telencephalic superventricle

anterior pool

Ammonic migration

x rni Fo

Dorsal hippocampus Fornical GEP

Diencephalic choroid plexus

Internal capsule

e at ud a C

foramen of monro

Cortical (temporal/parahippocampal) NEP intermingled with amygdaloid NEP

Hypothalamic NEP Arcuate nucleus

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Future primary olfactory cortex

Basal telencephalon Op tic tra ct

AMYGDALA

FUTURE TEMPORAL LOBE

SUBTHALAMUS Lateral hypothalamic area

PO US HYLAM A TH

Subthalamic NEP

Future insular gyrus

BASAL GANGLIA

THALAM (anterio US complexr)

Anteromedial ganglionic NEP and SVZ

Anterior thalamic NEP

(future third ventricle)

Globus pallidus

External capsule

diencephalic superventricle

Putamen

Lateral migratory stream?

Migrating ganglionic neurons

Dentate migration

Corticoganglionic NEP and SVZ

Frontal/ paracentral STF

Future cingulate gyrus

Hippocampal NEP

(future lateral ventricle)

Anterolateral ganglionic NEP and SVZ

PLATE 107B

Interhemispheric fissure

FUTURE FRONTAL LOBE/ PARACENTRAL LOBULE

Migrating hypothalamic neurons

Trigeminal boundary cap Nerve V (trigeminal, root)

External germinal layer

Cerebellar NEP

CEREBELLUM

rhombencephalic superventricle

(lateral recess, future fourth ventricle)

Auditory NEP?

Medial lemniscus and trapezoid body

PONS

Dorsal cochlear nucleus?

Inferior cerebellar peduncle Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Lateral lemniscus?

Raphe nuclear complex intermingled with midline raphe glial fibers (provide structural support for brainstem and spinal flexures)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures. ABBREVIATIONS: GEP - Glioepithelium G/EP - Glioepithelium/ependyma NEP - Neuroepithelium SVZ - Subventricular zone

Principal sensory nucleus (V)

UPPER MEDULLA

Spinal/medullary G/EP central canal SPINAL CORD/ LOWER MEDULLA

Superior olivary complex Reticular formation Spinal nucleus (V) Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Central autonomic area Dorsal gray (substantia gelatinosa) Dorsal funiculus (gracile and cuneate fasciculi)

276

PLATE 108A GW9 Coronal CR 42 mm M841 Level 9: Section 294

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

277 Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Cingulate STF STF4 Frontal/ Telencephalic paracentral choroid plexus STF

Cortical (cingulate) NEP

Dorsal hippocampus

Future cingulate gyrus

Hippocampal NEP

Gl pal obus l An s a i d u s lentic ularis

AMYGDALA

Premammillary area

Cortical (temporal/ parahippocampal) NEP

Migrating subthalamic neurons SUBTHALAMUS (Forel's fields)

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

PONS Raphe nuclear complex intermingled with midline raphe glial fibers (provide structural support for brainstem and spinal flexures)

Cerebellar NEP Rhombencephalic choroid plexus rhombencephalic superventricle

(future fourth ventricle, lateral recess)

Reticular tegmental nucleus

Principal sensory nucleus (V)

Reticular formation

Lateral lemniscus

Ventral rhombic lip

Bas o

Medial lemniscus and trapezoid body Lateral lemniscus and central trigeminal fibers

External germinal layer CEREBELLUM

Future primary olfactory cortex

Future temporal cortex Migrating amygdaloid neurons

Future entorhinal cortex

Hypothalamic NEP

MEDULLA

Spin

Vestibular nuclear complex?

Sojourning and migrating Purkinje cells

Dorsal cochlear nucleus? Inferior cerebellar peduncle

cl nu

Solitary tract

Area postrema?

nu

l cu

a te

ne

er

Dorsal sensory nucleus (X)?

Cu

rhombencephalic superventricle

(future fourth ventricle)

cleu s

ary

Medullary NEP

S olit

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

eu

s

Auditory NEP?

na

Dorsal rhombic lip (contains cerebellar germinal trigone)

com p

Migrating hypothalamic neurons

n

Central complex

lex

(future lateral ventricle, ventral pool)

halo Basal telencep

l

HYPOTHALAMUS

Amygdaloid NEP and SVZ

telencephalic superventricle

BASAL GANGLIA

Stria terminalis

Op tic tra ct Lateral hypothalamic area

FUTURE TEMPORAL LOBE

Future insular gyrus

e at ud a C

Corticomedia

Subthalamic NEP

Anterior complex Migrating thalamic neurons

nea te n ucl eu

en P u ta m

Anterior thalamic NEP

(future third ventricle)

Strionuclear GEP

diencephalic superventricle

Internal capsule

Lateral migratory stream?

Migrating ganglionic neurons

US AM AL TH

Corticoganglionic NEP and subventricular zone (SVZ)

External capsule

Diencephalic choroid plexus

x

Fo rn ix

Anterolateral ganglionic NEP and SVZ

Ammonic migration

Dentate migration

Fornical GEP Anteromedial ganglionic NEP and SVZ

l a teral com pl e

(future lateral ventricle, dorsal pool)

s

telencephalic superventricle

al n u cleus (V )

Cortical (frontal/ paracentral) NEP

PLATE 108B

Interhemispheric fissure

FUTURE FRONTAL LOBE/ PARACENTRAL LOBULE

E xt

Gracile nucleus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

278

PLATE 109A GW9 Coronal CR 42 mm M841 Level 10: Section 285

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

279

PLATE 109B Interhemispheric fissure

FUTURE PARACENTRAL LOBULE Cortical (cingulate) NEP Dorsal hippocampus telencephalic superventricle

Future cingulate gyrus

Hippocampal NEP

(future lateral ventricle, dorsal pool)

Fornical GEP Fo rn ix

Anteromedial ganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ

en P u ta m

ral a te so l le x Bacomp

FUTURE TEMPORAL LOBE

dial com e Corctiomplex

Central complex

bus pal lid u s

Subthalamic NEP

Amygdaloid NEP and SVZ

Dorsomedial nucleus

(future third ventricle)

External capsule

le us

telencephalic superventricle

(future lateral ventricle, ventral pool)

Migrating thalamic neurons Stria terminalis

SUBTHALAMUS (Forel's fields)

Medial lemniscus

PONS Raphe nuclear complex and midline glial fibers

(HEMISPHERE)

rhombencephalic superventricle (future fourth ventricle)

Cerebellar NEP

Pontine NEP

Reticular tegmental nucleus and incipient pontine gray

Reticular formation

Rhombencephalic choroid plexus

Vestibular

MEDULLA Vestibular nuclear complex

Ventral rhombic lip

Sojourning and migrating Purkinje cells

Ventral cochlear nucleus? Inferior cerebellar peduncle

at

en

uc leu

s

ary

nu

cl

Solitary tract

ne

rhombencephalic superventricle

(future fourth ventricle)

S olit

Medullary NEP

eu

s

Auditory NEP? Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Principal sensory nucleus (V)

nu cle a

Pontomedullary trench

rhombencephalic superventricle

(future fourth ventricle, lateral recess)

Precerebellar NEP

Future temporal cortex Migrating amygdaloid neurons

Future entorhinal cortex

Medial nucleus

External germinal layer CEREBELLUM

AMYGDALA

Migrating hypothalamic neurons

Lateral nucleus

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Dorsal rhombic lip (contains cerebellar germinal trigone)

Future insular cortex

Optic tract Migrating subthalamic neurons

HYPOTHALAMUS

Claustrum (infiltrated by the lateral migratory stream)

rc l e u om p le x s ( V)

Mammillary body

BASAL GANGLIA

SUBTHALAMUS (Forel's fields)

Hypothalamic NEP

Cortical (temporal/ parahippocampal) NEP

Migrating ganglionic neurons

THALAMUS

diencephalic superventricle

G lo

al rs lex Domp c nu co l ar ic u

Internal capsule

Thalamic NEP

Cau dat e Strionucleuar GEP

Ammonic migration

Dentate migration

Diencephalic choroid plexus

R et

Corticoganglionic NEP and SVZ

Stria medullaris

Spinal nu c

Cortical (paracentral) NEP

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Cingulate STF STF4 Paracentral Telencephalic STF choroid plexus

C

u

Dorsal sensory nucleus (X)? Gracile nucleus External cuneate nucleus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

280

PLATE 110A GW9 Coronal CR 42 mm M841 Level 11: Section 270

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

281

PLATE 110B Interhemispheric fissure Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 STF4 Paracentral STF

FUTURE PARACENTRAL LOBULE Cortical (cingulate) NEP

Cingulate STF Telencephalic choroid plexus

Dorsal hippocampus

Future cingulate gyrus

P u ta m

en

lar nucleus

Stria terminalis

Zona incerta Subthalamic NEP Ventromedial nucleus

Amygdaloid NEP and SVZ telencephalic superventricle

Ventral hippocampal NEP

(future lateral ventricle, ventral pool)

(future third ventricle)

AMYGDALA

FUTURE TEMPORAL LOBE

Ventral complex

Dorsal rhombic lip (contains cerebellar germinal trigone)

CEREBELLUM (HEMISPHERE)

s

ax on

ug

BASAL GANGLIA o-

Claustrum (infiltrated by the lateral migratory stream)

Subthalamic nucleus?

HYPOTHALAMUS

Temporal STF

Migrating amygdaloid neurons

Future entorhinal cortex Migrating hypothalamic neurons Medial lemniscus Lateral lemniscus Nuclei of the lateral lemniscus Superior cerebellar peduncle

Anterior extramural migratory stream (contains pontine gray and reticular tegmental neurons) Cerebellar deep neurons?

rt

Future insular cortex

Substantia nigra?

Mammillary body

External germinal layer

m

Co

SUBTHALAMUS

Hypothalamic NEP

Cortical (temporal/ parahippocampal) NEP

Migrating ganglionic neurons a al th fo r o n s x nel" "Fun tical a cor

icu

Corona radiata

Dentate migration

THAL AMUS

et

Thalamic NEP

Internal capsule

Sojour ning a

R

ate ud Ca

n d m i g r a ti n g t halamic neurons

Corticoganglionic NEP and SVZ

Sprouting thalamic axons? Posterior complex (in dorsal position) Dorsal complex

diencephalic superventricle

Posterior ganglionic NEP and SVZ

Ammonic migration

Diencephalic choroid plexus Lateral geniculate migration

Fo rn ix

Fornical GEP

Stria medullaris

of

(future lateral ventricle, dorsal pool)

al

Dorsal hippocampal NEP

telencephalic superventricle

ic

Cortical (paracentral) NEP

Reticular formation Facial motor nucleus (VII) Abducens nucleus (VI)

Future temporal cortex

Raphe nuclear complex and midline glial fibers

Cerebellar NEP

PONS

Sojourning and migrating Purkinje cells

Vestibular nuclear complex?

lateral recess

Rhombencephalic choroid plexus

Pontine NEP

Precerebellar NEP

(future fourth ventricle)

Ventral rhombic lip

Posterior extramural migratory stream (contains external cuneate and lateral reticular neurons)

Medullary NEP

MEDULLA

Posterior extramural migratory stream (external cuneate and lateral reticular neurons) Medullary velum

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Premigratory precerebellar neurons

rhombencephalic superventricle

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Solitary nucleus and tract?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

282

PLATE 111A GW9 Coronal CR 42 mm M841 Level 12: Section 255

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1-Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5-Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

283

PLATE 111B Interhemispheric fissure FUTURE PARACENTRAL LOBULE Cortical (cingulate) NEP

Dorsal hippocampus Stria medullaris

Ammonic migration

(future lateral ventricle, ventral pool)

hip Ve po ntr ca al mp us

Ventral hippocampal NEP

Medial lemniscus? S u tan bs Mesencephalic NEP

Ventral complex

Incipient cerebral peduncle

m

SUBTHALAMUS

Interpeduncular nucleus

MIDBRAIN TEGMENTUM Future entorhinal cortex

Medial lemniscus

(contains pontine gray and reticular tegmental neurons)

External germinal layer Dorsal rhombic lip (contains cerebellar germinal trigone)

Reticular formation

Cerebellar deep neurons?

(HEMISPHERE)

Cerebellar NEP lateral recess

Future insular cortex

o-

Amygdaloid NEP and SVZ Ammonic migration Dentate migration

Temporal STF Future temporal cortex

Lateral lemniscus Nuclei of the lateral lemniscus Superior cerebellar peduncle

Abducens nucleus (VI)

Vestibular nuclear complex

Sojourning and migrating Purkinje cells

Pontine NEP

Rhombencephalic choroid plexus

rhombencephalic superventricle

Precerebellar NEP

(future fourth ventricle)

Ventral rhombic lip

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

BASAL GANGLIA

Raphe nuclear complex and midline glial fibers

PONS

CEREBELLUM

Claustrum (infiltrated by the lateral migratory stream)

Migrating amygdaloid neurons

aqueduct

Cortical (temporal/ Subpial GEP parahippocampal) NEP Anterior extramural migratory stream

ns

r tic

Stria terminalis

AMYGDALA

ra tia nig

telencephalic superventricle

Zona incerta

Dorsal complex

a al th fo r o n s x nel" "Fun tical a cor

FUTURE TEMPORAL LOBE

Centromedian nucleus Subthalamic NEP

Migrating striatal neurons

THALAMUS

Posterior ganglionic NEP and SVZ

Thalamic NEP

Lateral geniculate migration

and migrating thalamic neurons

Fimbria

Internal capsule

Internal capsule

Caudate

Corona radiata

Reticular nucleus

Corticoganglionic NEP and SVZ

Dentate migration

Sojourning

Posterior ganglionic NEP and SVZ

Posterior complex (in dorsal position) Sprouting thalamic axons?

diencephalic superventricle (future third ventricle)

Fornical GEP

Fo rn ix

Diencephalic choroid plexus

al axo

Dorsal hippocampal NEP

(future lateral ventricle, dorsal pool)

ofug

telencephalic superventricle

Co

Cortical (paracentral) NEP

Layer I Cortical plate Subplate (layer VII)? STF1 t1 Cingulate STF STF5 STF4 Telencephalic Paracentral choroid plexus STF Future cingulate gyrus

Medullary (precerebellar) NEP

MEDULLA

Medullary velum

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Premigratory precerebellar neurons

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

284

PLATE 112A GW9 Coronal CR 42 mm M841 Level 13: Section 235

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1-Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5-Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

285

PLATE 112B Interhemispheric fissure FUTURE PARACENTRAL LOBULE Cortical (paracentral) NEP

Cortical (cingulate) NEP

Cingulate STF Telencephalic choroid plexus

Dorsal hippocampus telencephalic superventricle

Future cingulate gyrus

Sprouting thalamic axons?

Dorsal complex

Ventral complex

Fo rn ix

FUTURE TEMPORAL LOBE telencephalic superventricle

(future lateral ventricle, ventral pool)

Ventral hippocampus

Subst ant i

Cortical (temporal/ parahippocampal) NEP

nig r

a

Ventral hippocampal NEP

Medi al lem nis c

a

us?

Ventral tegmental area

Incipient cerebral peduncle

Interpeduncular nucleus

MIDBRAIN TEGMENTUM

Reticular formation

PONS

Midline glial fibers

(HEMISPHERE)

Pontine NEP

Precerebellar NEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Superior cerebellar peduncle Cerebellar deep neurons (dentate nucleus?)

Raphe nuclear complex

CEREBELLUM

Cerebellar (deep neurons) NEP

Temporal STF Future temporal cortex

Future entorhinal cortex

Medial lemniscus

Cerebellar (hemispheric Purkinje cell) NEP

Ammonic migration

cerebral aqueduct

Lateral lemniscus Nuclei of the lateral lemniscus

Dorsal rhombic lip (contains cerebellar germinal trigone)

Dentate migration

Lateral geniculate body (ventral)

Subpial GEP

External germinal layer

BASAL GANGLIA

a te

Thalamic NEP

Lateral geniculate body (dorsal)

C aud

(future third ventricle)

Fornical GEP

Dentate migration

THALAMUS

diencephalic superventricle

Choroid plexus stem cells

Ammonic migration

Lateral geniculate migration

Sojourning and migrating thalamic neurons

Posterior ganglionic NEP and SVZ

Diencephalic choroid plexus

Posterior complex (in dorsal position)

Fo rn ix

Fornical GEP

Paracentral STF

Stria medullaris

Dorsal hippocampal NEP

(future lateral ventricle, dorsal pool)

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 STF4

Vestibular nuclear complex?

Sojourning and migrating Purkinje cells

lateral recess

rhombencephalic superventricle (future fourth ventricle)

Rhombencephalic choroid plexus

Medullary velum

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

286

PLATE 113A GW9 Coronal CR 42 mm M841 Level 14: Section 220

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1-Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4 Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5-Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

287

PLATE 113B Interhemispheric fissure

Cortical (parietal) NEP FUTURE PARIETAL LOBE

Cortical (cingulate) NEP

telencephalic superventricle

(future lateral ventricle, dorsal pool)

Layer I Cortical plate Subplate (layer VII)? STF1 t1 Cingulate STF STF5 STF4 Telencephalic choroid plexus Parietal Future cingulate gyrus STF

Dorsal hippocampus Stria medullaris

Diencephalic choroid plexus

Hippocampal (dorsal Ammonic) NEP

Lateral geniculate migration

Posterior complex (in dorsal position)

(future third ventricle)

Hippocampal (ventral Ammonic) NEP

Thalamic NEP Lateral geniculate body (ventral) Medial lemniscus

telencephalic superventricle

Ventral hippocampus

ce

re

Mesencephalic NEP

a br al

Medial lemniscus ped

Red Internucleus peduncular nucleus Interpeduncular fossa

e

External germinal layer

Reticular formation

PONS CEREBELLUM

Vestibular nuclear complex?

MIDBRAIN TEGMENTUM Future temporal cortex

Future entorhinal cortex Superior cerebellar peduncle Cerebellar deep neurons (dentate nucleus?)

Midline raphe glial system (provides structural support for brainstem flexures) Raphe nuclear complex

Sojourning and migrating Purkinje cells

(HEMISPHERE)

Cerebellar (deep neurons) NEP

Temporal STF

Ammonic migration

cl

Lateral lemniscus

Dorsal rhombic lip (contains cerebellar germinal trigone)

Cerebellar (hemispheric Purkinje cell) NEP

Dentate migration

Ventral complex

un

Cortical (temporal/ parahippocampal) NEP

Posterior striatal NEP and SVZ

aqueduct r ig tia n tan t bs en Su ipi Inc

(future lateral ventricle, ventral pool)

Dorsal complex

rons

FUTURE TEMPORAL LOBE

g and migrating thalamic neu

diencephalic superventricle

THALAMUS

Hippocampal (dentate) NEP

Dentate migration

Sojournin

Sprouting thalamic axons?

Ammonic migration

Pontine NEP

rhombencephalic superventricle

(future fourth ventricle)

lateral recess

Sprouting fibers of hook bundle? Rhombencephalic choroid plexus

Medullary velum

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

288

PLATE 114A GW9 Coronal CR 42 mm M841 Level 15: Section 205

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1-Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4-Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5-Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

289

PLATE 114B Interhemispheric fissure

Cortical (parietal) NEP

FUTURE PARIETAL LOBE

Layer I Cortical plate Subplate (layer VII)? STF1 t1 Cingulate STF STF5 STF4 Parietal Future cingulate gyrus STF

Cortical (cingulate) NEP

telencephalic superventricle

(future lateral ventricle, dorsal pool)

Telencephalic choroid plexus

Stria medullaris Diencephalic choroid plexus

Lateral geniculate migration

Posterior complex (in dorsal position)

igrat ion

pus ocam

te m

diencephalic superventricle

u la

(future third ventricle)

telencephalic superventricle

Medial lemniscus

(future lateral ventricle, ventral pool)

Staining artifact

Cortical (temporal/ parahippocampal) NEP

Su bs ta nt ia

Incipient cerebral peduncle

Mesencephalic NEP ni gr

ereb ella rp ed

rio rc

External germinal layer Dorsal rhombic lip (contains cerebellar germinal trigone)

Cerebellar (hemispheric Purkinje cell) NEP

pe Su

Habenulointerpeduncular tract

Red Inter- nucleus MIDBRAIN peduncular nucleus TEGMENTUM

Medial lemniscus

a

Subpial GEP Lateral lemniscus

aqueduct

Posterior striatal NEP and SVZ

Ventral complex

ns

Medial geniculate body?

Dentate migration

S

Lateral ge nic

Thalamic NEP

Dorsal complex

THALAM U

Hipp

Sprouting thalamic axons?

euro

FUTURE TEMPORAL LOBE

Sojourning and migrating thalamic n

Hippocampal (Ammonic) NEP

Ammonic migration

Interpeduncular fossa

cle un

Midline raphe glial system

Reticular formation

Parabrachial nucleus

Dentate migration

Temporal STF

Ammonic migration Future temporal cortex

Future entorhinal cortex

Superior cerebellar peduncle Cerebellar deep neurons (interpositus nucleus?)

PONS

Raphe nuclear complex

lateral recess

CEREBELLUM (HEMISPHERE)

Cerebellar (deep neurons) NEP Sprouting fibers of hook bundle?

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Pontine NEP

rhombencephalic superventricle

(future fourth ventricle)

Medullary velum

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Sojourning and migrating Purkinje cells

Rhombencephalic choroid plexus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

290

PLATE 115A GW9 Coronal CR 42 mm M841 Level 16: Section 175

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1-Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF4-Complex middle layer where sojourning and migrating cortical neurons grow corticofugal axons and intermingle with corticopetal axons. STF5-Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

291

PLATE 115B Interhemispheric fissure

Cortical (parietal) NEP Cortical folding in the midline is a shrinkage artifact.

FUTURE PARIETAL LOBE

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Cingulate STF STF4 Parietal Future cingulate gyrus STF

Cortical (cingulate) NEP

telencephalic superventricle

Diencephalic choroid plexus

(future lateral ventricle, posterior pool)

Stria medullaris

Telencephalic choroid plexus

Lateral geniculate migration

Ventral complex

Thalamic NEP

Medial geniculate body

ron

aqueduct

Mesencephalic (tegmental) NEP Medial longitudinal fasciculus

Cortical (temporal/ parahippocampal) NEP Subpial GEP Lateral lemniscus Parabrachial nucleus

Dorsal rhombic lip (contains cerebellar germinal trigone)

Cerebellar (hemispheric Purkinje cell) NEP

Oculomotor nuclear complex (III) Red nucleus?

Raphe nuclear complex

Pontine NEP

CEREBELLUM (HEMISPHERE)

Future entorhinal cortex

Future temporal cortex

MIDBRAIN TEGMENTUM

UPPER PONS

External germinal layer

Temporal STF

Brachium of the inferior colliculus

Reticular formation

Superior cerebellar peduncle

Ammonic migration

Medial geniculate body

s

FUTURE TEMPORAL LOBE

(future third ventricle)

neu

Lateral ge nic u

te m igr ati o

Hip poc am pus la

diencephalic n superventricle

US LA M THA

Hippocampal (Ammonic) NEP

c alami Sojourning and migrating th

Posterior complex (in dorsal position)

Cerebellar deep neurons (fastigial nucleus?) Cerebellar deep neurons (interpositus nucleus?)

lateral recess

Cerebellar (deep neurons) NEP Sojourning and migrating Purkinje cells

rhombencephalic superventricle

Rhombencephalic choroid plexus

(future fourth ventricle)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

292

PLATE 116A GW9 Coronal CR 42 mm M841 Level 17: Section 155

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

293

PLATE 116B

Interhemispheric fissure

Cortical (parietal) NEP

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Parietal STF

Cortical folding in the midline is a shrinkage artifact.

FUTURE PARIETAL LOBE telencephalic superventricle

Telencephalic choroid plexus

(future lateral ventricle, posterior pool)

Diencephalic choroid plexus Stria medullaris

Migrating epithalamic neurons

Epithalamic NEP diencephalic superventricle

Habenulointerpeduncular tract

(future third ventricle)

Parabigeminal nucleus

Oculomotor nuclear complex (III) Cerebellar deep neurons (interpositus nucleus?)

Isthmal NEP isthmal canal

Lateral lemniscus Superior cerebellar peduncle

External germinal layer

Brachium of the inferior colliculus

Occipital STF

MIDBRAIN TEGMENTUM

Raphe nuclear complex

Parabrachial nucleus

s

Reticular formation

pu

Subpial GEP

Temporal STF

Medial geniculate body

Migrating red nucleus neurons?

Central gray

Medial longitudinal fasciculus

am

Mesencephalic (tegmental) NEP

Future temporal cortex

US

Red nucleus?

Nucleus of the optic tract?

oc

Rubral NEP?

FUTURE OCCIPITAL LOBE

pp

Cortical (occipital) NEP

AM

Medial geniculate body

Migrating thalamic neurons

Ammonic migration

Hi

AL

(future aqueduct)

Cortical (temporal) NEP

mesencephalic superventricle

FUTURE TEMPORAL LOBE

TH

Thalamic NEP

Lateral geniculate migration

Hippocampal (Ammonic) NEP

EPITHALAMUS

ISTHMUS Locus coeruleus

Trochlear nucleus (IV)?

lateral recess Dorsal rhombic lip (contains cerebellar germinal trigone)

CEREBELLUM (HEMISPHERE)

Cerebellar (deep neurons) NEP

Cerebellar (hemispheric Purkinje cell) NEP

Sojourning and migrating Purkinje cells

Rhombencephalic choroid plexus/medullary velum

rhombencephalic superventricle

(future fourth ventricle) Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

294

PLATE 117A GW9 Coronal CR 42 mm M841 Level 18: Section 135

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

295

PLATE 117B

Interhemispheric fissure

Cortical (parietal) NEP

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Parietal STF

Cortical folding in the midline is a shrinkage artifact.

FUTURE PARIETAL LOBE Diencephalic choroid plexus

telencephalic superventricle

(future lateral ventricle, posterior pool)

Migrating epithalamic neurons

Telencephalic choroid plexus

Epithalamic NEP Lateral nucleus Medial nucleus

diencephalic superventricle

(future third ventricle)

Habenulointerpeduncular tract

Reticular formation Mesencephalic (tegmental) NEP Nucleus of the optic tract?

PRETECTUM

(future aqueduct)

Cortical (occipital) NEP

Mesencephalic (pretectal) NEP

EPITHALAMUS

mesencephalic superventricle

FUTURE OCCIPITAL LOBE

Habenula

Medial longitudinal fasciculus Raphe nuclear complex mesencephalic superventricle

Central gray

MIDBRAIN TEGMENTUM

Occipital STF

Oculomotor nuclear complex (III)

(future aqueduct)

Lateral lemniscus

Mesencephalic (tegmental) NEP

Parabigeminal nucleus Cerebellar deep neurons (interpositus nucleus?)

Parabrachial nucleus? Superior cerebellar peduncle

Migrating and proliferating external germinal layer cells

External germinal layer

CEREBELLUM

Sojourning and migrating hemispheric Purkinje cells

(HEMISPHERE)

Dorsal rhombic lip (contains cerebellar germinal trigone)

Cerebellar (hemispheric Purkinje cell) NEP

Sojourning and migrating vermal Purkinje cells

Cerebellar (vermal Purkinje cell) NEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

rhombencephalic superventricle

(future fourth ventricle)

NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

296

PLATE 118A GW9 Coronal CR 42 mm M841 Level 19: Section 124

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

297

PLATE 118B

Cortical (parietal) NEP

Interhemispheric fissure

Cortical folding in the midline is a shrinkage artifact.

Layer I Cortical plate Subplate (layer VII)? STF1 t1 STF5 Parietal STF

FUTURE PARIETAL LOBE Diencephalic choroid plexus

telencephalic superventricle (future lateral ventricle, posterior pool)

pineal recess

Epithalamic NEP

(future third ventricle)

Lateral nucleus Medial nucleus

Habenulointerpeduncular tract

Mesencephalic (pretectal) NEP

Cortical (occipital) NEP

Migrating epithalamic neurons EPITHALAMUS

diencephalic superventricle

FUTURE OCCIPITAL LOBE

GEP (posterior commissure)

Posterior commissure

Central gray

mesencephalic superventricle

(future aqueduct)

Mesencephalic (superior colliculus) NEP

Habenula

PRETECTUM

Mesencephalic (superior colliculus) NEP

Nucleus of the optic tract?

Telencephalic choroid plexus

Occipital STF

Superior colliculus

MIDBRAIN TECTUM

Migrating inferior colliculus neurons Central nucleus

Inferior colliculus

Mesencephalic (inferior colliculus) NEP

CEREBELLUM (FUSING VERMIS)

External germinal layer

Sojourning and migrating hemispheric Purkinje cells

CEREBELLUM (HEMISPHERE)

Cerebellar (vermal Purkinje cell) NEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Sojourning and migrating vermal Purkinje cells

rhombencephalic superventricle

(future fourth ventricle)

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

298

PLATE 119A GW9 Coronal CR 42 mm M841 Level 20: Section 112

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

299

PLATE 119B

Interhemispheric fissure

Cortical (occipital) NEP

Layer I Cortical plate Subplate (layer VII)? STF1 t1 Occipital STF STF5

Cortical folding in the midline is a shrinkage artifact.

telencephalic superventricle (future lateral ventricle, posterior pool)

FUTURE OCCIPITAL LOBE

Telencephalic choroid plexus

Diencephalic choroid plexus

pineal recess

Mesencephalic (pretectal) NEP Posterior commissure

Mesencephalic (superior colliculus) NEP

MIDBRAIN TECTUM Mesencephalic (inferior colliculus) NEP

Central gray

(future aqueduct)

Nucleus of the optic tract?

mesencephalic superventricle

GEP (posterior commissure)

PRETECTUM

Migrating superior colliculus neurons

Superior colliculus Migrating inferior colliculus neurons

Inferior colliculus

Central nucleus

CEREBELLUM External germinal layer

(VERMIS)

Sojourning and migrating hemispheric Purkinje cells

CEREBELLUM (HEMISPHERE)

Sojourning and migrating vermal Purkinje cells

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

300

PLATE 120A GW9 Coronal CR 42 mm M841 Level 21: Section 96

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

301

PLATE 120B

Interhemispheric fissure Cortical (occipital) NEP Cortical folding in the midline is a shrinkage artifact.

Layer I Cortical plate Subplate (layer VII)? STF1 t1 Occipital STF STF5 telencephalic superventricle (future lateral ventricle, posterior pool)

FUTURE OCCIPITAL LOBE

Diencephalic choroid plexus

Telencephalic choroid plexus

pineal recess

Posterior commissure

Subcommissural organ

GEP (posterior commissure)

Mesencephalic (superior colliculus) NEP

Central gray

(future aqueduct)

Nucleus of the optic tract?

mesencephalic superventricle

Mesencephalic (pretectal) NEP

PRETECTUM

MIDBRAIN TECTUM Superior colliculus

Migrating superior colliculus neurons Migrating inferior colliculus neurons

Inferior colliculus Mesencephalic (inferior colliculus) NEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

CEREBELLUM

External germinal layer

(VERMIS)

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

302

PLATE 121A GW9 Coronal CR 42 mm M841 Level 22: Section 39

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

303

PLATE 121B

Interhemispheric fissure Cortical (occipital) NEP

Cortical folding in the midline is a shrinkage artifact. telencephalic superventricle

Layer I Cortical plate Subplate (layer VII)? STF1 t1 Occipital STF STF5

(future lateral ventricle, posterior pool)

FUTURE OCCIPITAL LOBE

Posterior commissure

GEP (posterior commissure)

Mesencephalic (superior colliculus) SVZ?

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

(future aqueduct)

Mesencephalic (superior colliculus) NEP

mesencephalic superventricle

MIDBRAIN TECTUM

Superior colliculus

Migrating superior colliculus neurons

Earliest settling superior colliculus neurons

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

304

PART PARTVII: VII: GW8 GW8 SAGITTAL SAGITTAL

This is specimen number145 in the Carnegie Collection, designated here as C145, a male with a crown-rump length (CR) of 33 mm estimated to be at gestational week (GW) 8. The entire fetus was cut in the sagittal plane. Information on the date of specimen collection, fixative, section thickness, and embedding medium was not available to us. The sections are thick (probably between 50 to 100 µm) and appear to be embedded in celloidin. Since there is no photograph of C145’s brain before histological processing, a specimen from Hochstetter (1919) that is comparable in age to C145 is used to show external brain features at GW8 (A, Figure 6). C145’s brain structures are easier to understand because sections are closely parallel to the midline; Figure 6 shows the approximate slight rotations in horizontal (B) and vertical (C) dimensions. Photographs of 10 sections (Levels 1-10) are illustrated at low magnification in four parts (Plates 122A-D through 131A-D). The A/B parts show the brain in place in the skull; the C/D parts show only the brain (and some peripheral ganglia) at slightly higher magnification. Plates 132-147 show high magnification views of various parts of the brain. All of the high-magnification plates are rotated 90˚ (landscape orientation) to show photographs at higer magnification in the available page space. C145 is considerably less mature than the GW9 specimens. One of the most notable features of this specimen is the larger volume of the brain ventricles when compared to the brain parenchyma (areas where neurons migrate, settle, and differentiate). The largest structure in each of the brain’s major subdivisions is the superventricles in their cores. For example, the telencephalon is largely occupied by the telencephalic superventricle. The thickness of the parenchyma is a key to the degree of maturation of the various brain structures. It is thickest in the medulla, pons, and midbrain tegmentum where most of the neurons have been generated and thinner in the cerebellum, midbrain tectum, and diencephalon. Within the telencephalon, the cerebral cortex has a very thin parenchyma, while the basal telen-

cephalon and parts of the basal ganglia have thick parenchymal components. Throughout the cerebral cortex, the neuroepithelium is prominent as the sole germinal matrix. The stratified transitional field (STF) contains STF1 and STF5 only in lateral areas. The pronounced anterolateral (thicker) to dorsomedial (thinner) maturation gradient is evident in both the cortical plate and the STF layers. The olfactory bulb is just beginning to evaginate in front of the basal telencephalic neuroepithelium. Neurons are just beginning to migrate in the hippocampus. A massive neuroepithelium/ subventricular zone overlies the amygdala, nucleus accumbens, and striatum (caudate and putamen) where neurons (and glia) are being generated. The cerebellum has a thicker neuroepithelium, indicating many Purkinje cells are being generated. Earlier-generated Purkinje cells are sojourning in a dense layer outside the neuroepithelium. Most of the deep neurons are superificial in the cerebellum. The external germinal layer (egl) is barely visible eminating from the germinal trigone in the dorsal rhombic lip. In sections near the midline, the brainstem neuroepithelium varies in thickness. It is thinner in the midbrain tegmentum, pons, and medulla in accordance with an earlier maturation gradient. Most neurons have been generated in these structures and are settling. In the cerebellum (see above), midbrain tectum, and diencephalon, the neuroepithelium is thicker indicating that substantial neurogenesis is happening in these structures, but many neurons have already been produced. However, more lateral sections have a thick precerebellar neuroepithelium in the medulla. Since the pontine gray is totally absent, nearly all of those neurons have yet to be generated in the precerebellar neuroepithelium; some of the earliest-generated pontine gray neurons are migrating in the anterior extramural migratory stream.

305

N O L

A H

BE

P

LO

E

S

R

U

A

R B

FU TUR E RA CE NTRAL LO BUL E

N

T

A

M

C

P

f

N

3.82˚

e d

rhombencephalic superventricle

S

M

E D U L

L

A

L A N I D SP OR C RHOMBENCEPHALON

) Level 2 (brainstem

rtex) Level 1 (cerebral co

m

Medullary velum

Right side

Right side

LU E B aEr Ly v e lMu R m l l E u

d g e

o

e

O

Left side

3.48˚

INFERIOR COLLICULUS

L

N E C E R E

O MP

M

TU

C BACK VIEW

TOP VIEW

TEGMEN

U

U

E

MES EN C M TU

IN

LA SU

RE TE Sections of C145's brain are very close to C PA A the midline both L N L D LO E I A BE horizontally (+3.48˚, H PREOPTIC top view) and vertically T AREA O (+3.82˚, back view). In P Y H each section illustrated on Olfactory bulb the following pages, the Pituitary gland anterior edge of the cortex (top Optic nerve (II) right) is tilted toward the observer, while Trigeminal nerve (V) the medulla and upper spinal cord Facial nerve (VII) (bottom) are tilted away from the observer. Vestibulocochlear nerve (VIII)

B

T

LON HA EP

L

I S P H E E M R H E

F

RO E F

T E L

H A L O N P

A

PA RA CE NT

TU

FU

E

SUPERIOR COLLICULUS

EPITHALAMUS

T

C

FU

C

RE

L RA

LE BU LO

E L LOB ITA CIP OC RE TU

FUTUR

A perfect sagittal cut through the brain bisects the cerebral cortex into two separate hemispheres by passing through the interhemispheric fissure, and does the same in the brainstem by passing through the midline of the ventricles.

A

E PARIETAL LOBE TUR FU

C u t

GW8 SAGITTAL

Left side

Figure 6. A, The lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 27 mm (modified from Figure 39, Table VII, Hochstetter, 1919) identifies external features of a brain similar to C145 (CR 33 mm). B, Top view of the brain with a crown-rump length of 38 mm (modified from Figure 45, Table VIII, Hochstetter, 1919) shows how C145’s sections rotate from a line parallel to the horizontal midline in the interhemispheric fissure. C, Back view of the brain in B (modified from Figure 44, Table VIII, Hochstetter, 1919) shows how C145’s sections rotate from a line parallel to the vertical midline in the brainstem and upper cervical spinal cord.

306

PLATE 122A

GW8 Sagittal, CR 33 mm, C145 Level 1: Slide 23, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

307

PLATE 122B

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

C

US

INFE RI

UL

ISTHMUS

IC

T

O LL

isthmal narrows

CE

N LO A CEREBELLUM PH

(LATERAL VERMIS)

rhombencephalic superventricle

RHO

(future fourth ventricle)

it a l

EN

S

Rhombencephalic choroid plexus

ip

N

E

I

MB

N

oc c

SE

D

P

HI PP O

T E L E N C PTUM

a Squ

mo

us

ica

ia

S

L NA I P

m

l ng a tg

RD O C n

Clavicle?

v Cer

mammillary recess

LOWER MEDULLA

Thyroid gland?

Do

N

E

C

Fronta l bo ne e ss

r oc

Meckel's cartilage

o ro al s r

S

O

UPPER MEDULLA

ital ccip al o

r o c ess

MENT U EG

M

B as

Oropharynx

rp

P

N ESE CE

P

x

y

MU

T SU

OR

l

T o n g u e

d ib ula

(future third ventricle)

Anterior part Sella turcica cleft p r s o Intragrandular Intermediate part p oc h es ary n Pituitary gland s

Oral cav it

an

diencephalic superventricle

UM

recess

M

infundibular recess

d

(future aqueduct) T RE E C T

AL O N

Pa

oi

mesencephalic superventricle

O pineal

A L H P

A H YPOTH A L

en

Ethmoid M a x i l l a N a lata

ALEPI AMUS

PH

optic recess

Sph

Nasal septum (cartilage)

M

E

C

e

M

on Fr

TH

THALAMUS

Diencephalic choroid plexus

IC PT O EA E R PR A

lp asa n to

US MP A C

T U C COLLICU LU EERIOR S

(future lateral ventricle)

on

lb

E

telencephalic superventricle

H

P

R

R

O N A L

a et

B

E

A

Fut ure par i

C O R T E X

L

l

o lc a r teb ver

lu

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

308

PLATE 122C

GW8 Sagittal, CR 33 mm, C145 Level 1: Slide 23, Section 2

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the midbrain medial to this section in Plates 138A and B to 139A and B.

side Left e ine Right sid Midl

BRAINSTEM FLEXURES

4 3

See a high-magnification view of the pons and medulla from this section in Plates 142A and B.

2

1

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

309 Layer I Incipient cortical plate STF1 t1 STF5

PLATE 122D

Cortical (paracentral) NEP Cortical (parietal) NEP

Cortical (posterior cingulate) NEP Cortical (hippocampal) NEP

Cortical (occipital) NEP

Cortical (frontal) NEP Fornical GEP

Fo rn ix

St

ria

med

ullaris?

Migrating habenular neurons

Dorsal and posterior thalamic NEP

Fornix

Posterior commissure

Sojourning and migrating thalamic neurons

Choroid plexus stem cells

Septal Anterior NEP thalamic Medial NEP septal

Ventral thalamic NEP

Pretectal NEP

Sojourning and migrating tegmental neurons

Mesencephalic (tectal, superior colliculus) NEP

Thalamic NEP

(reticular protuberance?)

Preoptic NEP

Mesencephalic (tegmental) NEP

Interpeduncular nucleus

Hypothalamic NEP

Sojourning and migrating superior colliculus neurons Substantia nigra/ ventral tegmental area

Posterior (mammillary)

Anterior

Middle

Sojourning and migrating hypothalamic neurons

Raphe nuclear co m

Pituitary gland Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Po

n tine

Reticular formation

ple

fas

l edia l l o n g i t u d i n a M

x

ci

icu

Sojourning and migrating deep neurons

Sojourning and migrating Purkinje cells

Superior cerebellar peduncle

External germinal layer

Dorsal rhombic lip

Cerebellar NEP

Choroid plexus stem cells

Lower medullary NEP

Medullary velum

lar

Ventral rhombic lip

formation

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

cu

Sprouting fibers of hook bundle?

Upper medullary NEP

Ret

rio r Infelive o

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Isthmal NEP

P NE

Medial lemniscus? Posterior intramural migratory stream (inferior olive neurons)

Mesencephalic (tectal, inferior colliculus) NEP

Midline raphe glial system (structural support for brainstem flexures)

Optic tract

Subpial GEP

Trochlear nucleus (IV)? Nerve IV decussation (trochlear)

s

Sojourning and migrating septal neurons Diagonal band of Broca (vertical limb) Sojourning and migrating preoptic neurons

nucleus

Sojourning and migrating pretectal neurons

Epithalamic NEP

lu

Cortical (anterior cingulate) NEP

GEP (posterior commissure)

Vestibular nuclear complex Cuneate fasciculus Cuneate nucleus Solitary nucleus and tract

Dorsal gray matter (substantia gelatinosa)

Subpial GEP?

Dorsal funiculus Lateral funiculus

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

310

PLATE 123A

GW8 Sagittal, CR 33 mm, C145 Level 2: Slide 22, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

311

PLATE 123B

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

R E

HI P

N

PR

n

US

UL

IC

UM A LREBREMLILS) H P E CE (VE

it a l Rhombencephalic choroid plexus

am Squ

ip

EN

MB

O LL

oc c

C

N

D I E

l c olu m

ra eb rt

ve

al

C

(future fourth ventricle)

RHO

r oc

ic

M

rv

U

ON

S

m

T

a

lu

COLLICULU

r teb ver l a v ic C er

o lc

R

S

C

Dorsal root ganglia

e

IO

C

INFE RI

rhombencephalic superventricle

LOWER MEDULLA

L NA I P

R

Esophagus

C

E

Thyroid gland?

S isthmal narrows

UPPER MEDULLA

P

e ss

U

Larynx

N

OR

t is

O

gland

ital ccip al o

Sternum?

Sella turcica

B as

ot

Oropharynx

gl

mammillary recess

ISTHMUS

P

x

i Ep

US

ON

id

Cridoid cartilage?

Clavicle?

infundibular recess

yn

bula Hyoid bone? r process Thyroid cartilage?

HA

M LA

GME TE N

AL

cav it

T o n g u e n di

H YPOT

Anterior part Intragrandular cleft Intermediate part Posterior part Na so ph Pituitary ar y

tal process Pala

Ma

superventricle

(future third ventricle)

H

e

no

Ethmoid

T CTUM ETE L O A pineal S recess P H E MESEN CE diencephalic

P

optic recess

Sph

i l l a M a x

mesencephalic superventricle

M TU

IC PT O EA E R PR A

as on t ity on c av l Fr sa Na

e

(future aqueduct)

THALAMUS

SEPTUM

p al

on

Diencephalic choroid plexus

foramen of monro

(future lateral ventricle)

Oral

PUS AM C EPITHALAMUS PO

E

T E L E N C

C

Front al b on e telencephalic superventricle

Telencephalic choroid plexus

lb

E

H

P

Fut ure par i

O N L A

a et

B

E

A

R

R T E X C O

L

ou

s

RD O C

n

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

312

PLATE 123C

GW8 Sagittal, CR 33 mm, C145 Level 2: Slide 22, Section 2 NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

side Left ide ine Right s Midl

BRAINSTEM FLEXURES

4 See a high-magnification view of the hypothalamus and basal telencephalon in Plates 133A and B, of the midbrain, pons, and medulla in Plates 143A and B.

3 2

1

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

313 Layer I Incipient cortical plate STF1 t1

Cortical (paracentral) NEP Cortical (hippocampal) NEP

Diagonal band of Broca (vertical limb)

lt ra

Mesencephalic (tectal, superior colliculus) NEP

Pituitary gland

Redeus? l nuc

Mesencephalic (tegmental) NEP

Substantia nigra/ ventral tegmental area

ral gray

Posterior (mammillary) Middle

Optic tract

Pretectal NEP

Cent

Anterior

Interpeduncular nucleus

Hypothalamic NEP

Epithalamic NEP

Ve

Sojourning and migrating hypothalamic neurons

Preoptic NEP

honeycomb matrix

Oculomotor nuclear complex (III)?

ha

Subthalamic NEP SU THAL BAMUS

Sojourning and migrating preoptic neurons

GEP (posterior commissure) Posterior commissure Infiltrating glia Superior collicular

nt

Medial septal nucleus?

lam

Anterior thalamic NEP

EP

Sojourning and migrating thalamic neurons

Septal NEP

Sojourning and migrating septal neurons

Habenular complex

Pioneer thalamocortical axons

Posterior thalamic NEP

Cortical (anterior cingulate) NEP

Dashed lines indicate staining and/or sectioning artifacts.

Stria medullaris?

Migrating posterior complex neurons

ic N

Choroid plexus stem cells

Cortical (occipital) NEP

Fo rn ix

Fornical GEP

Cortical (frontal) NEP

PLATE 123D

Cortical (parietal) NEP

Sojourning and migrating tegmental neurons

Midline glial raphe system (structural support for brainstem flexures) Raphe nuclear P E complex

Po n t i ne

Mesencephalic (tectal, inferior colliculus) NEP Isthmal NEP

N

Migrating raphe neurons infiltrate midline glial raphe fibers Sojourning and migrating Purkinje cells Upper medullary NEP

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Subpial GEP

Superior cerebellar peduncle

External germinal layer Cerebellar NEP

Medial lemniscus?

Choroid plexus stem cells

Medullary velum

Re

tic

Lower medullary NEP

ular

rio r Infelive o

forma

tio

Posterior intramural migratory stream (inferior olive neurons) Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Dorsal rhombic lip

Ventral rhombic lip

Vestibular nuclear complex

n

Cuneate fasciculus Cuneate nucleus

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold Subpial GEP

Dorsal funiculus Dorsal gray matter (substantia gelatinosa) Lateral funiculus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field

314

PLATE 124A

GW8 Sagittal, CR 33 mm, C145 Level 3: Slide 20, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

315

PLATE 124B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

PR

US

UL

IC

O LL

UM EBELISL) CER(V ERM

N EP H ALO Crhombencephalic superventricle

OM

(future fourth ventricle)

RH

"Budding" rhombencephalic choroid plexus

LOWER MEDULLA

Sq

ou s uam

tal

E

C

pi

N

D I E

B

lp

sa na

C

B

M

l ipita occ Axis

Odontoid process

U

al Oropharynx

Larynx

N

INFE RI

T

UPPER MEDULLA

S

isthmal narrows

LLICULU

B as

e tis

glot

Epi

S

CO

N

R

O

ISTHMUS

C

x

Pituitary gland

T o n g u

IO

P

Anterior part a r Intragrandular cleft Intermediate part

ca vi ty

Hyoid bone?

S

OR

s

E P

N

ces

SU

LO

ph

yn

Oral

ON

Sella turcica

so

T

R

Na

Palatal pro

(future aqueduct)

CTUM ETE O L A ME P H SE E NC T E S E G S UBTH A L A M U P

H Y P OTH ALAMU

id

mesencephalic superventricle

A

no

c avity

AL

e

H

al

N C E PH

optic recess

Nerve I (olfactory)

as

LE

on

NTUM ME

N

BASAL GANGLIA

e

Maxilla

on

TE

lb

E

ASAL

OLFACTORY BULB

ta

EPITHALAMUS

THALAMUS

Sph

Fr

CAMPUS PO IP H

PR E AR OPT EA IC

(future lateral ventricle)

ro c e s s

T E L E N C

C

Frontal bon e

E

E

"Blooming" telencephalic choroid plexus

telencephalic superventricle

to

H

P

Fu tur ep ar ie

O N L A

oc

ci

R

E

B

A

N

R

R T E X C O

L

C3 Esophagus

Cervical vertebral column

C4 C5

SP

AL IN

RD O C

central canal (spinal cord)

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

316

PLATE 124C

GW8 Sagittal, CR 33 mm, C145 Level 3: Slide 20, Section 2 NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages. BRAINSTEM FLEXURES

side Midline Left t side Righ

4 3 2

1

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

See high-magnification views of the diencephalon and basal telencephalon in Plates 134A and B, the midbrain, pons, and medulla in Plates 145A and B, the cerebellum in Plates 140A and B.

317

PLATE 124D

Cortical (parietal) NEP Layer I Incipient cortical plate STF1 t1

Cortical (paracentral) NEP Cortical (occipital) NEP

Primordial plexiform layer (cortical plate absent)

Cortical (hippocampal) NEP

nix For

Dashed lines indicate staining and/or sectioning artifacts.

Migrating posterior complex neurons

Cortical (frontal) NEP Choroid plexus stem cells

a l,

su

pe

ar c le nu h e p le x p R a com

jou r t ni

ha ng h a la m ic a n d n m la m e u r o ig r a ti ic n n NE s g P

So

ons neur lus icu oll colliculus) NEP rc rior

ct

c t i R e

a

P E N e t i n P o n Pontomedullary trench Sprouting fibers of hook bundle? Upper medullary NEP

Cerebellar NEP

Dorsal rhombic lip Choroid plexus stem cells

t

Medullary velum

i

u

e sul ap

o n

l

sc

rio r Infelive o

u live fib r o

ro

( te

r Inferio

Medial lemniscus?

m

l ic

f o

Subpial GEP

M (t ese co ecta ncep llic l, i h ulu nfe alic s) rior NE P Ne (tr rv e oc I h le V ar ) Superior cerebellar peduncle External germinal Sojourning and layer migrating deep neurons Sojourning and migrating Purkinje cells

P

r

Premigratory facial motor nucleus (VII) neurons?

phal i c (t

a

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Abducens nucleus (VI)?

gray

Pituitary gland

Central

ng igrati and meurons n rning Sojou othalamic hyp

Substantia nigra/ ventral tegmental area

Interpeduncular nucleus

ce

ic

ndle

egm e n t a l ) NE

la m

ray

tha

d ia Me

bu rain reb l fo

a

en

ral g

Optic tract

C ent

Preoptic NEP

d s? Re leu c nu

l p reo

po p ti c / hy

s ea ar

ph

Mes

le x

te r a

T

Forel's fields

Migrating Medial preoptic neurons forebrain bundle

La

Habenulointerpeduncular tract

li

r io

mp

Nerve I (olfactory)

Migratory stream at base of telencephalon

s le u u c t r ia d n e s lis Be f thmina o er t

Su bs ta nt ia in no m in at a

Mes en ce

pe

r co

Central complex

Se tt

Migrating and settling pretectal neurons

su

e rio

Basal telencephalic NEP

Funnel of thalamocortical axons

Migrating superior colliculus neurons

ng

Ant

Anteromedial ganglionic NEP and SVZ Cortical (olfactory) NEP

Posterior complex (pulvinar?)

Dorsal complex

Strionuclear NEP

Habenular complex

Ist hm al NE P

Fornical GEP

Lower medullary NEP

Raphe nuclear complex

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Ventral rhombic lip

Midline glial raphe system (structural support for brainstem flexures)

Migrating medullary neurons

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Migrating raphe neurons Permanent structure - Times Roman or Bold infiltrate midline raphe glia

Gracile fasciculus Gracile nucleus

Subpial GEP Spinal NEP Ventral gray matter

Intermediate gray matter

Ventral funiculus

Dorsal gray matter (substantia gelatinosa) Dorsal funiculus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

318

PLATE 125A

GW8 Sagittal, CR 33 mm, C145 Level 4: Slide 19, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

319

PLATE 125B

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

co lu m n

Axis

US

(future aqueduct)

UL

LO N

E AR OP EA TIC

LL I C

N CEREBELLUM

T

C E

(LATERAL VERMIS)

rhombencephalic superventricle (future fourth ventricle)

am Squ

LOWER Odontoid process MEDULLA

it a l

"Budding" rhombencephalic choroid plexus

ip

PR

pr

N

N E

T E L

O

OMBENCEPH

O AL

mesencephalic superventricle

oc c

o c e ss

L S

CO

M

ER R

isthmal narrows

U

Fr

S

A

T

ULU

PH

IC

Cridoid cartilage?

LL

Larynx

N

C

t is

ital ccip al o

lo t

O

R

B as

ig Ep

CE

ISTHMUS

UPPER MEDULLA Oropharynx

Hyoid bone?

process

Thyroid cartilage?

RH

nx

T o n g u e bula r

(anterior part)

US

IO

CO

Pituitary gland

ry

es cavity s

SEN

GME TE N

IO

as

AME

R

ON

N

oc

P

Sella turcica

d

pr

C

E AM D HIYPOTH AL

i

ha

n di

ity

op

Oral

av

o

E

P

H

PE

F

l c

n

N

A M US

SU

IN

sa

e

AL

T

M

L

h

TH

U

M TU

Na

i l l a M a x Palatal

Ma

UB

S

A

p

EPITHALAMUS

BASAL GANGLIA

optic recess

S

t on

al as n o

Nasal conchae

bon e

OCAMPUS HIPP

THALAMUS

BAS L TE OLFACTORY A LE BULB NC E PH

t al

E

(future lateral ventricle)

"Blooming" telencephalic choroid plexus

r ie

PRET

R

B E

R

Front al b o C E ne telencephalic superventricle

E

C

H

P

Fu tu r

O N L A

a ep

A

O

C

L

E X R T

ou

s

C3

Clavicle?

C5

b

r

a

l

C4

central canal (spinal cord)

e

r

V

T1

C7

CO RD

t

C6

SP IN AL

Esophagus

e

Trachea

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

320

PLATE 125C

GW8 Sagittal, CR 33 mm, C145 Level 4: Slide 19, Section 2 NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES See a high-magnification view of the diencephalon and basal telencephalon in Plates 135A and B.

BRAINSTEM FLEXURES

4 3 2

1

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

ne side Midli Left t side Righ

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

321

PLATE 125D

Cortical (parietal) NEP

Cortical (paracentral) NEP

Layer I Incipient cortical plate STF1 t1

Cortical (occipital) NEP

Choroid plexus stem cells

Dashed lines indicate staining and/or sectioning artifacts.

Strionuclear NEP

Anteromedial ganglionic NEP and SVZ Basal telencephalic NEP

Dorsal complex

P NE ic la m

Central complex

i

i M e d i al l o ng

c

u

o

s itu pos Pre

f r

a

s leu nuc

m

t n i o

Posterior intramural migratory stream (inferior olive neurons)

Inferior olive fibrous capsule

rio r Infelive o

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

tu d i

n

fas al

cic

ul u

N E

s

P

Superior cerebellar peduncle

Sojourning and migrating deep neurons

Pontomedullary trench

Subpial GEP?

Medial lemniscus?

Nerve IV (trochlear)

Isthmal NEP?

n e P o n t i

a r

Premigratory facial motor nucleus (VII) neurons?

Mesencephalic (tectal, inferior colliculus) NEP

Trochlear nucleus (IV)

l

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

neurons

Pituitary gland

Mesencephalic (tegmental) NEP

s culu o lli

Optic tract and chiasm

Interpeduncular nucleus

Mammillary body

Ventromedial nucleus

Substantia nigra

ia l n ed ai M rebr dle fo bun

M fore edial b bun rain dle

Migratory stream at base of telencephalon Migrating preoptic neurons Preoptic NEP

Settling tegmental neurons

Sojourning and migrating thalamic neurons

rc

For el's fiel ds

Se

Th a

Reticular nucleus

reas c/hypothalamic a Lateral preopti

Migrating basal telencephalic neurons

Settling pretectal neurons

r io

Substantia innominata

Settling thalamic neurons

pe

us nucle Bedthe strias of minali te r

Cortical (olfactory) NEP

Migrating superior colliculus neurons

Settling habenular complex neurons

u , al gs ct EP in (te ) N ttl ic s a l u lu p h lic ce ol en r c e s io M per ray ral g su C en t

Funnel of thalamocortical axons

Posterior complex (pulvinar?)

t R e

Cortical (frontal) NEP

Primordial plexiform layer (cortical plate absent)

Cortical (hippocampal) NEP

Fornical GEP

Sprouting fibers of hook bundle? Sojourning and migrating Purkinje cells

External germinal layer Dorsal rhombic lip

Upper medullary NEP

Cerebellar NEP Medullary velum

Choroid plexus stem cells

Lower medullary NEP Ventral rhombic lip Migrating gracile nucleus neurons?

Migrating spinal dorsal gray neurons Midline glial raphe system (structural support for brainstem flexures)

Gracile fasciculus?

Spinal GEP Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Migrating interfascicular glia infiltrate midline raphe glia?

Spinal NEP Ventral funiculus Ventral gray matter

Central autonomic area Dorsal funiculus Intermediate gray matter

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

322

PLATE 126A

GW8 Sagittal, CR 33 mm, C145 Level 5: Slide 18, Section 2 HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

323 Dashed lines indicate staining and/or sectioning artifacts.

Meninges (dura and arachnoid)

U

US UL

CO

M

R

mesencephalic superventricle (future aqueduct)

LL I C

N

CEREBELLUM (HEMISPHERE)

rhombencephalic superventricle (future fourth ventricle)

am Squ

ou

s

co lu m

n

LOWER MEDULLA

it a l

IE

US

D

UL

ER

ip

N E

T E L

LO N

o c e ss

pr

T

IC

Fr

LL

Odontoid process

C

Axis

IS TH M US

IO

Larynx

Cridoid cartilage?

HA

"Budding" rhombencephalic choroid plexus

ital

pharynx

Atlas?

S

EP

ON

Oro

Ep

Thyroid cartilage?

p cci l o Basa

x ttis iglo

NC

O M BENCEPHALO

UPPER MEDULLA

E

CO

d

yn

Hyoid bone?

process

TEGME

isthmal narrows

i ar

cavit s y

P

R

o

es

RH

MESE

N

SU

F

n a

T o n g u e bula r

O

E

T

UM

IN

e

n di

S THALAMU

P

Sella turcica

ph

O r a l

N

SUB

H

MUS ALA H T PO HY

so

Palatal pr oc

P

L

CT

IO

h Nasal cavity

i l l a M a x

Ma

p

bo ne

L

S

N

C

E

A

ON

UM NT

Nasal conchae

al

R

BASAL GANGLIA A NC E P H

iet

OCAMPUS HIPP EPITHALAMUS

THALAMUS

OLFACTORY BAS AL BULB TEL E

ar

E

(future lateral ventricle)

t on

"Blooming" telencephalic choroid plexus

ep

oc c

R

B E

E R

Front al b on e C telencephalic superventricle

l sa a on

E

C

H

P

Fu tu

O N L A

PRET

C

L

Brain surface (pia, heavier line)

E X R T

O

r

A

PLATE 126B

Skull and skin

Clavicle?

C4

Sternum?

r

a

l

Tracheal cartilagenous rings

Esophagus

V T3

C3

e

r

te

b

C5

C6

C7

T1

T2

D OR C AL N I P

central canal (spinal cord)

S

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

324

PLATE 126C

GW8 Sagittal, CR 33 mm, C145 Level 5: Slide 18, Section 2 NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES See a high-magnification view of the diencephalon and basal telencephalon in Plates 136A and B.

BRAINSTEM FLEXURES

4 3 2

1

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages. ine side Midl Left t side Righ

325 Cortical (paracentral) NEP

PLATE 126D

Cortical (parietal) NEP

Layer I Incipient cortical plate STF1 t1 Cortical (hippocampal) NEP Cortical (occipital) NEP

Fornical GEP Choroid plexus stem cells Cortical (frontal) NEP

Migrating posterior complex neurons

Settling habenular complex neurons

Posterior complex

Internal capsule

Dorsal complex Settling thalamic

neurons

pe

Sojourning and migrating deep neurons?

t i R e

c

e t i n P o n

l a r

N E

P

Superior cerebellar peduncle

Mesencephalic (tectal, inferior colliculus) NEP

Pontomedullary trench Upper medullary NEP

Sojourning and migrating Purkinje cells

s leu uc sn itu os ep Pr

f

o r

m

Cerebellar NEP

External germinal layer Dorsal rhombic lip

Medullary velum

a

Posterior intramural migratory stream (inferior olive neurons) Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

o n t i

rio r Infelive o

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Mesencephalic (tectal, superior colliculus) NEP

Parabrachial nucleus?

u

Reticular tegmental nucleus (intermingled with the raphe nuclear complex)

ons neur lus icu o ll

Superior cerebellar peduncle

Optic tract

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Settling tegmental neurons

rc

Migrating basal telencephalic neurons

rio

Substantia nigra

othalamic area Lateral hyp

Migratory stream at base of telencephalon

su

rain reb l fo diabundle e M

ng

Sojourning and migrating thalamic neurons

ray

Zona incerta

Thalamic NEP

i

ral g

G lo b us p a llid us Substantia innominata

Se ttl

Settling pretectal neurons

Ventral complex

Funnel of thalamocortical axons Central Bed nucleus complex Reticular of the stria nucleus terminalis

Migrating superior colliculus neurons

C ent

Basal telencephalic NEP Cortical (olfactory) NEP

Dashed lines indicate staining and/or sectioning artifacts.

Strionuclear NEP

Anteromedial ganglionic NEP and SVZ

Primordial plexiform layer (cortical plate absent)

Lower medullary NEP Ventral rhombic lip

Gracile fasciculus Gracile nucleus

Ventral gray matter Ventral funiculus ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Intermediate gray matter Dorsal funiculus Central autonomic area Spinal NEP

Arrows indicate the presumed direction of axon growth in brain fiber tracts. Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

326

PLATE 127A

GW8 Sagittal, CR 33 mm, C145 Level 6: Slide 16, Section 2 Left side of brain HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

327

PLATE 127B telencephalic superventricle

Skull and skin

(future lateral ventricle)

E

N

C E R

asa ton

Fr on

process

O M B E N C EPH A

Thyroid gland?

(future fourth ventricle)

ip

oc c

LOWER MEDULLA

a Squ

mo

us

C3

C5

a C6

O

r

b

C

C7

L

e

rhombencephalic superventricle

C4

e

r

t T1

A

V

(HEMISPHERE)

"Budding" rhombencephalic choroid plexus

Axis

l

First rib? Clavicle?

CEREBELLUM

LO N

D

Second rib?

Larynx

(future aqueduct)

R

Hyoid bone?

co lu mn

bula r

R CO

UPPER MEDULLA

c av i t y

ccipital al o

n di

O

S

B as

Ma

tal proces s ala

US

mesencephalic superventricle

U M

i l l a M a x

N

S

RH

O

T

P

LU

IS T HM

C

Orbitosphenoid

U IC ON I LL AL INFE R H

N

CO

LO

R

l pr

T

US

O

NC E P H A

bo ne

E

BASA LT ELE

Petrous temporal bone Temporal bone labyrinth

P O r a l

al

N SUPE RI A LO M H A T ES H E EP TEG NC C S M U E EP EN HALAM I T D S UB M LA

BASAL GANGLIA

OLFACTORY BULB

iet

AMPUS PPOC HI

T E L

Frontal b one

E

C

"Blooming" telencephalic choroid plexus

ar

UM NT

o c ess

E

H

P

Fu tu re p

O N A L

I C U L US

B

R

A

O

C

L

E X R T

it a l

Brain surface (pia, heavier line)

LL

Meninges (dura and arachnoid)

S

P

I

N

T2

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

328

PLATE 127C

GW8 Sagittal, CR 33 mm, C145 Level 6: Slide 16, Section 2 Left side of brain NEUROEPITHELIAL/ GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the diencephalon and basal telencephalon from slide 17 section 2 in Plates 137A and B.

BRAINSTEM FLEXURES 4 3 2

1

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

Layer I Incipient cortical plate STF1 t1

Choroid plexus stem cells Fornical GEP Cortical (hippocampal) NEP

Posterior ganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ

Cortical (frontal) NEP

Cortical (occipital) NEP Primordial plexiform layer (cortical plate absent)

Migrating posterior complex neurons

Settling super

Settling thalamic neurons

Settling tegmental neurons

neu

t

ro n

s

Subthalamic nucleus

Optic tract

Primary olfactory cortex Lateral olfactory tract

a ct i c tr Opt

S u b s t an

us

Reticular nucleus

co

l cu

Ventral complex

Funnel of thalamocortical axons

ior

a

Dorsal complex

l li

innominata

Internal capsule

nigra

e ul en s? ps ca l am axon a t n r Pu ugal Globus te Ex p a ll of id u s tic or rc e e n Substantia o Pi

Posterior complex

Ce n t r

Cauda te

ia

Cortical (olfactory) NEP

PLATE 127D

Cortical (parietal) NEP

Cortical (paracentral) NEP

329

Lateral lemniscus

lg

ray

Mesencephalic (tectal, superior colliculus) NEP

Nucleus of the lateral lemniscus

R

e

t

i

c

u

Po n

a

Petrous temporal bone

Sojourning and migrating deep neurons?

l

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Parabrachial nucleus

tine

NE

P

Pontomedullary trench

r

Sprouting fibers of hook bundle?

Temporal bone labyrinth

f

o

r

m

Cerebellar NEP

Sojourning and migrating Purkinje cells

a

Medullary velum

t

Ventral rhombic lip

i

Lower medullary NEP

o

Cuneate fasciculus Cuneate nucleus

n Solitary nucleus and tract

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Ventral gray matter

Dorsal rhombic lip

Upper medullary NEP

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Ventral funiculus

Superior cerebellar peduncle

Mesencephalic Mesencephalic (tectal, inferior (tectal, inferior colliculus) NEP colliculus) NEP External germinal layer

Intermediate gray matter Dorsal gray matter (substantia gelatinosa) Dorsal funiculus

Arrows indicate the presumed direction of axon growth in brain fiber tracts. Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

330

PLATE 128A

GW8 Sagittal, CR 33 mm, C145 Level 7: Slide 15, Section 1 Left side of brain HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

331

PLATE 128B

telencephalic superventricle

Skull and skin

(future lateral ventricle)

Meninges (dura and arachnoid) Brain surface (pia, heavier line) C

O

E X R T

A R B

E

C

"Blooming" telencephalic choroid plexus

T E L

BASAL GANGLIA EL

Orbitosphenoid

ENCE

THALAMUS

PH A L O

ISTHMUS

Trigeminal ganglion (V) Spiral ganglion (VIII)

(adjacent to temporal bone labyrinth)

P

O

Eustachian tube?

Nerve VIII (vestibulocochlear) Basal occipital?

N LO A H EP

(HEMISPHERE)

rhombencephalic superventricle (future fourth ventricle)

"Budding" rhombencephalic choroid plexus

LOWER MEDULLA

ou m

s

t ipi occ

al?

SP

IN AL

Ve

CEREBELLUM

CO RD

rt eb

ra

lc olu m

n

Inferior ganglion (X)?

S

RHO MB EN C

UPPER MEDULLA

Maxilla

N

INFERIOR COLLICULUS

Squ a

Petrous temporal bone

Nerve II (optic)

Dorsal root ganglion (boundary cap)

bo ne

MESENCEPHALON

AMYGDALA

EYE

Mandibular process

al

SUPERIOR COLLICULUS

DIENCEPHALON

N

Pigment layer of retina Sclera

Oral cavity

iet

UM CT TE

BASAL T

ar

AMPUS PPOC HI

E

N

C E R

Frontal bone

E

H

P

Fu tu re p

O N A L

L

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

332

PLATE 128C

GW8 Sagittal, CR 33 mm, C145 Level 7: Slide 15, Section 1 Left side of brain NEUROEPITHELIAL/ GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the basal ganglia and amygdala in Plates 132A and B.

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

333 Cortical (parietal) NEP

PLATE 128D

Cortical (paracentral) NEP Layer I Incipient cortical plate STF1 t1 STF5

Choroid plexus stem cells

Cortical (temporal/ occipital) NEP

Fornical GEP

Cortical (frontal) NEP

Posterior ganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ

Cortical (dorsal hippocampal) NEP

Primordial plexiform layer (cortical plate absent)

Cau date

I

nter s? nal c on apsu ax al le g n u f e o Thick bundled m ic t a r t o corticothalamic axons? c u P er G lo ne Anterior Central Pio commissure pall bus complex id us

Primary olfactory cortex Lateral olfactory tract

Substantia innominata

Cort ico com medial plex

Superior colliculus

Posterior complex

Optic trac t

Cortical (ventral hippocampal) NEP

Amygdaloid NEP

Lateral lemniscus

Inferior colliculus

Nuclei of the lateral lemniscus (dorsal and ventral) Principal sensory nucleus (V)? Nerve V (trigeminal)

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Sojourning and migrating deep neurons?

Sprouting fibers of hook bundle?

Trigeminal ganglion (V)

Superior cerebellar peduncle

Spiral ganglion (VIII)

Mesencephalic Mesencephalic (tectal, inferior (tectal, colliculus)inferior NEP colliculus) NEP External germinal layer

Dorsal rhombic lip

Petrous temporal bone

Cerebellar NEP

Sojourning and migrating Purkinje cells

Nerve VIII (vestibulocochlear) Superior olivary complex? Posterior intramural migratory stream (inferior olive neurons) Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Ventral rhombic lip

Vestibular nuclear complex Solitary nucleus and tract

Inferior ganglion (X)?

Dorsal funiculus

Dorsal root ganglion (boundary cap) Subpial GEP?

Dorsal gray matter (substantia gelatinosa) Lateral funiculus

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Arrows indicate the presumed direction of axon growth in brain fiber tracts. Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

334

PLATE 129A

GW8 Sagittal, CR 33 mm, C145 Level 8: Slide 13, Section 2 Left side of brain HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

335

PLATE 129B Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line) R

EYE

bit

o-

Intraretinal space

BASAL T

EL

ENCE

PH A L O

HIPPOC

BASAL GANGLIA N

iet

Vitreous body

bo ne

telencephalic superventricle

PUS AM

(future lateral ventricle)

MBENCEPHA LO RHO N

Nerve V (boundary cap) Nerve V (trigeminal)

N S P O

Spiral ganglion (VIII)

(adjacent to temporal bone labyrinth)

Eustachian tube?

Meckel's cartilage

Vestibular ganglion (VIII)

Nerve VIII (vestibulocochlear) Nerve IX (glossopharyngeal) Nerve X (vagus)

(future fourth ventricle)

Rhombencephalic choroid plexus

ou m

s

t ipi occ

al?

n m

u

o

l

b

r

V

e

r

t

e

o D

r

sa

l

a

r

V

o

e

o

c

t

r

t

g

l

a

e

n

b

g

r

a

li a

l

c

o

l

u

m

n

Squ a

Superior ganglia (X)? Inferior ganglion (X)?

rhombencephalic superventricle

LOWER M EDULLA

Petrous temporal bone

(HEMISPHERE)

X d ? an aps IX y c es ar rv nd Nebou

Oral cavity?

CEREBELLUM

M UP ED P U ER LL A

Facial ganglion (VII)

Mandibular process

al

enoAMYGDALA id

Trigeminal ganglion (V)

Maxilla

ar

sph

Eyelid Neural retina

Telencephalic choroid plexus

E L

T E Or

Sclera Pigment layer of retina

ep

N

Frontal bone

C

E

E

C

H

P

R

E

Fu tu

O N A L

r

B

R T E X C O

A L

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

336

PLATE 129C

GW8 Sagittal, CR 33 mm, C145 Level 8: Slide 13, Section 2 Left side of brain

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the basal pons and peripheral ganglia from the right side of the brain in Plates 146 to 147A and B.

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

337

PLATE 129D

Cortical (parietal) NEP

Cortical (paracentral) NEP

ex cort

Ca ud ter ate na lc ap su Putamen le

l ca

t in

Lateral olfactory tract

er na

ie n

E

xt

Primary olfactory cortex

Anterolateral ganglionic NEP and SVZ Posterior ganglionic NEP and SVZ

In

Pioneer corticofugal axons?

Lateral migratory stream?

ad

Corticoganglionic NEP and SVZ

gr

Layer I Cortical plate STF1 t1 STF 5

ore (m ior r te

ic

An

Cortical (frontal) NEP

(less mature) morph oge posterior e) to r ne u t t ma

Compact-bundled corticothalamic axons? p sul e Globus tele Bas pallidus

nce al pha lon

Primordial plexiform layer (cortical plate absent)

Cortical (temporal/occipital) NEP

Cortical (dorsal hippocampal) NEP al er lat x so mple a B co

Amygdaloid NEP

Co rti com com ple edia x l

Cortical (ventral hippocampal) NEP

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Nerve V (trigeminal, boundary cap) Nerve V (trigeminal)

Lateral lemniscus?

Sprouting fibers of hook bundle?

Reticular formation

Trigeminal ganglion (V)

Sojourning and migrating deep neurons? Sojourning and migrating Purkinje cells External germinal layer Superior cerebellar peduncle

Dorsal rhombic lip

Vestibular ganglion (VIII) Pontine NEP

Facial ganglion (VII)?

Spiral ganglion (VIII)

Petrous temporal bone

Upper medullary NEP

Ve n sti co ucl bul m ea ar pl r ex

Cerebellar NEP

Inferior cerebellar peduncle

Nerve VIII (vestibulocochlear) Nerve IX (glossopharyngeal)? Nerve X (vagus)?

Posterior precerebellar NEP Anterior precerebellar NEP

Ventral rhombic lip

Inferior ganglion (X)? Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

338

PLATE 130A

GW8 Sagittal, CR 33 mm, C145 Level 9: Slide 12, Section 4 Left side of brain HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

339

PLATE 130B

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

E

R E

L

E

N

C

ENCE

PH A L O

HIPPOC

T E o-

EL

N

AMYGDALA

sph

eno

id

ENCEPHA LO OMB H R N U L M L

Nerve V (boundary cap) Nerve VIII (vestibulocochlear) Nerve V (trigeminal)

Trigeminal ganglion (V) Spiral ganglion (VIII)

PONS

(adjacent to temporal bone labyrinth)

BE RE CE

Meckel's cartilage

(H EM

ISP

HE R E )

rh omb e ence icl phali c superventr le) M UP c

Facial ganglion (VII) Eustachian tube?

N bo erv E P un e s D U E R da IX ry an LL ca d A ps X ?

Vestibular ganglion (VIII)

Petrous temporal bone

Nerve X (vagus)

Superior ganglion (IX)? Superior ganglion (X)?

Nerve IX (glossopharyngeal)

i

Rhombencephalic choroid plexus

cc i so u mo ua q S

pit

a

n m

u l

l

a

e

r e

V

D

o

t

r

sa

b

l

r

r

V

o

e

o

r

t

c

t

o

g

e

a

b

n

r

g

a

l

li a

c

o

l

u

m

n

Inferior ganglion (X)?

ntr ( f uture fourth ve

LOWER MEDULLA

Mandibular process

PUS AM

l?

Frontal bone

ne bo

Vitreous body

Intraretinal space

Maxilla

t al

bit

Eyelid Neural retina

(future lateral ventricle)

e ari ep ur

Or

Sclera Pigment layer of retina

telencephalic superventricle

Telencephalic choroid plexus

BASAL GANGLIA

BASAL T

EYE

H

P

E

C

O N A L

t Fu

B

L

A

R

X R T E C O

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

340

PLATE 130C

GW8 Sagittal, CR 33 mm, C145 Level 9: Slide 12, Section 4 Left side of brain

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the basal pons and peripheral ganglia from the right side of the brain in Plates 146 to 147A and B.

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

See a highmagnification view of the cerebellum from this section in Plates 141A and B.

341

PLATE 130D

Cortical (paracentral) NEP

Cortical (frontal) NEP

Cortical (parietal) NEP

ie ad gr

ture) morphogen ss ma eti c or (le i r e t s o po t ) re atu em r o

Corticoganglionic NEP and SVZ

E xt

Lateral migratory stream

ern

Pioneer corticofugal axons?

al

Putamen

p

su

Ca ter ud na ate lc ap su le

Thick bundled corticothalamic axons?

ca

Primary olfactory cortex

le

Su innobstant min ia ata?

Lateral olfactory tract

Anterolateral ganglionic NEP and SVZ

Cortical (temporal) NEP

Posterior ganglionic NEP and SVZ Primordial plexiform layer (cortical plate absent)

Cortical (dorsal hippocampal) NEP Globus pallidus

Amygdaloid NEP

Ba co sola m te pl ra ex l

In

x orte

An ter ior

(

in c

m

nt

Layer I Cortical plate STF1 t1 STF 5

Cortical (ventral hippocampal) NEP

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Principal sensory nucleus (V)? Nerve V (trigeminal, boundary cap) Nerve V (trigeminal) Trigeminal ganglion (V)

Sprouting fibers of hook bundle?

Vestibular nuclear complex

Sojourning and migrating deep neurons? Sojourning and migrating Purkinje cells External germinal layer

Pontine NEP

Nerve VIII (vestibulocochlear, boundary cap) Nerve VIII (vestibulocochlear)

Superior cerebellar peduncle

Dorsal rhombic lip

Vestibular ganglion (VIII)

Spiral ganglion (VIII)

Petrous temporal bone

Superior ganglion (IX)?

io r r f e r lla In rebe ncle ce edu p

Facial ganglion (VII)?

Upper medullary NEP

Nerve X (vagus)? Nerve IX (glossopharyngeal)?

Inferior ganglion (X)?

Cerebellar NEP

Reticular formation

Superior ganglion (X)?

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Posterior precerebellar NEP Anterior precerebellar NEP Ventral rhombic lip

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

342

PLATE 131A

GW8 Sagittal, CR 33 mm, C145 Level 10: Slide 11, Section 4 Left side of brain HEAD STRUCTURES, MAJOR BRAIN REGIONS, AND VENTRICULAR DIVISIONS

Neuroepithelial divisions, glioepithelial divisions, and differentiating structures are labeled in Parts C and D of this plate on the following pages.

343

PLATE 131B

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

it o

-s

Eyelid

(future lateral ventricle)

Vitreous body

PH A L O

en

oi

N

d

Nerve VIII (boundary cap) Nerve VIII (vestibulocochlear) Nerve V (trigeminal)

Intraretinal space Pigment layer of retina

ENCEPHA LO OMB H R N

PON

Trigeminal ganglion (V) Vestibular ganglion (VIII)

U BELL M (HE RE MI S PH CE ER E)

rho icl mben cephalic superventr ricle M UP t n e ED P th v ( f u t u r e f our U ER LL A

)

S

Maxilla? Petrous temporal bone

Meckel's cartilage

Nerve IX (glossopharyngeal)

Spiral ganglion (VIII)

Rhombencephalic choroid plexus

Inferior ganglion (IX)? Petrous temporal bone

Nerve X (vagus)

ou am

ra

l

V

e

r

t

e

b

r

a

l

c

o

l

u

m

n

Inferior ganglion (X)?

Sq u

Superior ganglion (X)?

(adjacent to temporal bone labyrinth)

o mp s te

?

Eustachian tube?

Mandibular process

iet al bo ne

P PO CA M PU S

ENCE

AMYGDALA ph

ar

HI

rb

ur ep

telencephalic superventricle

BASAL GANGLIA

EL

Fu

e

Sclera

Neural retina

E

TE L BASAL T

O

EYE

C

N LO A PH

E

Frontal bone

C

N

E

R

E

R

L

A

t

B

X R T E C O

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

344

PLATE 131C

GW8 Sagittal, CR 33 mm, C145 Level 10: Slide 11, Section 4 Left side of brain

NEUROEPITHELIAL/GLIOEPITHELIAL DIVISIONS AND DIFFERENTIATING BRAIN STRUCTURES

See a high-magnification view of the basal pons and peripheral ganglia from the right side of the brain in Plates 146A and B to 147A and B.

The head, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

345

PLATE 131D

Cortical (paracentral) NEP

Cortical (parietal) NEP

Anterior (more mature) to posterior (less mature) morphogenetic gradient in cortex

Layer I Cortical plate STF1 t1 STF 5

Corticoganglionic NEP and SVZ

Lateral olfactory tract Primary olfactory cortex

In ter na l

Pioneer corticofugal axons?

Ca ca ps uda ule te

S innubst om ant ina ia ta

Primordial plexiform layer (cortical plate absent)

Posterior ganglionic NEP and SVZ

Compact-bundled corticothalamic axons?

Ba c o so la m te r pl a ex l

Lateral migratory stream (percolates through external capsule)

Cortical (temporal) NEP

Anterolateral ganglionic NEP and SVZ

Cortical (hippocampal) NEP

Amygdaloid NEP Cortical (parahippocampal) NEP

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons) Cochlear nuclei? Nerve VIII (vestibulocochlear, boundary cap) Nerve V (trigeminal) Trigeminal ganglion (V)

Sojourning and migrating deep neurons? Sojourning and migrating Purkinje cells External germinal layer?

Superior cerebellar peduncle

Vestibular ganglion (VIII)

Spiral ganglion (VIII)

Sprouting fibers of hook bundle?

Inferior cerebellar peduncle

Pontine NEP

Petrous temporal bone

Dorsal rhombic lip

Cerebellar NEP

Anterior precerebellar NEP in ventral rhombic lip

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Inferior ganglion (IX)?

Superior ganglion (X)? Nerve IX (glossopharyngeal) Nerve X (vagus) Inferior ganglion (X)?

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

GW8 Sagittal, CR 33 mm, C145 Level 7: Slide 15, Section 1

See the entire section in Plates 128A-D.

BASAL GANGLIA, BASAL TELENCEPHALON, AND AMYGDALA

346

PLATE 132A

PLATE 132B

telencephalic superventricle

telencephalic superventricle

(future lateral ventricle)

Migrating basal ganglia neurons

R

Diffuse region with corticofugal axons?

M

In ter na l

e ul

Migrating ganglionic neurons

ca ps ule

l

ca

BASAL GANGLIA Central complex

Anterior commissure?

Globus pallidus

AMYGDALA

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

NEP

Basal telencephalon (substantia innominata)

daloid

Corticomedial complex

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Choroid plexus stem cells

Compact-bundled corticothalamic axons?

Putamen

ps

Caudate

A my g

Externa

U

hippocampal) NEP

S

T

A

I

T

Telencephalic choroid plexus

ntral C o r tical (ve

c ni io P) VZ) l g E a n (N e (S g al m on er eliu ar z t a l ol ith u er oep tric t A n eu r ven n ub s d n a

c ni io gl Z an V rg S io nd er a st EP Po N

(future lateral ventricle)

347

GW8 Sagittal, CR 33 mm, C145 Level 2: Slide 22, Section 2

See the entire section in Plates 123A-D.

HYPOTHALAMUS AND PREOPTIC AREA

348

PLATE 133A

PLATE 133B

p y

H

N E P t i c

p

r

in

fu n re di ce bu ss la

PR EO PT IC

Mi dd le

P

NE

P

Optic tract

E

Sojourning and migrating hypothalamic neurons

N

Median eminence

c m i la

P r e o

P

ic

d

hy

m

id

(future third ventricle)

y p ot h

A n t e rior

th po

ala

M

diencephalic superventricle

m preoptic recess

N E P

H

la

NE

diencephalic superventricle

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

o

Hypothalamic i c neuroepithelium (NEP)

(future third ventricle)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

alami c th

le

ha

Diagonal band of Broca (vertical limb)?

Sojourning and migrating hypothalamic neurons

t rior hypo

Sojourning and migrating preoptic neurons

HYPOTHALAMUS

a

SEPTUM

Ante

AR EA

Medial septal nucleus?

Sojourning and migrating hypothalamic neurons (future arcuate nucleus?)

Tuberal part Anterior lobe (adenohypophysis)

Pituitary gland

Distal part Intraglandular cleft Intermediate part Posterior lobe (neurohypophysis)

349

See the entire section in Plates 124A-D.

DIENCEPHALON AND BASAL TELENCEPHALON

350

PLATE 134A GW8 Sagittal, CR 33 mm, C145 Level 3: Slide 20, Section 2

Anteromedial ganglionic NEP and subventricular zone (SVZ)

PREOPTIC AREA

Pituitary gland

yp

ot

ha

HYPOTHALAMUS

B

T

H

Central complex? A

L A Forel's fields M

la

m

ic

ar

m a nd

i gr

U

S

Su

la btha

ea

Primordial plexiform layer (cortical plate absent)

a ti

n

am

o

EPITHALAMUS (Habenular complex)

ic rning la m u a o h P oj E al t e n tr i c N C e n t r a l/ v

s

m

PRETECTUM Migrating and settling pretectal neurons

Me dia

l for So ebr ain jou bun hy rni dle po n Subs tha g a Interventral tanti lam nd peduncular teg a m ic me n i nucleus ne grat ur i on ng s

/ ra ea ig tal ar n

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ic/h

U

l ha gt

r eu

en

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

opt

S

Ventral complex?

ab

Optic tract

Medial forebrain bundle

p re

Reticular nucleus

Stria medullaris

H

Migrating preoptic L a t era neurons l

Preoptic NEP preoptic recess

THALAMUS

ns

Bed nucleus of the stria terminalis

n

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Posterior complex (pulvinar?)

ic

BASAL TELENCEPHALON

Strionuclear NEP

Cortical (occipital) NEP

M ig co rat m in g pl p ex o n e ste u r r io on r s

lla ris

Dorsal complex

Funnel of thalamocortical axons in internal capsule

S

Migratory stream at base of telencephalon

(future lateral ventricle, posterior pool)

N te r EP pe du nc ula rt ra ct

BASAL GANGLIA

Migrating ganglionic neurons

telencephalic superventricle

HI PP O Str CA MP Ammonic migration ia me US du

Basal telencephalic NEP

Migrating basal telencephalic neurons

Nerve I (olfactory) olfactory recess

Fornix Dentate migrati on

in

(future lateral ventricle, anterior pool)

Ante rior c ompl ex

OLFACTORY BULB

Telencephalic choroid plexus

Cortical (hippocampal ammonic) NEP

o-

Cortical (frontal) neuroepithelium telencephalic (NEP) superventricle Cortical (olfactory) NEP

Cortical (hippocampal dentate) NEP

Fornical glioepithelium (GEP) Choroid plexus stem cells

ul

PLATE 134B

Mesencephalic (tectal, superior colliculus) NEP

MIDBRAIN TEGMENTUM

Mesencephalic (tegmental) NEP

mesencephalic superventricle

(future cerebral aqueduct)

Central gray

351

See the entire section in Plates 125A-D.

DIENCEPHALON AND BASAL TELENCEPHALON

352

PLATE 135A GW8 Sagittal, CR 33 mm, C145 Level 4: Slide 19, Section 2

PLATE 135B

Cortical (hippocampal dentate) NEP

Fornical GEP Choroid plexus stem cells

Telencephalic choroid plexus

Cortical (frontal) neuroepithelium (NEP) telencephalic superventricle

Cortical (olfactory) NEP Migrating basal telencephalic neurons

Fornix

Anteromedial ganglionic NEP and subventricular zone (SVZ)

(future lateral ventricle, anterior pool)

Migrating striatal neurons

Funnel of thalamocortical axons in internal capsule

Strionuclear NEP

Dorsal complex

BASAL GANGLIA BASAL TELENCEPHALON

La

PREOPTIC AREA

Migrating preoptic neurons

/ hy

po

th

B T Fo H re A l's L fie A lds M

al

M for ed i bu ebra al nd in le

ct

HYPOTHALAMUS Ventromedial nucleus

am

ic

ar

ea

U

S

s

Interpeduncular nucleus Mammillary body

al Medi ain r foreb dle bun

Su

nigra tia tan bs

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

O

p

c ti

a tr

al p reo pti c

U

IN RA M DB TU MI MEN G TE

preoptic recess Optic chiasm Glioepithelium (GEP) (optic chiasm and tract)

ter

Posterior complex (pulvinar?)

Habenulons interpero u duncular e n tract ic m l la a a r t h P x n EPIgt Ve mple NE THALAMUS tin a c o r i c (Habenular ig m la complex) dm a n th ga l n ni ra ur nt Subthalamic NEP jo e o V S

Reticular nucleus

S

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

M ig ra c o m tin g p o p le x s te r n e u io r ron s

THALAMUS

Bed nucleus of the stria terminalis

Migratory stream at base of telencephalon

Preoptic NEP

Primordial plexiform layer

(cortical plate absent) H Str IPPO Ammonic migration C ia A MPU me d S

ull ar is

OLFACTORY BULB

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

(future lateral ventricle, posterior pool)

Dentate mig ration

Basal telencephalic NEP

Nerve I (olfactory) olfactory recess

Cortical (hippocampal ammonic) NEP telencephalic superventricle

353

GW8 Sagittal, CR 33 mm, C145 Level 5: Slide 18, Section 2

See the entire section in Plates 126A-D.

BASAL TELENCEPHALON AND DIENCEPHALON

354

PLATE 136A

PLATE 136B

Layer I Cortical plate STF1 t1

Fornical GEP Choroid plexus stem cells

Telencephalic choroid plexus

telencephalic superventricle

telencephalic superventricle

Forn Dentate ix migratio n

(future lateral ventricle, anterior pool)

Cortical (olfactory) NEP Migrating basal telencephalic neurons

H IP P O

Basal telencephalic NEP Migrating ganglionic neurons

OLFACTORY BULB

Stria

Funnel of thalamocortical axons in internal capsule

US

M ig medu r a ti llaris ng p

o s te rio r com p le x neu ron s

Dorsal complex

Posterior complex (pulvinar?)

Lat

B T H A For L A el's M fiel U ds S

eral h ypot hal am ic Dorsomedial ar ea nucleus? ?

Medial forebrain bundle

Mammillary body?

Interpeduncular nucleus?

S

ni

ur

o oj

ng

d

an

r

ig

m

in at

EPITHALAMUS (Habenular complex)

Red nucleus? Su bs

N AI M BR TU ID N M ME G TE igra

HYPOTHALAMUS

g

Central complex

th

n

TUM

S U

Reticular nucleus

ic

m

a al

s

TEC

Globus pallidus

on

r eu

PRE

al n tr le x e p V m co

Bed nucleus of the stria terminalis

Ventromedial nucleus?

CAMP

Primordial plexiform layer (cortical plate absent)

Ammonic migration

n ia nt ta

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Strionuclear NEP

BASAL GANGLIA

TE Migratory stream LE B at base of telencephalon NC AS EP AL Nerve I (olfactory) H AL olfactory recess O N Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain Optic fiber tracts. tract

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium STF - Stratified transitional field SVZ - Subventricular zone

(future lateral ventricle, posterior pool)

N EP

Anteromedial ganglionic NEP and SVZ

Cortical (hippocampal ammonic) NEP

Cortical (hippocampal dentate) NEP

Ve nt ra lt ha la m ic

Cortical (frontal) NEP

355

GW8 Sagittal, CR 33 mm, C145 Between levels 5 and 6: Slide 17, Section 2

See level 5 in Plates 126A-D, level 6 in Plates 127A-D.

BASAL TELENCEPHALON AND DIENCEPHALON

356

PLATE 137A

PLATE 137B

Fornical GEP

Cortical (frontal) NEP Anterolateral ganglionic NEP and subventricular zone (SVZ)

Strionuclear GEP

s ic n lam tha tin g So

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Lateral hypothalamic area HYPO THAL AMUS

Subthalamic nucleus?

Sub sta nt i

a

Optic tract

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Central S U complex B T H A Fore L A l's fie M U lds/z S ona i ncer ta

N AI M BR TU ID EN M GM TE ra nig

Nerve I (olfactory) olfactory recess

Reticular nucleus

igr a

Globus pallidus

M TU EC ET PR

Ventral complex

BASAL GANGLIA

TE LE BA NC SAL EP Migratory stream HA LO at base of telencephalon N

Posterior complex (pulvinar?)

Ventral complex

eu

Pioneer corticofugal axons?

Dorsal complex

Funnel of thalamocortical axons in internal capsule

ro n

Stria terminalis

dm

M

an

R

IA

TU

Primordial plexiform layer (cortical plate absent)

posterior complex ne ting uro g ra ns i M

ing

T

Putamen/ ventral striatum Olfactory tubercle?

Dentate migration

Stria medullaris

rn

Migrating ganglionic neurons

Ammonic migration

HIPPOCAMPUS

Caudate

S

Cortical (olfactory) NEP

(future lateral ventricle, posterior pool)

x Forni

(future lateral ventricle, anterior pool)

Basal telencephalic NEP

telencephalic superventricle

Telencephalic choroid plexus

jou

telencephalic superventricle

Choroid plexus stem cells

Posterior ganglionic NEP and SVZ

Cortical (hippocampal ammonic) NEP

Cortical (hippocampal dentate) NEP

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

357

See level 1 in Plates 122A-D.

GW8 Sagittal, CR 33 mm, C145 Medial to level 1: Slide 24, Section 2

MIDBRAIN TECTUM AND TEGMENTUM

358

PLATE 138A

PLATE 138B

Optic (?) fibers intermingle with migrating superior colliculus neurons in a honeycomb matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Future gray layers of the superior colliculus

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

PRETECTUM

MIDBRAIN TECTUM

c

o

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Dashed lines indicate staining and/or sectioning artifacts.

SUPERIOR sencephalic (te Me c t a COLLICULUS l, su pe ri o r

ll ic

e cl

ar

co

m

plex (III)

r

to

eu

s

Oculomo

cl

nu

Substantia nigra/ventral tegmental area

Medial longitudinal fasciculus

Midline raphe glial system (structural support for brainstem flexures)

Central gray Mesencephalic reticular formation

CEREBELLUM (LATERAL VERMIS) Superior cerebellar peduncle Sojourning and migrating Purkinje cells

NEP

ed u n c

r ula

Sojourning and migrating deep neurons

l) enta gm (te

te rp

INFERIOR COLLICULUS

ic

In

Isthmal NEP o st eri or me se n

al

MIDBRAIN TEGMENTUM

n

u

(teg me nt al )

Central gray

Mesencephalic (tectal, inferior colliculus) NEP Sojourning and migrating Trochlear nucleus (IV)? inferior colliculus neurons

ph

Anterior mesenceph a li c

P NE

P

ce

Thalamic NEP

esencephalic (teg Middle m me nta l) N EP Sojourning and migrating tegmental neurons

E

P

(future third ventricle)

N

)

GEP (posterior commissure)

diencephalic superventricle

mesencephalic superventricle (future aqueduct)

mis c om sur e

Sojourning and migrating superior colliculus neurons

us

or

Post eri

ul

Pretectal NEP

Cerebellar NEP

Sprouting fibers of hook bundle?

359

360

PLATE 139A

GW8 Sagittal, CR 33 mm, C145 Level 1: Slide 23, Section 2

See the entire section in Plates 122A-D.

MIDBRAIN TEGMENTUM

PLATE 139B

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

esencepha lic (tegmental) N EP dle m d i M mesencephalic superventricle

gm e (t e ic

ce ph al en

Sub Ventra stanti l teg a n me n

Oculomotor

nu

cl

ea

es m or

d

i a

l

lo

Raphe neurons migrating between midline glial fibers

n

g

i

t

d

Diencephalic flexure

Subpial GEP

e

Mesencephalic reticular formation

Region between the mesencephalic and diencephalic flexures

EP l) N nta me teg u s c( u l ali i c ph y s c a ce gr f a en al l r a nt Ce in

a/ igr l area ta

Midline raphe glial system (structural support for brainstem flexures)

M

u

e

I ) ?

I

t An

r

c

omplex

Midline raphe GEP

es rm io

Sojourning and migrating tegmental neurons

(I

ri

Central gray

MIDBRAIN TEGMENTUM

er st Po

(future aqueduct)

EP )N l a nt

Mesencephalic flexure 361

GW8 Sagittal CR 33 mm, C145 Level 3: Slide 20, Section 2

See the entire section in Plates 124A-D.

CEREBELLUM: LATERAL VERMIS

362

PLATE 140A

mesencephalic superventricle (future aqueduct)

INFERIOR COLLICULUS

Mesencephalic (tectal, inferior colliculus) NEP

Ex

Sojourning and migrating inferior colliculus neurons

Isthmal NEP?

d

c un

le

ri

pe

Migrating and proliferating external germinal layer cells

rating

mig

nd

deep

neuro n s

nd

ga ti n g

Trajectory of Purkinje cell migration

a

rnin gra

Choroid plexus stem cells Medullary velum

Su

S ojou FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

l layer

CEREBELLUM (LATERAL VERMIS)

Soj

NEP - Neuroepithelium Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

mina

(contains cerebellar germinal trigone)

Sojourning and migrating deep neurons mi

Cerebellar (deep neuron) NEP?

ar

pe

t

n er

ger al

Dorsal rhombic lip

ce

re

Trajectories of deep neuron migration

b

l el

or

Nerve IV (trochlear)

Dashed lines indicate staining and/or sectioning artifacts.

Purkinje cells

PLATE 140B

Sprouting fibers of hook bundle?

n our

in

g

Cerebellar (Purkinje cell) NEP

rhombencephalic superventricle (future fourth ventricle) 363

GW8 Sagittal CR 33 mm, C145 Level 9: Slide 12, Section 4

See the entire section in Plates 130A-D.

CEREBELLUM: HEMISPHERE

364

PLATE 141A

PLATE 141B Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Dashed lines indicate staining and/or sectioning artifacts.

NEP - Neuroepithelium

Trajectory of Purkinje cell migration

neurons deep g n ti igra m d an ing n r ou Soj Trajectories of deep

e nal g Exter

neuron migration

Vestibular nuclear complex

Upper medullary NEP

s

ll

s

ron

in

ep

je

ce

neu

ni

ga nd settli n g

rk

u

ur

tin

P

jo

ra

ng

n

g

So

ig

de

M

Pontine NEP

Choroid plexus stem cells

CEREBELLUM (HEMISPHERE) Superior cerebellar peduncle

Cerebellar (deep neuron) NEP?

l layer rmina

an

d m gr i

i at

Sprouting fibers of hook bundle?

For a description of the development of the hook bundle in the rat cerebellum, see Altman and Bayer (1996) pp.71-72, 202-204.

rhombencephalic superventricle (future fourth ventricle)

Dorsal rhombic lip (contains cerebellar germinal trigone)

Cerebellar (hemispheric Purkinje cell) NEP

365

GW8 Sagittal CR 33 mm, C145 Level 1: Slide 23, Section 2

See the entire section in Plates 122A-D.

PONS AND MEDULLA

366

PLATE 142A

PLATE 142B

Mesencephalic (tegmental) NEP

M

MIDBRAIN TEGMENTUM

e

Medullary velum

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

C e l i a

d

Pontine reticular formation

a ry edull

medullary NEP Upper lar tibu Ve s

n

rm Lowe ar ucle

Medullary reticular formation

C u Medullary Cu n e at ne flexure e ate nu f a cle s c us

LOWER MEDULLA

ule ps ca s u

Inferior olive

or

Subpial GEP

Posterior intramural migratory stream (inferior olive neurons) Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Intermediate Ventral gray gray Ventral funiculus SPINAL

CORD

iculus

l l emn iscus?

fun

In fe

rio

sal

ia

Subpial GEP

D r (substantia gelatinosa) matte ray lg

o

plex com Soli tar and y nucl trac eus t

Ventral rhombic lip

sa

r live fi b ro

P

r Do

UPPER MEDULLA

NE

s

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Pontomedullary trench

lu

ed

(future fourth ventricle)

u

M

Rhombencephalic choroid plexus

rhombencephalic superventricle

ic

Pontine flexure

N E P

PONS

f a s s c i c u l u

Raphe nuclear complex

P o n t i n e

PONS

g r a y a l n t r u d t i n a n g i l l o

Midline raphe glial system (structural support for brainstem flexures)

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

367

GW8 Sagittal CR 33 mm, C145 Level 2: Slide 22, Section 2

See the entire section in Plates 123A-D.

PONS AND MEDULLA

368

PLATE 143A

PLATE 143B Mesencephalic (tegmental) NEP Medullary velum

rhombencephalic superventricle

(future fourth ventricle)

Ventral rhombic lip

ne at e

te

fa

Medullary flexure

sc ic nu cle u

icul us

ntia gelatinosa)

369

SPINAL CORD

un l f

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

sta sa er (sub matt ray lg

Subpial GEP

or

Posterior intramural migratory stream (inferior olive neurons)

Intermediate gray

sa

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Medial lemniscus?

ay l gr tr a Ven s u lu n ic l fu tr a Ven

Pontine Raphe nuclear complex flexure

D

Inferior olive

Subpial GEP

r Do

r olive Inferio capsule s u o r fib

ea

s

Migrating raphe neurons infiltrate midline glial fibers

Cu

lu

Medullary reticular formation

LOWER MEDULLA

un

V) s( leu uc ln ina Sp

UPPER MEDULLA

Ve

b sti

C

u

Pontomedullary P NE trench y r a l l edu er m Upp

N x ry ple m edulla m o r e r c Low lea c u r n ula

s

Raphe nuclear complex

N E P

PONS

i n e n t

Cell bodies of midline raphe glia system?

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

o

Pontine reticular formation

Rhombencephalic choroid plexus

P

Midline raphe glial system (structural support for brainstem flexures)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

EP

MIDBRAIN TEGMENTUM

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

GW8 Sagittal CR 33 mm, C145 Between levels 2 and 3: Slide 21, Section 2

See level 2 in Plates 123A-D, level 3 in Plates 124A-D.

BRAINSTEM

370

PLATE 144A

PLATE 144B

Medullary velum

Mesencephalic (tegmental) NEP?

M

Rhombencephalic choroid plexus

ia

Pontine reticular formation

PONS

(future fourth ventricle)

Ventral rhombic lip Pontomedullary trench edullary NEP Upper m s

LOWER MEDULLA

c il

e/C

un

ra

ci

le

ea te nu

/c

un

Medullary flexure

e

s

Inferior olive

ulu

Dor

Medial lemniscus?

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

s

o latin tia ge sa)

e diat rme Inte gray

ay l gr tr a Ven s u lu n ic l fu tr a Ven

Posterior intramural migratory stream (inferior olive neurons)

niculu sal fu

SPINAL CORD Subpial GEP

Subpial GEP

b sta n l gray matter (su Dorsa

Raphe nuclear complex

G

cic

Inferior olive fibrous capsule

ra

as

Migrating raphe neurons infiltrate midline glial fibers

Midline raphe glial system (structural support for brainstem flexures)

UPPER MEDULLA Medullary Pontine reticular flexure formation

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

ul u

s nucleus Prepositu

ef

l fa s cic udina t i Medi g a l l on

ullary N E er med Low

s eu cl

Premigratory facial motor nucleus (VII) neurons?

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

at

Abducens nucleus (VI)?

P

rhombencephalic superventricle

P

PONS

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

G

t i n e N E P o n g r a y r a l n t inal fasci cul itud C e us ong l l

ed

MIDBRAIN TEGMENTUM?

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

371

GW8 Sagittal CR 33 mm, C145 Level 3: Slide 20, Section 2

See the entire section in Plates 124A-D.

BRAINSTEM

372

PLATE 145A

PLATE 145B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Medullary velum

N e t i n o n Central gray P s ay ulu g r ascic a l nal f t r tudi i

Me dia C e l lo n ng

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Rhombencephalic choroid plexus

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

PONS

rhombencephalic superventricle

Pontine reticular formation

P

Pontomedullary trench y NEP r medullar Uppe

Migrating raphe neurons infiltrate midline glial fibers

Medullary flexure

Lower medulla ry NE P

G G rac ra ci l

Prepositus nucleus

s nucleus Prepositu

al

a

l

f In

SPINAL CORD

e d ia te Intermray g

s niculu a l fu Dors er y matt a l g ra osa) Dors gelatin tantia (subs

d NEP

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

gray Ventral

Posterior intramural migratory stream (inferior olive neurons)

iculus Ventral fun

Medial lemniscus?

or

l

Raphe nuclear complex

c

na ca

Midline raphe glial system (structural support for brainstem flexures) u s p le ca i or o l s r u i e ve fi b r o

Inferior olive Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

in

tr

Pontine flexure

p

n ce

UPPER MEDULLA

Medullary reticular formation

LOWER MEDULLA

S

Premigratory facial motor nucleus (VII) neurons?

PONS

Ventral rhombic lip

s lu icu sc s fa leu ile nuc e

Abducens nucleus (VI)?

E

PONS

(future fourth ventricle)

Subpial GEP

373

LATERAL PONS, MEDULLA, AND SENSORY GANGLIA

GW8 Sagittal CR 33 mm, C145 Similar to Levels 8, 9, and 10: Slide 27, Section 3

See similar areas from the left side of the brain in Plates 129A-D to 132A-D.

374

PLATE 146A

PLATE 146B

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Neuroepithelium - NEP

Central trigeminal nerve fibers (sparse glia)

Rhombencephalic choroid plexus

rhombencephalic superventricle

NE

Trigeminal motor nucleus (V)?

lar

(future fourth ventricle) NEP l lar be e r ce re p r re rio Ce te n Po A nti n eN llary NEP EP Upper medu

CEREBELLUM (HEMISPHERE) Pontine reticular formation Principal sensory nucleus (V)?

V

es ti bu l a r

r n u c l e a

ex pl m o c

Medullary reticular formation Lateral lemniscus? Nucleus of the lateral lemniscus?

Anterior extramural migratory stream Nerve V (trigeminal, dense glia)

Ventral rhombic lip Premigratory precerebellar neurons

UPPER MEDULLA

PONS

Nerve V (trigeminal, boundary cap)

Inferior cerebellar peduncle

Cochlear nucleus?

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Nerve VIII (vestibulocochlear, boundary cap) Nerve VIII (vestibulocochlear, dense glia) Superior ganglion (IX)?

Temporal bone labyrinth Trigeminal ganglion (V)

P

Sojourning and migrating Purkinje cells Sprouting fibers of hook bundle?

el

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Sojourning and migrating deep neurons?

b

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Vestibular ganglion (VIII)

Petrous temporal bone

375

LATERAL PONS, MEDULLA, AND SENSORY GANGLIA

GW8 Sagittal CR 33 mm, C145 Similar to Levels 8, 9, and 10: Slide 27, Section 4

See similar areas from the left side of the brain in Plates 129A-D to 132A-D.

376

PLATE 147A

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

lar

(future fourth ventricle)

el

Trigeminal motor nucleus (V)?

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

Principal sensory nucleus (V)?

Neuroepithelium - NEP

PONS

V

Ce

re

t An

er

i

or

pr

ec

e er

be

l l a r NEP

P Po ry NE n tin es d u l la e e NE m r e p ti P Up bu x la p l e r n u c l e a r c o m

Pontine reticular formation

Ventral rhombic lip

UPPER MEDULLA Lateral lemniscus?

Central trigeminal nerve fibers (sparse glia) Nerve V (trigeminal, boundary cap)

Rhombencephalic choroid plexus

rhombencephalic superventricle

b

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

CEREBELLUM (HEMISPHERE)

Sojourning and migrating deep neurons? Sojourning and migrating Purkinje cells Sprouting fibers of hook bundle?

NEP

PLATE 147B

Premigratory precerebellar neurons

Inferior cerebellar peduncle

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Cochlear nucleus?

Nerve VIII (vestibulocochlear, boundary cap) Anterior extramural migratory stream Nerve V (trigeminal, dense glia)

Trigeminal ganglion (V)

Nerve VIII (vestibulocochlear, dense glia) Spiral ganglion (VIII) adjacent to temporal bone labyrinth

Petrous temporal bone

Vestibular ganglion (VIII)

377

378

PART PARTVIII: VIII: GW8 GW8 CORONAL CORONAL This is specimen number 9226 in the Carnegie Collection, designated here as C9226. A normal male fetus with a crown-rump length (CR) of 31 mm was collected in 1954, and is estimated to be in gestational week (GW) 8. The entire fetus was embedded in paraffin mixed with 8% celloidin, cut transversely in 10 µm thick sections, and stained with azan. The histology of this specimen is remarkable, and the sections are nearly perfectly bilateral. Since there is no photograph of this brain before it was embedded and cut, a specimen from Hochstetter (1919) that is only partially comparable to C9226 has been modified to show the approximate section plane and external features of the brain at GW8 (Figure 7). Like most of the specimens in this Volume, the sections are not cut exactly in one plane; C9226’s cortex is cut midway between coronal and horizontal planes. Since the cerebral cortex is in every section and the brainstem is cut in a more horizontal orientation, the brain more closely resembles a coronally sectioned brain. Unfortunately, the Hochstetter specimen is less mature (CR27 mm) and we could not find a drawing of a brain specimen that would fit C9226. The C9226 sections through the cortex and brainstem are not in the same plane when transferred to Hochstetter’s CR27 mm specimen. Instead, brainstem planes of section appear to fan upward and downward from sections in the cortex. We interpret this to indicate that the brain flexures are more loosely folded in the Hochstetter specimen than in C9226. If one “squeezes” the brainstem to make the folds tighter, the cortex and brainstem planes would line up. Photographs of 23 sections (Levels 1-23) are illustrated at low magnification in Plates 148-167. High-magnification views of different areas of the cerebral cortex are shown in Plates 168-169. C9226 is similar to the other GW8 specimens and shows brain maturation in a different perspective. Each of the brain’s major subdivisions has a large superventricle in the cores, especially the telencephalon and the rhombencephalon. Midline sagittal sections have large diencephalic and mesencephalic superventricles because the cuts are parallel to their dorsoventral and anteroposterior axes (see C145 in Part VII). C9226’s coronal sections show the slit-like shapes of the diencephalic and mesencephalic superventricles in the midline. The parenchyma, the area between the superficial border of the neuroepithelium (NEP) / subventricular zone (SVZ) and the pial membrane, is the region where neurons migrate, settle, and differentiate. The thicknesses of the neuroepithelium and the parenchyma are clues to the level of maturation of a developing brain structure.

The parenchyma is thick and bordered by a thin NEP in the medulla, pons, and midbrain tegmentum, indicating that most neurons have been generated in these structures. Furthermore, the lack of dense accumulations of cells just outside the NEP in the midbrain tegmentum, pons, and medulla indicate that very few neurons are being generated, few are migrating, and most are settled and differentiating. There are two exceptions in the medulla and pons. First, near the pontomedullary trench, presumptive facial motor neurons are migrating toward their ventral pontine/ medullary settling sites. Second, the precerebellar neuroepithelium in the medulla is thicker and generating pontine gray (and possibly other neurons); many precerebellar neurons are migrating in the anterior and posterior extramural migratory streams. The cerebellar NEP is thicker than that in the pons and medulla. The cerebellar parenchyma contains a very dense Purkinje cell sojourn zone outside the NEP and presumptive earlier-generated deep neurons lie in a superficial position. Like C145, the external germinal layer (egl) is barely visible emanating from the germinal trigone in the dorsal rhombic lip. The mesencephalic tectal NEP is thicker than the tegmental NEP and its very thin parenchyma contains dense sojourning and migrating tectal neurons adjacent to the NEP. The tectum is one of the most immature brain structures. The diencephalic NEP is thicker indicating that many neurons are still being generated even though there is also a thick parenchyma, especially in the thalamus. That is because the thalamus is very large in the mature human brain. There are dense accumulations of young neurons in sojourn zones outside the hypothalamic and thalamic NEPs, indicating that cell migration is more active than final settling and differentiation. Within the telencephalon, the cerebral cortex has a thick NEP and a very thin parenchyma, indicating that it is the most immature brain structure. The cerebral cortical NEP is the sole germinal matrix. The stratified transitional field (STF) contains STF1 and STF5 only in lateral areas. The pronounced anterolateral (thicker) to dorsomedial (thinner) maturation gradient is evident in both the cortical plate and the STF layers. In contrast, both the basal telencephalic NEP/SVZ and parenchyma are thick. That is because the basal telencephalon contains many early-generated neuronal populations (for example, globus pallidus and substantia innominata) and massive late-generated populations (striatal neurons in the caudate and putamen). Most of the neurons settling in the basal telencephalon at GW8 are those of the early-generated populations.

379

GW8 "CORONAL" SECTION PLANES

CORONAL PLANE (90˚)

LE V EL :S EC TI O N

58 :1 23 70 :1 22 6 0 :2 21 34 :2 20 52 :2 19 276 : 18 24 :3 17 90 :3 16 :402 15 438 : 68 14 4 : 13 504 1 : 12 :53 46 11 :5 87 10 9:5 05 5 6 9 8: :63 653 95 1 3 83 5 7 6: 6 75 3:79 2:80 1: 5: 4:

C9226's cutting angle in the cerebral cortex rotates 45˚ counterclockwise from the true coronal plane (90˚), exactly between true horizontal and true coronal. The dorsal (top) part of each section is anterior to the ventral (bottom) part. The illustrated brain is less mature (CR 27 mm) than the brain of C9226 (CR 31 mm), and brain flexures in the midbrain, pons, and medulla are more loosely folded. That is why the cutting planes in C9226 fan outward from those in the cortex.

23:158

22:170 21:206 20:234 19:252 18:276 17:324

HORIZONTAL PLANE (0˚)

OCCIPITAL LOBE PARIETAL LOBE

DIENCEPHALON (EPITHALAMUS)

LON HA EP MISPHERE

BE LO

SUL

L

RA O

Olfactory bulb Optic nerve

DIENCEPHALON

(HYPOTHALAMUS)

12:504

Pituitary gland Trigeminal (V) nerve VII nerve VIII nerve

11:531

TECTUM TEGMENTUM

PONS CEREBELLUM MEDULLA

RHOMBENCEPHALON

CEREB RA L IN

HE

TEM P

13:468 7:635

MESENCEPHALON

A

FRONTAL LOBE

TELE NC

PARACENTRAL LOBULE

16:390 15:402 14:438

10:546 9:587

8:605

LEVEL:SECTION SPINAL CORD

Figure 7. The lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 27 mm (modified from Figure 37, Table VII, Hochstetter, 1919) serves to show the approximate locations and cutting angles of the illustrated sections of C9226 in the following pages. The small inset identifies the major structural features. The line in the cerebellum and dorsal edges of the pons and medulla is the cut edge of the medullary velum.

380

PLATE 148A

Level 1: Section 820

GW8 Coronal CR 31 mm C9226

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

Level 2: Section 803

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

Level 3: Section 791

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

381 Interhemispheric fissure

Cortical (frontal) neuroepithelium (NEP)

PLATE 148B

Level 1: Section 820

Layer I Cortical plate STF1 t1 Frontal STF STF5

FUTURE FRONTAL LOBE

Cortical (cingulate) NEP

telencephalic superventricle (future lateral ventricle)

anterior pool

Cortical (orbitofrontal) NEP Subpial GEP

(enlarged in ventrolateral cortex)

Lateral migratory stream?

OLFACTORY BULB

Interhemispheric fissure

Interhemispheric fissure

Cortical (frontal) NEP

Level 2: Section 803

Layer I Cortical plate STF1 t1 Frontal STF STF5

FUTURE FRONTAL LOBE Cortical (cingulate) NEP

Cortical (orbitofrontal) NEP

Nerve I (olfactory)

telencephalic superventricle (future lateral ventricle)

anterior pool

Basal telencephalic NEP

Lateral migratory stream?

Subpial GEP

(enlarged in ventrolateral cortex)

olfactory recess

Cortical (olfactory) NEP

OLFACTORY BULB

Interhemispheric fissure

Nerve I (olfactory)

Level 3: Section 791

Interhemispheric fissure

Layer I Cortical plate STF1 t1 Frontal STF STF5

FUTURE FRONTAL LOBE Cortical (frontal) NEP

Cortical (cingulate) NEP

telencephalic superventricle (future lateral ventricle)

anterior pool

Cortical (orbitofrontal) NEP Basal telencephalic NEP Subpial GEP

Lateral migratory stream?

(enlarged in ventrolateral cortex)

Cortical (olfactory) NEP ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Interhemispheric fissure

olfactory recess OLFACTORY BULB

Nerve I (olfactory)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

382

PLATE 149A GW8 Coronal CR 31 mm C9226

Level 4: Section 755

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter.

Level 5: Section 695

STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

383

PLATE 149B Layer I Cortical plate STF1 t1 Frontal STF STF5

Level 4: Section 755

Interhemispheric fissure FUTURE FRONTAL Cortical (frontal) LOBE NEP

telencephalic superventricle

Cortical (cingulate) NEP

(future lateral ventricle)

anterior pool

Tenia tecta

Corticoganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ

SEPTUM

Subpial GEP (enlarged in ventral forebrain)

Diagonal band of Broca (vertical limb)

Level 5: Section 695

Interhemispheric fissure

Layer I Cortical plate STF1 t1 Frontal STF STF5

FUTURE FRONTAL LOBE

Telencephalic choroid plexus

Cortical (cingulate) NEP Cortical (hippocampal) NEP

Corticoganglionic NEP and SVZ

Future primary olfactory cortex? (deep layers)

Lateral septal nucleus

Septal NEP

Interhemispheric fissure

Cortical (frontal) NEP

Lateral migratory stream?

L A SA LI BA NG A G

telencephalic superventricle (future lateral ventricle)

HIPPOCAMPUS

anterior pool

Lateral migratory stream?

Septal NEP

Anterolateral ganglionic NEP and SVZ

BASAL GANGLIA Anteromedial ganglionic/ basal telencephalic Basal NEP and SVZ telencephalon

Lateral septal nucleus

ate ud Ca

SEPTUM y ctor Olfa ercle tub

Diagonal band of Broca (vertical limb)

preoptic recess

PREOPTIC AREA

optic recess

Preoptic NEP Subpial GEP Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

en Putam

Future primary olfactory cortex (superficial layers)

Lateral olfactory tract diencephalic superventricle

(future third ventricle)

Optic chiasm

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

384

PLATE 150A GW8 Coronal CR 31 mm C9226 Level 6: Section 653

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

385

PLATE 150B

Layer I Cortical plate STF1 t1 Frontal STF STF5

Interhemispheric fissure FUTURE FRONTAL LOBE

telencephalic superventricle

Cortical (cingulate) NEP Cortical (hippocampal) NEP

(future lateral ventricle)

anterior pool HIPPOCAMPUS

Telencephalic choroid plexus

Septal NEP

Lateral septal nucleus Medial septal nucleus

BASAL GANGLIA

Anteromedial ganglionic NEP and SVZ

SEPTUM

Future primary olfactory cortex (superficial layers)

Anterior commissure? Substantia innominata Bed nucleus of the stria terminalis Anterior hypothalamus

Hypothalamic NEP diencephalic superventricle

Trigeminal ganglion (V)

Ex

Lateral migratory stream?

sal on Ba phal ce n Lateral olfactory tract e tel

Strionuclear NEP and SVZ

(future third ventricle)

ate ud Ca en Putam S

TR I AT U M rn al ca p s u le

Anterolateral ganglionic NEP and SVZ

Forn ix

Fornical GEP

Corticoganglionic NEP and SVZ

te

Cortical (frontal) NEP

HYPOTHALAMUS

Optic tract

Distal part Intraglandular cleft Pituitary gland (anterior lobe, adenohypophysis)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

386

PLATE 151A GW8 Coronal CR 31 mm C9226 Level 7: Section 635

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

387

PLATE 151B

Layer I Cortical plate STF1 t1 Frontal/paracentral STF5 STF

Interhemispheric fissure FUTURE FRONTAL LOBE/ PARACENTRAL LOBULE

telencephalic superventricle

Cortical (cingulate) NEP

(future lateral ventricle)

anterior pool

Cortical (hippocampal) NEP

HIPPOCAMPUS

Anteromedial ganglionic NEP and SVZ

M

l ca

Ex t e r

Strionuclear NEP and SVZ

tel

Hypothalamic NEP

Anterior lobe, adenohypophysis

l Basahalon p ence

Future primary olfactory cortex (superficial layers) Lateral olfactory tract

Substantia innominata Anterior commissure? Bed nucleus of the stria terminalis

diencephalic superventricle

Pituitary gland

U AT n

S T RI

le

Caudate

Medial septal nucleus

SEPTUM

(future third ventricle)

Lateral migratory stream?

Lateral septal nucleus?

Pu tam e

BASAL GANGLIA

Septal NEP

na

Anterolateral ganglionic NEP and SVZ

Telencephalic choroid plexus

Fornix

Fornical GEP

Corticoganglionic NEP and SVZ

p su

Cortical (frontal/ paracentral) NEP

HYPOTHALAMUS

Medial forebrain bundle Optic tract

Posterior lobe, neurohypophysis

Trigeminal ganglion (V) Spinal nucleus (v)?

Reticular formation

MEDULLA

Nerve VIII (vestibulocochlear, boundary cap)

Subpial GEP

Superior ganglion (IX)? Midline raphe glial system (provides structural support for brainstem and spinal flexures)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

388

PLATE 152A GW8 Coronal CR 31 mm C9226 Level 8: Section 605

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

389

PLATE 152B

Layer I Cortical plate STF1 t1 Paracentral STF STF5

Interhemispheric fissure

telencephalic superventricle

Cortical (cingulate) NEP Cortical (hippocampal) NEP

(future lateral ventricle)

HIPPOCAMPUS

Anteromedial ganglionic NEP and SVZ

Substan

Strionuclear GEP

al

am

Subpial GEP

Globus pallidus

Supraoptic nucleus?

po hy al r e

Hypothalamic NEP

at Medial forebrain bundle

ti a i n

nomina

u le

Lateral migratory stream? Lateral olfactory tract

ta

Basal telencephalon Channels for pioneer fibers of various future fiber tracts (anterior commissure, internal capsule, stria terminalis)?

Future primary olfactory cortex (superficial layers)

tra

ct

L

HYPOTHALAMUS

th

Putamen

I AT U M

BASAL GANGLIA

ate ud Ca

SEPTUM

STR

Septal NEP

us

Anterolateral ganglionic NEP and SVZ

Pioneer corticofugal fibers?

t ernal caps

Fornix

Fornical GEP

Corticoganglionic NEP and SVZ

Telencephalic choroid plexus

Ex

Cortical (paracentral) NEP

FUTURE PARACENTRAL LOBULE

diencephalic superventricle

O

pt

ic

(future third ventricle)

Superior olivary complex?

Midline raphe glial system (provides structural support for brainstem flexures)

Nerve V (trigeminal) Nerve V (trigeminal, boundary cap)

PONS

MEDULLA

Raphe nuclear complex

Cochlear nucleus (ventral) Nucleus ambiguus?

Spinal nucleus (V)?

r Reticulaon formati

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Nerve VIII (vestibulocochlear) Nerve IX (glossopharyngeal)? Inferior cerebellar peduncle? Capsule Principal nucleus Medial accessory nucleus

Inferior olive

Posterior intramural migratory stream (inferior olive neurons) Posterior extramural migratory stream (external cuneate and lateral reticular neurons cross midline)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Medial lemniscus (intermingled with the midline raphe glial system)

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

390

PLATE 153A GW8 Coronal CR 31 mm C9226 Level 9: Section 587

See high-magnification views of the cerebral cortex from nearby sections in Plates 168A and B to 169A and B.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

391

PLATE 153B Layer I Cortical plate STF1 t1 Paracentral STF5 agranular stratified transitional field (STF)

Interhemispheric fissure FUTURE PARACENTRAL LOBULE

telencephalic superventricle

Cortical (cingulate) NEP

(future lateral ventricle)

Cortical (hippocampal) NEP

HIPPOCAMPUS

Fornix

Fornical GEP

BASAL GANGLIA

Caudate

Internal capsule

AT U

Anterolateral ganglionic NEP and SVZ

foramen of monro Anterior commissure?

Anteromedial ganglionic NEP and SVZ

Globus pallidus Substan

Strionuclear GEP

Medial forebrain bundle

ac

Hypothalamic NEP

t

HYPOTHALAMUS

Supraoptic nucleus?

ic

diencephalic superventricle

pt

(future third ventricle)

O

Superior olivary complex? Anterior extramural migratory stream

Reticular formation

MEDULLA

Nucleus ambiguus?

Raphe nuclear complex

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

ti a i n

ST

nomina

Lateral olfactory tract

ta

External capsule

Channels for fibers of various future fiber tracts (anterior commissure, internal capsule, stria terminalis)?

Nerve IX (glossopharyngeal, boundary cap)? Inferior cerebellar peduncle? Capsule Principal nucleus

Inferior olive

Medial accessory nucleus Medial lemniscus Posterior extramural migratory stream (external cuneate and lateral reticular neurons cross midline)

Posterior intramural migratory stream (inferior olive neurons)

SPINAL CORD

Ventral funiculus Ventral gray matter Lateral funiculus

central canal (spinal cord)

Intermediate gray matter

Spinal cord NEP

Dorsal gray matter (substantia gelatinosa)

Subpial GEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Future primary olfactory cortex (superficial layers)

Nerve V (trigeminal) Nerve V (trigeminal, boundary cap) Trigeminal motor nucleus (V)? Principal sensory nucleus (V)? Nerve VIII (vestibulocochlear) Nerve VIII (boundary cap)

PONS

Cochlear nucleus (ventral)

Internal capsule

Midline raphe glial system (provide structural support for brainstem flexures)

Trapezoid body

Cochlear nucleus (dorsal)

Lateral migratory stream?

Putamen

Basal telencephalon

Lateral hypothalamus

tr

Subpial GEP

Pioneer corticofugal fibers?

RI

Corticoganglionic NEP and SVZ

Telencephalic choroid plexus

M

Cortical (paracentral) NEP

Dorsal funiculus

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

392

PLATE 154A GW8 Coronal CR 31 mm C9226 Level 10: Section 546

See high-magnification views of the cerebral cortex from nearby sections in Plates 168A and B to 169A and B.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

393

PLATE 154B Layer I Cortical plate STF1 t1 Paracentral STF STF5

Interhemispheric fissure FUTURE PARACENTRAL LOBULE

telencephalic superventricle

Cortical (cingulate) NEP

(future lateral ventricle)

HIPPOCAMPUS

Diencephalic choroid plexus

FUTURE TEMPORAL LOBE

Globus pallidus

(future third ventricle) Lateral hypothalamus

Thalamic NEP

Strionuclear GEP

HYPOTHALAMUS

Medial forebrain bundle

pt

ic O

Superior olivary complex? Anterior extramural migratory stream

Principal sensory nucleus (V)? Central trigeminal tract (V)? Lateral lemniscus?

PONS

Ventral rhombic lip

MEDULLA

Medial lemniscus

s( V

Cochlear nucleus (dorsal) Inferior cerebellar peduncle?

Inferior olive

Medial accessory nucleus Lateral funiculus

central canal (spinal cord)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

(future fourth ventricle, lateral recess)

Capsule Principal nucleus

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Spinal cord NEP Subpial GEP

Reticular formation

S p i n a l nucleu

Raphe nuclear complex

Auditory NEP

CEREBELLUM (HEMISPHERE) rhombencephalic superventricle

)

Pontine/ medullary NEP

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Basal telencephalon/ anterior amygdala

Midline raphe glial system (provides structural support for brainstem flexures) Trapezoid body

Dorsal rhombic lip Cerebellar NEP

Putamen

External capsule Substantia i nnominata

tr

Hypothalamic NEP

Internal capsule

Stria terminalis

diencephalic superventricle

RI

BASAL GANGLIA

Caudate

Anterior complex

Lateral migratory stream?

ST

foramen of monro THALAMUS

Anterolateral ganglionic NEP and SVZ Anteromedial ganglionic NEP and SVZ

t

Corticoganglionic NEP and SVZ

Pioneer corticofugal fibers?

M

Fornical GEP

Telencephalic choroid plexus

Channels for pioneer fibers of various future fiber tracts (internal capsule, stria terminalis)?

AT U

n ix For

Cortical (hippocampal) NEP

ac

Cortical (paracentral) NEP

Intermediate gray matter Dorsal gray matter (substantia gelatinosa)

SPINAL CORD

Dorsal funiculus

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

394

PLATE 155A GW8 Coronal CR 31 mm C9226 Level 11: Section 531

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

395

PLATE 155B Layer I Cortical plate STF1 t1 Paracentral/parietal STF5 STF

Interhemispheric fissure FUTURE PARACENTRAL LOBULE/ PARIETAL LOBE

telencephalic superventricle

Cortical (cingulate) NEP

(future lateral ventricle)

ix rn Fo

Diencephalic choroid plexus

Strionuclear GEP

FUTURE TEMPORAL LOBE

A AL D YG AM

Subthalamic NEP

HYPOTHALAMUS Hypothalamic NEP

Stria medullaris

Caudate

Reticular nucleus SUBTHALAMUS Forel's fields

PONS

Dorsal rhombic lip

Internal capsule

Globus pallidus

Lateral hypothalamus l ia in ed ra M reb ndle fo bu i c pt O

Ventromedial nucleus

S

Stria terminalis

Putamen Central complex

Corticomedial Basolateral complex complex

Midline raphe glial system Trapezoid body

External germinal layer

Lateral migratory stream?

Anterior complex

Superior olivary complex? Subpial GEP

Pioneer corticofugal fibers?

rhombencephalic superventricle

Migrating facial motor neurons?

Abducens nucleus (VI)?

Upper medullary NEP Raphe nuclear complex

Auditory NEP Ventral rhombic lip

Reticular formation

)

Cochlear nucleus (dorsal) Inferior cerebellar peduncle?

Capsule Principal nucleus

(external cuneate and lateral reticular neurons)

central canal (spinal cord)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

CEREBELLUM (HEMISPHERE)

Pontomedullary trench

S

Posterior extramural migratory stream

Spinal cord NEP Subpial GEP

Temporal STF

pin

MEDULLA

Premigratory facial motor neurons?

a l nucleus (V

rhombencephalic superventricle

(future fourth ventricle, lateral recess)

External capsule

Principal sensory nucleus (V)? Central trigeminal tract (V)? Lateral lemniscus?

Pontine NEP

Cerebellar NEP

External caps ule IATUM TR

BASAL GANGLIA

(future third ventricle)

THALAMUS

diencephalic superventricle

Thalamic NEP

choroid plexus

ac

Corticoganglionic NEP and SVZ

Anterolateral ganglionic NEP and SVZ Anteromedial/posterior ganglionic NEP and SVZ

Channels for pioneer fibers of various future fiber tracts (internal capsule, Telencephalic stria terminalis)?

HIPPOCAMPUS

t

Cortical (hippocampal) NEP Fornical GEP

tr

Cortical (paracentral/ parietal) NEP

Inferior olive

Intermediate gray matter Dorsal gray matter (substantia gelatinosa)

SPINAL CORD

Dorsal funiculus

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

396

PLATE 156A GW8 Coronal CR 31 mm C9226 Level 12: Section 504

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

397

PLATE 156B Layer I Cortical plate STF1 t1 Parietal STF STF5

Interhemispheric fissure FUTURE PARIETAL LOBE

telencephalic superventricle

Cortical (cingulate) NEP

(future lateral ventricle)

Cortical (hippocampal) NEP

Fo rni x

Fornical GEP

Diencephalic choroid plexus Stria medullaris

Amygdaloid NEP

AMYGDALA

FUTURE TEMPORAL LOBE

Subthalamic NEP

HYPOTHALAMUS

Hypothalamic NEP

Nucleus of the trapezoid body? Subpial GEP External germinal layer

Pontine NEP

Posterior precerebellar NEP

(future fourth ventricle)

Raphe nuclear complex

MEDULLA

central canal (spinal cord) Spinal cord NEP Subpial GEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Lateral hypothalamus l ia in ed ra M reb ndle ic fo bu pt O

Premammillary area

Solitary nucleus and tract

rhombencephalic superventricle

Ventral rhombic lip

Putamen Corticomedial complex

Central complex

al er at x ol ple s Ba com

Temporal STF Principal sensory nucleus (V) Central trigeminal tract (V) Lateral lemniscus? Superior cerebellar peduncle?

Vestibular nuclear complex

Medullary NEP

(future fourth ventricle, lateral recess)

SUBTHALAMUS Forel's fields

CEREBELLUM (HEMISPHERE)

Cerebellar notch

rhombencephalic superventricle

Internal capsule

Facial motor nucleus (VII)? Abducens nucleus (VI)?

PONS

Cerebellar NEP

Caudate

Stria terminalis

Midline glial raphe system

Trapezoid body

Dorsal rhombic lip (cerebellar germinal trigone)

Reticular nucleus

t

Cortical (temporal) NEP

Dorsal complex

ac

Strionuclear GEP

(future third ventricle)

THALAMUS

diencephalic superventricle

Thalamic NEP

Pioneer corticofugal fibers?

tr

Corticoganglionic NEP and SVZ

BASAL GANGLIA

Channels for pioneer fibers of various future fiber tracts (internal capsule, stria terminalis)?

Reticular formation

Rhombencephalic choroid plexus (V)

Posterior ganglionic NEP and SVZ

Telencephalic choroid plexus

HIPPOCAMPUS

Spinal n ucleus

Cortical (parietal) NEP

Inferior cerebellar peduncle?

Posterior extramural migratory stream (contains external cuneate and lateral reticular neurons)

Intermediate gray matter Dorsal gray matter (substantia gelatinosa)

SPINAL CORD

Dorsal funiculus

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

398

PLATE 157A GW8 Coronal CR 31 mm C9226 Level 13: Section 468

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

399

PLATE 157B Layer I Cortical plate STF1 t1 Parietal STF STF5

Interhemispheric fissure FUTURE PARIETAL LOBE Cortical (parietal) NEP

telencephalic superventricle

Cortical (cingulate) NEP

dorsal pool

HIPPOCAMPUS

Diencephalic choroid plexus

THALAMUS

HYPOTHALAMUS Hypothalamic NEP

Amygdaloid NEP?

External germinal layer

tic u Re

Forel's fields

Lateral hypothalamus l ia in ed ra PreM eb dle mammillary for un b area

PONS

Raphe nuclear complex

Pontine NEP

Parabrachial nucleus?

Cerebellar NEP rhombencephalic superventricle

Posterior precerebellar NEP

(future fourth ventricle)

Vestibular nuclear complex

Hypoglossal nucleus (XII)?

ucl

MEDULLA

Superior cerebellar peduncle?

Expanding fetal rhombencephalic choroid plexus

Posterior extramural migratory stream (external cuneate and lateral reticular neurons) Inferior cerebellar peduncle?

at en

Medullary NEP

ei

Solitary nucleus and tract

Ventral rhombic lip

Migrating and proliferating external germinal layer cells

CEREBELLUM (HEMISPHERE)

Cerebellar notch

lateral recess

ventral pool

Lateral lemniscus?

Medial longitudinal fasciculus?

Abducens nucleus (VI)?

al er at x? ol ple s Bacom

Temporal STF

Midline raphe glial system

Dorsal rhombic lip (cerebellar germinal trigone)

Pioneer corticofugal fibers?

Caudate

Central complex? t

FUTURE TEMPORAL LOBE

Subthalamic NEP

Stria terminalis

trac

AMYGDALA?

Internal capsule

tic

SUBTHALAMUS

Dorsal complex

Pioneer thalamocortical fibers?

en am Put

BASAL GANGLIA

(future third ventricle)

Strionuclear GEP

diencephalic superventricle

Thalamic NEP

Cortical (temporal) NEP

Telencephalic choroid plexus

Fo rn ix

Op

Fornical GEP

Stria medullaris

la r n u c l e u s

Cortical (hippocampal) NEP Posterior ganglionic NEP and SVZ

(future lateral ventricle)

cu

ne

Reticular formation Gr

il ac

ea

nd

Gracile and cuneate fasciculi

Subpial GEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

400

PLATE 158A GW8 Coronal CR 31 mm C9226 Level 14: Section 438

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

401

PLATE 158B Interhemispheric fissure

Layer I Cortical plate STF1 t1 Parietal STF STF5

FUTURE PARIETAL LOBE Cortical (parietal) NEP

telencephalic superventricle (future lateral ventricle)

Cortical (cingulate) NEP

Diencephalic choroid plexus Stria medullaris Pioneer thalamocortical fibers? Pioneer thalamocortical fibers? Fornix Fornix Telencephalic choroid plexus

Cortical (dorsal hippocampal) NEP

DORSAL HIPPOCAMPUS

Fornical GEP

Posterior complex

Cortical (ventral hippocampal) NEP

HYPOTHALAMUS

Cortical (parahippocampal) NEP

FUTURE TEMPORAL LOBE

Hypothalamic NEP

Mammillary body

Lateral hypothalamus?

CEREBELLUM (HEMISPHERE)

lateral recess

Pontine NEP

Parahippocampal STF

lemniscus? Deep cerebellar neurons? Migrating and proliferating external germinal layer cells

Reticular Parabrachial nucleus? formation Dorsal tegmental nucleus?

Sojourning and migrating Purkinje cells Superior cerebellar peduncle?

Cerebellar notch

Anterior precerebellar NEP

rhombencephalic superventricle

(future fourth ventricle)

Expanding fetal rhombencephalic choroid plexus

Vestibular nuclear complex?

Posterior precerebellar NEP

Dorsal sensory nucleus (X)?

Premigratory precerebellar neurons

Dorsal motor nucleus (X)?

te n

uc

Ventral rhombic lip

ea

Medullary NEP

MEDULLA Gr

a ci

Temporal STF

Subthalamic nucleus (Luysian) Lateral migration?

Midline raphe glial system Raphe nuclear complex

ventral pool

Subthalamic nucleus?

lei

Cerebellar NEP

PONS

la r n u c l e u s

Medial forebrain bundle?

External germinal layer Dorsal rhombic lip (cerebellar germinal trigone)

Zona incerta

Forel's fields

tic tr act

SUBTHALAMUS

Subthalamic NEP

Op

BASAL GANGLIA

Ventral complex

Lateral geniculate migration

tic u

Thalamic NEP

(future third ventricle)

Cortical (temporal) NEP

Sojourning and migrating thalamic neurons

Dorsal complex

diencephalic superventricle

THALAMUS

Re

Posterior ganglionic NEP and SVZ

dorsal pool

le

d an

cu

n

Posterior extramural migratory stream (external cuneate and lateral reticular neurons) Inferior cerebellar peduncle?

Gracile and cuneate fasciculi

Subpial GEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

402

PLATE 159A GW8 Coronal CR 31 mm C9226 Level 15: Section 402

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

403

PLATE 159B Interhemispheric fissure

telencephalic superventricle

Cortical (cingulate) NEP Cortical (dorsal hippocampal) NEP

Stria medullaris Pioneer thalamocortical fibers?

(future third ventricle)

SUBTHALAMUS Subthalamic NEP

LOBE

HYPOTHALAMUS

Ventral complex

Sojourning and migrating thalamic neurons

Fornix Forel's fields Zona incerta Medial forebrain bundle

Hypothalamic NEP M

External germinal layer Dorsal rhombic lip (cerebellar germinal trigone)

CEREBELLUM (HEMISPHERE)

a m mil y b od la r

Reticular formation

Medial longitudinal fasciculus?

Raphe nuclear complex

Parabrachial nucleus?

Pontine NEP Cen

Cerebellar notch

lateral recess

tral gray

rhombencephalic superventricle

(future fourth ventricle)

Posterior precerebellar NEP Ventral rhombic lip

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ventral pool

Parahippocampal STF

Lateral lemniscus? Deep cerebellar neurons?

Midline raphe glial system

PONS

Temporal STF

Subthalamic nucleus (Luysian) migration?

y

Subpial GEP

Lateral geniculate migration

ic tract

Thalamic NEP

Cortical FUTURE (parahippocampal) NEP TEMPORAL

Dorsal complex

Opt

THALAMUS

VENTRAL HIPPOCAMPUS

Fornix

Posterior complex

diencephalic superventricle

Fornical GEP Cortical (temporal) Cortical NEP (ventral hippocampal) NEP

Diencephalic choroid plexus

DORSAL HIPPOCAMPUS

Telencephalic choroid plexus

dorsal pool

(future lateral ventricle)

Reticular nucleus

Cortical (parietal) NEP

Cerebellar NEP

Layer I Cortical plate STF1 t1 Parietal STF STF5

FUTURE PARIETAL LOBE

Migrating and proliferating external germinal layer cells

Sojourning and migrating Purkinje cells Superior cerebellar peduncle? Sprouting fibers of hook bundle?

Circumferential fetal rhombencephalic choroid plexus

Medullary NEP MEDULLA

Medullary velum

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

404

PLATE 160A GW8 Coronal CR 31 mm C9226 Level 16: Section 390

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

405

PLATE 160B Interhemispheric fissure FUTURE PARIETAL LOBE

Cortical (parietal) NEP

telencephalic superventricle

Layer I Cortical plate STF1 t1 Parietal STF STF5

(future lateral ventricle)

Cortical (cingulate) NEP

dorsal pool Diencephalic choroid plexus

Cortical (dorsal hippocampal) NEP Telencephalic choroid plexus

Stria medullaris

Pioneer thalamocortical fibers?

DORSAL HIPPOCAMPUS

THALAMUS Thalamic NEP

Cortical (temporal) Cortical NEP (ventral hippocampal) NEP

Sojourning and migrating thalamic neurons Lateral geniculate migration

Ventral complex

Ventral lateral geniculate body?

diencephalic superventricle

(future third ventricle)

Subpial GEP

MESENCEPHALIC TEGMENTUM

Op

Interpeduncular gr ni nucleus ti a n a st HYPOTHALAMUS Subthalamic S ub nucleus (Luysian) migration? Hypothalamic NEP M a m mil y b od mammillary recess la r

PONS CEREBELLUM (HEMISPHERE)

a?

Mesencephalic (tegmental) NEP

External germinal layer

Dorsal rhombic lip (cerebellar germinal trigone)

Forel's fields future aqueduct Medial forebrain bundle

tic

Subthalamic NEP

ventral pool

Parahippocampal STF

Reticular formation

Lateral lemniscus Deep cerebellar neurons?

Midline raphe glial system

Migrating and proliferating external germinal layer cells

Medial longitudinal fasciculus?

Raphe nuclear complex

Parabrachial nucleus?

Sojourning and migrating Purkinje cells

Pontine NEP Cen

tral gray

Cerebellar notch

lateral recess

Temporal STF

y

LOBE

Fornix

Zona incerta

tract

SUBTHALAMUS

Cortical FUTURE (parahippocampal) NEP TEMPORAL

Cerebellar NEP

Dorsal complex

Reticular nucleus

Fornical GEP

VENTRAL HIPPOCAMPUS

Fornix

Posterior complex

Superior cerebellar peduncle?

rhombencephalic superventricle

(future fourth ventricle)

Sprouting fibers of hook bundle?

Rhombencephalic choroid plexus

Medullary NEP

Medullary velum

Ventral rhombic lip

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

406

PLATE 161A GW8 Coronal CR 31 mm C9226 Level 17: Section 324

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

407

PLATE 161B Interhemispheric fissure Layer I Cortical plate STF1 t1 Parietal STF STF5

FUTURE PARIETAL LOBE

Cortical (parietal) NEP

telencephalic superventricle (future lateral ventricle)

Cortical (cingulate) NEP

dorsal pool

Diencephalic choroid plexus Stria medullaris Pioneer thalamocortical fibers?

Cortical (hippocampal) NEP

H IP PO CA M PU S

Dorsal complex

Thalamic NEP

Lateral geniculate migration

ul a

THALAMUS

ti c

Telencephalic choroid plexus

Sojourning and migrating thalamic neurons Re

Cortical (temporal) NEP

Posterior complex

rn

(future third ventricle)

Cortical (parahippocampal) NEP

Temporal STF ventral pool

future aqueduct

tic

Oculomotor nuclear complex (III)?

Mesencephalic (tegmental) NEP

tr ac

t

Subpial GEP

s

Ventral complex? Op

FUTURE TEMPORAL LOBE

eu

l uc

diencephalic superventricle

MESENCEPHALIC TEGMENTUM

Parahippocampal STF

Interpeduncular nucleus Medial forebrain bundle? Substantia nigra

Interpeduncular fossa

Ventral tegmental area

Midline raphe glial system External germinal layer

PONS

Raphe nuclear complex

Lateral lemniscus Medial longitudinal fasciculus?

Reticular formation

Dorsal rhombic lip (cerebellar germinal trigone)

CEREBELLUM (HEMISPHERE)

Ce

Pontine NEP

ntr

Deep cerebellar neurons? Migrating and proliferating external germinal layer cells

Parabrachial nucleus?

al gray

Cerebellar notch

Sojourning and migrating Purkinje cells

lateral recess

Cerebellar NEP

CEREBELLUM (VERMIS)

Superior cerebellar peduncle? Medullary velum

cerebellar circumferential pool

rhombencephalic superventricle

(future fourth ventricle)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

408

PLATE 162A GW8 Coronal CR 31 mm C9226 Level 18: Section 276

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

409

PLATE 162B

Interhemispheric fissure

Layer I Cortical plate STF1 t1 Parietal STF STF5

FUTURE PARIETAL LOBE

Cortical (parietal) NEP

Diencephalic choroid plexus Stria medullaris

telencephalic superventricle

EPITHALAMUS

(future lateral ventricle)

Cortical (occipital) NEP Cortical (occipital) NEP

TH

FUTURE OCCIPITAL LOBE

A

Habenulo-interpeduncular tract

Epithalamic NEP

LA

M

U

Pioneer thalamocortical fibers?

S

Re

Thalamic NEP

tic

ul

Sojourning and migrating thalamic neurons Optic tract ar

n Posterior ucle us complex

diencephalic superventricle

Lateral geniculate migration

(future third ventricle)

Medial geniculate body?

mesencephalic superventricle

posterior pool

(future aqueduct)

Rubral NEP?

Central gray

Red nucleus?

Mesencephalic (tegmental) NEP

Subpial GEP

MESENCEPHALIC TEGMENTUM

Raphe nuclear complex?

Isthmal NEP External germinal layer

ISTHMUS

Brachium of the inferior colliculus Oculomotor nuclear complex (III)?

Reticular formation

Parabigeminal nuclei?

Medial longitudinal fasciculus?

Central gray

mesencephalic superventricle (isthmal canal)

Parabrachial nucleus?

Lateral lemniscus

CEREBELLUM (HEMISPHERE) Cerebellar NEP

CE RE (VE BEL RM LU IS) M

Deep cerebellar neurons?

rhombencephalic superventricle

Migrating and proliferating external germinal layer cells

Sojourning and migrating Purkinje cells Medullary velum Superior cerebellar peduncle?

(future fourth ventricle, cerebellar circumferential pool)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

410

PLATE 163A GW8 Coronal CR 31 mm C9226 Level 19: Section 252

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

411

PLATE 163B

Interhemispheric fissure

Layer I Cortical plate STF1 t1 Occipital STF5 STF

FUTURE OCCIPITAL LOBE

Cortical (occipital) NEP

Diencephalic choroid plexus

telencephalic superventricle (future lateral ventricle)

TH

A

LA

M

Sojourning and migrating thalamic neurons

U

Re

Thalamic NEP

FUTURE OCCIPITAL LOBE

Habenulo-interpeduncular tract

Epithalamic S NEP

posterior pool

Cortical (occipital) NEP

Migrating habenular neurons

EPITHALAMUS

diencephalic superventricle

(future third ventricle)

Rubral NEP?

tic

ul

ar

Optic tract nu

c Posterior leus complex

Medial geniculate body?

mesencephalic superventricle (future aqueduct)

Central gray

Subpial GEP

Reticular formation Oculomotor nuclear complex (III)? Medial longitudinal fasciculus?

Raphe nuclear complex

mesencephalic superventricle (isthmal canal)

Central gray

Superior cerebellar peduncle? Parabrachial nucleus?

MESENCEPHALIC TECTUM INFERIOR CE COLLICULUS

C (FU ERE SIN BEL G V LU ER M MI S)

External germinal layer

Lateral lemniscus Migrating inferior colliculus neurons

Deep cerebellar neurons?

Cerebellar NEP rhombencephalic superventricle

(future fourth ventricle, cerebellar circumferential pool)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Subpial GEP Lateral lemniscus

Isthmal NEP

ISTHMUS

(H R E EM B IS E L L PH U ER M E)

Habenulointerpeduncular tract?

Brachium of the inferior colliculus

Mesencephalic (tegmental) NEP

MESENCEPHALIC TEGMENTUM

Red nucleus?

Lateral geniculate migration

Mesencephalic (tectal, inferior colliculus) NEP Sojourning and migrating Purkinje cells Superior cerebellar peduncle?

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

412

PLATE 164A GW8 Coronal CR 31 mm C9226 Level 20: Section 234

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

413

PLATE 164B

Interhemispheric fissure

Layer I Cortical plate STF1 t1 Occipital STF STF5

FUTURE OCCIPITAL LOBE

Cortical (occipital) NEP

Diencephalic choroid plexus

telencephalic superventricle (future lateral ventricle)

posterior pool

LA

Habenulo-interpeduncular tract?

Epithalamic NEP S U M

diencephalic superventricle

P om c

A TH Thalamic NEP

Sojourning and migrating thalamic neurons u cle nu ar ul r t i c r io R e s te p le x o

Cortical (occipital) NEP

Migrating habenular neurons

EPITHALAMUS

(future third ventricle)

Medial geniculate body? Habenulointerpeduncular tract?

s

FUTURE OCCIPITAL LOBE

mesencephalic superventricle (future aqueduct)

Mesencephalic (tegmental) NEP

Subpial GEP

Central gray

Brachium of the inferior colliculus Reticular formation

MESENCEPHALIC TEGMENTUM Raphe nuclear complex

Mesencephalic (tegmental) NEP

Medial longitudinal fasciculus?

Subpial GEP Lateral lemniscus

Central gray

mesencephalic superventricle

MESENCEPHALIC TECTUM

(future aqueduct)

Migrating inferior colliculus neurons

Mesencephalic (tectal, inferior colliculus) NEP INFERIOR COLLICULUS

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

mesencephalic superventricle (inferior colliculus recess)

ISTHMUS

Trochlear nucleus (IV)? Nerve IV (trochlear, decussation)?

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

414

PLATE 165A GW8 Coronal CR 31 mm C9226 Level 21: Section 206

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

415

PLATE 165B

Interhemispheric fissure FUTURE OCCIPITAL LOBE

Cortical (occipital) NEP

Diencephalic choroid plexus

telencephalic superventricle (future lateral ventricle) posterior pool

Cortical (occipital) NEP

Layer I Cortical plate STF1 t1 Occipital STF STF5

diencephalic superventricle

(future third ventricle)

Migrating habenular neurons

EPITHALAMUS

Epithalamic NEP Sojourning and migrating pretectal neurons

FUTURE OCCIPITAL LOBE Subpial GEP

Reticular formation

tr al gray

Mesencephalic (tegmental) NEP

C

Nucleus of the optic tract? mesencephalic superventricle

Cen

MESENCEPHALIC TEGMENTUM

PRETECTUM

C e ntral gr ay

Pretectal NEP

(future aqueduct)

Optic tract? en

tra

l gr

ay

Mesencephalic (tectal, inferior colliculus) NEP

MESENCEPHALIC TECTUM

Mesencephalic (tectal, superior colliculus) NEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

INFERIOR COLLICULUS

Future gray layers? (superior colliculus) Migrating superior colliculus neurons

SUPERIOR COLLICULUS

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Optic tract

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

416

PLATE 166A GW8 Coronal CR 31 mm C9226 Level 22: Section 170

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

417

PLATE 166B

Interhemispheric fissure

Diencephalic choroid plexus diencephalic superventricle (future third ventricle)

FUTURE OCCIPITAL LOBE

Layer I Cortical plate STF1 t1 STF5

telencephalic superventricle (future lateral ventricle)

Cortical (occipital) NEP

posterior pool

Subpial GEP

Epithalamic NEP

EPITHALAMUS

Occipital STF Migrating habenular neurons

GEP (posterior commissure) Ce

Pretectal NEP

ntr

PRETECTUM

Posterior commissure

ay al gr

Centr a l

Mesencephalic (tegmental) NEP

Nucleus of the optic tract

Reticular formation

Optic tract?

gr

MESENCEPHALIC TEGMENTUM

ay

mesencephalic superventricle

Future gray layers? (superior colliculus)

(future aqueduct)

MESENCEPHALIC TECTUM Mesencephalic (tectal, superior colliculus) NEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Migrating superior colliculus neurons SUPERIOR COLLICULUS

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Optic tract

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

418

PLATE 167A GW8 Coronal CR 31 mm C9226 Level 23: Section 158

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

419

PLATE 167B

Pineal gland pineal recess

Interhemispheric fissure

diencephalic superventricle

FUTURE OCCIPITAL LOBE ic al e ph ricll e c en enttera tel ervre laicle) p su (futuentr

Cortical (occipital) NEP

st po erio ol r

Epithalamic NEP

EPITHALAMUS

Migrating habenular neurons

GEP (posterior commissure)

Posterior commissure

ntr ray al g

Pretectal NEP

Occipital STF

Ce

PRETECTUM

Layer I Cortical plate STF1 t1 STF5

po

v

Subpial GEP

(future third ventricle)

Nucleus of the optic tract

Cen tral gray

mesencephalic superventricle

Optic tract?

(future aqueduct)

MESENCEPHALIC TECTUM

Future gray layers? (superior colliculus) Migrating superior colliculus neurons

Mesencephalic (tectal, superior colliculus) NEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Optic tract SUPERIOR COLLICULUS

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

GW8 Coronal CR 31 mm, C9226 Between levels 9 and 10: Section 564 CEREBRAL CORTEX Enlarged in Plates 169A and B.

See levels 9 and 10 in Plates 153A and B to 154A and B.

420

PLATE 168A

PLATE 168B

Thin, continuous cortical plate Thin STF layers

GRADIENT OF MORPHOLOGICAL MATURATION: MOST LAYERS IN THE VENTROLATERAL CORTEX ARE THICKER THAN THOSE IN THE DORSOMEDIAL CORTEX, HOWEVER, THE CORTICAL NEUROEPITHELIUM AND LAYER I HAVE A CONSTANT THICKNESS.

CINGULATE CORTEX

FUTURE PARACENTRAL LOBULE

PARACENTRAL CORTEX

Cortical (cingulate) NEP Thin, fragmented cortical plate

Very thin STF layers

Cortical (paracentral) neuroepithelium (NEP)

telencephalic superventricle (future lateral ventricle)

Layer I Cortical plate STF1 t1 STF4 STF5

HIPPOCAMPUS Cortical (hippocampal ammonic) NEP

Fornix

Telencephalic choroid plexus

Paracentral (agranular) stratified transitional field (STF)

Thick cortical plate Thick STF layers

Cortical (hippocampal dentate) NEP Fornical glioepithelium

Lateral migratory stream? (intermingled with STF4)

421

GW8 Coronal, CR 31 mm, C9226 Between levels 9 and 10 PARACENTRAL CEREBRAL CORTEX Section 564

Section 570

See levels 9 and 10 in Plates 153A and B to 154A and B.

422

PLATE 169A

PLATE 169B

Cajal-Retzius cells

Dorsomedial

Layer I Cortical plate (LESS dense) Stratified transitional field (STF)1 t1 STF5

Ventrolateral

Layer VII neurons temporarily settled in cortical plate? Migrating layer VI neurons? Sojourning layer VI neurons?

Cortical (paracentral) neuroepithelium (NEP) Layer I

MATURATION GRADIENT

Cells of the pia mater

Section 564

This area of cortex is dorsomedial to the area from Section 570 and is slightly less mature.

Cortical plate (MORE dense) STF1 t1 STF5

Section 570

Cortical (paracentral) NEP

Experimental studies in the developing rat cerebral cortex (Bayer and Altman, 1991) with tritiated-thymidine autoradiography have shown that the first cells in the cortical plate are subplate (Layer VII) neurons. Subplate neurons are transient cortical plate residents. At a later stage of development, layer VII neurons delaminate to settle permanently in the subplate.

This area of cortex is ventrolateral to the area from Section 564 and is slightly more mature.

Proliferating precursors of layers VI-II neurons and cortical glia.

423

424

PART PARTIX: IX: GW8 GW8 HORIZONTAL NORIZONTAL This is specimen number 609 in the Carnegie Collection, designated here as C609. A normal female fetus with a crown-rump length (CR) of 32 mm was collected in 1916, and is estimated to be in gestational week (GW) 8. The entire fetus was embedded in paraffin, cut transversely in 50 µm thick sections, and stained with aluminum cochineal. Since there is no photograph of this brain before it was embedded and cut, a specimen from Hochstetter (1919) that is only partially comparable to C609 has been modified to show the approximate section plane and external features of the brain at GW8 (Figure 8). Like most of the specimens in this Volume, the sections are not cut exactly in one plane; C609’s cortex is cut midway between coronal and horizontal planes, and is presented as a “horizontal” brain. The C609 section planes through the cortex and brainstem are not at the same angle when transferred to Hochstetter’s CR27 mm specimen. Instead, brainstem planes of section appear to fan upward and downward from sections in the cortex apparently around a fulcrum centering in the invagination of the medullary velum overlying the rhombencephalic superventricle. We interpret this to indicate that the brain flexures are more loosely folded in the Hochstetter specimen than in C609. But it is difficult to determine how the brainstem is folded in C609 to make the section planes line up with those in the cortex. Photographs of 23 sections (Levels 1-10) are illustrated at low magnification in Plates 170-179. High-magnification views of different areas of the brain are shown in Plates 180-185. To maximize image size within page space, all of C609’s sections are rotated 90˚ (landscape orientation). The anterior part of each section is on the left (page bottom), and the posterior part of each section is on the right (page top). C609 is similar to the other GW8 specimens and shows brain maturation in still another perspective. The telencephalic and rhombencephalic superventricles are obvious, along with the slit-like diencephalic and mesencephalic superventricles. The parenchyma, the area between the superficial border of the neuroepithelium (NEP) / subventricular zone (SVZ) and the pial membrane, is the region where neurons migrate, settle, and differentiate. The thicknesses of the neuroepithelium and the parenchyma are similar to those in C9226 throughout the brain indicating brain maturation in both specimens is similar. The parenchyma is thick and bordered by a thin NEP in the medulla, pons, and midbrain tegmentum without sur-

rounding dense sojourn zones. Most neurons have been generated here, few are migrating, and most are settled and differentiating. The two exceptions seen in C9226 are also seen in C145. First, presumptive facial motor neurons are clumped near the pontomedullary trench and some are migrating toward their ventral pontine/medullary settling sites. Second, the thicker precerebellar neuroepithelium in the medulla is generating predominantly pontine gray neurons; many precerebellar neurons are migrating in the anterior and posterior extramural migratory streams. The cerebellar NEP is thicker than that in the pons and medulla, and the cerebellar parenchyma has a dense Purkinje cell sojourn zone below presumptive earlier-generated deep neurons; the external germinal layer (egl) is rudimentary. The mesencephalic tectal NEP is thick adjacent to a thin parenchyma that contains dense sojourning and migrating neurons; substantial neurogenesis is ongoing in both the superior and inferior colliculi in the midbrain tectum. The prominent diencephalic NEP and thick parenchyma filled with dense zones of sojourning and migrating neurons is remarkable in C609. Many migratory streams are visible in the thalamus, and migrating subthalamic nucleus neurons can be followed from the posterior hypothalamic NEP to the subthalamic nucleus. Although many diencephalic neurons have been generated by GW8, most of them are still migrating and few have settled. In spite of that, there are large accumulations of fibers (presumably thalamic axons) in the lateral thalamus and internal capsule, indicating that young thalamic neurons grow axons toward the cerebral cortex before settling and differentiating. Within the telencephalon, the cerebral cortex has a thick NEP and a very thin parenchyma, indicating that most of its neurons are still not generated. The cerebral cortical NEP is the sole germinal matrix. The stratified transitional field (STF) contains STF1 and STF5 only in lateral areas. The pronounced anterolateral (thicker) to dorsomedial (thinner) maturation gradient is evident in the cerebral cortex. The basal telencephalic NEP/SVZ and parenchyma are both thick because there are large early-generated neuronal populations (for example, globus pallidus and substantia innominata) and massive late-generated populations (striatal neurons in the caudate and putamen). Most of the neurons settling in the basal telencephalon at GW8 are those of the early-generated populations, while many striatal neurons have not been generated yet.

425

GW8 "HORIZONTAL" SECTION PLANES

C609's cutting angle in the cerebral cortex rotates 45˚ counterclockwise from the true coronal plane (90˚), exactly between true horizontal and true coronal.

8: 65

7: 74

6:

LE V EL :S EC TI O N

45

6

9:

:3

10

This brain is less mature (CR 27 mm) with more loosely folded flexures than C609's brain (CR 32 mm). That is why cutting planes in C609's brainstem differ considerably from those in the cortex, many are horizontal. In the illustrated sections on the following pages, the anterior part of each section (left side) is dorsal to the posterior part (right side).

86

5:

97

4:

9

10

3: 8

12 2: 13

7

16

1:

10:36

6

0

CORONAL PLANE (90˚)

9

8

5

9:45

4 2

6

3 5

7

8

8:65 7:74 6:86

HORIZONTAL PLANE (0˚)

5:97 4:109

OCCIPITAL LOBE PARIETAL LOBE

(EPITHALAMUS)

LON HA EP MISPHERE

TECTUM BE

LO

SUL

L RA

O

Olfactory bulb Optic nerve

DIENCEPHALON

(HYPOTHALAMUS)

Pituitary gland Trigeminal (V) nerve VII nerve VIII nerve

PONS CEREBELLUM MEDULLA

2:139 1:160

TEGMENTUM

RHOMBENCEPHALON

CEREB RA L IN

HE

TEM P

3:128

MESENCEPHALON

A

FRONTAL LOBE

TELE NC

PARACENTRAL LOBULE

DIENCEPHALON

LEVEL:SECTION

SPINAL CORD

Figure 8. The lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 27 mm (modified from Figure 37, Table VII, Hochstetter, 1919) serves to show the approximate locations and cutting angles of the illustrated sections of C609 in the following pages. The small inset identifies the major structural features. The line in the cerebellum and dorsal edges of the pons and medulla is the cut edge of the medullary velum.

GW8 Horizontal CR 32 mm C609 Level 1: Section 160

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

426

PLATE 170A

PLATE 170B Frontal STF Sclera

STF5 STF1 t1

Pigment layer of retina Intraretinal space

Cortical plate

Neural retina

Layer I

telencephalic superventricle

Vitreous body

(future lateral ventricle)

Extraocular muscle

anteroventral pool

Facial ganglion (VII)? Nerve VII (facial)? Nerve II (optic)

Extraocular muscle

Lateral funiculus

Extraocular muscle?

Trigeminal ganglion (V) Nerve I (olfactory)

olfactory recess

Interhemispheric fissure

Ciliary ganglion (III)?

Dorsal gray

Intermediate gray

Substantia gelatinosa

Ventral gray

Dorsal funiculus

Ventral funiculus Olfactory epithelium (I)

Subpial GEP? OLFACTORY BULB

central canal Central autonomic area

FUTURE FRONTAL LOBE

Subpial GEP

Spinal nerve roots Spinal cord NEP

Cortical (frontal) NEP

SPINAL CORD

Cortical (cingulate) NEP Cortical (orbitofrontal) NEP

EYE

Cortical (olfactory) NEP

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

427

GW8 Horizontal CR 32 mm C609 Level 2: Section 139

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

428

PLATE 171A

PLATE 171B Frontal STF STF5 STF1 t1

Lateral migratory stream? Lateral olfactory tract

Cortical plate Layer I

on hal cep n e l l te

telencephalic superventricle

Caudate

(future lateral ventricle)

anteroventral pool

B asa

Substantia gelatinosa

(future third ventricle)

Preoptic NEP SEPTUM

Pituitary gland

(anterior lobe, adenohypophysis)

Anteromedial ganglionic/ basal telencephalic NEP and SVZ

PREOPTIC AREA

Intermediate gray

(external cuneate and lateral reticular neurons)

Intermediate part Intraglandular cleft

cipal Prin n

Medial accessory nucleus Raphe nuclear complex Medial lemniscus

Distal part

Inferior cerebellar peduncle Vestibular ganglion (VIII)

Inferior olive

central canal

MEDULLA

Spinal cord NEP

SPINAL CORD

GABAS NG AL LI A

Septal NEP

Posterior extramural migratory stream

Suprachiasmatic nucleus?

Lateral septal nucleus

Interhemispheric fissure

Cortical (frontal) NEP

Dorsal funiculus

diencephalic superventricle preoptic part

Cortical (cingulate) NEP

Subpial GEP

r ula n tic tio Re ma for s leu uc

Medial septal nucleus/ diagonal band of Broca (vertical limb) Tenia tecta

Superior ganglion (IX)? Trigeminal ganglion (V)

Optic chiasm

FUTURE FRONTAL LOBE

Spiral ganglion (VIII) adjacent to temporal bone labyrinth

Future primary olfactory cortex

Endopiriform nucleus? (infiltrated by lateral migratory stream) Anterolateral ganglionic NEP and SVZ

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Petrous temporal bone Corticoganglionic NEP and SVZ

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

429

GW8 Horizontal CR 32 mm C609 Level 3: Section 128

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

430

PLATE 172A

PLATE 172B Frontal STF Temporal bone labyrinth

STF5 STF1 t1

Lateral migratory stream? Lateral olfactory tract

Cortical plate Layer I

Future primary olfactory cortex

FUTURE FRONTAL LOBE

Puta men

anterior pool

lencephalon

Globus pallidus

diencephalic superventricle

(future third ventricle)

Medial septal nucleus/ diagonal band of Broca (vertical limb) Tenia tecta?

Optic tract

Anterior hypothalamic nuclei Supraoptic nucleus?

Lateral septal nucleus

Forn ix? Interhemispheric fissure

Anterior commissure

Fornical GEP

Septal NEP

Posterior extramural migratory stream

(external cuneate and lateral reticular neurons)

Inferior olive capsule Pr

Medial accessory nucleus Medial lemniscus

SEPTUM Cortical (cingulate) NEP

Hypothalamic NEP

PREOPTIC HYPOTHALAMUS AREA

Anteromedial ganglionic NEP and SVZ

Preoptic NEP

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

GABAS NG AL LI A

ipal nucle

us

Raphe nuclear com plex

Inferior olive

central canal

Inferior cerebellar peduncle Lateral reticular nucleus?

Anterior commissure

Spinal cord NEP

SPINAL CORD

Subpial GEP

Endopiriform nucleus? (infiltrated by lateral migratory stream)

Anterolateral ganglionic NEP and SVZ

inc

MEDULLA

Strionuclear NEP Cortical (frontal) NEP

Subpial GEP Dorsal funiculus Substantia gelatinosa Intermediate gray

r ula n tic tio Re rma fo

(future lateral ventricle)

Vestibular ganglion (VIII)?

Bed nucleus of the stria terminalis

B a s a l te

telencephalic superventricle

External capsule

a te ud Ca

Telencephalic choroid plexus

Trigeminal ganglion and proximal nerve (V)

Petrous temporal bone

Corticoganglionic NEP and SVZ ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

431

GW8 Horizontal CR 32 mm C609 Level 4: Section 109

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

432

PLATE 173A

PLATE 173B Frontal STF Future insular cortex Future primary olfactory cortex?

STF5 STF1 t1 Cortical plate Layer I

Cochlear nucleus (ventral) External capsule

FUTURE FRONTAL LOBE a te ud Ca

Telencephalic choroid plexus telencephalic superventricle (future lateral ventricle)

Putamen

Anterior complex

anterior pool

foramen of monro

Fornix

Periventricular complex

Spinal nucleus (V)

Spinal nucleus (V)

Solit

ary n

Superior olivary complex?

Arcuate nucleus?

Dorsal sensory nucleus (X)?

Medial lemniscus? Paraventricular nucleus?

Fornix

Interhemispheric fissure

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

(future third ventricle)

Optic tract

Posterior extramural migratory stream (external cuneate and lateral reticular neurons)

Late ral l emn iscu s

diencephalic superventricle

Bed nucleus of the stria terminalis

Hippocampus

Inferior cerebellar peduncle

Nucleus of the lateral lemniscus (ventral)?

Central complex?

Globus pallidus

Internal capsule

Nerve VIII (vestibulocochlear)?

Lateral olfactory tract

External cuneate nucleus

Cu nea te n ucl ucleu eus s and tra ct

Prepositus nucleus

Medial longitudinal fasciculus

Raphe nuclear complex

rhombencephalic superventricle

(future fourth ventricle)

Thalamic NEP

Cortical (cingulate) NEP

THALAMUS

Cortical (hippocampal) NEP

HYPO- Hypothalamic THALAMUS NEP rea

Fornical GEP Anteromedial ganglionic NEP and SVZ

Cortical (frontal) NEP

Anterolateral ganglionic NEP and SVZ

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

BASAL GANGLIA

Corticoganglionic NEP and SVZ

ALA AM YG D

Strionuclear NEP

Subpial GEP

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Reticular formation

a m ic h a la ypot h l a r Midline raphe glial system L a te (provides structural support for brainstem flexures)

MEDULLA

Medullary NEP

Ventral rhombic lip (contains auditory NEP)

Petrous temporal bone

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

433

434

PLATE 174A GW8 Horizontal CR 32 mm C609 Level 5: Section 97

See a high-magnification view of the diencephalon and basal ganglia in Plates 180A and B.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 174B

Paracentral STF

FUTURE TEMPORAL LOBE

Future insular cortex

STF5 STF1 t1 Cortical plate

Future temporal cortex

Telencephalic choroid plexus

Fornix Diencephalic choroid plexus

Interhemispheric fissure

Cortical (dorsal hippocampal) NEP

Optic tract?

diencephalic superventricle

Fornical GEP Anteromedial ganglionic NEP and SVZ

Cortical (paracentral) NEP

Anterolateral ganglionic NEP and SVZ

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Mammillary body

Sojourning and migrating deep neurons Central trigeminal tract (V) Principal sensory nucleus (V)

Anterior extramural migratory stream (pontine gray and Su reticular tegmental neurons) bt nu halam cle us ic

Superior olivary complex?

Vestibular nuclear complex Premigratory facial motor neurons (VII)?

Medial lemniscus?

Fornix

Medullary velum Medullary velum

Medial longitudinal fasciculus

Raphe nuclear complex

(future third ventricle)

Subthalamic Hypothalamic NEP NEP

SUBTHALAMUS HYPOTHALAMUS

rhombencephalic superventricle

(future fourth ventricle)

Reticular formation

PONS

Pontine NEP

Midline raphe glial system (provides structural support for brainstem flexures)

Strionuclear GEP

BASAL GANGLIA

Rhombencephalic choroid plexus

Cortical (ventral hippocampal) NEP Lateral lemniscus?

Zona incerta Latera l hyp o area thalam ic Forel's Dorsomedial/ fields ventromedial nuclei?

Ventral complex?

THALAMUS

Cortical (parahippocampal) NEP

Basolateral complex?

Central complex?

Internal capsule Corticomedial (funnel for complex? thalamocortical axons)

Thalamic NEP Cortical (cingulate) NEP

ventral pool

AM YG DA LA

Hippocampus

s leu uc rn a u tic Re Dorsal complex?

Sojourning and migrating Purkinje cells

(future lateral ventricle)

Cau date

Caudate

(future lateral ventricle)

anterior pool

Migrating and proliferating external germinal layer cells

telencephalic superventricle

Putamen (islands)

telencephalic superventricle

FUTURE PARACENTRAL LOBULE

Amygdaloid NEP

External capsule

Layer I

Superior/inferior cerebellar peduncles

Corticoganglionic NEP and SVZ ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Cerebellar notch External germinal layer

CEREBELLUM (HEMISPHERE)

Cerebellar NEP

Anterior

Posterior

Precerebellar NEP

Dorsal rhombic lip (contains cerebellar germinal trigone)

Subpial GEP

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

435

GW8 Horizontal CR 32 mm C609 Level 6: Section 86

See high-magnification views of the diencephalon from section 91 in Plates 181A and B, from this section in Plates 182A and B, and of the hypothalamus from section 92 in Plates 185A and B.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

436

PLATE 175A

PLATE 175B

STF5 Paracentral STF STF1 t1 Cortical plate Layer I

FUTURE TEMPORAL LOBE

telencephalic superventricle (future lateral ventricle)

Telencephalic choroid plexus

Superior/inferior cerebellar peduncles Lateral lemniscus?

e dat Cau

Anterior extramural migratory stream (pontine gray and reticular tegmental neurons)

Stria terminalis

Migrating posterior complex neurons

Dorsal hippocampus Fo rn ix

(future lateral ventricle)

anterior pool

Diencephalic choroid plexus

ic fissure Interhemispher

Posterior complex?

Internal capsule (funnel for thalamocortical axons) Dorsal complex?

Sojou rning an

Forel's fields

d migratin g thalamic neurons

Cortical (dorsal hippocampal) NEP

THALAMUS

Subthalamic NEP

diencephalic superventricle (future third ventricle)

Cortical (ventral hippocampal) NEP

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Cortical (parahippocampal) NEP

Premigratory facial motor neurons (VII)?

PONS Principal sensory nucleus (V)? Trigeminal motor nucleus (V)?

External germinal layer

Am yg NE dalo P id

DA LA AM

YG

BASAL GANGLIA

Vestibular nuclear complex

rhombencephalic superventricle

(future fourth ventricle)

Reticular formation

Hypothalamic NEP

(provides structural support for brainstem flexures)

Strionuclear glioepithelium

Cortical (paracentral) NEP

Fornix? Mammillary body

HYPOSUB- THALAMUS THALAMUS Midline raphe glial system

Fornical GEP

Posterior striatal NEP and SVZ

Abducens nucleus (VI) Medial longitudinal fasciculus Medial lemniscus? Raphe nuclear complex

Medial forebrain bundle?

Thalamic NEP Cortical (cingulate) NEP

Nuclei of the lateral lemniscus?

Migrating subthalamic nucleus neurons

Zona incerta

Ventral complex?

Sojourning and migrating deep neurons

Subthalamic nucleus

Optic tract?

telencephalic superventricle

Sojourning and migrating Purkinje cells Rhombencephalic choroid plexus

Future parahippocampal cortex

Ventral hippocampus

FUTURE PARACENTRAL LOBULE

Migrating and proliferating external germinal layer cells

posterior pool

Future temporal cortex

Pontine NEP

Cerebellar notch

Medullary velum

CEREBELLUM (HEMISPHERE)

Dorsal rhombic lip (contains cerebellar germinal trigone)

Cerebellar NEP

Cortical (temporal) NEP ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

437

GW8 Horizontal CR 32 mm C609 Level 7: Section 74

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

438

PLATE 176A

PLATE 176B

FUTURE TEMPORAL LOBE

STF5 STF1 t1 Cortical plate

Future parahippocampal cortex

Future temporal cortex

Migrating and proliferating external germinal layer cells

Sojourning and migrating Purkinje cells Rhombencephalic choroid plexus

telencephalic superventricle

Layer I

(future lateral ventricle)

posterior pool

Paracentral STF

Ventral hippocampus

Telencephalic choroid plexus

FUTURE PARACENTRAL LOBULE

Dorsal hippocampus

Migrating posterior complex neurons

Optic tract?

Ventral complex? Dorsal complex?

anterior pool

ic fissure Interhemispher

Diencephalic choroid plexus

Sojou rning an

Posterior complex (medial geniculate)? Red nucleus?

THALAMUS (future third ventricle)

mesencephalic superventricle (future cerebral aqueduct)

Cortical (paracentral) NEP

rhombencephalic superventricle

Raphe nuclear complex

(future fourth ventricle)

Pontine NEP Cerebellar notch

PONS

Parabrachial nucleus?

Nucleus of the lateral lemniscus (dorsal)?

CEREBELLUM (HEMISPHERE)

Cortical (ventral hippocampal) NEP Cortical (temporal) NEP

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Midline raphe glial system (provides structural support for brainstem flexures)

External germinal layer

Fornical GEP

Central gray

Reticular formation

MESENCEPHALIC TEGMENTUM

Stem cells of choroid plexus

Sojourning and migrating deep neurons

Medial longitudinal fasciculus

Mesencephalic (tegmental) NEP

diencephalic superventricle

Cortical (dorsal hippocampal) NEP

Medial lemniscus?

Interpeduncular nucleus

Thalamic NEP Cortical (cingulate) NEP

Nuclei of the lateral lemniscus?

Subpial GEP

d migratin g thalamic neurons

Medullary velum

Lateral lemniscus?

Substantia nigra?

x rni Fo

telencephalic superventricle (future lateral ventricle)

Superior/inferior cerebellar peduncles

Fornix

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Cortical (parahippocampal) NEP

Dorsal rhombic lip (contains cerebellar germinal trigone)

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Cerebellar NEP

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

439

GW8 Horizontal CR 32 mm C609 Level 8: Section 65

440

PLATE 177A

See high-magnification views of the diencephalon and midbrain tegmentum from section 66 in Plates 183A and B.

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

PLATE 177B STF5

Future temporal cortex

Parietal STF

FUTURE TEMPORAL LOBE

STF1 t1 Cortical plate Layer I

telencephalic superventricle (future lateral ventricle)

Migrating and proliferating external germinal layer cells

posterior pool

Rhombencephalic choroid plexus Superior/inferior cerebellar peduncles

Telencephalic choroid plexus

Sojourning and migrating Purkinje cells

Subpial GEP Lateral lemniscus?

FUTURE PARIETAL LOBE

Migrating posterior complex neurons

Optic tract?

Parabigeminal nucleus?

Posterior complex (medial geniculate)?

telencephalic superventricle (future lateral ventricle)

anterodorsal pool

ic fissure Interhemispher

Diencephalic choroid plexus

Sub st nig antia ra Medial longitudinal Ventral fasciculus tegmental area Medial lemniscus? Oculomotor nuclear complex (III)?

Dorsal complex? Posterior complex (lateral geniculate/ pulvinar)? Sojourn neurons ing a n d m igrating thalamic

Sojourning and migrating deep neurons

rhombencephalic superventricle

(future fourth ventricle)

Thalamic NEP

InterRed nucleus? peduncular nucleus

THALAMUS

Cortical (cingulate) NEP

diencephalic superventricle

Rubral NEP?

(future third ventricle)

mesencephalic superventricle

Hip

(future cerebral aqueduct)

poc am p

Mesencephalic (tegmental) NEP

MESENCEPHALIC TEGMENTUM

us

Subpial GEP? Cortical (parietal) NEP

Central gray

Cortical (hippocampal) NEP

Midline raphe glial system (provides structural support for brainstem flexures)

Raphe nuclear complex Reticular formation

PONS/ ISTHMUS

Cerebellar notch

CEREBELLUM (LATERAL VERMIS)

Medullary velum

Parabrachial nucleus?

External germinal layer

Cortical (parahippocampal) NEP Cortical (temporal) NEP

Pontine/isthmal NEP

CEREBELLUM (HEMISPHERE)

Dorsal rhombic lip (contains cerebellar germinal trigone)

Cerebellar NEP

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

441

GW8 Horizontal CR 32 mm C609 Level 9: Section 45

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

442

PLATE 178A

PLATE 178B STF5 Parietal STF STF1 t1 Cortical plate

FUTURE OCCIPITAL LOBE

Layer I

telencephalic superventricle

(future lateral ventricle)

dorsal pool

Future occipital cortex

Telencephalic choroid plexus Subpial GEP?

FUTURE PARIETAL LOBE

Lateral lemniscus?

Nucleus of the optic tract?

telencephalic superventricle

(future lateral ventricle)

Migrating habenular neurons

dorsal pool

diencephalic superventricle

(future third ventricle)

Inferior colliculus

Optic tract? Reticular formation Medial longitudinal Habenulofasciculus interpeduncular tract? Oculomotor nuclear complex (III)?

Reticular formation

Sojourning and migrating Purkinje cells

Trochlear nucleus (IV)?

y ra lg tra n Ce

Nerve IV (trochlear)?

rhombencephalic superventricle (future fourth ventricle)

ic fissure Interhemispher

Diencephalic choroid plexus

Medullary velum

Epithalamic NEP EPITHALAMUS

Mesencephalic (tegmental) NEP

CEREBELLUM (VERMIS)

mesencephalic superventricle (future aqueduct)

Cortical (parietal) NEP

Cerebellar NEP

MESENCEPHALIC TEGMENTUM Subpial GEP?

Cortical (occipital) NEP

External germinal layer

Mesencephalic (tectal, inferior colliculus) NEP

MESENCEPHALIC TECTUM

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

443

GW8 Horizontal CR 32 mm C609 Level 10: Section 36

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

444

PLATE 179A

PLATE 179B STF5 Occipital STF STF1 t1 Cortical plate Layer I

FUTURE OCCIPITAL LOBE

Future occipital cortex

Telencephalic choroid plexus

telencephalic superventricle

Nucleus of the optic tract? Optic tract?

(future lateral ventricle)

dorsal pool

FUTURE OCCIPITAL LOBE

diencephalic superventricle

(future third ventricle) pineal recess

Interhemispheric

Superior colliculus

Posterior commissure Diencephalic choroid plexus

PRETECTUM tral Cen

gray

Central

gray

Inferior colliculus

fissure

GEP (posterior commissure) Cortical (occipital) NEP

Subpial GEP

Mesencephalic (tectal, inferior colliculus) NEP Mesencephalic (tegmental) NEP mesencephalic superventricle (future aqueduct)

MESENCEPHALIC TEGMENTUM

Mesencephalic (tectal, superior colliculus) NEP

MESENCEPHALIC TECTUM

Dashed lines indicate staining and/or sectioning artifacts. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

445

GW8 Coronal CR 32 mm C609 Level 5: Section 97 DIENCEPHALON AND BASAL GANGLIA

LAYERS OF THE CORTICAL STRATIFIED TRANSITIONAL FIELD (STF) STF1 Superficial fibrous layer with an early developmental stage (t1) when many cells are migrating through it, followed by a late stage (t2) with sparse cells. Endures as the subcortical white matter. STF5 Deep cellular layer that is prominent during the first trimester, the first sojourn zone to appear outside the germinal matrix.

See level 5 in Plates 174A and B.

446

PLATE 180A

PLATE 180B FUTURE PARACENTRAL LOBULE

Layer I

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Dashed lines indicate staining and/or sectioning artifacts.

Cortical plate STF1 t1 STF5

FUTURE TEMPORAL LOBE

Future insular cortex

Paracentral STF

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone Future temporal cortex

External capsule

S

R

e?

(future lateral ventricle)

ventral pool

Central complex? Trajectory of corticofugal axons

BASAL GANGLIA

AMYGDALA

Cortical (temporal) NEP

Amygdaloid NEP

Cau

Anterolateral ganglionic NEP and SVZ

date

anterior pool

T

telencephalic superventricle

Basolateral complex?

(future lateral ventricle)

BASAL GANGLIA

d at

telencephalic superventricle

U M T I A

C au

Cortical (paracentral) NEP

Corticoganglionic NEP and SVZ Putamen (islands)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Corticomedial complex? Anteromedial ganglionic NEP and SVZ

Internal capsule

O

(funnel for thalamocortical axons)

In

a ct ebral p c i p i e n t cer e

cl e

Stria terminalis

p t i c tr

n du

Telencephalic choroid plexus

Strionuclear GEP

O

Fornical GEP Cortical

(dorsal hippocampal)

is lar nu cl icu lar eu ul R e t d s e m a i r St Dorsal complex?

NEP

Ret

THALAMUS

Thalamic NEP

Hippocampus Diencephalic choroid plexus

diencephalic superventricle

ar

nu

SUBTHALAMUS

cl

s

Ventral complex?

iclu

eu

Sojourning and migrating thalamic neurons Fornix

Zona incerta

Subthalamic NEP Forel's fields

(future third ventricle)

Arrows indicate the presumed direction of axon growth in brain fiber tracts.

t i c Evaginations and invaginations of the t r Su neuroepithelium are mosaic compartments a bth c ala t that give rise to different brain structures. mi cn Me u dia cle us l fo La reb ter al r ain hy bu po nd tha le lam ic a rea

?

Choroid plexus stem cells

p

Cortical (parahippocampal) NEP

F o r n i x

HYPOTHALAMUS

Mammillary body

Dorsomedial/ ventromedial nuclei?

447

Hypothalamic NEP

mammillary recess

GW8 Coronal CR 32 mm C609 Between levels 5 and 6: Section 91 DIENCEPHALON

See levels 5 and 6 in Plates 174A and B to 175A and B.

448

PLATE 181A

PLATE 181B

telencephalic superventricle

Stria terminalis

Somatosensory radiation

Caudate

telencephalic superventricle

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

(future lateral ventricle)

AMYGDALA

(future lateral ventricle)

I nc

Migrating lateral geniculate and pulvinar neurons?

Stria medullaris

Hippocampus Diencephalic choroid plexus

nt c e rebral pe

Soj

cl eus

(funnel for thalamocortical axons)

Posterior complex?

Fornix

t r a c t du n c l e

Internal capsule

Re tic ul ar nuc leu s Dorsal complex?

Retic u l a r

Sprouting thalamic axons?

nin

g an dm igra tin

Su bth a

Zona incerta

lam

Forel's fields Medial lemniscus fibers penetrating the ventral complex?

diencephalic superventricle

(future third ventricle)

Reticular nucleus NEP?

Dorsal complex NEP?

Thalamic NEP

(dorsal hippocampal)

NEP

Fornical GEP

GEP (stria medullaris)

THALAMUS

HYPOTHALAMUS

Subthalamic NEP

SUBTHALAMUS

Subthalamic nucleus

Internal capsule Anteromedial ganglionic NEP and SVZ

Cortical (parahippocampal) NEP

Stria terminalis Strionuclear GEP

(future third ventricle)

Hypothalamic NEP

Choroid plexus stem cells

Telencephalic choroid plexus

Migrating subthalamic (Luysian) nucleus neurons that originate in the hypothalamic NEP

Dorsomedial/ ventromedial nuclei?

Ventral complex NEP?

Cortical

nu cle us

Mammillary body

g thalamic neurons

diencephalic superventricle

Posterior complex NEP?

ic

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Me dia l fo reb rai La nb ter un al dle hy po tha lam ic a rea

n

Ventral complex?

our

Future parahippocampal cortex

O p t i c

u

Sojourning lateral geniculate and pulvinar neurons?

i p ie

Amygdaloid NEP

Arrows indicate the presumed direction of axon growth in brain fiber tracts. Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

449

GW8 Coronal, CR 32 mm, C609, Level 6: Section 86 DIENCEPHALON

See level 6 in Plates 175A and B.

450

PLATE 182A

PLATE 182B

telencephalic superventricle

Caudate

(future lateral ventricle)

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

ix Fimbria/forn

c O p t i

Ventral Hippocampus

t r a c t

Migrating lateral geniculate and pulvinar neurons?

Fo rn ix

Dorsal Hippocampus

Soj

Ventral complex?

our

nin

Sprouting thalamic axons? diencephalic superventricle (future third ventricle) Diencephalic choroid plexus Posterior complex NEP?

GEP (stria medullaris)

Cortical

(dorsal hippocampal)

g an dm igra t

le u s

Medial lemniscus fibers penetrating the ventral complex?

Forel's fields

Arrows indicate the presumed direction of axon growth in brain fiber tracts. Migrating subthalamic (Luysian) nucleus neurons that originate in the hypothalamic NEP

le ?

Posterior complex?

Zona incerta

Su bt nu hala cle m us ic

nc e du

Internal capsule

(funnel for thalamocortical Re axons) ti cu c la u r n n ucl r eus la R e t i c u Dorsal complex?

lp ra

Incipi ent c ere b

Sojourning lateral geniculate and pulvinar neurons?

Stria medullaris

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Stria terminalis

Me dia l fo reb rai nb un Later dle al hyp othala mic a rea

Supra-/premammillary area

ing tha lamic neurons

Mammillary body

Ventral complex NEP? Reticular nucleus NEP?

Dorsal complex NEP?

Thalamic NEP

THALAMUS

Subthalamic (Forelian) NEP

SUBTHALAMUS

Hypothalamic NEP

HYPOTHALAMUS diencephalic superventricle (future third ventricle)

NEP

Fornical GEP Telencephalic choroid plexus

Choroid plexus stem cells

Anteromedial ganglionic neuroepithelium NEP and SVZ

ic lam s a h u bt cle Su nu

Internal capsule

Stria terminalis Strionuclear GEP

Optic tract

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

451

Enlarged in Plates 184A and B.

GW8 Coronal, CR 32 mm, C609 Near level 8: Section 66 DIENCEPHALON AND MIDBRAIN TEGMENTUM

See level 8 in Plates 177A and B.

452

PLATE 183A

PLATE 183B

(future lateral ventricle)

Telencephalic choroid plexus

H ip

p

m oca

pu

s Migrating lateral geniculate neurons?

Posterior complex (lateral geniculate/ pulvinar)? Sojourning lateral geniculate and pulvinar neurons?

Sojourni

Sprouting thalamic axons?

e u s nucl

Reticular nucleus

s

Optic tract?

r icula Ret

Stria medullaris

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

telencephalic superventricle

r la u c ti Re

n

u

e cl

u

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium Posterior complex (medial geniculate)?

Dorsal complex?

Zona incerta

Su

(future aqueduct)

Medial longitudinal fasciculus?

(future third ventricle)

on ng and migrating thalamic ne u r

s

ta

nt

Medial forebrain bundle

mesencephalic superventricle diencephalic superventricle

bs

ia

ni

gra

Ventral tegmental area Interpeduncular nucleus

Oculomotor nuclear complex (III)?

Subpial GEP

Posterior complex (lateral geniculate) NEP? GEP (stria medullaris)

Posterior complex (medial geniculate)NEP?

THALAMUS T h a l a m i c

Cortical (hippocampal) NEP

Mesencephalic (tegmental) NEP

Dorsal complex NEP?

Reticular nucleus NEP?

N E P

Subthalamic NEP?

Interpeduncular fossa

MESENCEPHALIC TEGMENTUM

SUBTHALAMUS?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

453

GW8 Coronal, CR 32 mm, C609, Near level 8: Section 66 THALAMUS (TRANSIENT DEVELOPMENTAL LAYERS)

See level 8 in Plates 177A and B.

454

PLATE 184A

PLATE 184B

(future lateral ventricle)

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold Bold Telencephalic choroid plexus

C

or

ti

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

telencephalic superventricle

l ca H

(h i p

p ip p

o

o

m ca

c

a

m

p

NE ) l a

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

P

s p u

a l t e r L a

n i o a t s? r xon i g al a c m i t or n moc r o hala u t r h e ct n wit c tra ula g le d c n O p ti l a t e i i rm et i n te i c u c r i b ers i f g e n m t la tr a c Dorsal tha O pti c

the s in n o r neu Settled

fut

ure

g l i n t t S e

c nu

le

us

Posterior complex (medial geniculate)?

complex?

i c l a m a t h

n s r o u n e

THALAMUS

Posterior complex (pulvinar)?

ioneer e layer (p t i h w r e t u o c i Thalam

Stria medullaris

thalam

g m i g r a t i n

on cal ax i t r o c o

s?)

o n s n e u r

T h a l a m i c rons) amic ing neu sojourn t a r g i m w fe zone (many sojo Tha urning neurons intermingled with a lam ic i n n e r w h i t e l a y e r ( s p r o u t i n g t h a l a m i c a x o n s ? )Posterior complex

Thal

Posterior complex GEP (lateral geniculate/pulvinar) NEP? (stria medullaris) diencephalic superventricle (future third ventricle)

Dorsal complex NEP?

(medial geniculate)NEP?

Thalamic NEP

455

See levels 5 and 6 in Plates 174A and B to 175A and B.

GW8 Coronal, CR 32 mm, C609 Between levels 5 and 6: Section 92 HYPOTHALAMUS AND SUBTHALAMUS

456

PLATE 185A

PLATE 185B Optic tract?

Subthalamic NEP

Zona incerta Forel's fields

SUBTHALAMUS

Migrating subthalamic neurons diencephalic superventricle

Dorsal hypothalamic NEP

Dorsomedial nucleus? Lateral hypothalamic area

HYPOTHALAMUS

Ventromedial nucleus?

Middle hypothalamic NEP

Settling subthalamic (Luysian) nucleus neurons

Medial forebrain bundle ix rn Fo

HYPOTHALAMUS NEP - Neuroepithelium

Mammillary body

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures. FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Migrating hypothalamic neurons

Su bt (c o h a l a rp mi us c n Lu uc y s le u i) s

(future third ventricle)

Posterior hypothalamic (mammillary and Luysian) NEP

Mammillary body

Migrating subthalamic nucleus neurons that originate in the hypothalamic (Luysian) NEP

457

458

PART PARTX: X: GW7.5 GW7.5 CORONAL CORONAL This is specimen number 966 in the Carnegie Collection, designated here as C966. A normal female fetus with a crown-rump length (CR) of 23 mm was collected in 1914. The fetus is estimated to be at gestational week (GW) 7.5. The entire fetus was fixed in bichloric acetic acid, embedded in celloidin, cut transversely in 40 µm sections, and was stained with aluminum cochineal. The histological preservation of this specimen is excellent, and the sections are cut nearly perfectly bilaterally. Several years ago, an excellent 3-D reconstruction of the brain and upper cervical spinal cord was done by piecing together cardboard cutouts of the brain outlines in each section and then gluing them together; the rhombencephalic superventricle was not included in that reconstruction. A photograph of that model (which is still part of the Carnegie Collection today) shows us the exact location and cutting plane of C966’s sections (Figure 9). Like most of the specimens in this Volume, the sections are not cut exactly in one plane, but C966’s sections are much closer to the coronal than the horizontal plane. Photographs of 21 sections (Levels 1-21) of the brain in the head are shown in Plates 186-206. Our computer-aided three-dimensional reconstructions of the brain, ventricles (including the rhombencephalic superventricle), and selected neuroepithelial components are shown on the cover and in Figures 10-19. C966 is considerably less mature than the GW8 specimens. The superventricles are large in the centers of all brain structures, especially in the telencephalon and rhombencephon. Even though the diencephalic superventricle is approaching a slit-like shape, it is wider than that in the GW8 specimens, and the mesencephalic superventricle forms a more balloon-like expansion beneath the rudimentary tectum. Like the GW8 specimens, the respective thicknesses of the neuroepithelium (NEP) and parenchyma are keys to determining the degree of maturation of various brain structures. The parenchyma is thick and bordered by a thin NEP in the medulla and pons, indicating that many neurons have been generated here, but the production of late-generated neurons continues. There are layers of dense cells adjacent to the lateral pontine NEP where vestibular nuclear neurons and trigeminal nuclear neurons may be sojourning prior to migration and settling. There is a larger accumula-

tion of presumptive facial motor neurons near the midline NEP in the pontomedullary trench and some are migrating toward the indistinct facial motor nucleus. The precerebellar neuroepithelium in the medulla is thicker and generating more precerebellar neurons than at GW8; many neurons are entering the inferior olive after migrating in the posterior intramural migratory stream, but the anterior and posterior extramural migratory streams are absent; that confirms neurogenetic data in rats that the inferior olive contains the earliest-generated precerebellar neurons. The cerebellar NEP is thick and difficult to distinguish from an adjacent dense sojourn zone in the cerebellar parenchyma, called cerebellar transitional field (CTF) 6. The remaining CTF has alternating layers of cells and fibers (CTF1-5). The external germinal layer (egl) is completely absent. If one can extrapolate from data on cerebellar neurogenesis in rats, the human cerebellar NEP by GW7.5 has generated all of the deep neurons and is now producing “middle-aged” Purkinje cells; the oldest Purkinje cells are sojourning in CTF6. Both the mesencephalic tegmental NEP and the isthmal NEP are nearly the same thickness as the pontine and medullary NEPs, but dense sojourn zones of young neurons are more obvious in the adjacent parenchyma. The superficial border of a thick mesencephalic tectal NEP is difficult to distinguish from dense wavefronts of young neurons extending into a thin parenchyma. The majority of neurons in both the superior and inferior colliculi have not yet been generated by GW7.5. The diencephalic NEP is thicker at GW7.5 than at GW8, and the thin parenchyma is filled with dense zones of sojourning and migrating neurons. There is no internal capsule, but some pioneer axons are accumulating in inner and outer white layers in the thalamic parenchyma. The telencephalic NEP is thick in all areas, and the oldest basal telencephalic and basal ganglionic neurons are settling in the thick parenchyma. Most neurons in the septum and striatum have yet to be generated. In the cerebral cortex, the NEP is bordered by a thin primordial plexiform layer that contains the oldest cortical neurons (Cajal-Retzius cells) and subplate neurons; there is no cortical plate. The cortical NEP is expanding and increasing its number of neural stem cells as the telencephalic superventricle grows; nearly all cortical neurons in layers II-VI have still to be generated.

459

GW7.5 CORONAL SECTION PLANES LEVEL SECTION

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 10 34 40 52 58 70 76 84 92 98 105 112 119 125 128 139 147 157 163 171 179

CORONAL PLANE (90˚)

C966's cutting angle rotates 25˚ counterclockwise from the true coronal plane (90˚). The dorsal part (top) of each section is posterior to the ventral part (bottom).

HORIZONTAL PLANE (0˚)

H A LON

EP C

CEREB RA L

LUM EBEL CER MEDUL LA

RHOMBENCEPHALON

N

NS

E DI

C

PI O NA L RD

S

SPH MI HE

PO

Olfactory bulb

MESENC

LON HA EP ERE

LON HA EP

TELE NC

Medullary velum

Figure 9. The lateral view of a 3-D model of C966’s brain and upper cervical spinal cord (part of the Carnegie Collection at the National Museum of Health and Medicine) shows the exact locations and cutting angles of the illustrated sections of C966 in the following pages. The small inset identifies the major structural features. The medullary velum was not reconstructed so that the rhombencephalic superventricle appears as an open gap beneath the cerebellum.

460

PLATE 186A GW7.5 Coronal/horizontal CR 23 mm C966 Level 1: Section 10

461

PLATE 186B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

NEP - Neuroepithelium

arietal bon es ure p Fut

Interhemispheric fissure FUTURE PARACENTRAL LOBULE Cortical (paracentral) NEP

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

Primordial plexiform layer

telencephalic superventricle

(future lateral ventricle) anterior pool

Settling Cajal-Retzius cells

Cortical (frontal) NEP

Migrating subplate neurons FUTURE FRONTAL LOBE F ut

ure f

r o n t a l b o ne

The cerebral cortex in this specimen does not have a cortical plate and a stratified transitional field outside the cortical neuroepithelium. Instead, there is a primordial plexiform layer composed of early-generated Cajal-Retzius cells and the slightly later-generated subplate neurons. The large Cajal-Retzius cells settle subjacent to the pia meninx and remain superficial in cortical Layer I throughout later development. The deep border of Layer I is not defined until a cortical plate appears. Subplate neurons accumulate in a loosely defined network beneath the CajalRetzius cells. In later development they become radially aligned and are the pioneer neurons in the cortical plate. Eventually, they delaminate and settle in the subplate (cortical Layer VII).

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

462

PLATE 187A GW7.5 Coronal/horizontal CR 23 mm C966 Level 2: Section 34

463

PLATE 187B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Skull and skin

ure parietal bones Fut

Meninges (dura and arachnoid) Brain surface (pia, heavier line)

Cortical (posterior cingulate) NEP

FUTURE PARIETAL LOBE

Primordial plexiform layer

Cortical (paracentral/parietal) NEP

FUTURE PARACENTRAL LOBULE

Cortical (hippocampal) NEP

Fornical GEP

Corticoganglionic NEP and SVZ

Interhemispheric fissure

posterodorsal pool

Settling Cajal-Retzius cells Migrating subplate neurons

Fornix

Telencephalic choroid plexus

Lateral migratory stream? Migrating neurons of the endopiriform nucleus and claustrum?

telencephalic superventricle Cortical (anterior cingulate) NEP

Anterolateral ganglionic NEP and SVZ

Cortical (orbitofrontal) NEP

(future lateral ventricle)

anteroventral pool

FUTURE FRONTAL LOBE

Future frontal bone

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Migrating and settling basal ganglionic and basal telencephalic neurons

464

PLATE 188A GW7.5 Coronal/horizontal CR 23 mm C966 Level 3: Section 40

465

PLATE 188B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

Future parietal bone s

Skull and skin

diencephalic superventricle (future third ventricle)

Thalamic (dorsal complex) NEP Cortical (posterior cingulate) NEP

Meninges (dura and arachnoid) Brain surface (pia, heavier line)

FUTURE PARIETAL/ OCCIPITAL LOBES posterodorsal pool

Cortical (parietal/ occipital) NEP

FUTURE PARACENTRAL LOBULE Cortical (paracentral) NEP

Cortical (hippocampal) NEP

Fornix

THALAMUS

Fornical GEP Choroid plexus stem cells

Anterolateral ganglionic NEP and SVZ

Choroid plexus stem cells

BASAL GANGLIA

Migrating subplate neurons

Expanding fetal telencephalic choroid plexus

Vascular bed of the telencephalic choroid plexus

telencephalic superventricle (future lateral ventricle)

anteroventral pool

Septal NEP SEPTUM

Basal telencephalic NEP

Settling Cajal-Retzius cells

Lateral migratory stream?

Thalamic (anterior complex) NEP

Corticoganglionic NEP and SVZ

Primordial plexiform layer

olfactory recess

OLFACTORY BULB

Migrating neurons of the endopiriform nucleus and claustrum?

Settling basal telencephalic neurons intermingle with those of the lateral migratory stream? Migrating basal ganglionic and basal telencephalic neurons

Migrating and settling olfactory bulb neurons

Cortical (olfactory) NEP

Migrating and settling medial septal neurons (nucleus of the diagonal band, vertical limb?) Interhemispheric fissure

Fronto-nasal process

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

466

PLATE 189A GW7.5 Coronal/horizontal CR 23 mm C966 Level 4: Section 52

467

PLATE 189B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone Epithalamic (habenular complex) NEP Thalamic (posterior complex) NEP

Layers of the developing thalamus Sojourning neurons Inner white layer Migrating and settling neurons Outer white layer

Thalamic (dorsal complex) NEP Cortical (posterior cingulate) NEP Cortical (occipital) NEP

(future third ventricle)

Cortical (hippocampal) NEP Fornical GEP Choroid plexus stem cells

(future lateral ventricle) posterodorsal pool

Primordial plexiform layer Fornix

Settling CajalRetzius cells

Expanding fetal telencephalic choroid plexus

Migrating subplate neurons

Vascular bed of the telencephalic choroid plexus

Stria medullaris?

Migrating neurons of the endopiriform nucleus and claustrum?

fo

Corticoganglionic NEP and SVZ

telencephalic superventricle

THALAMUS

FUTURE PARIETAL/ TEMPORAL LOBES

diencephalic superventricle

FUTURE OCCIPITAL LOBE

Cortical (parietal/ temporal) NEP

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

parietal bone ture s Fu

ra

me

Thalamic (anterior complex) NEP

Anterolateral ganglionic NEP and SVZ

BASAL GANGLIA Anteromedial ganglionic NEP and SVZ

n of o n r o m

Primordial cortical plate (insular area?)

telencephalic superventricle (future lateral ventricle) anteroventral pool

Migrating striatal and basal ganglia neurons Settling basal ganglia neurons (putamen and globus pallidus)?

Septal NEP

Basal telencephalic NEP

Settling basal telencephalic neurons (substantia innominata)?

SEPTUM

Migrating and settling medial septal neurons (medial septal nucleus?)

OLFACTORY BULB

Interhemispheric fissure

Nasal cavity

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Nostril

Nerve I (olfactory)

Nasal septum

Olfactory epithelium

Lateral migratory stream?

Fronto-nasal process

Area of future zygomatic bone?

Area of future maxilla?

468

PLATE 190A GW7.5 Coronal/horizontal CR 23 mm C966 Level 5: Section 58

469

PLATE 190B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

diencephalic superventricle

Cortical (parahippocampal) NEP FUTURE OCCIPITAL/ TEMPORAL LOBES

Cortical (hippocampal) NEP Fornical GEP Choroid plexus stem cells

Corticoganglionic NEP and SVZ Anterolateral ganglionic NEP and SVZ

o re

rb

he

Fornix

no

id

pro

ces

Telencephalic choroid plexus Vascular bed of the telencephalic choroid plexus Stria medullaris?

Migrating neurons of the endopiriform nucleus and claustrum?

SEPTUM

s?

Lateral migratory stream?

Channels for internal capsule?

Settling basal ganglia neurons (putamen and globus pallidus)? Settling basal telencephalic neurons (substantia innominata)?

Nasal cavity

Migrating and settling bed nucleus of the stria terminalis neurons? Migrating and settling medial septal nucleus neurons?

Nasal septum

Olfactory epithelium

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Migrating subplate neurons

Primordial cortical plate (insular area?)

Septal NEP

Nerve I (olfactory)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Settling CajalRetzius cells

Migrating basal ganglia neurons

Interhemispheric fissure Pigment layer of retina

Primordial plexiform layer

future lateral ventricle anteroventral pool

Basal telencephalic NEP?

tu

-s p

(future lateral ventricle) posterodorsal pool

Strionuclear NEP?

Fu

it o

telencephalic superventricle

foramen of monro

BASAL GANGLIA

Anteromedial/posterior ganglionic NEP and SVZ?

Layers of the developing thalamus Sojourning neurons Inner white layer? Migrating and settling neurons Outer white layer

Thalamic (reticular protuberance) NEP

Thalamic (anterior complex) NEP

Meninges (dura and arachnoid) Brain surface (pia, heavier line)

THALAMUS

(future third ventricle, thalamic pool)

Epithalamic (habenular complex) NEP Thalamic (posterior complex) NEP Thalamic (dorsal complex) NEP

Cortical (occipital/ temporal) NEP

Skull and skin

arietal bones ure p t u F

Fronto-nasal process

Nasal conchae Area of future zygomatic bone? Maxilla?

Vitreous body Cornea Lens Neural retina Intraretinal space Pigment layer of retina Sclera Eyelid

Eye

470

PLATE 191A GW7.5 Coronal/horizontal CR 23 mm C966 Level 6: Section 70

471

PLATE 191B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

re parietal bones Futu

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

GEP (posterior commissure)

Posterior commissure Migrating habenular neurons

Epithalamic (habenular complex) NEP

diencephalic superventricle

epithalamic/ EPIthalamic THALAMUS pool Thalamic (posterior complex) NEP

Cortical (parahippocampal) NEP

Cortical (hippocampal) NEP

FUTURE OCCIPITAL/ TEMPORAL LOBES

Corticoganglionic NEP and SVZ?

THALAMUS

Cortical (temporal/ occipital) NEP

Fornical GEP Choroid plexus stem cells

Thalamic (reticular protuberance) NEP Thalamic (reticular) NEP

Cortical (insular?) NEP Posterior ganglionic NEP and SVZ

tu

re o

rb

Outer white layer Migrating ventral complex neurons

telencephalic superventricle

(future lateral ventricle) posterior pool

Stria medullaris? Migrating reticular nucleus neurons

-s p

h en

Primordial cortical plate (primary olfactory cortex?) Lateral olfactory tract Migrating striatal and basal ganglia neurons Settling basal ganglia neurons (putamen and globus pallidus)?

preoptic pool

Settling basal telencephalic neurons (basal nucleus of Meynert)? Anterior commissure? Migrating and settling bed nucleus of the stria terminalis neurons?

PREOPTIC AREA oid pro ces s ?

Migrating lateral preoptic neurons? Fornix? Sojourning preoptic neurons?

Olfactory epithelium

Nasal cavity

Nasal septum

Nerve I (olfactory)

Lens

Palatal process

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Ciliary ganglion (III)?

Nasal conchae

Vitreous body Neural retina Intraretinal space Pigment layer of retina Sclera Eyelid

Eye

Area of future zygomatic bone?

Maxilla

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Lateral migratory stream?

Stria terminalis?

Preoptic NEP

it o

Primordial plexiform layer

Fornix

subthalamic pool

Subthalamic NEP

Settling basal telencephalic neurons (substantia innominata)?

Fu

BTHAL SU

Strionuclear NEP?

Migrating posterior complex neurons

Migrating subthalamic (Forel's fields, zona incerta) neurons

US AM

BASAL GANGLIA

Channels for internal capsule and lateral olfactory tract?

Layers of the developing thalamus

Sojourning neurons

(future third ventricle)

Thalamic (dorsal and ventral complexes) NEP

Habenulo-interpeduncular tract

Maxilla Oral cavity

472

PLATE 192A GW7.5 Coronal/horizontal CR 23 mm C966 Level 7: Section 76

473

PLATE 192B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

re parietal bones Futu

GEP (posterior commissure)

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

EPITHALAMUS Posterior commissure

Migrating habenular neurons

epithalamic/ thalamic pool

Epithalamic (habenular complex) NEP Thalamic (posterior complex) NEP

Habenulo-interpeduncular tract

Layers of the developing thalamus

Sojourning neurons

Cortical (temporal) NEP

Corticoganglionic NEP and SVZ? Posterior ganglionic NEP and SVZ

Cortical (hippocampal) NEP

Thalamic (reticular protuberance) NEP Thalamic (reticular) NEP

Strionuclear NEP?

Migrating posterior complex neurons Outer white layer Migrating ventral complex neurons telencephalic superventricle

(future lateral ventricle) posterior pool

Stria medullaris? Migrating reticular nucleus neurons

Lateral olfactory tract

Migrating striatal (putamen) neurons

Subthalamic NEP

Migrating and settling bed nucleus of the stria terminalis neurons?

Medial forebrain bundle

subthalamic/ hypothalamic pool

PREOPTIC AREA

Nasal cavity

Palatal process Maxilla

Sojourning and migrating lateral preoptic neurons?

Settling medial preoptic neurons?

s

Oral/nasal cavity Maxilla

Settling lateral preoptic neurons?

Sojourning and migrating medial preoptic neurons?

Nasal septum

Preoptic NEP O rb itosph en oid pro ces

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Lateral migratory stream?

Stria terminalis?

Migrating Forel's field and zona incerta neurons

BASAL GANGLIA SUBTHALAMUS

Settling basal telencephalic neurons (globus pallidus)? Ansa lenticularis?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Primordial plexiform layer

Forn ix

Cortical (temporal) NEP

(future third ventricle)

US LAM A H T

Cortical (parahippocampal) NEP

diencephalic superventricle

Thalamic (ventral complex) NEP

FUTURE TEMPORAL LOBE

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

Tongue Oral cavity Fused mandibular processes

Nasal conchae Area of future zygomatic bone

Sclera Vitreous body Neural retina Intraretinal space Pigment layer of retina Eyelid

Eye

474

PLATE 193A GW7.5 Coronal/horizontal CR 23 mm C966 Level 8: Section 84

475 FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

GEP (posterior commissure) Epithalamic (habenular complex) NEP

Amygdaloid NEP and SVZ

AMYGDALA

SUBTHALAMUS

Subthalamic NEP

Medial forebrain bundle?

Preoptic NEP

to

subthalamic/ preoptic pool Optic chiasm GEP?

id no he - sp

Sojourning neurons (posterior complex) Migrating posterior complex neurons (pulvinar and lateral geniculate body) Outer white layer

Ventral lateral geniculate body?

Migrating reticular nucleus neurons

Primordial plexiform layer telencephalic superventricle (future lateral ventricle) posterior pool

Migrating amygdaloid neurons Settling subthalamic neurons (zona incerta?) Migrating subthalamic (Forel's field) neurons

Sojourning and migrating lateral preoptic neurons? Optic tract? Sojourning and migrating medial preoptic neurons? Settling medial preoptic neurons?

pr

ce

o

Sclera Pigment layer of retina Intraretinal space Neural retina Eyelid

Habenulo-interpeduncular tract

Settling lateral preoptic neurons?

PREOPTIC AREA

bi

O r

Migrating habenular neurons

thalamic pool

(future third ventricle)

THALAMUS

Thalamic (reticular) NEP

diencephalic superventricle

ari eta lb on e

Fut ure p

Thalamic (reticular protuberance) NEP

FUTURE TEMPORAL LOBE

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

Layers of the developing thalamus

Thalamic (posterior complex) NEP

Cortical (temporal) NEP

Posterior commissure

epithalamic pool

TH EPI AL AM US

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium SVZ - Subventricular zone

PLATE 193B

e parietal bo nes Futur

ss

Optic nerve and chiasm GEP

optic recess

Sphenoid

Migrating optic nerve and chiasm glia?

Eye

Area of future zygomatic bone

Maxilla Palatal process

Tongue

Maxilla Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Fused mandibular processes

Oral cavity

476

PLATE 194A GW7.5 Coronal/horizontal CR 23 mm C966 Level 9: Section 92

477 FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

GEP (posterior commissure)

bo

ne

Epithalamic (habenular complex) NEP

Skull and skin Meninges (dura and arachnoid)

TH EPI AL AM US

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

PLATE 194B

e parietal bones Futur

Brain surface (pia, heavier line)

Posterior commissure

Migrating habenular neurons Habenulo-interpeduncular tract

Layers of the developing thalamus Sojourning neurons (posterior complex)

diencephalic superventricle

THALAM

US

Futu re p a

rie

t al

epithalamic/ thalamic pool

(future third ventricle)

Migrating posterior complex neurons (medial geniculate body)

Thalamic (posterior complex) NEP Thalamic (reticular protuberance) NEP?

SUBUS THALAM

Thalamic (reticular) NEP?

Outer white layer

Migrating reticular nucleus neurons?

Migrating subthalamic neurons (Forel's fields?) Settling subthalamic neurons (zona incerta?)

subthalamic/ hypothalamic pool

Subthalamic NEP

pt

O

Area of future zygomatic bone?

MUS ALA c tract? H T ti O Op HYP r o i r c i e Ant halam ot P p y E h N

Medial forebrain bundle (dispersed among settling lateral hypothalamic neurons)?

Ali-spheno id pr oc e

ss

ic t

Settling lateral hypothalamic neurons? Sojourning and migrating lateral hypothalamic neurons? Sojourning and migrating anterior hypothalamic neurons? Settling anterior hypothalamic neurons?

Trigeminal ganglion (V)

ract

Nerve V (trigeminal, distal) ?

Sphenoid

Migrating and settling anterobasal neurons?

Maxilla

Palatal process

Tongue Oral cavity

Oral cavity

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Fused mandibular processes

Maxilla

478

PLATE 195A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 10: Section 98

479 FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

GEP (posterior commissure)

(future aqueduct)

mesencephalic superventricle

Posterior commissure

Pretectal neuroepithelium (NEP)

PRETECTUM

Futur e pa rieta l bo ne

PLATE 195B

Future parietal bones

Migrating glia invade posterior commissure?

Sojourning and migrating pretectal neurons Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line) Sojourning and migrating interpeduncular nucleus neurons?

Mesencephalic tegmental NEP

Substantia nigra neurons?

diencephalic superventricle

Sojourning and migrating subthalamic neurons (Forel's fields?) Settling subthalamic neurons (zona incerta?)

Settling lateral hypothalamic neurons? Sojourning and migrating lateral hypothalamic neurons? Sojourning and migrating middle hypothalamic neurons? Migrating and settling arcuate nucleus neurons?

Trigeminal ganglion (V)

H

M US ALptAic tract? H T O YPO

Medial forebrain bundle (dispersed among settling lateral hypothalamic neurons)?

thalamic NEP Middle hypo

Subthalamic NEP

Settling interpeduncular nucleus neurons?

(future third ventricle, subthalamic/ hypothalamic pool)

US SUBTHALAM

MIDBRAIN TEGMENTUM

A li- s

Area of future zygomatic bone?

p he

noi

dp

roc e

ss

Sella turcica

Sphenoid

Distal part Intraglandular cleft Intermediate part

Nerve V (trigeminal, distal)

Pituitary gland

(anterior lobe, adenohypophysis)

Maxilla Tongue

Palatal process

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Oral cavity

Mandibular process (Meckel's cartilage)

480

PLATE 196A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 11: Section 105

481 FONT KEY: GEP (posterior ventricular divisions - capitals commissure) Germinal zone - Helvetica bold Transient structure - Times bold italic MESENCEPHALIC Permanent structure - Times Roman or Bold TECTUM

PLATE 196B

Future pariet al b one s

(SUPERIOR COLLICULUS)

Migrating glia invade posterior commissure?

(future aqueduct)

mesencephalic superventricle

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

Mesencephalic tectal (superior colliculus) NEP

Posterior commissure

Fu

Sojourning and migrating superior colliculusa neurons Skull and skin Meninges (dura and arachnoid)

tu

re par

Sojourning and migrating central gray neurons?

Rubral NEP?

Brain surface (pia, heavier line)

ieta l

Settling central gray neurons?

bon e

Mesencephalic tegmental NEP

Sojourning and migrating interpeduncular nucleus neurons? Habenulo-interpeduncular tract?

Red nucleus?

Settling interpeduncular nucleus neurons?

MESENCEPHALIC TEGMENTUM

Substantia nigra neurons? Ventral tegmental area neurons?

Hypothalamic (supramammillary) NEP

diencephalic superventricle (future third ventricle, mammillary recess)

Medial forebrain bundle?

Sojourning and migrating premammillary neurons

Hypothalamic (premammillary) NEP

Settling lateral hypothalamic neurons?

HYPOTHALAMUS Future

infundibular recess

Optic tract?

s q ua

Sojourning and migrating ventromedial nucleus neurons?

s tem m ou

Middle hypothalamic (arcuate and ventromedial nuclear) NEP

Sojourning and migrating arcuate nucleus neurons?

o al b por

Sojourning and migrating ventromedial nucleus neurons?

ne

Nerve V (trigeminal, proximal)

Al Area of future zygomatic bone?

i-s ph

Sella turcica eno

id p

roce s

s

Trigeminal ganglion (V)

Distal part Intermediate part

Sphenoid

Pituitary gland

(anterior lobe, adenohypophysis)

Maxilla

Palatal process

Tongue

Oral cavity

Mandibular process (Meckel's cartilage) Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

482

PLATE 197A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 12: Section 112

483 GEP (posterior commissure)

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

MESENCEPHALIC TECTUM

PLATE 197B rie tal bo ne

Posterior commissure

(future aqueduct)

mesencephalic superventricle

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

F utur e pa

(SUPERIOR COLLICULUS) Mesencephalic tectal (superior colliculus) NEP (thick) Rubral NEP (thin)?

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line) Sojourning and migrating superior colliculus neurons Sojourning and migrating red nucleus neurons?

Mesencephalic tegmental NEP (thin)

Sojourning and migrating oculomotor complex (III) neurons?

Fu

MESENCEPHALIC TEGMENTUM

ture pari

Substantia nigra neurons? Ventral tegmental area neurons?

etal b one

Hypothalamic (supramammillary) NEP

Sojourning and migrating premammillary neurons

diencephalic superventricle

HYPOTHALAMUS

(future third ventricle, mammillary recess)

(MAMMILLARY BODY) Hypothalamic (mammillary) NEP

Sojourning and migrating mammillary neurons

Future squ

Raphe domain

ain Medial dom

bo ne

Future petrous temporal bone

Intermedia

l ora

Lateral

te m p

Trigeminal ganglion (V)

te domain

PONS domain

a m o us

Trigeminal nuclear complex

Superior olivary complex? Medial lemniscus and trapezoid body?

Raphe nuclear complex

Medial lemniscus?

Longitudinal bands of the pontine reticular formation

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Central trigeminal tract (devoid of glia) Nerve V (trigeminal, boundary cap) Nerve V (trigeminal, proximal, many glia)

Midline raphe glial system (provides structural support for brainstem flexures)

Medial longitudinal fasciculus?

Area of future temporal/ mandibular joint?

Trigeminal nuclear complex

Trigeminal ganglion (V) Nerve V (trigeminal, distal, many glia)

Temporal bone labyrinth

Sphenoid

Maxilla/ palatine?

Oropharynx Mandibular process (Meckel's cartilage)

Tongue

Fu

tu

re

bo hyoid

ne

?

484

PLATE 198A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 13: Section 119

485 FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

GEP (posterior commissure)

F u t u re p a rie

(future aqueduct)

mesencephalic superventricle

Mesencephalic tectal (superior colliculus) NEP (thick)

MESENCEPHALIC TECTUM

(SUPERIOR COLLICULUS) ABBREVIATIONS: Rubral NEP (thin)? GEP - Glioepithelium NEP - Neuroepithelium Mesencephalic tegmental NEP (thin)

PLATE 198B tal bon es

Sojourning and migrating superior colliculusa neurons Skull and skin

Posterior commissure

Meninges (dura and arachnoid) Brain surface (pia, heavier line) Sojourning and migrating central gray neurons? Settling reticular formation neurons? Sojourning and migrating oculomotor complex (III) neurons?

F u tur e

MESENCEPHALIC TEGMENTUM

Red nucleus? Substantia nigra?

p ari etal

Ventral tegmental area?

Nerve III (oculomotor)

b o n e

Midline raphe glial system

(provides structural support for brainstem flexures) Medial lemniscus?

Longitudinal bands of the pontine reticular formation

al nucleus and trac Spin t (V

ain Raphe dom

Raphe nuclear complex

ain Medial dom

ne l bo ora emp ous t

Intermedia

sq uam

te domain

PONS domain

Future Cochlear nuclei?

Principal sensory nucleus?

Lateral

Lateral lemniscus?

Trigeminal nuclear complex

Pontine NEP

)?

Lateral lemniscus?

Nuclei of the lateral lemniscus?

Facial motor nucleus (VII) Nerve VII (facial)

Nerve VII (facial, boundary cap) Superior olivary complex? Medial lemniscus and trapezoid body? Medial longitudinal fasciculus?

Future petrous temporal bone

Cochlear nuclei?

Midline raphe glial system

Facial ganglion (VII)? Temporal bone labyrinth

Basal occipital?

Meckel's cartilage (future middle ear components)

Epiglottis? Oropharynx

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Tongue

Temporal bone styloid process?

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Fut

ure hyoid bone?

Meckel's cartilage (future temporal/ mandibular joint?)

486

PLATE 199A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 14: Section 125

487 FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

NEP - Neuroepithelium

PLATE 199B Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

MESENCEPHALIC TECTUM

(SUPERIOR COLLICULUS)

Sojourning and migrating superior colliculus neurons Skull and skin

Mesencephalic tectal (superior colliculus) NEP (thick)

Meninges (dura and arachnoid)

mesencephalic superventricle (future aqueduct)

Brain surface (pia, heavier line) Sojourning and migrating central gray neurons?

Rubral NEP (thin)?

Settling reticular formation neurons?

F u tur e

Mesencephalic tegmental NEP (thin)

Sojourning and migrating oculomotor complex (III) neurons?

MESENCEPHALIC TEGMENTUM

Red nucleus? Substantia nigra?

p ari etal

ISTHMUS rhombencephalic superventricle

Ventral tegmental area?

Midline raphe glial system (provides structural support for brainstem flexures)

b o n e

(future fourth ventricle, lateral recess)

Pontine NEP Medullary NEP

PONS

Future

Cerebellar NEP

rhombencephalic superventricle

Principal sensory nucleus?

Medial lemniscus?

(future fourth ventricle)

Sojourning and migrating deep neurons

Raphe nuclear complex

Reticular formation

CEREBELLUM (HEMISPHERE)

Premigratory facial motor neurons?

sq uam

ne l bo ora emp ous t Future petrous temporal bone

Sojourning and migrating Purkinje cells

Auditory NEP

Spinal nucleus and tract (V)?

Medial longitudinal fasciculus?

Facial motor nucleus (VII)?

Lateral lemniscus? Nerve VIII (vestibulocochlear)

MEDULLA Superior olivary complex? Medial lemniscus and trapezoid body?

Raphe nuclear complex

Cochlear nuclei Nuclei of the lateral lemniscus? Nerve VIII (vestibulocochlear, boundary cap)

Vestibular ganglion (VIII)

Midline raphe glial system

Basal occipital?

Temporal bone labyrinth Meckel's cartilage (future middle ear components)

Epiglottis Laryngopharynx Temporal bone styloid process?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

External auditory meatus

Larynx?

Future hyoid bone?

488

PLATE 200A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 15: Section 128

489 FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

PLATE 200B Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

MESENCEPHALIC TECTUM (SUPERIOR COLLICULUS)

NEP - Neuroepithelium

Sojourning and migrating superior colliculus neurons

Mesencephalic tectal (superior colliculus) NEP (thick)

Skull and skin Meninges (dura and arachnoid) Brain surface (pia, heavier line)

mesencephalic superventricle (future aqueduct)

F u tur e

Rubral NEP (thin)?

Sojourning and migrating central gray neurons?

Mesencephalic tegmental NEP (thin)

Settling reticular formation neurons?

par ieta l

MESENCEPHALIC TEGMENTUM

Red nucleus? Sojourning and migrating oculomotor complex (III) neurons?

Isthmal NEP

Settling oculomotor complex (III) neurons?

b o n e

ISTHMUS Midline raphe glial system (provides structural support for brainstem flexures) Medial lemniscus?

Cerebellar NEP

Future

sq uam

CEREBELLUM (HEMISPHERE)

ne l bo ora emp ous t

Auditory NEP

Reticular formation

Sojourning and migrating Purkinje cells

Dorsal rhombic lip Medullary NEP

Facial motor nucleus (VII)?

MEDULLA Reticular formation

Vestibular nuclear complex?

Medial longitudinal fasciculus?

Cochlear nuclei

Raphe nuclear complex

Temporal bone labyrinth

Midline raphe glial system

Basal occipital?

Epiglottis

Ventral rhombic lip

Nerve VIII (vestibulocochlear, boundary cap)

Superior olivary complex?

Future petrous temporal bone

Medullary velum lateral recess

Abducens nucleus (VI)?

Spinal nucleus and tract (V)?

Medial lemniscus and trapezoid body?

Spiral ganglion (VIII)? Temporal bone labyrinth

Meckel's cartilage (future middle ear components) Pinna

External auditory meatus Eustachian tube

Laryngopharynx

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Sojourning and migrating deep neurons

Medullary Pontine NEP (vestibular) NEP

Lateral lemniscus? Nerve VIII (vestibulocochlear)

(future fourth ventricle)

Raphe nuclear complex

PONS

rhombencephalic superventricle

Larynx?

490

PLATE 201A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 16: Section 139

491

PLATE 201B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: NEP - Neuroepithelium CTF - Cerebellar transitional field

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

MESENCEPHALIC TECTUM (SUPERIOR COLLICULUS)

Sojourning and migrating superior colliculus neurons

Mesencephalic tectal (superior colliculus) NEP (thick)

Skull and skin Meninges (dura and arachnoid)

F

mesencephalic superventricle

ut ur e

Brain surface (pia, heavier line)

(future aqueduct)

p a ri et a l

Sojourning and migrating central gray neurons?

Mesencephalic tegmental NEP (thin)

Settling reticular formation neurons?

bon e

MESENCEPHALIC TEGMENTUM

Sojourning and migrating oculomotor complex (III) neurons? Settling oculomotor complex (III) neurons?

Isthmal NEP

Medial longitudinal fasciculus?

ISTHMUS

Futu re sq uamou s

Sojourning and migrating deep neurons (CTF2+4)

Reticular formation

Sojourning and migrating Purkinje cells (CTF6)

Lateral lemniscus?

CTF1 (fibers) CTF2 (cells) CTF3 (cells and fibers) CTF4 (cells) CTF5 (cells and fibers) CTF6 (cells)

Raphe nuclear complex?

Pontine NEP

Cerebellar NEP

temporal bone

PONS

CEREBELLUM (HEMISPHERE)

isthmal canal

Dorsal rhombic lip

Cerebellar notch rhombencephalic superventricle Medullary (vestibular) Precerebellar NEP NEP

Medullary NEP

Vestibular nuclear complex?

Prepositus nucleus? Medial longitudinal fasciculus?

MEDULLA Reticular formation Spinal nucleus and tract (V)?

Future petrous temporal bone

Medial lemniscus

Pinna

Spiral ganglion (VIII)?

Raphe nuclear complex

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

lateral recess

Expanding fetal rhombencephalic choroid plexus

Ventral rhombic lip Inferior cerebellar peduncle?

Midline raphe glial system (provides structural support for brainstem flexures)

Basal occipital

Pharynx Glossopharyngeal ganglion (IX)?

Medullary velum

(future fourth ventricle)

Larynx?

Temporal bone labyrinth

492

PLATE 202A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 17: Section 147

493

PLATE 202B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

NEP - Neuroepithelium

Sojourning and migrating superior colliculus neurons

Mesencephalic tectal (superior colliculus) NEP

Skull and skin

F

Meninges (dura and arachnoid)

ut ur e pa ri et a l

MESENCEPHALIC TECTUM

mesencephalic superventricle

Brain surface (pia, heavier line)

(future aqueduct)

bon e

Mesencephalic tectal (inferior colliculus?) NEP

Sojourning and migrating deep neurons

Sojourning and migrating inferior colliculus neurons? Settling reticular formation neurons? Parabigeminal nucleus? Lateral lemniscus?

ISTHMUS

CEREBELLUM (HEMISPHERE)

Isthmal NEP Raphe nuclear complex

Sojourning and migrating Purkinje cells

Reticular formation

Cerebellar NEP

Locus coeruleus?

CTF 1 (fibers) CTF 2 (cells) CTF 3 (cells and fibers) CTF 4 (cells) CTF 5 (cells and fibers) CTF 6 (cells)

Future s

isthmal canal

Dorsal rhombic lip

Cerebellar notch

qua m

rhombencephalic superventricle

e bon oral emp ous t

Medullary (vestibular) NEP

(future fourth ventricle)

Medullary NEP

Precerebellar NEP

MEDULLA

Nerve IX (glossopharyngeal)?

Spinal nucleus and tract (V)?

Future petrous temporal bone

Medial lemniscus

Glossopharyngeal ganglion (IX)?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

lateral recess Prepositus nucleus?

Reticular formation

Nerve IX (boundary cap)?

Medial longitudinal fasciculus? Raphe nuclear complex Midline raphe glial system (provides structural support for brainstem flexures)

Basal occipital

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Medullary velum

Vestibular nuclear complex?

Expanding fetal rhombencephalic choroid plexus

Ventral rhombic lip Inferior cerebellar peduncle?

Temporal bone labyrinth

494

PLATE 203A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 18: Section 157

495

PLATE 203B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold SUPERIOR COLLICULUS

ABBREVIATIONS: NEP - Neuroepithelium CTF - Cerebellar transitional field Mesencephalic tectal (superior colliculus) NEP

Sojourning and migrating superior colliculus neurons Skull and skin

mesencephalic superventricle

F u tu re

MESENCEPHALIC TECTUM

Mesencephalic tectal (inferior colliculus) NEP

pa ri et a l b on e?

INFERIOR COLLICULUS

Meninges (dura and arachnoid)

(future aqueduct)

Brain surface (pia, heavier line) Sojourning and migrating trochlear nucleus (IV) neurons? Lateral lemniscus? M i g r a ti n g i s t h m

Isthmal NEP Sojourning and migrating deep neurons (CTF2+4)

isthmal canal

ISTHMUS

al

Sojourning and migrating Purkinje cells (CTF6)

CEREBELLUM (HEMISPHERE)

n

eu

ro n

s?

CTF1 (fibers) CTF2 (cells) CTF3 (cells and fibers) CTF4 (cells) CTF5 (cells and fibers) CTF6 (cells)

Cerebellar notch

P

er

b e llar

N

E

(future fourth ventricle)

squa

Precerebellar NEP

e? bon tal cipi s oc mo u

lateral recess

Medullary NEP Vestibular nuclear complex?

Prepositus nucleus? Medial longitudinal fasciculus?

Reticular formation

Inferior olive complex

Nerve IX (boundary cap)? Medial lemniscus

Solitary nucleus and tract

Atlas transverse process?

Basal occipital?

Axis transverse process?

Axis body?

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Expanding fetal rhombencephalic choroid plexus Inferior cerebellar peduncle?

Raphe nuclear complex Midline raphe glial system (provides structural support for brainstem flexures)

Glossopharyngeal ganglion (IX)?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Ventral rhombic lip

Spinal nucleus and tract (V)?

MEDULLA

Nerve IX (glossopharyngeal)?

Medullary velum

Ba sal occ ipi tal ?

C

Future

e

Dorsal rhombic lip

rhombencephalic superventricle

496

PLATE 204A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 19: Section 163

497

PLATE 204B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: NEP - Neuroepithelium CTF - Cerebellar transitional field

SUPERIOR COLLICULUS

Mesencephalic tectal (superior colliculus) NEP

Sequestered superior colliculus neurons in the neuroepithelium?

mesencephalic superventricle

Skull and skin

F u tu re

(future aqueduct)

Meninges (dura and arachnoid)

MESENCEPHALIC TECTUM Mesencephalic tectal

p a ri et a l bo ne ?

(inferior colliculus) NEP

Brain surface (pia, heavier line) Nerve IV (trochlear, decussation)

INFERIOR COLLICULUS

C

er

Future

bel

lar

N

E

s q ua

Medullary NEP

e? bon tal cipi s oc mou

MEDULLA Inferior cerebellar peduncle?

Raphe nuclear complex

Inferior olive complex

Medullary velum

Ventral rhombic lip

Prepositus nucleus? Medial longitudinal fasciculus?

Expanding fetal rhombencephalic choroid plexus

Solitary Reticular nucleus formation and tract

Medial lemniscus Midline raphe glial system (provides structural support for brainstem flexures)

Glossopharyngeal ganglion (IX)?

Atlas?

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Vestibular nuclear complex?

Posterior intramural migratory stream (inferior olive neurons)

Nerve IX (glossopharyngeal)?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Dorsal rhombic lip

(future fourth ventricle)

Precerebellar NEP lateral recess

Spinal nucleus (V)?

Lateral lemniscus?

CTF1 (fibers) CTF2 (cells) CTF3 (cells and fibers) CTF4 (cells) CTF5 (cells and fibers) CTF6 (cells)

rhombencephalic superventricle

P

Sojourning and migrating deep neurons (CTF2+4) Sojourning and migrating Purkinje cells (CTF6)

e

CEREBELLUM (HEMISPHERE)

ISTHMUS? Isthmal NEP? Cerebellar notch? isthmal canal?

Foramen magnum?

Basal occipital?

498

PLATE 205A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 20: Section 171

499

PLATE 205B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: NEP - Neuroepithelium CTF - Cerebellar transitional field

SUPERIOR COLLICULUS

Mesencephalic tectal (superior colliculus) NEP

MESENCEPHALIC TECTUM

Skull and skin

mesencephalic superventricle

Meninges (dura and arachnoid)

(future aqueduct)

INFERIOR COLLICULUS

Brain surface (pia, heavier line)

CEREBELLUM (HEMISPHERE)

rm

Sojourning and migrating deep neurons (CTF2+4) Sojourning and migrating Purkinje cells (CTF6)

ph

r l b erhombencephalic e r Ce superventricle la

one?

mis

NE

(he

ta l b

Dorsal rhombic lip

P

(ve

F

utu re p arie

CTF1 (fibers) CEREBELLUM CTF2 (cells) (VERMIS) CTF3 (cells and fibers) CTF4 (cells) CTF5 (cells and fibers) CTF6 (cells)

is)

Mesencephalic tectal (inferior colliculus) NEP

Sequestered superior colliculus neurons in the neuroepithelium?

e

r e)

e squ F utur

Precerebellar NEP lateral recess

a mo e? bon ital ccip us o

Spinal nucleus (V)? Inferior cerebellar peduncle?

(future fourth ventricle)

MEDULLA Raphe nuclear complex

Inferior olive complex

Medial lemniscus

Ventral rhombic lip

Prepositus nucleus? Solitary Medial nucleus longitudinal and tract fasciculus?

Vestibular nuclear complex?

Reticular formation

Posterior intramural migratory stream (inferior olive neurons) Midline raphe glial system (provides structural support for brainstem flexures)

Glossopharyngeal ganglion (IX)? Foramen magnum?

Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Expanding fetal rhombencephalic choroid plexus

Medullary NEP

Nerve IX (glossopharyngeal, traces)?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

Medullary velum

Basal occipital?

500

PLATE 206A GW7.5 Coronal/horizontal CR 23 mm, C966 Level 21: Section 179

501

PLATE 206B

FONT KEY: ventricular divisions - capitals Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold ABBREVIATIONS: NEP - Neuroepithelium CTF - Cerebellar transitional field

MESENCEPHALIC TECTUM

INFERIOR COLLICULUS

Skull and skin Meninges (dura and arachnoid)

Mesencephalic tectal (inferior colliculus) NEP l ta ie r a e p e? ur bon t Fu

Brain surface (pia, heavier line)

CEREBELLUM (HEMISPHERE)

Sojourning and migrating deep neurons (CTF2+4)

CTF1 (fibers) CTF2 (cells) CTF3 (cells and fibers) CTF4 (cells) CTF6 (cells)

CEREBELLUM

Sojourning and migrating Purkinje cells (CTF6)

( v er

mis)

(VERMIS)

e

re

lateral recess

Dorsal rhombic lip

lla rN EP

ph mis

(he

be ) C ere rhombencephalic superventricle

Precerebellar NEP

(future fourth ventricle)

Medullary NEP

F ut u

re sq

MEDULLA

ous ua m

Spinal nucleus (V)? Inferior cerebellar peduncle?

Raphe nuclear complex

e? on al b ipit occ

Inferior olive complex

Medullary velum

Expanding fetal rhombencephalic choroid plexus Ventral rhombic lip

Reticular formation

Medial longitudinal fasciculus?

Vestibular nuclear complex?

Solitary nucleus and tract

Posterior intramural migratory stream (inferior olive neurons)

Midline raphe glial system Medial lemniscus (provide structural support for brainstem flexures)

Basal occipital?

Vagal inferior ganglion (X)?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. Evaginations and invaginations of the neuroepithelium are mosaic compartments that give rise to different brain structures.

Vagal superior ganglion (X)?

Foramen magnum?

FUTURE PARIETAL LOBE

LI

M

C

E

C

T

U

M

C

The observer is looking straight down on the top of the brain. Note the small size of the telencephalon. In a mature brain, the only structure visible from the top is the telencephalon. At GW 7.5, the telencephalon does not yet cover the dorsal surface of the diencephalon. All of the mesencephalic tectum is visible. The cerebellum appears as a wide ledge forming a horseshoe-shaped understory beneath the tectum. The pons is only partly visible connecting to the anteroventral edge of the cerebellum. The medullary velum is all that is visible of the medulla.

E

L L U B E M r

ur

th

future ventromedial fourth ventricle v

fu

r tu

e

su per ve

1 mm Slightly thicker brain wall (lateral cerebral cortex)

eph

uct

future aqu ed

uc

t

l ric

alic

supervent

er

l ic

nc

ued

v

en

tr

ic

le

p

ha

q e a

ntr

su

ep

fo

e

t

hi

ventricle rd

diencephali cs upe le m e s rve ntric e nc

al

le

future

Thin brain wall (medial cerebral cortex) le

ter

ic

tu

ola

tr

fu

te

A substantial portion of the brain's volume is occupied by the ventricles. In a mature brain, the ventricles are small, central cavities. At GW 7.5, the diencephalic and mesencephalic superventricles are already narrowing to resemble their adult shapes, and the brain wall is thickest in that region. Most of the telencephalon is filled with the paired telencephalic superventricles, but note that the brain wall is thicker laterally than medially in accordance with the ventrolateral (earlier maturing) to dorsomedial (later maturing) developmental gradient. The dark areas within the brain wall are caused by looking through more than one thickness.

el

e at

l ra

future dor s

cle tri ven

n

B. TOP VIEW SHOWING THE SUPERVENTRICLES

B

E

P H A L O N

R

E

EP HAL O ON M E L A S E H N C E P PONS

D U L L

T

E

L

E

A. TOP VIEW OF THE BRAIN SURFACE

R M I S V E S

E 1 mm

C

NC

SUPERIOR CO L

PRE M U TECT

LU

T N

IE

US AM AL H T

E P ITHALAMUS

U

D

IN

E E

C RE TU U F

S YRU EG AT L GU

M I S P H E H

R

FUTURE FRONTAL LOBE

Medullary velum

FUTURE OCCIPITAL LOBE

N

FUTURE PARACENTRAL LOBULE

A

A

GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION

ic l e

rh Thick brain wall (midbrain and pons)

ombencepha

li

c

Very thin wall of the medullary velum

502

FIGURE 10

GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION

f

u ut

l re

e at

l ra

posterodorsal pool

le ric nt ve

(lateral) pontomedullary trench

hippocampal pool

inferior

o

m

o

evagination in midline of posterior superior colliculus

super ventri cl

e (future

a

d que

uc

t)

th

halic

ve

icl

e)

c

su

pe

ut

li

Indent artifact of 3-D reconstruction rv

en tri cle

(f

a

le

h

ic

p

ur

e

fo

n cep

r nt

o

mo n r o

o

ur

me s e

p

p o

e third ventricle)

of

l poo

a r y l l

p

t al

c o l l i c u l u s

u

pool

ec r et

o r p e r i s u

d

e

p

e

c

r

dial)

t

n

colliculus pool

(me

am en

e

la

l

e p i t h a l a m ic

o l p o

dienceph alic s uper ventr fo icle (futur r

l

el

l

m i c t h a l a

cingulate pool

e

eb

o

anterodorsal pool

cer

l

FIGURE 11

rho

mbe

nce p h a l i c s u p

er

n ve

tr

1 mm

TOP VIEW OF THE EXPOSED SUPERVENTRICLES Enlarged view of Figure 10B showing only the ventricles. Because the ventricles contain fluid, subdivisions are called "pools." The various pools are named according to adjacent structures, which often produce evaginations into the ventricle (such as the cingulate and hippocampal pools). The complex shape of the brain ventricles is primarily a result of (1) localized differential proliferation in the adjacent neuroepithelium and (2) flexures in the diencephalon, midbrain, pons, and medulla during development.

Indent artifacts of 3-D reconstruction

503

FUTURE TEMPORAL LOBE

FUTURE INSULAR AREA AND PRIMARY OLFACTORY CORTEX

MISPH HE ER

FUTURE PREFRONTAL AREA

Artifact of 3-D reconstruction

E

LOWER MEDULLA

INFUNDIBULUM

BASAL TELENCEPHALON PREOPTIC AREA SEPTUM

UPPER MEDULLA

PONS

FUTURE ORBITOFRONTAL AREA

HYPOTHALAMUS

A

GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION

SPINAL CORD

OPTIC RECESS

T

E

L

E

N

1 mm

OLFACTORY BULB

C E P H A L O N

DIENCEPHALON

Artifact of 3-D reconstruction

C E R EBELLU

M

mesencephalic superventricle (future aqueduct)

re lateral rec futu ess

of th fourth ventr e icl e

Thin brain wall (medial cerebral cortex)

f

u ut

re

la

te

future posteroventral fourth ventricle

cle tri ven l ra

future anteroventral fourth ventricle

le

te

The brain wall is thickest in the pons from this viewpoint because the pontine parenchyma is in front of the anterior edge of the rhombencephalic superventricle. In the telencephalon, the lateral brain wall is thicker than the medial wall in accordance with the ventrolateral (earlier maturing) to dorsomedial (later maturing) developmental gradient. As in Figure 10B, the dark areas within the brain wall are caused by looking through more than one thickness.

The observer is below, looking straight up at the bottom of the brain and spinal cord. Note the olfactory bulb is located behind the cortex and evaginates from the basal telencephalic area (just above the developing olfactory epithelium in the skull, see Plates 188 and 189). The enormous growth of the prefrontal area of the cortex eventually displaces the bulb to lie in a more anterior position. This ventral view shows little of the ventral mesencephalon, because the tegmentum is folded above the ventral diencephalon. The cerebellum still appears as a wide ledge on the lateral edge of the pons that arches over the upper and lower medulla. The spinal cord is coming straight down from the lower medulla.

(future third ventricle)

B B. BOTTOM VIEW SHOWING THE SUPERVENTRICLES

diencephalic superventricle

A. BOTTOM VIEW OF THE BRAIN SURFACE

nc

r h om b en c ep h alic su p er ven t r ic le ep

ha

l ic

su per ve

1 mm Slightly thicker brain wall (ventrolateral cerebral cortex)

ntr

ic l e

Thick brain wall (pons)

central canal (spinal cord)

504

FIGURE 12

FIGURE 13

GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION m e d

cerebellar pool

u

dorsal rhombic lip

t

e

n

c

e

p

h

a

li

c

su

infundibular recess preoptic/hypothalamic midbrain pool tegmental he pool t l f e o ra nc lates e e lu d nf an icl co ird ntr th ve c/ li ha p e ic nc n le lio l te ng oo diencephalic l a p sa g superventricle ba (future third ventricle)

pe

rv

en tri cle

mesencephalic superventricle (future aqueduct)

pontine pool

Complex folding of the ventricular surface overlying the precerebellar neuroepithelium

upper medullary pool

lower medullary pool

l

cingulate pool

l

pontomedullary trench

pt n a al/ rr st owria s ta l olfactory recess

anteroventral pool

e

ganglionic evagination (dorsal) optic recess

o

se

posteroventral pool

p o

re tu fu

e icl tr en v al ter la

a r y l l

ventral rhombic lip

ventricular evagination in the midline pons and medulla

rhombencephalic superventricle (future fourth ventricle)

central canal (spinal cord)

Artifact of 3-D reconstruction

1 mm

BOTTOM VIEW OF THE EXPOSED SUPERVENTRICLES Enlarged view of Figure 12B showing only the ventricles. The complex evaginations of the ventricular surface indicate the heterogeneous nature of the neuroepithelium that lines different ventricular divisions.

505

506

FIGURE 14

GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION

O N A L

I Y H

TH PO

vent

ricl

e)

Pontine flexure

(futu re third

e

mammillary recess

en di

H

P

SU

IN F

CU

LU

S

S

mes en ce ph a (fu tu lic r

ERIO

R CO

LL

I

U

Medullary velum Artifact of 3-D reconstruction

PER M

EDUL L A

LOWER MEDULLA

Medullary flexure

aq u

SPINAL CORD

isthmal canal

ce ph al ic

olfactory recess

UP

cle tri en rv pe ct) su edu

su pe rv ent ric le

(future lateral ventricle)

r h om b en c ep h alic su p er ven t r ic le

infundibular recess

Thicker brain wall (pons)

Thickest brain wall (lower medulla)

central canal (spinal cord)

l re ra tu n t le f u o v e t r ic r en ste v po rth u fo

future lateral recess fourth ventricle

1 mm

Mammillary body

Mesencephalic flexure

S

telencephalic superventricle

C

M R M IS L U VE E LR E B E E H R S P C E H E M I

AM AL

N

B

E

E

C

SU

E

Diencephalic flexure

O

Infundibulum

optic recess

N

UM

O P LL MES ENC C T EP HA TEGM EN L T

P

L SA EN ON BA EL AL T PH CE

IC PT A EO E P R AR D

Thin brain wall (telencephalon, cerebral cortex)

Thicker brain wall (basal telencephalon)

MU

LA

BT

HA

OLFACTORY BULB

T

M

FUTURE TEMPORAL LOBE

ECT

ON

FUTURE ORBITOFRONTAL AREA

ET

R S IO LU ER CU I

TELENCEPHALON

PR

U

FUTURE FRONTAL LOBE

S

FUTURE PARACENTRAL LOBULE

UM

The observer is beside the model, looking at the lateral surface of the brain and upper cervical spinal cord. Note the posterior-facing olfactory bulb beneath the basal telencephaon. This lateral view shows most clearly all of the flexures in the brainstem.

EPITHAL AM U

S

A. SIDE VIEW OF THE BRAIN SURFACE

FUTURE OCCIPITAL LOBE

FUTURE PARIETAL LOBE

LAMUS THA

A

B. SIDE VIEW SHOWING THE SUPERVENTRICLES The varying thicknesses of the brain wall mirror a maturation gradient: the medulla has the thickest wall and is most mature, while the thin wall of the cerebral cortex is one of the least mature brain areas. As in Figures 10B and 12B, the dark areas within the brain wall are caused by looking through more than one thickness.

507

ol

po

(futu

en

isthmal canal

rv m a

a h

y

p

o

t

h

a

l

ph

ce

en infundibular recess

di

optic recess

i

c

li

basal telencephalic pool preoptic pool

c

s

p

u

o

o

pe

cle

mammillary recess

p o o l

tri

an te ro m e ol at er

l

t)

ant er

a

c

en

ol

v

e

q

u

l te

t

a

e

s r

ganglionic evaginations

t

ic

re

tegmenta l p rain o idb

n

d

m

tu

i

c

(fu

al

a

e

pha

ph

r

e

e nc

nce

b

u

ior t er

olfactory recesses

al

s po

anterolateral pool

ventrolateral pool

mese

d

p

al di

i

u

lic superv

en

lateral pool

ic

(f

le ic

tr

dorsal pool

m

lam

posterodorsal pool

epitha

te

le)

l

la

ric

tric e l

e

nt

p o o l i c a m a l h t re third ventricle)

u

r

e l v ra

FIGURE 15

u

t

GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION

pontomedullary trench

o po e n ti on here p p is m he

l

r ve

Artifact cere

la bel

o r p

Complex folds caused by undulations in the precerebellar neuroepithelium

Artifact of 3-D reconstruction

lower medullary pool

SIDE VIEW OF THE EXPOSED SUPERVENTRICLES Enlarged view of Figure 14B showing only the ventricular surface. The complex evaginations of lateral parts of the ventricular divisions indicate the heterogeneous nature of the neuroepithelium that lines different ventricular divisions.

is

ol

rhombenc e superven pha tr i c ll i c future lateral recess e of fourth ventricle

upper medullary pool

m

central canal (spinal cord) 1 mm

GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION OF THE LATERAL TELENCEPHALIC NEUROEPITHELIUM

Orbitofrontal NEP

B

Occipital NEP

Temporal NEP

Ant ero m e

g

Cor tico

Ganglionic N EP a nd S

VZ and S P NE c i terior n Pos

VZ

Amygdaloid NEP and SVZ al di

Occipital NEP

l NEP

Ventral cut edge of NEP

Orbitofrontal NEP

Olfactory NEP

Basal telencephalic NEP 1 mm

Ventral cut edge of NEP A. is an inside "camera" view of the lateral half of the telencephalic neuroepithelium and subventricular zone; the medial half is not reconstructed so that the ganglionic and olfactory evaginations are visible. The reconstruction includes sections 22 (between Levels 1 and 2, Plates 187 and 188) through 76 (Level 7, Plate 192). The camera is looking straight (0˚ pitch) at the reconstruction with a +60˚rotation (heading). The large ganglionic evagination is evident in the ventrolateral NEP and SVZ.

n

Bas al

c

P NE

ni

C er

(section 76)

Olfactory NEP

ti c a l c or

e) l NE P ebra hymal fac c ca n e i r (p a ParaTemporal cort f central o S d V n Z NEP e ic NEP a NEP g n d ) t e n g l i o lar face Posterior c l u a s u r c a Do tri

Posterior cut edge of cortical NEP

(

Parietal NEP

te le

Ant ero

P

Ganglio

l cortical NEP a r b re cular face) e C ventri

ge cut ed r o i r Ante

of cortical NEP (section 22)

Paracentral NEP

t edge of co l cu rti a s ca r lN Do E

g C o r t i c o angl i o Anterolateral

A

Anterola (ve ter al

Parietal NEP

nc ep

1 mm

and SVZ

ial ed m

ha

li c N E P

Amygdaloid NEP and SVZ Posterior edge of ganglionic NEP and SVZ fuses with the preoptic NEP.

Ventral cut edge of NEP B. is another inside "camera" view of the same reconstruction in A. The camera is looking down (-70˚ pitch) at the reconstruction with a +90˚rotation (heading). From that angle, the superficial face of the dorsal cortical NEP is visible, and the large ganglionic evagination rises up into the future lateral ventricle. The posterior edge of the ganglionic NEP and SVZ fuses with the preoptic NEP posterior to the foramen of Monro. See that transition between Level 5 (Plate 190) and Level 6 (Plate 191).

ABBREVIATIONS: NEP - Neuroepithelium SVZ - Subventricular zone

Neuroepithelial compartments labeled in Helvetica Bold.

508

FIGURE 16

th

al

P NE

omplex NEP rc o i r NE

Po st e

Dorsal complex NEP

B

to mesencephalic superventricle

P

P

tr a l/ c p en l a rot tra ub r lc al N eran om E ce am P pl ex ic

Thalamic NEP

V

ar

Anterior complex NEP

S ub

to telencephalic superventricle

m

NEP profile in section 62

Mammillary NEP

th

Hypothalamic NEP

tic P r e op P NE

1m

EP rN

optic recess

le NEP Midd

l R e ti c u u ic Ret

Po st er io

en

N EP profile in section 44

i Ep

ic am

ctal NEP Prete

Pineal evagination

NEP cut in dorsal midline

NE

A

pineal recess

or NEP eri t An

NEP cut in ventral midline preoptic recess

mammillary recess

diencephalic superventricle (future third ventricle)

FIGURE 17

Pretectal/tectal NEP (profile in section 102) Epithalamic NEP

Thalamic NEP

Posterior complex NEP

Tegmental NEP (profile in section 102) Anterior complex NEP

Mammillary NEP (profile in section 112) Optic recess NEP

NEP cut in ventral midline infundibular recess

Infundibulum

Middle NEP 1 mm

Hypothalamic NEP

GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION OF THE DIENCEPHALIC NEUROEPITHELIUM

Two inside "camera" views of the right half of the diencephalic neuroepithelium that includes section 44 (near Level 3, Plate 188) through section 112 (Level 12, Plate 197); the NEP in all sections has been cut where it bridges the midline dorsally and ventrally so that its folds and undulations can be observed. A. The camera views the front of the reconstruction with +45˚heading and -25˚ pitch. From this angle, we see the ventricular face of the NEP. B. The camera views the back of the reconstruction with 180˚ heading and -10˚ pitch. From this angle, we see some of the parenchymal face of the NEP. Note the prominent folding in the anterior complex NEP, the thick posterior complex NEP, and the back wall of the NEP lining the optic recess. It is postulated that the multiple evaginations and invaginations of the diencephalic neuroepithelium are mosaic compartments that give rise to different thalamic, hypothalamic, and preoptic nuclei.

ABBREVIATION: NEP - Neuroepithelium

Neuroepithelial compartments labeled in Helvetica Bold. ventricular divisions labeled in capitals.

509

B ROOF ALONE (

re

be

lla

be

The reconstruction includes section 128 (Level 15, Plate 200) through section 193 (posterior to Level 21, Plate 179); the NEP in all sections has been cut where it bridges the midline dorsally and ventrally, and only the right half is shown. The camera is looking at the front of the NEP (0˚ heading, -10˚ pitch).

re

ar n

bell

Cere

Parenchymal face of NEP on

P

B. shows the parenchymal face of the roof NEP bordering the differentiating zones of the pons, isthmus, and cerebellum. Since the edges between CTF6 (Purkinje cell sojourn zone) and the cerebellar NEP are virtually indistinguishable, both are included in the reconstruction.

Ist

re)

hm

Ce

Ce

(hemisphe

A. shows both the roof and floor plates of the rhombencephalic NEP with orientation labels.

tine N E P Tangential cut of pontine NEP exaggerates thickness

Cerebellar NEP

C. shows the ventricular face of the floor NEP overlying the upper (adjacent to pons) and lower medulla (adjacent to spinal cord).

CTF 6 (dense Purkinje cell sojourn zone)

1 mm

C FLOOR ALONE e llar N EP

POSTERODORSAL

ic lip (cut edge)

MIDLINE

LATERAL

TOGETHER

NEP profile in section 128

1 mm

ABBREVIATIONS: CTF - Cerebellar transitional field NEP - Neuroepithelium

Neuroepithelial compartments labeled in Helvetica Bold. Transient developmental structures labeled in Times Bold Italic

rh al r t Ven

Midline medullary NEP evagination

Lower medu llary NE P

Ventricular face of NEP

Upp

mb

ANTEROVENTRAL

Prec ere b

A ROOF AND FLOOR

s)

t ch

EP

mi

rn o

ar

N

ll

Dorsal rhombic lip (cut edge)

r ve

al N EP

FIGURE 18 GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION OF THE RHOMBENCEPHALIC NEUROEPITHELIUM

o t ch

510

er medull

ar y N E P

o

Vestibular NEP Auditory NEP

1 mm

Medial medullary NEP

511

FIGURE 19 GW7.5, CR23 mm, C966, COMPUTER-AIDED 3-D RECONSTRUCTION OF THE RHOMBENCEPHALIC NEUROEPITHELIUM

B ROOF ALONE

Cerebellar NEP (vermis)

ce

)

The camera is viewing the same reconstruction in Figure 18 with a 45˚ heading and a -10˚ pitch.

en

cu

l

fa

A ROOF AND

FLOOR TOGETHER

L A R LA TE

rn

Isth

lla be

re Ce

PO S T DOR EROSA L

rhombencephalic superventricle

E N LI ID M L EN V

nti

Po

r P Ventral rhombic lip (cut edge) NE terio r EP a s y N ell po r b ta re li ce o e s Pr r Lower r/ o a i l r medullary NEP u te P ib t an s E

Pontine NEP

Ve

N

a v

d

e

r a

a

on ti

g

E

N

l

u

a

l

y

in

Ventricular face of NEP

r

r

y

Upper medullary NEP

ll a

l

i

a

t

N

m

b

s V e

E

u

e

P

l

C FLOOR ALONE

A

ne

ERO VEN TRA L 1 mm

P

Dorsal rhombic lip (cut edge)

ANT

TR

NE

ch ot rn

la el eb er

C

1 mm

Ventral rhombic lip (cut edge)

DORS AL M ID L

P

NE

h

E

P

ar

Ce reb ell CTF6 + Cerebellar NEP

tc

mal

) o

re

NE P

is em h (

e ph

N

I

(v

Parenchymal face of NEP

i tr

ar

M

u d

d

e

e

m

Auditory NEP

i

e

1 mm M

id

n li

ABBREVIATIONS: CTF - Cerebellar transitional field NEP - Neuroepithelium

ventricular divisions labeled in capitals Neuroepithelial compartments labeled in Helvetica Bold. Transient developmental structures labeled in Times Bold Italic

512

PART PARTXI: XI: GW7.5 GW7.5 SAGITTAL SAGITTAL

This specimen number 6202 in the Carnegie Collection, designated here as C6202, is a fetus of unknown sex with a crown-rump length (CR) of 21 mm estimated to be at gestational week (GW) 7.5. The entire fetus was cut in the sagittal plane in 20 µm sections and stained with hematoxylin and eosin. Information on the date of specimen collection, fixative, and embedding medium was not available to us. Since there is no photograph of this specimen before histological processing, a specimen from Hochstetter (1919) that is comparable in age to C6202 is used to show external brain features at GW7.5 (A, Figure 20). Like all other sagittal specimens in this Volume, C6202’s sections are not cut parallel to the midline; Figure 20 shows the approximate rotations in horizontal (B) and vertical (C) dimensions. Photographs of 7 sections (Levels 1-7) are illustrated at low magnification in four parts (Plates 207A-D through 213A-D). The A/B parts show the brain in place in the skull; the C/D parts show only the brain (and some peripheral ganglia) at slightly higher magnification. Plates 214-221 show high-magnification views of various parts of the brain at different levels from the cerebral cortex (Plate 214) to the midline raphe glial structure in the midbrain and cervical spinal cord (Plate 221). Most of the high-magnification plates are rotated 90˚ (landscape orientation) to more efficiently use page space. C6202 is less mature than C966 even though it is only 2 mm shorter in CR length. The superventricles are large in the centers of all brain structures, especially in the telencephalon and rhombencephon, but the telencephalon is smaller than it is in C966. Sections near the midline show the enormous size of the diencephalic and mesencephalic superventricles. The respective thicknesses of the neuroepithelium (NEP) and parenchyma are keys to determining the degree of maturation of various brain structures.

The parenchyma is thick and bordered by a thin NEP in the medial medulla, indicating that many neurons have been generated here, but the production of late-generated neurons continues. The parenchyma is thinner and the NEP is thicker in the lateral medulla, entire pons, and entire midbrain tegmentum. There are layers of dense cells adjacent to the NEP where neurons are sojourning and the rest of the pontine and mesencephalic tegmental parenchyma is filled with migrating and settling neurons. The precerebellar neuroepithelium in the lateral medulla is thick and many neurons are entering the posterior intramural migratory stream, but few have accumulated in the indistinct inferior olive in the medial medulla. The cerebellar parenchyma has only four layers in the cerebellar transitional field (CTF). The cells in CTF2, 3, and 4 are probably deep neurons that will eventually settle in the dentate, interpositus, and fastigial nuclei. CTF5 and 6 are present in C966 and presumably contain Purkinje cells, but these layers are absent in C6202. The cerebellar NEP is thicker than it is in C966 and is now producing the oldest Purkinje cells. The mesencephalic tectal NEP is very thick and lies adjacent to a thin parenchyma. The majority of neurons in both the superior and inferior colliculi have not yet been generated. The diencephalic NEP is thick and the adjacent parenchyma is filled with dense zones of sojourning and migrating neurons. The basal telencephalic NEP and the basal ganglionic NEP are thick, and the oldest neurons are settling in the adjacent parenchyma. Many neurons in the basal telencephalon have yet to be generated. In the cerebral cortex, the NEP is bordered by a thin primordial plexiform layer that contains the oldest cortical neurons (CajalRetzius cells) and subplate neurons. The cortical NEP is expanding and increasing its number of neural stem cells as the telencephalic superventricle grows; nearly all cortical neurons in layers II-VI have still to be generated.

513

GW7.5 SAGITTAL

TU M EC ET PR

O

L

H

N

H

M

A

GMENT TE

S L U

INFERIOR COLLICULUS

M A

C

LUM EBEL R E

ed

O

ge

T

P

H

A

L

Sections of C6202's C N brain rotate 10.5˚ lum ve E y counterclockwise from Future olfactory bulb medu llar D I O of the horizontal midline P running through the Y H rhombencephalic cerebral cortex and Optic nerve (II) superventricle midbrain tectum (top view). C6202's sections are quite Pituitary gland Medullary velum close to the vertical midline, Trigeminal nerve (V) rotating only 2.8˚ counterclockwise (back Facial nerve (VII) view). In the sections illustrated on the following pages, the telencephalon and M E D U Vestibulocochlear nerve (VIII) diencephalon (top) are tilted away from the L Glossopharyngeal nerve (IX) observer, while the medulla and upper spinal cord (bottom) are tilted toward the Vagus nerve (X) observer. ge ed

ed

t Cu

m

ul

la

m

f

S

o

Cu t

N

velu ry

-2.8˚

TOP VIEW Right side Level 1 (cere

bral co rtex

and mid brain te ctum) -10.5˚

Left side

Left side

Right side

Level 1 (brainstem)

B

S P C IN O R AL D

L A

C BACK VIEW

RHOMBENCEPHALON

N L LO SA BA PHA E NC PREOPTIC LE AREA TE

U

E

S

P

A

U

R

C

P

LO

C E R E B

L

T

ISTHMUS

SUBTHALAMUS

O

I

SENCE ME UM

R E

TE L

EN

N LO A PH E C

C

C

A

L

E

T

U

I S P E M H H

S U P E R I O R

L

A

N

EPITHALAMUS

E

A perfect sagittal cut through the brain bisects the cerebral cortex into two separate hemispheres by passing through the interhemispheric fissure, and does the same in the brainstem by passing through the midline of the ventricles.

Future pineal gland

Figure 20. A, The lateral view of the brain and upper cervical spinal cord from a specimen with a crown-rump length of 19.4 mm (modified from Figure 35, Table VI, Hochstetter, 1919) identifies external features of a brain similar to C6202 (CR 21 mm). B, Top view of the brain in A (modified from Figure 37, Table VI, Hochstetter, 1919) shows how C6202’s sections rotate from a line parallel to the horizontal midline in the interhemispheric fissure and midbrain tectum. C, Back view of the brain with a crown-rump length of 38 mm (modified from Figure 44, Table VIII, Hochstetter, 1919) shows how C6202’s sections rotate from a line parallel to the vertical midline in the brainstem and upper cervical spinal cord.

514

PLATE 207A

GW7.5 Sagittal CR 21 mm, C6202 Level 1: Slide 30, Section 2 SKULL, MAJOR BRAIN STRUCTURES, AND VENTRICULAR DIVISIONS

Neuroepithelial and parenchymal structures are labeled in Parts C and D of this plate on the following pages.

515

PLATE 207B F utu

re p a

icle E ntr e rv icle) pe entr

H IP PO C A M PU S

al

THALAMUS

"Budding" telencephalic choroid plexus*

fo of ram mo en nr o

Diencephalic choroid plexus

DIENCEPHALON

TH HYP AL OAM US Sphenoid

Anterior part Pituitary Intraglandular cleft gland Intermediate part Posterior part Tongue Sella Oral cavity turcica

p ha

Atlas

so

r

x

gus

La

yn

RHOMBENCEPHALON

o cc

Glottis

E

Axis

ra

Ve c

me

Medullary velum

UPPER MEDULLA

n

ma

gn

Incipient rhombencephalic choroid plexus*

um

LOWER MEDULLA it a

lb

on

e

C3

Fo

CEREBELLUM

(future fourth ventricle)

r ol te b r um al n

p ar

Pharynx

l bu

Epiglottis

rhombencephalic superventricle

ry rte r a ipital

di

Basal

an s

Meckel's cartilage

Basila

M

Tongue

ISTHMUS

PONS

Oral cavity

es

isthmal canal

R O US RI UL FE IC IN LL CO

Maxilla

US LAM HA T PO HY

infundibular recess

SUPERIOR COLLICULUS

diencephalic superventricle

TECTUM

(future a qued uct )

Nasal cavity

N

TEGMENTUM

SEPTUM

Nostril

nc ep h

M E S E

(future third ventricle, hypothalamic part) PREOPTIC AREA mammillary Olfactory optic recess recess epithelium

Nasal concha

ro c

PR ET EC TU me M se

L O N H A

Frontonasal process

Brain surface (pia, heavier line)

P

BASAL TELENCEPHALON

Meninges (dura and arachnoid) US

diencephalic superventricle (future third ventricle, thalamic part)

TELENCEPHALON

Skull and skin

TH EP A L IAM

e ntricl rve pe su

frontal bone Future CEREBR AL

v

o ne

E

Nerve I (olfactory)

al b

C

OLFACTORY BULB

riet

ic al

CO telenceph R ali T (futu cs re la u te r

X

cc

ip

SPINAL CORD

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

e sq F ut u r

ua

m

s ou

o

*At GW7.5, the telencephalic choroid plexus is already "budding", while the rhombencephalic choroid plexus is still incipient. Compare with the GW9 specimen shown in Plates 58A and B on pages 137-138.

516

PLATE 207C

Midline Right side

Left side

GW7.5 Sagittal CR 21 mm, C6202 Level 1: Slide 30, Section 2 NEUROEPITHELIAL AND PARENCHYMAL BRAIN STRUCTURES

BRAINSTEM FLEXURES

4

3

Right side Midline Left side

2

1

1. Medullary 2. Pontine 3. Mesencephalic 4. Diencephalic

The skull, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

See these plates for details of brain structures in nearby sections: Cerebral cortex (214A and B) Olfactory bulb (215A and B) Cerebellum (219A and B) Midline glial fibers (221A and B)

517 Cortical (parietal) NEP Primordial plexiform layer

Sojourning and migrating thalamic neurons

Cortical (hippocampal) NEP

Posterior commissure

Cortical (paracentral) NEP GEP (fornix)

Pretectal NEP?

Ventral tegmental area?

a

cN

EP

ex

Posterior (mammillary)

Middle

Anterior

Future optic tract? he

gl

ia

tem s ys

(s t r uctu

r ral sup p o r t f o

Migrating isthmal neurons Trochlear nucleus (IV)? Nerve IV decussation (trochlear)

Mesencephalic (tectal, inferior colliculus) NEP

a

i ne

Mi d l

Pituitary gland Raphe GEP (midline raphe glia structure)

es)

b

Medial longitudinal fasciculus?

ra

p

Sojourning and migrating hypothalamic neurons

ur

l N EP

Hy

th po

i la m

Mesencephalic (tectal, superior colliculus) NEP

Sojourning and migrating tegmental neurons

r a in

Pr

eo

pt

ic N

EP

Migrating and settling basal telencephalic neurons Sojourning and migrating septal neurons Sojourning and migrating preoptic neurons

Mesencephalic (tegmental) NEP

fl

Basal telencephalic NEP

Septal NEP

Anterior thalamic NEP

s t em

Cortical (olfactory) NEP

GEP (posterior commissure)

Epithalamic NEP

Thalamic (posterior complex) NEP?

Thalamic (dorsal complex) NEP?

Cortical (frontal) NEP

Nerve I (olfactory)

PLATE 207D

Cortical (occipital) NEP?

Pontine NEP Pontomedullary trench

Upper medullary NEP

m Isth CTF1 (fibers)

CTF 2 (cells) CTF 3 (cells and fibers) CTF 4 (cells)

Cerebellar NEP

Medial lemniscus? (intermingled with midline glial raphe system) Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

R e t

a r f o r m u l a t io ic r olive rio

In

Ventral funiculus Ventral gray matter Intermediate gray matter Dorsal gray matter (substantia gelatinosa) Dorsal funiculus

n

FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

fe

ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium CTF - Cerebellar transitional field

Lower medullary NEP

Ventral rhombic lip

Vestibular nuclear complex? Solitary nucleus and tract Cuneate fasciculus Cuneate nucleus

Sojourning and migrating deep neurons Dorsal rhombic lip

518

PLATE 208A

GW7.5 Sagittal CR 21 mm, C6202 Level 2: Slide 26, Section 2 SKULL, MAJOR BRAIN STRUCTURES, AND VENTRICULAR DIVISIONS

Neuroepithelial and parenchymal structures are labeled in Parts C and D of this plate on the following pages.

519

PLATE 208B Future telencephalic superventricle

(future lateral ventricle)

ne

Skull and skin

EPIT HA LA M U

Meninges (dura and arachnoid) Brain surface (pia, heavier line)

S

diencephalic superventricle (future third ventricle, thalamic part)

PR

Diencephalic choroid plexus

DIENCEPHALON

op

Sphenoid Maxilla

Pituitary gland Oral cavity

ti

H

c

c re

Y

es

s

O

P

T

Anterior part Intraglandular cleft Intermediate part

Tongue

H

P

Sella turcica

A

L

O

A

M

N

ISTHMUS

S

M an

rhombencephalic superventricle (future fourth ventricle)

s es oc pr

UPPER MEDULLA

Basal

lar bu di

Oral cavity

Tongue

RHOMBENCEPHALON Medullary velum

o cc

Rhombencephalic choroid plexus

La

ipital

Epiglottis

ry nx

Pharynx Atlas

LOWER MEDULLA

r ol te b r um al n

Axis

Ve c

cc

ip

it a

lb

on

e

Dorsal root ganglion

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

CEREBELLUM

e sq F ut u r

ua

u mo

so

ERIOR COLLICULUS

PREOPTIC AREA

S

U

TECTUM

SUP

(future third ventricle, hypothalamic part)

SEPTUM

Olfactory epithelium Nasal septum

TEGMENTUM

diencephalic superventricle

M

erventricle sup ct) ic quedu al re a

Nerve I (olfactory)

foramen of monro

TU

me se nc e

C

BASAL TELENCEPHALON

E S E

M

EC

u ph (fut O N FERIOURLUS L IN LIC H A L CO E P

TELENCEPHALON

ET

N

re frontal bone Futu

al b o

THALAMUS

CEREBRAL CORTEX Telencephalic choroid plexus

Frontonasal process

p a riet

520

PLATE 208C

Midline Right Left side side

GW7.5 Sagittal CR 21 mm, C6202 Level 2: Slide 26, Section 2 NEUROEPITHELIAL AND PARENCHYMAL BRAIN STRUCTURES

Right side Midline Left side BRAINSTEM FLEXURES

4 3 2

2. Pontine 3. Mesencephalic 4. Diencephalic

The skull, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

See Plates 210A and B for details of the anterior and middle hypothalamus, Plates 218A and B for details of the midbrain tegmentum in nearby sections.

521

PLATE 208D Stem cells of diencephalic choroid plexus

Primordial plexiform layer

Epithalamic NEP

Posterior commissure GEP (posterior commissure)

Pretectal NEP Mesencephalic (tegmental) NEP

Basal telencephalic NEP

Sojourning and migrating tegmental neurons

Septal NEP

Hy

po

th a

i la m

cN

EP

Mesencephalic (tectal, superior colliculus) NEP

Middle Midline raphe glial system (provides structural support for brainstem flexures)

Pr

Sojourning and migrating septal neurons

Interpeduncular nucleus?

Posterior (mammillary)

eo

p ti cN

EP

Migrating and settling basal telencephalic neurons

Ventral tegmental area/ substantia nigra?

Anterior

Sojourning and migrating preoptic neurons

Migrating isthmal neurons Mesencephalic (tectal, inferior colliculus) NEP

Future optic tract? Sojourning and migrating hypothalamic neurons

Pituitary gland

Raphe nuclear complex?

Reticular formation

Pontine NEP Pontomedullary trench

Reticular formation Upper medullary NEP

Solitary nucleus Solitary tract

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium CTF - Cerebellar transitional field FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Cerebellar notch CTF1 (fibers)

Sojourning and migrating deep neurons

CTF 2 (cells) Dorsal rhombic lip

CTF 3 (cells and fibers) CTF 4 (cells)

Cerebellar NEP

Lower medullary NEP

Spinal nucleus (V)? Ventral rhombic lip

Vestibular nuclear complex?

Inferior cerebellar peduncle?

522

PLATE 209A

GW7.5 Sagittal CR 21 mm, C6202 Level 3: Slide 24, Section 2 Left side of brain SKULL, MAJOR BRAIN STRUCTURES, AND VENTRICULAR DIVISIONS

Neuroepithelial and parenchymal structures are labeled in Parts C and D of this plate on the following pages.

523

PLATE 209B telencephalic superventricle

Future

(future lateral ventricle)

p a riet

U M

A

PRETE C

L A H

PR E AR OP c EA TIC re ce ss ti op

Tongue

O

N

S

O N A L

P

H

ISTHMUS

P

O

A

M

OR S RI LU FE U IN LIC L CO

P

H

A

S

T U M

Y

T

L

U

C

E

N

id no he Sp

H

N

TECTUM

rhombencephalic superventricle CEREBELLUM

Oral cavity

M an

(future fourth ventricle)

lar bu di

UPPER MEDULLA

Tongue

s es oc pr

Temporal bone labyrinth

La

Pharynx

RHOMBENCEPHALON Incipient rhombencephalic choroid plexus

Petrous temporal bone

ry nx ?

LOWER MEDULLA

r ol te b r um al n

Atlas Axis

Ve c

on

e

C3

Dorsal root ganglia

Future squ FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

amo

us

c oc

ip

it

b al

Medullary velum

LICULUS R COL

M

R IO

E

M E S E G

TECTUM PE SU

T

DIENCEPHALON

M TU

E

Olfactory epithelium

(future aqueduct)

MU S LA

al bone re front Futu

A

(future third ventricle, thalamic part)

SEPTUM

Nerve I (olfactory)

Oral cavity

mesencephalic superventricle

H

diencephalic superventricle

T

BASAL TELENCEPHALON

Maxilla

Brain surface (pia, heavier line) T

Nostril

Meninges (dura and arachnoid)

S I

TELENCEPHALON

Nasal cavity

Skull and skin

P

"Budding" telencephalic choroid plexus

Frontonasal process

ne

E

CEREBRAL CORTEX

al b o

524

PLATE 209C

GW7.5 Sagittal CR 21 mm, C6202 Level 3: Slide 24, Section 2 Left side of brain NEUROEPITHELIAL AND PARENCHYMAL BRAIN STRUCTURES

BRAINSTEM FLEXURES

4 3 2

2. Pontine 3. Mesencephalic 4. Diencephalic

The skull, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

525

PLATE 209D Cortical (parietal?) NEP

Primordial plexiform layer Settling Cajal-Retzius cells Migrating subplate neurons

Cortical (posterior cingulate?) NEP

d

Cortical (hippocampal) NEP

ig

in

g

Habenulo-interpeduncular tract?

rn jou Fornical GEP

Choroid plexus stem cells

Thalamic (reticular?) NEP

mi

n

ur jo

So

ea

?

e

a

ar

Habenulointerpeduncular tract? Interpeduncular nucleus?

Lateral lemnis

Pontine NEP

Future optic tract and chiasm?

cus

t

egmental neuro g t ns

at

al

se

a?

L

h

th

d

S ub sta n

ig r

Preoptic NEP

l ra

o yp

an

n tia

Nerve I (olfactory)

c mi

grating,

in

Subthalamic NEP

Migrating and settling basal telencephalic neurons Sojourning and migrating septal neurons Sojourning and migrating preoptic neurons

Mesencephalic (tectal, superior colliculus) NEP

i

n

g,

Pretectal NEP

tl

Septal NEP?

Hypothalamic NEP (anterior) Sojourning, migrating, and settling hypothalamic neurons

Posterior commissure

Thalamic (ventral complex?) NEP Thalamic (reticular protuberance?) Mesencephalic NEP (tegmental) NEP

Strionuclear NEP? Basal telencephalic NEP

Epithalamic NEP

Thalamic (dorsal complex?) NEP

So Cortical (anterior cingulate?) NEP

Cortical (orbitofrontal) NEP

Thalamic (posterior complex?) NEP

t h a l a m ic neurons

an

Cortical (paracentral?) NEP

m

ing rat

Migrating isthmal neurons?

?

Parabrachial nucleus?

Reticular formation Pontomedullary trench

Upper medullary NEP Solitary nucleus

Lateral lemniscus?

Cerebellar notch CTF1 (fibers) CTF 2 (cells) CTF 3 (cells and fibers) CTF 4 (cells)

Cerebellar NEP

Mesencephalic (tectal, inferior colliculus) NEP

Dorsal rhombic lip Sojourning and migrating deep neurons

Solitary tract

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium CTF - Cerebellar transitional field FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Vestibular nuclear complex?

Lower medullary (vestibular complex?) NEP Ventral rhombic lip

Inferior cerebellar peduncle?

526

PLATE 210A

GW7.5 Sagittal CR 21 mm, C6202 Level 4: Slide 22, Section 2 Left side of brain SKULL, MAJOR BRAIN STRUCTURES, AND VENTRICULAR DIVISIONS

Neuroepithelial and parenchymal structures are labeled in Parts C and D of this plate on the following pages.

527

PLATE 210B

diencephalic superventricle

Future

(future third ventricle, thalamic part)

p a riet

CEREBRAL CORTEX

A

TELENCEPHALON

ET

EC

US

AL

H T

ON

PR

SU

HYPOTHALAMUS

optic recess

Nerve VIII (vestibulocochlear) Vestibular ganglion (VIII)

Nerve VIII (vestibulocochlear, boundary cap)

PONS

PONS

id

Petrous temporal bone

eno

Sph

Maxilla

B

CO

E AR OP E A T IC

C E PH A L

rhombencephalic superventricle

Oral cavity

EP

AM

T

C

L

LEN

SE

N

SA

TE

T U M?

M? NTU ME EG

BA

BASAL GANGLIA

TE

ME

DIENCEPHALON

Olfactory epithelium

Nasal cavity

CEREBELLUM

(future fourth ventricle)

R A PE LL UP DU E M

Meckel's cartilage

R

TEC T UM U LUS T M LICU COL C OR N RI O PE OR S L RI LU SU FE U HA IN L IC L

T H A L

"Budding" telencephalic choroid plexus

Brain surface (pia, heavier line)

EP I

P

al bone re front Futu

(future lateral ventricle)

Mandibular process

U S

AMUS AL TH

M

telencephalic superventricle

Nerve I (olfactory) Frontonasal process

Skull and skin

ne

Meninges (dura and arachnoid)

HIPPOCAMPUS

OLFACTORY BULB

al b o

Eustachian tube? Temporal bone labyrinth Inferior ganglion (IX)

RHOMBENCEPHALON

LL A

Nerve X (vagus)

r ol te b r um al n

Inferior ganglion (X)

Ve c

C3

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

Incipient

Nerve IX rhombencephalic (glossopharyngeal) choroid plexus Superior L ganglion (IX) Medullary O Superior ME W velum DU ER ganglion (X) Nerve X (vagus)

Atlas Dorsal root ganglion

Axis

c ci p F ut u r e sq u a m o u s o

b it al

on

e

528

PLATE 210C

GW7.5 Sagittal CR 21 mm, C6202 Level 4: Slide 22, Section 2 Left side of brain NEUROEPITHELIAL AND PARENCHYMAL BRAIN STRUCTURES, PERIPHERAL GANGLIA

BRAINSTEM FLEXURES

4

3 2 2. Pontine 3. Mesencephalic 4. Diencephalic

The skull, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

529

PLATE 210D

Cortical (parietal?) NEP

Primordial plexiform layer Settling Cajal-Retzius cells Migrating subplate neurons

Cortical (occipital?) NEP Epithalamic NEP

Cortical (hippocampal) NEP

al ge ni d n m a i g gra tin c nin r g u o th oj a

Cortical (paracentral?) NEP

ns u r o eurons n e ic n e a t lam ul

Thalamic (ventral complex?) NEP

V ge ent nic ra ula l la te ter bo al dy ?

Subthalamic nucleus?

Migrating and settling inferior colliculus neurons

Pontine NEP

Preoptic NEP

g

? ns

Sojourning and migrating preoptic neurons

te

euro l n

Lateral hypothalamic area

Sojourning and migrating basal ganglionic neurons

g

ta

Migrating and settling basal telencephalic neurons

in

en

Zona incerta?/

Bed nucleus of the stria terminalis

tl

m

Cortical (olfactory) NEP

et

Subthalamic NEP

Ventral complex of thalamus?

Mesencephalic (tectal, superior colliculus) NEP

S

Strionuclear NEP

Nerve I (olfactory)

Migrating and settling superior colliculus neurons

S

Choroid plexus stem cells Cortical (orbitofrontal) NEP Anteromedial basal ganglionic NEP Basal telencephalic NEP

Migrating and settling pretectal neurons Thalamic (posterior complex?) NEP

Migra t i ng late r

Fornical GEP

Migrating and settling habenular neurons

Latera l

Hypothalamic NEP (anterior) Sojourning, migrating, and settling hypothalamic neurons

m l e

Reticular formation

Parabrachial nucleus?

Future optic tract? Principal sensory nucleus (V)?

Pontomedullary trench

Nucleus of the lateral lemniscus?

Cerebellar notch

a l

ul

n

ar

n uc lear u co cl eu s (V )

le x mp

Inferior ganglion (IX)

Nerve X (vagus)

Inferior ganglion (X)

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium CTF - Cerebellar transitional field FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Dorsal rhombic lip

CTF 3 (cells and fibers)

t

in

s Ve

Sp

ib

Mesencephalic (tectal, inferior colliculus) NEP

CTF1 (fibers) Upper medullary CTF 2 (cells) NEP

Nerve VIII (vestibulocochlear) Vestibular ganglion (VIII)

scus ni

CTF 4 (cells)

Sojourning and migrating deep neurons

Cerebellar NEP

Lower medullary (posterior precerebellar) NEP in ventral rhombic lip

Inferior cerebellar peduncle? Posterior intramural migratory stream? Superior ganglion (X) (inferior olive neurons) Superior ganglion (IX) Nerve X (vagus) Nerve IX (glossopharyngeal)

530

PLATE 211A

GW7.5 Sagittal CR 21 mm, C6202 Level 5: Slide 21, Section 2 Left side of brain SKULL, MAJOR BRAIN STRUCTURES, AND VENTRICULAR DIVISIONS

Neuroepithelial and parenchymal structures are labeled in Parts C and D of this plate on the following pages.

531

PLATE 211B Future pariet

al b o n

e

diencephalic superventricle

CEREBRAL CORTEX

(future third ventricle, thalamic part)

HIPPOCAMPUS

telencephalic superventricle

A T H A L

U AM

AL PR E AR OP EA TI C

TE CT U

H

HYPOTHALAMUS

BT

M

SU

TU

N

C

LO

PHALON

E N C E PH A

LUS LICU COL

CE

SA

T EL

SE

N

S

OR RI

ME

DIENCEPHALON

BA L

M

optic recess

Nerve VIII (vestibulocochlear)

Sp he no id

Petrous temporal bone

Meckel's cartilage

Brain surface

T

BASAL GANGLIA

Frontonasal process

Mandibular process

Meninges

E

TELENCEPHALON

Skull and skin

PE SU

re frontal bone Futu

"Budding" telencephalic choroid plexus

Maxilla

EP I

AMUS AL TH

(future lateral ventricle)

OLFACTORY BULB

U S

M

PONS

Vestibular ganglion (VIII)

Oral cavity

rhombencephalic superventricle

(future fourth ventricle)

M UP ED PE UL R Spiral LA

Eustachian tube?

PONS

CEREBELLUM

RHOMBENCEPHALON Incipient rhombencephalic choroid plexus

ganglion (VIII)?

Temporal bone labyrinth

Medullary velum

L ME OW DU ER LL A

Nerve X (boundary cap)

Nerve X (vagus)

Nerve X (vagus) Nerve IX (boundary cap)

Inferior ganglion (X)

Nerve IX (glossopharyngeal)

las At

Superior ganglion (X)

Superior ganglion (IX)

c F ut u r e squ a m o u s o

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

b t al ci pi

on

e

532

PLATE 211C

GW7.5 Sagittal CR 21 mm, C6202 Level 5: Slide 21, Section 2 Left side of brain NEUROEPITHELIAL AND PARENCHYMAL BRAIN STRUCTURES, PERIPHERAL GANGLIA

The skull, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

533

PLATE 211D

Primordial plexiform layer

Cortical (parietal?) NEP

Settling Cajal-Retzius cells Migrating subplate neurons Cortical (occipital?) NEP Thalamic (posterior complex?) NEP Cortical (hippocampal) NEP

Fornical GEP

Choroid plexus stem cells

Thalamic (ventral complex?) NEP

Strionuclear NEP

Basal ganglionic NEP Basal telencephalic NEP Anteromedial

Cortical (olfactory) NEP

Bed nucleus of the stria terminalis

Migrating and settling basal telencephalic neurons Sojourning and migrating basal ganglionic neurons Sojourning and migrating preoptic neurons

Hypothalamic NEP (anterior)

Future optic tract?

Migrating and settling superior colliculus neurons

ic lam tha eus? b u l S uc n

Lateral hypothalamic area

Preoptic NEP

Subthalamic NEP?

Ventral complex of thalamus? Stria Zona terminalis incerta?/

Posterior

ge Ven ni tr cu al la la te te bo ral dy ?

Cortical (orbitofrontal) NEP

Settling habenular neurons?

Stria me dul l ati Migr n g latera a r i l g s? en ic g and mi gra u tin nin r g u o th j a So

Cortical (paracentral?) NEP

Habenulo-interpeduncular tract

ons eu r neurons n c i te l a lam

Pontine NEP Parabrachial nucleus?

Reticular formation

Sojourning, migrating, and settling hypothalamic neurons

CTF1 (fibers) CTF 2 (cells) CTF 3 (cells and fibers) CTF 4 (cells)

Principal sensory nucleus (V)?

a

l

n

Spiral ganglion? (VIII) Nerve IX (boundary cap) Nerve IX (glossopharyngeal) Inferior ganglion (X) Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium CTF - Cerebellar transitional field FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Dorsal rhombic lip

Upper medullary NEP

in

Vestibular ganglion (VIII)

S p

Nerve VIII (vestibulocochlear)

Cerebellar notch

Pontomedullary trench

u

cl eu

Ve sti bu comlar n ple ucle ar x s

(V

)

Nerve X (boundary cap)

Cerebellar NEP

Sojourning and migrating deep neurons

Lower medullary (anterior precerebellar) NEP in ventral rhombic lip Lower medullary (posterior precerebellar) NEP in ventral rhombic lip

Nerve X (vagus) Superior ganglion (X) Superior ganglion (IX) Nerve X (vagus)

Inferior cerebellar peduncle?

534

PLATE 212A

GW7.5 Sagittal CR 21 mm, C6202 Level 6: Slide 18, Section 2 Left side of brain SKULL, MAJOR BRAIN STRUCTURES, AND VENTRICULAR DIVISIONS

Neuroepithelial and parenchymal structures are labeled in Parts C and D of this plate on the following pages.

535

PLATE 212B Future par

CEREBRAL CORTEX

i e t al

bon

e Skull and skin

HIPPOCAMPUS

Meninges (dura and arachnoid)

telencephalic superventricle

Brain surface (pia, heavier line)

re frontal bone Futu

(future lateral ventricle) "Budding" telencephalic choroid plexus

THALAMUS

TELENCEPHALON

DIENCEPHALON THALAMUS

BASAL GANGLIA

PRIMARY OLFACTORY CORTEX

BA S

A L T ELENC EPHA

AMYGDALA

LO N

Trigeminal ganglion (V)

Sp he

Nerve V(trigeminal)

no

Nerve V (boundary cap)

id

Frontonasal process

RHOMBENCEPHALON PONS CEREBELLUM

Nerve VIII (boundary cap)

Eustachian tube? Meckel's cartilage

rhombencephalic

superventricle M UP ED PE (future fourth ventricle) UL R LA Incipient rhombencephalic choroid plexus

Medullary velum

ne

Vestibular ganglion (VIII)

Nerve VIII (vestibulocochlear)

so

Petrous temporal bone

m

ou

Temporal bone labyrinth

ua

Oral cavity

Mandibular process

c ci pit al b o

Maxilla

Ba

Sq

sa

l

oc

c i pit a l b o n e

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

536

PLATE 212C

GW7.5 Sagittal CR 21 mm, C6202 Level 6: Slide 18, Section 2

See details of the cerebral cortex in Plates 214A and B.

See details of the hippocampus, basal ganglia, and amygdala in Plates 216A and B.

Left side of brain NEUROEPITHELIAL AND PARENCHYMAL BRAIN STRUCTURES, PERIPHERAL GANGLIA

See details of the cerebellum in Plates 219A and B.

See details of the peripheral ganglia and lateral pons in Plates 220A and B.

The skull, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

537

PLATE 212D

Cortical (parietal?) NEP

Primordial plexiform layer Settling Cajal-Retzius cells Migrating subplate neurons

Cortical (temporal?) NEP Cortical (dorsal hippocampal) NEP

Cortical (paracentral?) NEP

Fornical GEP

Choroid plexus stem cells

Posterior complex of thalamus?

Fornical GEP

Cortical (insular?) NEP

Migrating lateral geniculate neurons

Amygdaloid NEP Basal ganglionic NEP Posterior

Basal telencephalic NEP Anterolateral

Ventral lateral geniculate body?

Cortical (primary olfactory) NEP

Cortical (ventral hippocampal) NEP

Sojourning and migrating amygdaloid neurons Migrating and settling basal telencephalic neurons

Sojourning and migrating basal ganglionic neurons CTF1 (fibers)

Nerve V (boundary cap) Nerve V (trigeminal)

CTF 2 (cells)

Cerebellar notch

CTF 3 (cells and fibers) CTF 4 (cells) Sojourning and migrating deep neurons

Trigeminal ganglion (V)

Sojourning Purkinje cells?

Pontine NEP

Lateral lemniscus Nucleus of the lateral lemniscus?

Auditory NEP?

Vestibular ganglion (VIII) Nerve VIII (vestibulocochlear) Nerve VIII (boundary cap) Cochlear nuclei?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium CTF - Cerebellar transitional field FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Ce

re

be

E llar N

Upper medullary (anterior precerebellar) NEP in ventral rhombic lip

P

Dorsal rhombic lip

538

PLATE 213A

GW7.5 Sagittal CR 21 mm, C6202 Level 7: Slide 17, Section 2 Left side of brain SKULL, MAJOR BRAIN STRUCTURES, AND VENTRICULAR DIVISIONS

Neuroepithelial and parenchymal structures are labeled in Parts C and D of this plate on the following pages.

539

PLATE 213B Future par

CEREBRAL CORTEX

i e t al

bon

Skull and skin

e

Meninges (dura and arachnoid) Brain surface (pia, heavier line)

HIPPOCAMPUS

telencephalic superventricle

re frontal bone Futu

(future lateral ventricle)

"Budding" telencephalic choroid plexus

DIENCEPHALON

TELENCEPHALON

THALAMUS

BASAL GANGLIA

PRIMARY OLFACTORY CORTEX

BA S

T ELENCE

AMYGDALA

PHAL O N

Sp

Trigeminal ganglion (V)

id no he

Frontonasal process

AL

Nerve V(trigeminal) Nerve V (boundary cap)

RHOMBENCEPHALON

Nerve VIII (boundary cap) Vestibular ganglion (VIII)

Medullary velum

Meckel's cartilage

ne

Eustachian tube?

(future fourth ventricle)

c ci pit al b o

Future middle ear ossicles?

Nerve VIII (vestibulocochlear) Incipient rhombencephalic choroid plexus

m

Petrous temporal bone Temporal bone labyrinth

ua

Mandibular process

rhombencephalic superventricle

so

Oral cavity

CEREBELLUM

PONS

ou

Maxilla

Ba

Sq

sa

l

oc

c i pit a l b o n e

FONT KEY: ventricular divisions - capitals Major brain structure - Times Bold CAPITALS All other structures - Times Roman or Bold

540

PLATE 213C

GW7.5 Sagittal CR 21 mm, C6202 Level 7: Slide 17, Section 2

Left side of brain NEUROEPITHELIAL AND PARENCHYMAL BRAIN STRUCTURES, PERIPHERAL GANGLIA

The skull, major brain structures, and ventricular divisions are labeled in Parts A and B of this plate on the preceding pages.

541

PLATE 213D

Cortical (parietal?) NEP

Primordial plexiform layer Settling Cajal-Retzius cells Migrating subplate neurons

Cortical (temporal?) NEP Cortical (dorsal hippocampal) NEP Cortical (paracentral?) NEP

Fornical GEP

Choroid plexus stem cells

Cortical (insular?) Amygdaloid NEP NEP Basal ganglionic NEP Basal telencephalic NEP Posterior

Posterior complex of thalamus?

Fornical GEP

Anterolateral

Cortical (primary olfactory) NEP Migrating and settling primary olfactory cortex neurons?

Cortical (ventral hippocampal) NEP Sojourning and migrating amygdaloid neurons

Migrating and settling basal telencephalic neurons

Sojourning and migrating basal ganglionic neurons CTF1 (fibers)

Nerve V (boundary cap) Nerve V (trigeminal)

CTF 2 (cells)

Cerebellar notch

CTF 3 (cells and fibers) CTF 4 (cells) Sojourning and migrating deep neurons

C Pontine NEP

Lateral lemniscus Nucleus of the lateral lemniscus?

er eb e l l a r

Auditory NEP?

Vestibular ganglion (VIII) Nerve VIII (vestibulocochlear)

Ventral rhombic lip

Nerve VIII (boundary cap) Cochlear nuclei?

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium CTF - Cerebellar transitional field FONT KEY: Germinal zone - Helvetica bold Transient structure - Times bold italic Permanent structure - Times Roman or Bold

Choroid plexus stem cells

P

Sojourning Purkinje cells?

Trigeminal ganglion (V)

N

E

Dorsal rhombic lip

Medial to Level 1: Slide 32, Section 2 MEDIAL (right hemisphere)

Level 6: Slide 18, Section 2 LATERAL (left hemisphere)

GW7.5 Sagittal CR 21 mm, C6202 DORSAL CEREBRAL CORTEX

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

See level 1 in Plates 207 A-D, level 6 in Plates 212 A-D.

542

PLATE 214A

PLATE 214B l s a lo n Blood vesse Pial surface (heavy line)

g pial surface

Settling Cajal-Retzius cell?

Medial to Level 1: Slide 32, Section 2 MEDIAL (right hemisphere)

Primordial plexiform layer

Migrating Cajal-Retzius cells and subplate neurons

Cortical neuroepithelium (NEP)

Cortical NEP (mitotic zone and end feet of neuroepithelial cells) Pial surface (heavy line)

Blood vessels along pial surface

Settling Cajal-Retzius cell?

Level 6: Slide 18, Section 2 LATERAL (left hemisphere)

Primordial plexiform layer Migrating Cajal-Retzius cells and subplate neurons Cortical NEP

Cortical NEP (mitotic zone and end feet of neuroepithelial cells)

Note that there is no evidence of a lateral (more mature) to medial (less mature) morphogenetic gradient during this early stage of cerebral cortex development. A lateral (older) to medial (younger) gradient of neurogenesis in not present in Cajal-Retzius cells in rats, and is very small among subplate neurons (Bayer and Altman, 1991). This specimen shows the same type of developmental pattern in the human cerebral cortex.

543

544

PLATE 215A

GW7.5 Sagittal CR 21 mm, C6202 Medial to Level 1: Slide 31, Section 2 Right side of brain OLFACTORY BULB AND BASAL TELENCEPHALON

See level 1 in Plates 207A-D.

545

PLATE 215B

Cortical (orbitofrontal) neuroepithelium (NEP)

Pial surface (heavy line)

B

Cor N

P

bu

lb

)

a l

l (o l fa

ry

c a l i e p h e n c t e l

) r y o c t ( o l f a

o

t

Nerve I entry zone fuses with brain surface

et

at

Mi gr

de

P

te e

let ot eI

c

rv

n

ium hel pi t

p

Ne

le

ye

h

a n

e u

ro

Areas where mensenchymal cells from the periphery enter the basal telencephalon?

c li

n

s

erior nasal concha n sup

Nasal cavity

Migratory cells (neurons?) enter olfactory nerve?

t or

i lium the pi

e

ou t si

ac olf

ry

ll s

ro

ce

E

l sa ba

in

g

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

N

tl

g in at gr Mi

N e rv e I r o o

N e r v e

I

Migratng olfactory bulb neurons

Olf ac to

Cell nuclei in the pseudostratified neuroepithelium

s

E

a

tic a c

Mitotic zone and end feet of neuroepithelial cells

Pial surface (heavy line)

546

PLATE 216A

GW7.5 Sagittal CR 21 mm, C6202 Level 6: Slide 18, Section 2 Left side of brain

HIPPOCAMPUS, BASAL GANGLIA, AND AMYGDALA

See Level 6 in Plates 212 A-D.

547 Primordial plexiform layer

Cortical (temporal?) NEP

Settling Cajal-Retzius cells

PLATE 216B

Migrating subplate neurons

TELENCEPHALON

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

telencephalic superventricle

(future lateral ventricle)

Cortical (dorsal hippocampal) NEP

DORSAL HIPPOCAMPUS

THALAMUS

Fornical GEP Choroid plexus stem cells

Posterior complex?

"Budding" telencephalic choroid plexus

Vascular bed (stroma) Choroid plexus stem cells

Basal ganglionic NEP

Fornical GEP?

Cortical (ventral hippocampal?) NEP

Sojourning and migrating basal ganglionic neurons

BASAL GANGLIA (putamen and globus pallidus?_ Amygdaloid NEP AMYGDALA Migrating and settling basal telencephalic neurons BASAL TELENCEPHALON

M gen igra icu ting late la neu teral ron s?

VENTRAL HIPPOCAMPUS?

Posterior

Anterolateral

DIENCEPHALON

Ans

a le

ntic

Ventral lateral geniculate body?

THALAMUS

ular

is? Sojourning and migrating amygdaloid neurons ABBREVIATIONS: GEP - Glioepithelium NEP - Neuroepithelium

GW7.5 Sagittal CR 21 mm, C6202 Between Levels 1 and 2: Slide 28, Section 3 HYPOTHALAMUS

See level 1 in Plates 207A-D, level 2 in Plates 208 A-D.

548

PLATE 217A

PLATE 217B N E P

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

diencephalic superventricle

t h a l a m i c

MIDDLE HYPOTHALAMUS

(future third ventricle, hypothalamic part)

Mitotic zone and end feet of neuroepithelial cells

Preoptic NEP Migrating preoptic neurons

Nuclei in the pseudostratified neuroepithelium

optic recess

y

p

o

infundibular recess

A

nt

er

i o r hyp

o

am thal

ic

epith neuro

e l i u m ( N E P)

M

i d

d

ANTERIOR HYPOTHALAMUS Brain surface (heavy line)

ure

Sojourning and migrating hypothalamic neurons

PONS

rt

Sojourning and migrating hypothalamic neurons Fut

le

h

io

ter n A

opt ic t rac t?

Sphenoid

a rp

Pituitary gland

t ar p e

a

l du

n la g a

tr

In

t lef c r

t ia d e m r e

t In

Sella turcica

549

See level 1 in Plates 207 A-D, level 2 in Plates 208 A-D.

GW7.5 Sagittal CR 21 mm, C6202 Between Levels 1 and 2: Slide 28, Section 3 MIDBRAIN TEGMENTUM

550

PLATE 218A

PLATE 218B Ventricular surface

mesencephalic superventricle

(future aqueduct)

Mitotic zone and end feet of neuroepithelial cells

c e p h a l i c ( t e g m n e s e n Deep fibrous zone ( M e sprou t a ti n g axon l ) s of e n u r l o a ns? (late r e ce ment g e t n g n t w i l t y a Mig

TEGMENTUM

l ta n me g te r fi

gen era

te d

neu

r

N E P

c

fi ial

bro

us

zo n e

Pial surface

(a x o n

bstantia a/su e r a

s o f te g

nig ra ?

rons intermingle with afferent axo mental neu ns an d mi dlin e ra ph

eg li a

?)

nta ln eu ro ns in ter m in gl ew ith

af fe re nt ax

) s? on

pe Su

ve)

o ns i n te al neurons? ( t n e rm dee ing egm p t le w ) g ith n affe i n re n t r axon u o s?) j o Migrati S ng t egm ent al ne n l e a u r t o ns? (su ur en m on p g erfic e t s? g i a n l) i (m n r u id Mi d o j dl dl e So e fi b r wa o t n a u l n e e u r o n s m s? (e zon ve eg t a g rly e( ) in t a a xo r wa g ns i M of ve teg me )

MIDBRAIN

l ra t n Ve

ra

Nuclei in the pseudostratified neuroepithelium

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

551

HEMISPHERE Level 6: Slide 18, Section 2

VERMIS Between Levels 1 and 2: Slide 29, Section 2

See level 1 in Plates 207 A-D, level 2 in Plates 208 A-D, and level 6 in Plates 212 A-D.

552

GW7.5 Sagittal CR 21 mm, C6202 CEREBELLUM

PLATE 219A

PLATE 219B

eric neuroep

VERMIS Arrows indicate the presumed direction of neuron migration from neuroepithelial sources. There is a lateral (more mature) to medial (less mature) morphogenetic gradient between the hemisphere and vermis of the cerebellum. The larger hemisphere has better defined and more transitional layers than the smaller vermis. Deep neurons predominate in the transitional field outside the germinal matrix throughout the cerebellum, indicating that they are earlier-generated neurons. Within both the hemispheric and vermal parts of the cerebellar neuroepithelium, more Purkinje cells and fewer deep neurons are being generated. Note that the external germinal layer is not present at this stage of cerebellar development.

(C

(N

E c

Choroid plexus stem cells in the medullary velum

ith

Sojourning and migrating deep neurons

e

TF)

1 (fibers) C C T F 2 (cells) TF rs) 3 (c ells and fibe ls) CTF 4 (cel

C

er

Sojou r

eb

P

isph

ing Purkinje

s?

ni n g Pur k i n j e c e l l

ell

s

NE

hem

urn

P)

Choroid plexus stem cells in the medullary velum

al

llar

jo

l el

m

So

Sojourning and migrating deep neurons

u

ebe

al fi eld CTF 2 ( (CT cells) F) CTF 3 ( 1 cells (f ib CTF 4 and fi er (cel ber s) l s s) CTF 5 (cell ) s a nd fib ers )

?

Cer

lar transition

m

Cerebel

li

HEMISPHERE

ar ver

553

See level 6 in Plates 212 A-D.

GW7.5 Sagittal CR 21 mm, C6202 Level 6: Slide 18, Section 2 PONS AND PERIPHERAL GANGLIA

554

PLATE 220A

PLATE 220B

Layers of the developing cerebellum

Arrows indicate the presumed direction of neuron migration from neuroepithelial sources.

rhombencephalic superventricle

Cerebellar NEP

(future fourth ventricle) Upper medullary (anterior precerebellar) NEP

Arrows indicate the presumed direction of axon growth from peripheral nerves.

Pontine neuroepithelium (NEP) Auditory NEP? Spina

c l tra

Nerve V (boundary cap)

Principal sensory nucleus (V)?

V t(

PONS

)?

UPPER MEDULLA

Note that peripheral nerves are full of glia while central fiber tracts are devoid of glia.

Cochlear nuclei?

Nucleus of the lateral lemniscus? Nerve V (trigeminal)

La

tera

Note the absence of migratory streams leaving the precerebellar NEP.

l lemniscus

Nerve VIII (boundary cap)

Nerve VIII (vestibulocochlear) Vestibular ganglion (VIII)

Trigeminal ganglion (V)

Temporal bone labyrinth Spiral ganglion? (VIII)

Sphenoid Petrous temporal bone

555

GW7.5 Sagittal CR 21 mm, C6202 Medial to Level 1 MIDLINE RAPHE GLIAL STRUCTURE Pons adjacent to the pontine flexure in slide 31, section 2.

Cervical spinal cord adjacent to the medullary flexure in slide 32, section 2.

See level 1 in Plates 207A-D.

556

PLATE 221A

PLATE 221B PONS

li Mid n zo our Soj

n

glioepithelium? (rare mito phe tic fig a r Spr e u

l a y er body l l e c r n e? o

o u ti n res) g fibe ? of nonmigrating ra r s of recent phe ly g e glia n era l cel te d g l i a ? ls ( M ORPHOC YTES )

Scattered cell bodies of another type of glia migrating among the fibrous palisades.

er li n d i M

a

e ph

g li

a

be l fi

rp

a

d es lis a

(from

morphocyte cell b odie si

CERVICAL SPINAL CORD

n th ec ell den se lay er a

dja

ce n

t to

the

g li o

e p it

heli um? )

Cell body layer of spinal cord morphocytes (glioepithelium absent?) Midline raphe glial fiber palisades

Scattered cell bodies of another type of glia migrating among the fibrous palisades.

The midline raphe glial system is prominent in regions where the shape of the brain and spinal cord sharply change curvature. Van Hartesveldt et al. (1986) described this in rats, and it is virtually identical in man. The strong fibrous palisades may provide structural stability in the region of these curvatures. Consequently, we call the specialized glia MORPHOCYTES. There is structural variability between the pons and spinal cord. In the PONS (top panel) there are two cell-dense layers near the ventricular surface. Since mitotic figures are rare in the layer adjacent to the ventricle, it may not be an active germinal zone generating glia. However, at earlier stages of development (to be described in Volume 5), this layer is full of stem cells generating midline raphe glia. The second layer is most likely the densely packed cell bodies that have long fibrous processes extending to the pial surface rather than a premigratory sojourn zone. Morphocytes may be predominantly nonmigratory cells that differentiate at the site of their generation (similar to the ependymal cells that eventually line the ventricular system). In the SPINAL CORD (bottom panel) there is one cell-dense layer adjacent to the central canal. These are the cell bodies with relatively short (compared to the pons) fibrous processes that extend to the pial surface. In both regions, there are widely scattered cells dispersed between the fibers. These are most likely other types of glial cells that do not play a structural role (nonmorphocytes) in the raphe system.

557

558

GLOSSARY GLOSSARY

An asterisk in front of a term indicates that it is a separate entry in the Glossary with additional information. Terms referring to transient developmental structures are underlined. A Abducens nucleus (VI) – An aggregate of cranial nerve motor neurons situated beneath the fourth ventricle in the *pons. The nucleus receives input from the *vestibular nuclear complex and is the source of motor fibers of cranial *nerve VI that innervate the lateral rectus muscle of the eye. Accessory nucleus (XI) – A column of motor neurons that extends from the region of the *nucleus ambiguus in the medulla to segments 5-6 of the cervical spinal cord. Its axons form *nerve XI that innervates the sternocleidomastoid and trapezius muscles.

Amygdaloid NEP – Neuroepithelial lining of the anterior wall of the posteroventral *telencephalic superventricle, the presumptive site of origin of neurons and glia of the *amygdala. It is continuous rostrally with the posterior *striatal NEP and caudally with the ventral *hippocampal NEP. Amygdalohippocampal area – Also called the cortical amygdaloid transition area, connected in the mature brain with the *bed nucleus of the stria terminalis and the *ventromedial hypothalamic nucleus.

t

Accumbent NEP – Neuroepithelial source of the neurons and neuroglia of the *nucleus accumbens. After cessation of neurogenesis, this germinal matrix is transformed into a *glioepithelium. Alisphenoid process – A cartilaginous structure in the developing skull that surrounds part of the trigeminal nerve and the facial nerve; eventually it becomes the posterior wing of the *sphenoid bone. Allocortex (embryonic) – Portion of the cerebral hemispheres that, in contrast to the *neocortex, develops into a “three-layered” (oligolaminar) cortex. Among prominent allocortical regions are the *hippocampus, the *primary olfactory cortex, and the *entorhinal cortex. Ammon’s horn (hippocampus) – Part of the *hippocampus that contains a prominent layer of large pyramidal cells. Ammonic migration and sojourn zone – Migrating pyramidal cells originating in the *ammonic NEP that settle in *Ammon’s horn. Ammonic NEP – Neuroepithelial patch of the *hippocampal NEP, the putative source of the pyramidal cells of Ammon’s horn. Amygdala – A large subcortical structure with several subdivisions in the temporal lobe, implicated in adults in behavioral aggression.

Ansa lenticularis – Fiber tract that originates in the internal (medial) segment of the *globus pallidus, courses dorsal to the *zona incerta, and terminates in the *thalamus, in particular the *ventral complex and the *centromedian nucleus. Anterior amygdaloid area – A region of small to mediumsized cells in the mature *amygdala that represents a transition zone between the *substantia innominata and the amygdaloid complex proper. Anterior commissure (embryonic) – Large fiber bundle that crosses in the ventral telencephalon and interconnects in the mature brain several forebrain structures on the right and left sides, including the *primary olfactory cortex, the *entorhinal cortex, the *amygdala, and some components of the *temporal lobe. Some of its fibers have crossed the midline by GW9. Anterior complex (thalamus) – A group of anterior thalamic nuclei with related connections. Components of the anterior thalamic complex are the anterodorsal nucleus, the anteromedial nucleus, and the anteroventral nucleus. In he mature brain, the afferents of the anterior complex come principally from the *hippocampal region and the *mammillary body. The ascending efferents terminate in the *cingulate gyrus, while the descending efferents terminate in the *mammillary body. The anterior thalamic complex is a component of the “limbic system.” Anterior extramural migratory stream – Large stream of young neurons migrating anteroventrally from the *anterior precerebellar NEP to the *pontine gray and the *reticular tegmental nucleus. The stream forms during the latter part of the late first trimester.

GLOSSARY Anterior pituitary gland (embryonic) – The anterior lobe of the pituitary gland, also known as the adenohypophysis. It is derived from Rathke’s pouch during embryonic development. Anterior precerebellar NEP – Neuroepithelial source of neurons of the *pontine gray and *reticular tegmental nucleus. It lines the *rhombencephalic superventricle dorsally and the young neurons migrate to their target structures by way of the *anterior extramural migratory stream. Aqueduct (embryonic) – See Mesencephalic superventricle Arcuate nucleus (hypothalamus) – A small-celled nucleus that surrounds the base of the third ventricle posteriorly. It contains releasing hormones and is involved in the central nervous regulation of the anterior pituitary gland. Atlas – The first cervical vertebra. Auditory germinal trigone – Proliferative site in the *rhombencephalon that contains the NEP and the external germinal layer of the *cochlear nuclei and contributes stem cells to the rhombencephalic *choroid plexus. Axis – The second cervical vertebra.

B Basal ganglia – A broad term that includes three large ganglionic (subcortical) components of the telencephalon, the *caudate nucleus, the *putamen, and the *globus pallidus. The latter two are also referred to as the *striatum. Basal ganglia pathologies have been linked to Parkinsonism, Huntington’s disease, and other motor abnormalities. Basal ganglionic NEP and SVZ – Composed of three large hillocks or eminences protruding into the *telencephalic superventricle – the anterolateral, the anteromedial, and the posterior – and contain the neuroepithelial and subventricular stem cells that furnish neurons and neuroglia to the *basal ganglia. A fourth component is the cortico-ganglionic NEP/SVZ. The SVZ is far more prominent in the basal ganglia than in the developing *cerebral cortex. Basal nucleus (amygdala) – The largest nucleus in the amygdala that forms a major part of the *basolateral complex. It is separated from the *lateral nucleus by a thin fibrous band.

559 Basal nucleus of Meynert – Large-celled component of the *substantia innominata that provides in the mature brain cholinergic input to the *cerebral cortex. Basal occipital – The occipital bone surrounding the *foramen magnum. Basal telencephalic NEP and SVZ – Putative source of neurons and neuroglia of the *basal nucleus of Meynert and the *substantia innominata. Basolateral complex (amygdala) – The largest and best differentiated part of the amygdala in humans. Its principal components are the *basal nucleus and the *lateral nucleus. Bed nucleus of the stria terminalis – A large subcortical telencephalic field with indistinct boundaries. It is situated medial to the *globus pallidus, lateral to the *septum, and is transected by the *anterior commissure; a thin portion extends back to the *amygdala adjacent to the *stria terminalis. It has its own germinal source, the *strionuclear NEP and GEP. Boundary cap – A thin ring of proliferative cells surrounding the spinal and cranial nerves at the site they enter the central nervous system. Brachium of the inferior colliculus – A fiber tract situated superficially in the fibrous layer covering of the *inferior colliculus. It is composed of ascending auditory fibers from the inferior colliculus and auditory nuclei in the *pons to the *medial geniculate body.

C Calcarine sulcus (embryonic) – Cortical fissure in the occipital lobe; its wall is the target of the visual fibers from the *lateral geniculate body. It is recognizable in incipient form by the end of the first trimester. Caudate nucleus – Elongated and arched component of the *basal ganglia beneath the *cerebral cortex. It abuts the lateral ventricle and extends from anterodorsal (its “head”) to posteroventral (its “tail”). Cajal-Retzius cells – The earliest-generated *cerebral cortex neurons. Their perikarya are oriented parallel to the pial surface in *layer I. Central autonomic area (spinal cord) – Region of the spinal cord that surrounds the *central canal and is implicated in nociceptive and autonomic functions. It may be continuous rostrally with the periaqueductal *central gray.

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GLOSSARY Central canal (embryonic) – Portion of the ventricular system that extends caudally from the cervical to the sacral segments of the *spinal cord. During embryonic development, the proliferative *neuroepithelium lining this canal is the source of neurons and neuroglia of the spinal cord. After the cessation of neurogenesis, the shrunken central canal is lined by the *ependyma. Central complex (thalamus) – A group of contiguous central thalamic nuclei, including the *centromedian, central lateral, and paracentral nuclei. Central gray (periaqueductal) – Oval shaped region in the core of the mesencephalon that surrounds the *aqueduct and is capped by the *superior colliculus and the *inferior colliculus. Central nucleus (amygdala) – Part of the *corticomedial complex that is sometimes put in a class by itself. A large nucleus situated lateral to the medial nucleus that extends from the *anterior amygdaloid area to the caudal pole of the amygdala where it blends with the *putamen and the tail of the *caudate nucleus. Central nucleus (inferior colliculus) – Laminated core of the *inferior colliculus where auditory fibers of the *lateral lemniscus terminate in a tonotopic order. Centromedian nucleus (thalamus, embryonic) – Large spherical structure surrounded by fibers of the internal medullary lamina, classified with the *central complex of the thalamus. It is a paleothalamic structure that has extensive connections with the *striatum and the *reticular formation of the midbrain and is prominent by the end of the first trimester. Cerebellar NEP – An extensive neuroepithelial matrix that lines the *rhombencephalic superventricle lateral to the *dorsal rhombic lip. It is the direct source of the neurons of the *cerebellar deep nuclei and the *Purkinje cells, and an indirect source of its basket, stellate and granule cells, by way of its secondary proliferative matrix, the *external germinal layer. Cerebellar transitional field (CTF) – Transient cellular and fibrous layers, composed of migrating deep neurons and Purkinje cells, and of exiting and entering fiber tracts, prior to the formation of the cerebellar cortex during the second trimester.

Cerebellum (deep nuclei) – Three pairs of ganglionic structures in the depth of the cerebellum: the medial *fastigial nucleus; the intermediate *interpositus nucleus, and the lateral *dentate nucleus. The efferent fibers of cerebellar *Purkinje cells synapse with the neurons of the cerebellar deep nuclei which, in

turn, are the source of cerebellofugal fibers that terminate in structures outside the cerebellum. The earlygenerated deep nuclei neurons are mostly situated superficially (above the later generated Purkinje cells) during the late first trimester. Cerebellum (hemisphere) – Portion of the cerebellum situated on either side of the midline *vermis. It is prominent in the cerebellum in higher mammals and man. Cerebellum (vermis) – Midline portion of the cerebellar cortex. It is a relatively small part of the cerebellum in higher mammals and man. Cerebral cortex (embryonic) – The expanding and differentiating bilateral brain tissue covering the lateral, dorsal and medial aspects of the telencephalic superventricles. It has two major components, the *neocortex and the *allocortex. The *stratified transitional field and the *cortical plate begin to form during the late first trimester. Cerebral peduncle (embryonic) – Fibrous region along the ventrolateral aspect of the diencephalon and mesencephalon, containing fibers of the *corticofugal tract. It begins to form by the end of the first trimester and some of its fibers reach the formative *pontine gray. Choroid plexus (embryonic) – Glycogen-rich epithelial tissue that forms and begins to expand during the later first trimester in the *rhombencephalic and *telencephalic superventricles. It is formed by proliferative stem cells associated with the cerebellar *germinal trigone and an analogous germinal site in the *hippocampus. The fetal choroid plexus may play a role in the anaerobic metabolism of the early developing brain. During late-fetal development, it becomes gradually transformed into the mature choroid plexus of the shrunken fourth ventricle, with a different cellular composition and perhaps a different function. Cingulate cortex – A rostrocaudally extending medial region of the cerebral cortex with an *allocortical organization. By virtue of its structure and principal connections, it is considered a component of the “limbic system.” Cingulate NEP – Long neuroepithelial stretch along the medial bank of the *telencephalic superventricle that generates the neurons and glia of the *cingulate cortex. Claustrum (embryonic) – Subcortical gray matter adjacent to the *insula. During embryonic development, it is in the path of the *lateral migratory stream.

GLOSSARY Cochlear NEP – Neuroepithelial patch in the vicinity of the *ventral rhombic lip, the putative source of neurons and glia of the ventral and dorsal *cochlear nuclei. Cochlear nuclei – The dorsal and ventral auditory nuclei are targets of *nerve VIII auditory fibers. Both nuclei contribute axons to the *lateral lemniscus that terminate in the *nuclei of the lateral lemniscus, the *inferior colliculus, and the *medial geniculate body. Cortical NEP – Extensive and continuous neuroepithelial lining of the lateral, dorsal and medial banks of the *telencephalic superventricle. It is the sole constituent of the *cerebral cortex during the early embryonic period but, following a strict timetable and spatial gradient, it expands and then shrinks as a class of differentiating neurons and glia leave it to enter the *stratified transitional field and migrate to the *cortical plate. The cortical NEP is also the source of a secondary proliferative matrix, the *subventricular zone, and of a fate-restricted *glioepithelium and the cells that line the enduring *ependyma. Cortical nucleus (amygdala) – Also called the periamygdaloid cortex, part of the *corticomedial complex in the superficial amygdala. Cortical plate – The densely packed cellular band in the embryonic and fetal *cerebral cortex that later becomes the laminated *gray matter. It is situated between the future molecular layer, or *layer I and the subplate (the future layer VII). Corticofugal fibers (embryonic) – Collective term for the efferent fiber system (the traditional pyramidal tract) that originates in the cerebral cortex and terminates in subcortical structures. It is known by different names along its path from rostral to caudal: *internal capsule, *cerebral peduncle, *transpontine corticofugal tract, and corticospinal tract. The corticofugal tract begins to form during the end of the late first trimester but its fibers do not reach the spinal cord before the end of the second trimester. Corticoganglionic NEP – A transitional neuroepithelium at the junction between the *cortical NEP and the *basal ganglionic NEP and SVZ. Corticomedial complex (amygdala) – Portion of the *amygdala that includes the *anterior amygdaloid area, the *central nucleus, and the *cortical nucleus. Cricoid cartilage – A ring-shaped cartilage that forms the base of the larynx.

561 Cuneate fasciculus – A large fiber tract in the dorsolateral *spinal cord. It is composed of the ascending branch of the primary sensory axons of dorsal root ganglion cells that terminate topographically in the *cuneate nucleus. Cuneate nucleus (embryonic) – The target of the *cuneate fasciculus in the lower *medulla and the source of second-order somatosensory fibers that cross the midline and enter the contralateral *medial lemniscus. It is recognizable by GW8.

D Dentate gyrus – Curved small-celled component of the *hippocampus, interlocked with the large-celled *Ammon’s horn. Although the *dentate migration is recognizable by the end of the first trimester, the blades of the dentate gyrus do not form until the second trimester. Dentate migration – Precursors of granule cells of the *dentate gyrus that migrate from a patch of the *hippocampal NEP to form what will later become the secondary germinal matrix of the hippocampus, the *subgranular zone. Dentate nucleus (embryonic) – Lobulated and largest of the *cerebellar deep nuclei in the core of the cerebellar hemispheres, it is the principal source of efferent fibers of the *superior cerebellar peduncle. In the embryonic cerebellum, the early-generated neurons of the dentate nucleus are situated superficially and do not descend until after the late-generated *Purkinje cells migrate toward the surface to form the cerebellar cortex toward the early fetal period. Diagonal band of Broca – Oblique nucleus situated ventral to the medial *septum. It is subdivided into a vertical limb dorsally and a horizontal limb ventrally. Diencephalic NEP – The extensive neuroepithelial lining of the *diencephalic superventricle. Its different mosaic components, distinguished by their bilaterally symmetrical variable thicknesses and evaginations or invaginations into the ventricle, are the source of neurons and glia of the different nuclei of the *diencephalon. Diencephalic superventricle – Large midline component of the embryonic ventricular system that is later reduced to the small and narrow third ventricle. It is confluent laterally, by way of the foramen of Monro, with the *telencephalic superventricle, and caudally with the *mesencephalic superventricle. Its lining, the *diencephalic NEP, is the source of all the neurons and glia of the *diencephalon.

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GLOSSARY Diencephalon (embryonic) – Extensive forebrain region flanked laterally by the telencephalon and continuous caudally with the mesencephalon. Among its larger components are the *epithalamus and the *thalamus dorsally; the *preoptic area, *hypothalamus, and *subthalamus ventrally; and the *pretectum caudally. Its development precedes that of dorsal *telencephalon. Dorsal complex (thalamus) – Collective term for two structurally and functionally related dorsally situated thalamic regions, the *dorsomedial nucleus and the dorsolateral nucleus. Dorsal funiculus – See Dorsal white matter Dorsal gray matter (spinal cord) – Wing-shaped region of the spinal gray matter, the target of the local collaterals dorsal root afferent fibers. Its principal component is the small-celled substantia gelatinosa. The neurons of the dorsal gray matter originate in the *neuroepithelium flanking the transient dorsal spinal canal. Dorsal hippocampus (embryonic) – The portion of the *hippocampus located above the thalamus during the early stages of embryonic development. In the late second trimester, this region is displaced by the expanding *cerebral cortex laterally and then ventrally. Dorsal motor nucleus (X) (embryonic) – An early-forming column of parasympathetic preganglionic motor neurons dorsolateral to the *hypoglossal nucleus. Their axons leave the brain in cranial *nerve X and terminate in the parasympathetic ganglia supplying the viscera of the thoracic, pericardial, and abdominal cavities. See also Nerve X. Dorsal rhombic lip – The dorsolateral anchoring point of the *medullary velum that covers the expanding *rhombencephalic superventricle. Following the formation of the cerebellar *external germinal layer by the end of the first trimester, it is recognized as the *germinal trigone. The *ventral rhombic lip forms the ventrolateral anchoring point of the medullary velum.

Dorsal sensory nucleus (X) (embryonic) – A medial nucleus in the early-forming *solitary nuclear complex of the *medulla that lies dorsolateral to the *dorsal motor nucleus (X). See also Nerve X. Dorsal tegmental nucleus – Situated in the central gray dorsal to the *trochlear nucleus and extending caudally into the pons. It is targeted by fibers of the *mammillotegmental tract.

Dorsal white matter (spinal cord) – Medial fibrous component of the white matter situated between the wings of the *dorsal gray matter; also known as the dorsal column or the dorsal funiculus. It contains ascending somatosensory and proprioceptive fibers that terminate in the dorsal column nuclei of the medulla. In the upper spinal cord it has two distinguishable parts, the *gracile fasciculus medially, and the *cuneate fasciculus laterally. Dorsomedial nucleus (hypothalamus) – Area situated above the more distinct *ventromedial nucleus of the hypothalamus. Its principal connections are with the *bed nucleus of the stria terminalis and the *septum. Dorsomedial nucleus (thalamus) – Also known as the medial dorsal nucleus, this component of the *dorsal complex is situated between the internal medullary lamina and the periventricular gray. Its principal connections are with the *amygdala, the *hypothalamus, the *olfactory tubercle, and the *orbital gyrus. It is considered a paleothalamic component of the limbic system rather than as a neothalamic relay nucleus to the neocortex.

E Endopiriform nucleus (embryonic) – Small telencephalic nucleus deep to the *primary olfactory cortex and ventral to the *claustrum. The *lateral migratory stream percolates through this nucleus during development. Entorhinal cortex – Allocortical component of the *parahippocampal gyrus. It is bordered internally by the *subicular complex and is separated from the *neocortex in the maturing brain by the rhinal sulcus. It is the source of the perforant pathway to the *hippocampus. Ependyma – Layer of cuboidal cells that line the lumen of the permanent brain *ventricles and *central canal after dissolution of the proliferative *neuroepithelium. Epithalamic NEP – Neuroepithelial patch of the *diencephalic NEP, the putative source of neurons and glia of the *epithalamus. Epithalamus – Collective term for the region of the dorsal diencephalon consisting of the *habenular nuclei, the stria medullaris, and the *habenulo-interpeduncular tract. Ethmoid – A cranial bone that lies beneath the olfactory bult and forms part of the nasal septum.

GLOSSARY

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Eustachian tube – A canal between the oral cavity and the middle ear.

Fourth ventricle (embryonic) – See Rhombencephalic superventricle

External capsule – Slender fiber band situated between the *claustrum and the *putamen.

Frontal bone – Part of the skull that lies over the frontal lobes of the cerebral cortex.

External cuneate nucleus – Situated lateral to the *cuneate nucleus in the *medulla, also known as the accessory cuneate nucleus, it is the source of the cuneocerebellar tract. The nucleus relays somesthetic and proprioceptive information from anterior regions of the body to the *cerebellum.

Frontal lobe or cortex (embryonic) – Region of the developing *cerebral cortex that will grow into the large frontal lobe anterior to the central sulcus. The *orbital cortex is sometimes distinguished as a separate component.

External germinal layer (cerebellum) – Subpial, secondary germinal matrix of the cerebellar cortex, the source of its late-differentiating granule, stellate, and basket cells. It begins to form at the end of the first trimester and persists as a source of neurons over the surface of the human cerebellar cortex until the end of the second year of postnatal life.

Frontal NEP – Long stretch of the cortical neuroepithelium that is presumed to generate the cells of the *frontal lobe. Before settling in the *cortical plate, the migrating and sojourning neurons form a site-specific *stratified transitional field. Frontal nasal process – A primordium in the immature skull of the future frontal and nasal bones.

F

G

Facial motor nucleus – A large aggregate of somatic motor neurons in the ventrolateral pons dorsal to the *superior olive complex. It is the source of the motor fibers of *nerve VII that innervate the facial mimetic muscles. Subdivisions of this nucleus innervate different facial muscles.

Ganglionic narrows – Ventricular region where the *basal ganglionic eminences protrude into the lumen of the *telencephalic superventricle.

Fastigial nucleus (cerebellum) – A deep nucleus of the *cerebellum, also known as the medial cerebellar nucleus. It is the target of Purkinje cell axons that originate in the *vermis. Its axons contribute to the large efferent system that leaves the cerebellum. Foramen magnum – The large opening in the occipital bone that surrounds the spinal cord. Foramen of Monro (embryonic) – Large bilateral channels that connect the paired *telencephalic superventricles with the midline *diencephalic superventricle. Forel’s fields (embryonic) – Early differentiating subthalamic tegmental field (H1and H2) traversed by fibers of the *ansa lenticularis, lenticular fasciculus, and subthalamic fasciculus. Fornical GEP – Fate-restricted germinal extension of the hippocampal NEP, the glioepithelium that surrounds the fornix. It may be the germinal source of the oligodendrocytes of the fornix. Fornix – An early forming fiber tract of the *hippocampus that distributes fibers in the mature brain to the *septum and the thalamic *anterior complex, and terminates in the *mammillary body.

Germinal trigone (cerebellum) – Proliferative germinal matrix of the *dorsal rhombic lip with three prongs: the *cerebellar NEP, the *external germinal layer, and the stem cells of the rhombencephalic *choroid plexus. Glioepithelium (GEP) – Fate-restricted transient germinal matrix in the developing brain, the presumed source of neuroglia (astrocytes and oligodendroglia) precursors. There are two types of glioepithelia, the *perifascicular GEP that surround fiber tracts, such as the *fornical GEP, and another that covers the surface of the brain, the *subpial granular layer. Glioepithelia are easiest to recognize without special glial markers at sites of considerable distance from neuronal aggregates or their migratory routes. Glioepithelium/Ependyma (G/EP) – Transient proliferative linings of the ventricle that endure into adulthood and give rise to both glia and cells of the *ependyma. Globus pallidus – Component of the *striatum, situated medial to the *putamen, with an external (lateral) and internal (medial) segment. Pallidal fibers are the principal efferents from the striatum to the *thalamus, the *subthalamus, and the *tegmentum. Gracile fasciculus – A large fiber tract in the dorsomedial *spinal cord. It is composed of the branch of axons of dorsal root ganglia that convey somatosensory input

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GLOSSARY from lower parts of the body. The fibers terminate topographically in the *gracile nucleus. Gracile nucleus (embryonic) – Gray mass in the core of the *gracile fasciculus that receives input from that fiber tract. Axons of these neurons cross the midline in the *medulla, enter the contralateral *medial lemniscus. It is recognizable by GW8.

Gray matter (embryonic) – General term for the laminated component of the mature cerebral cortex with a high concentration of neuronal cell bodies and nerve processes but few myelinated fibers. In the embryonic cerebral cortex, the unlaminated cortical gray matter is known as the *cortical plate.

H Habenular nuclei (complex) – Mediodorsally situated nuclei in the posterodorsal *thalamus; sometimes distinguished from the thalamus proper as the *epithalamus. Its two distinct components are the medial and the lateral habenular nuclei. Habenular afferents come principally from the *septum and the *hypothalamus, and its efferents form the *habenulo-interpeduncular tract. Habenulo-interpeduncular tract (embryonic) – An early forming fiber bundle, also known as the fasciculus retroflexus, that originates in the *habenular nuclei. It courses through the posterior *thalamus and terminates in the *interpeduncular nucleus of the midbrain. Hippocampal NEP – Long medial stretch of the *cortical NEP, the putative neuroepithelial source of neurons and glia of the hippocampus. It has three distinctive parts, the *ammonic NEP, the *dentate migration, and the *fornical GEP. Hippocampal region – An inclusive term (also called the hippocampal formation) that includes not only the *hippocampus proper but also the *subicular complex and other components of the *parahippocampal cortex. Hippocampus – A distinctive allocortical (three-layered or oligolaminar) region formed by the interlocking *dentate gyrus and *Ammon’s horn. The hippocampus is continuous with the *subicular complex. The principal afferents of the hippocampus travel in the alveolar and perforant paths; its efferents leave by way of the *fimbria that join the *fornix. Honeycomb matrix – Strands of radially oriented fibers surrounded by migrating cells that may be present by the end of the first trimester in the *superior colliculus

and forms during the second trimester in the *stratified transitional field of the sensory areas of the developing *cerebral cortex. Hook bundle (embryonic) – Intracerebellar decussating fiber tract that originates in the deep nuclei of the cerebellum and presumed to leave it contralaterally as the uncinate fasciculus. A prominent fibrous region identified at the base of the cerebellum in GW8-GW9 specimens may be the sprouting fibers of this tract. Hypoglossal nucleus (XII) – A column of somatic motor neurons near the floor of the *fourth ventricle in the caudal medulla. Their axons form cranial *nerve XII that innervate the intrinsic and extrinsic muscles of the tongue. Hyoid bone – A small bone embedded in the throat muscles that lies below the tongue and above the larynx. Hypothalamic NEP – Stretch of the *diencephalic NEP, situated posterior to the preoptic NEP and ventral to the subthalamic NEP. It is the source of neurons and glia of the nuclei of the *hypothalamus. Hypothalamus (embryonic) – Early differentiating large diencephalic region that surrounds the ventral (or hypothalamic) portion of *diencephalic superventricle. It is continuous anteriorly with the *preoptic area and merges caudally with the midbrain *tegmentum. The hypothalamus contains a large number of discrete nuclei, among them the *suprachiasmatic nucleus, the *supraoptic nucleus, the *paraventricular nucleus, the *arcuate nucleus, the *ventromedial nucleus, the *dorsomedial nucleus, the *lateral tuberal nucleus, and the *mammillary body.

I Inferior cerebellar peduncle – Large fiber tract, also known as the restiform body. It contains ascending afferents to the cerebellum from the *spinal cord, the *external cuneate nucleus, the *inferior olive, and the *lateral reticular nucleus. Inferior collicular NEP – Distinctive neuroepithelial component of the *tectal NEP surrounding the posterior pool of the mesencephalic syperventricle and the source of neurons of the *inferior colliculus. Inferior colliculus – Paired inferior hillocks of the midbrain *tectum that receive primary, secondary, and higher order auditory afferents. The output of the inferior colliculus is mainly to the *medial geniculate body in the thalamus, but some axons extend to the primary auditory cortex in the *temporal lobe.

GLOSSARY Inferior olive – A distinctive convoluted region in the ventrolateral *medulla, with the large principal nucleus and the smaller accessory nuclei. Its axons join the contralateral *inferior cerebellar peduncle and terminate in the *cerebellar cortex as climbing fibers. Inferior olive (embryonic) – A compact cell aggregate in the lower *medulla, formed by neurons of the *posterior intramural migratory stream during the late first trimester. Its lamination does not begin until the end of the second trimester. Inferior vestibular nucleus – This nucleus begins caudally in the *medulla near the *external cuneate nucleus and extends rostrally along the medial border of the *inferior cerebellar peduncle. Infundibular recess – Small recess of the third ventricle that evaginates into the *infundibulum. Infundibulum – Stalk extending from the ventral *hypothalamus that forms a link with the pituitary gland. Insula (insular cortex) – Large buried neocortical region that is continuous internally with the *frontal, *parietal and *temporal lobes. Interhemispheric fissure – Longitudinal cleft that separates the two cerebral hemispheres. The corpus callosum that traversed it in the maturing brain has not yet started to form in the first trimester.

565 L Lateral geniculate body – Large posteroventral thalamic region, composed in the maturing brain of the laminated dorsal lateral geniculate nucleus and its capsule of ipsi- and contralateral *optic tract fibers. Its axons project, by way of the *visual radiation, to the ipsilateral *occipital lobe. Lateral geniculate nucleus (embryonic) – The neurons of this prominent thalamic nucleus appear to be generated dorsally in a distinct neuroepithelial locus and migrate ventrolaterally where they meet the incoming *optic tract fibers. Lateral hypothalamic area – An ill-defined fibrous region of the *hypothalamus with scattered neurons medial to the cerebral peduncle. It is traversed by many fiber tracts, including the *medial forebrain bundle. Lateral lemniscus – The fiber tract on the lateral surface of the *pons that contains secondary auditory fibers from the dorsal and ventral *cochlear nuclei and higherorder auditory fibers from the *superior olivary complex. The dorsal and ventral *nuclei of the lateral lemniscus are embedded within the fiber tract.

Internal capsule (embryonic) – Massive fiber tract between the *thalamus and *striatum, composed of *thalamocortical and *corticofugal fibers. It is continuous with the incipient *cerebral peduncle caudally.

Lateral migratory stream (cortical) – Tangentially migrating neurons and glia in the developing *cerebral cortex that leave dorsal *cortical NEP and migrate laterally and ventrally to the *insula, the *temporal lobe, and other telencephalic structures that lack a nearby germinal matrix. The bulk of the lateral migratory stream follows a trajectory outlined by the receding *subventricular zone between the *basal ganglia and the lateral cortex.

Interpeduncular nucleus – Midline mesencephalic structure above the interpeduncular fossa and between the *cerebral peduncles. It is the target of fibers of the *habenulo-interpeduncular tract.

Lateral nucleus (amygdala) – The most lateral nucleus in the *basolateral complex of the *amygdala. Cells from the *lateral migratory stream appear to enter the nucleus at the distinctive saw-toothed lateral edge.

Interpositus nucleus (cerebellum) – A deep cerebellar nucleus located between the *dentate nucleus and the *fastigial nucleus. It contains a lateral and a medial group of neurons, the emboliform near the *dentate nucleus, and the globosus near the *fastigial nucleus.

Lateral olfactory tract – See Olfactory tract

Isthmal canal – Channel that interconnects the *mesencephalic and *rhombencephalic superventricles. Isthmal NEP – The putative source of neurons and glia of the *isthmus. Isthmus – Transitional brain region between the *midbrain tectum, the *pons, and the *cerebellum.

Lateral preoptic area – An anterior continuation of the *lateral hypothalamic area in the *preoptic area. Lateral reticular nucleus – A relatively discrete group of neurons in the caudal medulla, dorsolateral to the *inferior olive. The neurons of this precerebellar relay nucleus receive topographic exteroceptive and proprioceptive afferents from the *spinal cord and project ipsilaterally to the *cerebellum via the *inferior cerebellar peduncle.

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GLOSSARY Lateral septal nucleus – An indistinct gray mass in the lateral *septum that is closely associated with the *fornix, which provides input to these neurons.

Meckel’s cartilage – Cartilage of the first pharyngeal arch that is associated with the formation of the mandible (lower jaw bone) and the ossicles of the middle ear.

Lateral tuberal nucleus (hypothalamus) – Two or three distinct spherical masses near the inferior surface of the *lateral hypothalamic area.

Medial accessory olive – A small nucleus in the *inferior olive complex that contains densely packed neurons along the lateral border of the medial lemniscus. It receives proprioceptive input from the spinal cord and its efferents reach the contralateral cerebellum (mainly the vermis) by way of the *inferior cerebellar peduncle.

Lateral ventricles – See Telencephalic superventricle Lateral vestibular nucleus – Also called Deiter’s nucleus. A collection of large neurons lying dorsolaterally along the wall of the *fourth ventricle. It receives primary sensory input from the vestibular ganglion via cranial *nerve VIII and its large neurons are the source of the vestibulospinal tract. Layer I (embryonic) – Cell sparse layer beneath the pia throughout the *cerebral cortex. This is the first cortical layer to develop and contains the earliest generated cortical neurons, including the *Cajal-Retzius cells. Locus coeruleus – Aggregate of large pigmented cells in the *pons. It is the major source of ascending and descending noradrenergic fibers that are widely distributed throughout the central nervous system. Luysian NEP – Putative source of neurons of the so-called *subthalamic nucleus (corpus Luysi) in the *hypothalamic NEP. The intramural migration of these neurons has been traced from the region of the formative *mammillary body to the level of the subthalamus dorsolaterally.

M Mammillary body – Distinctive region in the posteroventral hypothalamus, composed of the medial and lateral mammillary nuclei. Its principal afferents are from the *septum and *subiculum that course in the *fornix; its efferents form the *mammillothalamic and *mammillotegmental tracts. Mammillotegmental tract – Descending fiber bundle containing *mammillary body efferents to the brain stem, including the *dorsal tegmental nucleus. Mammillothalamic tract – Ascending fiber bundle containing efferents of the *mammillary body that terminate in the thalamic *anterior complex. Mandible – The lower jaw bone. Maxilla – The upper jaw bone.

Medial forebrain bundle – A diffuse fiber tract that extends from the *olfactory tubercle, through the *lateral hypothalamic area, to the *substantia nigra in the midbrain *tegmentum. Medial geniculate body – Principal thalamic relay station in the auditory pathway to the *cerebral cortex. Its afferents originate in the *trapezoid body, the *superior olivary complex, the * nuclei of the lateral lemniscus, and the *inferior colliculus. Its efferents form the auditory radiation that terminates in the *temporal lobe. Medial lemniscus – Large fiber bundle conveying tactile and other somatosensory input to the thalamus. It originates in the *gracile and *cuneate nuclei in the *medulla, crosses to the opposite side, ascends through the *pons and *midbrain, and terminates in the *ventral posterolateral and *ventral posteromedial nuclei of the thalamus. Medial lemniscus (decussation) – Also known as the sensory decussation, it is composed of ascending fibers of the medial lemniscus that cross to the opposite side in the medulla. Medial longitudinal fasciculus – A dorsomedial tract in the *midbrain, *pons, and *medulla that contains ascending and descending vestibular fibers coursing beneath the *oculomotor nuclear complex, the *trochlear nucleus, the *abducens nucleus, and the *hypoglossal nucleus. It turns ventrally in the posterior medulla and extends into the ventral funiculus of the cervical spinal cord. Medial preoptic area – A rounded mass of neurons implicated in reproductive functions. Medial septal nucleus – An indistinct nucleus in the midline septum that is continuous with the vertical limb of the *diagonal band of Broca. Medial vestibular nucleus – Component of the *vestibular nuclear complex situated underneath the *fourth ventricle medial to the other vestibular nuclei. Its

GLOSSARY

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neurons receive primary sensory input from the vestibular ganglion via cranial *nerve VIII and project to the cerebellum. Median preoptic nucleus – A small nucleus in the *preoptic area that forms a narrow cap around the *anterior commissure in the midline. Medulla (embryonic) – Region of the neuraxis, also known as the medulla oblongata, surrounding the posterior *rhombencephalic superventricle and bounded by the *pons rostrally and the *spinal cord caudally. An extremely heterogeneous region containing sensory, somatic motor, and visceral motor nuclei as well as several ascending, descending, and decussating fiber tracts. Medullary NEP – Extensive neuroepithelial site that lines the variegated caudal bank of the *rhombencephalic superventricle. Its several subdivisions are the source of neurons and glia of the different sensory, relay and motor nuclei of the medulla. Medullary velum – Membranous roof of the expanding *rhombencephalic superventricle. Its lateral anchor to the *rhombencephalon is known as the *dorsal rhombic lip and the *ventral rhombic lip, and its inner surface serves as a substratum for the expanding rhombencephalic choroid plexus. Mesencephalic NEP – The extensive neuroepithelium that lines the large *mesencephalic superventricle. Its major divisions are the anterior *pretectal NEP, the dorsal *tectal NEP, the ventral *tegmental NEP, and the posterior *isthmal NEP. Subdivisions are the source, among others, of neurons and glia of the *superior colliculus and *inferior colliculus dorsally, and of the *red nucleus, the *oculomotor nuclear complex, and several tegmental nuclei ventrally. Mesencephalic nucleus (V) – Large neurons scattered along the lateral border of the *central gray of the midbrain and pons. They are primary sensory neurons that enter the brain from the periphery early in development relaying proprioceptive information from the muscles of mastication. Mesencephalic superventricle – Greatly inflated lumen of the embryonic *mesencephalon, situated between the *diencephalic superventricle rostrally and the *rhombencephalic superventricle caudally. The connection with the latter is by way of the *isthmal canal. It shrinks in the maturing brain into the narrow aqueduct. Mesencephalon (embryonic) – Anterior part of the developing brainstem surrounding the *mesence-

phalic superventricle consisting of the *pretectum and *tectum dorsally, and of the *tegmentum ventrally. Among the intermediate components of the mesencephalon are the *central gray, the *oculomotor nuclear complex, the *red nucleus and the *reticular formation. Meyer’s loop – Part of the *visual radiation that takes a sharp curve in the *temporal lobe as it proceeds to the *occipital lobe. Midbrain – See Mesencephalon Middle cerebellar peduncle – Massive tract of *pontocerebellar fibers that originate in the *pontine gray and enter the cerebellum posterolateral to the *inferior cerebellar peduncle. The earliest fibers of this system emerge at the end of the first trimester. Motor nucleus, V – See Trigeminal, motor nucleus Motor nucleus, VII – See Facial, motor nucleus

N Nasal conchae – Scroll-like processes of the *ethmoid and *maxilla that project into the lateral nasal cavity. Neocortex (embryonic) – Portion of the cerebral hemispheres that develops a “six-layered” (multilaminar) cortical *gray matter. Neocortical development begins with the expansion of the primordial *cortical NEP devoid of differentiated neurons. It is followed by the formation of the *cortical plate, the *subventricular zone, and the different layers of the *stratified transitional field, in association with the ingrowth of *thalamocortical fibers, the outgrowth of *corticofugal fibers and the onset of the formation of intracortical connections. The principal divisions of the neocortex are the *frontal lobe, the *paracentral lobule, the *parietal lobe, the *temporal lobe, and the *occipital lobe. Neocortical NEP – Extensive *neuroepithelium that lines the lateral and dorsal aspects the *telencephalic superventricles. The proliferating neocortical NEP cells are the source of neurons and glia that migrate to the nearby *cortical plate by way of the *stratified transitional field. Some of its cells may move to more distant sites by way of the *lateral migratory stream. Nerve I – See Olfactory nerve Nerve II – See Optic nerve Nerve III (oculomotor) – Cranial motor nerve originating in the *oculomotor nuclear complex. It innervates

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GLOSSARY all the extraocular muscles – except the lateral rectus and superior oblique – and the skeletal muscles of the eyelid, the smooth sphincter muscles of the iris, and the ciliary muscles of the lens. Nerve IV (trochlear) – Cranial motor nerve composed of axons of the *trochlear nucleus that innervates the superior oblique muscle of the eye. This nerve is unique because it exits from the dorsal surface of the *midbrain behind the *inferior colliculus. Nerve V and ganglia (trigeminal)– A mixed sensory and motor cranial nerve that has three peripheral branches, the ophthalmic, the maxillary, and the mandibular. All three branches contain peripheral sensory fibers from the trigeminal ganglion that terminate in the *trigeminal principal sensory nucleus, the *trigeminal spinal nucleus, and the substantia gelatinosa in upper cervical segments of the *spinal cord. A bundle of fibers in the mandibular branch, originating in the *trigeminal motor nucleus, innervates the muscles of mastication. Nerve VI (abducens) – A motor cranial nerve that originates in the *abducens nucleus and emerges near the midline at the caudal border of the *pons. The fibers innervate the lateral rectus muscle of the eye. Nerve VII and ganglion (facial) – A mixed sensory and motor nerve, the facial nerve has three components. Primary sensory gustatory fibers from the geniculate ganglion enter the *solitary tract and nucleus. Somatic motor fibers from the *facial motor nucleus innervate the mimetic muscles. Visceral motor (parasympathetic) fibers from preganglionic neurons of the indistinct salivatory nucleus target the pterygopalatine and submandibular ganglia. Nerve VIII and ganglia (cochlear, vestibular) – A sensory cranial nerve that contains primary auditory afferents from the spiral ganglion in the cochlea and primary vestibular afferents from the vestibular (Scarpa’s) ganglion. The auditory afferents terminate in the dorsal and ventral *cochlear nuclei; the vestibular afferents terminate in the nuclei of the *vestibular nuclear complex and some reach the *cerebellum. Nerve IX and ganglia (glossopharyngeal) – A mixed sensory and motor cranial nerve. The sensory part of nerve IX originates in the superior and inferior ganglia, and relays gustatory input from the posterior third of the tongue and visceral sensory input from the tonsils, the Eustachian tube, and the carotid sinus. These fibers enter the solitary tract and terminate in the *solitary nucleus. The somatic motor part of nerve IX originates in the *nucleus ambiguus and innervates the pharyngeal and laryngeal muscles. The

visceral motor fibers from parasympathetic preganglionic neurons in the salivatory nucleus terminate in the otic ganglion. Nerve X and ganglia (vagus) – A mixed sensory and motor nerve, with some somatic and many visceral afferents and efferents associated with the craniosacral parasympathetic ganglia. The sensory fibers originate peripherally in the superior and inferior ganglia and are widely distributed throughout the body, including the pharynx, larynx, trachea, esophagus, and all the thoracic and abdominal viscera. They terminate centrally in the *solitary nucleus and at other medullary sites. Most of its preganglionic motor neurons are located in the *dorsal motor nucleus (X). Nerve XI (accessory) – This motor nerve has a cranial and a spinal component. The cranial fibers originate in the *nucleus ambiguus and innervate the muscles of the larynx and pharynx. The spinal motor fibers originate in a motor column of the cervical *spinal cord and innervate the sternocleidomastoid and upper trapezius muscles. Nerve XII (hypoglossal) – A somatic motor cranial nerve that originates in the *hypoglossal nucleus and innervates the intrinsic and extrinsic muscles of the tongue. Neuroepithelium (NEP) – Pluripotential pseudostratified tissue of neural stem cells that extends from the frontal pole rostrally to the last segment of the spinal cord caudally and is the source of all neurons and neuroglia of the developing central nervous system. The NEP cells initially form the neural plate, then fold dorsally and fuse to form the neural tube (future spinal cord) caudally and the variegated cephalic vesicles (the future brain) rostrally. After that closure, the lumen of the cephalic vesicles expands enormously to form the *rhombencephalic, *mesencephalic, *diencephalic, and *telencephalic superventricles. This expansion provides the space for the mitotic division of NEP cell nuclei that have to shuttle to the fluidfilled lumen to undergo mitosis. The continuous but variegated cephalic NEP lining the ventricles has a mosaic organization, being composed of bilaterally symmetrical long and intermediate stretches, and short patches that give rise to neurons and glia of different brain regions, distinct structures, and specific cell types. Examples of long stretches are the *cortical NEP and the *cerebellar NEP; of intermediate stretches, the *thalamic NEP and the *hypothalamic NEP of the inclusive *diencephalic NEP; and of short patches, the *ammonic NEP and *dentate NEP of the inclusive *hippocampal NEP. The primary NEP is also the source of several *secondary germinal matrices that generate microneurons with locally arboriz-

GLOSSARY ing axons. Finally, as neurogenesis winds down the pluripotential NEP is transformed at many sites into a *glioepithelium, such as the *fornical GEP, or into the *ependyma that lines the enduring ventricles. Nuclei of the lateral lemniscus – Both components of this system, the dorsal nucleus and the ventral nucleus, receive their major input from the *cochlear nuclei and the *superior olivary complex by way of the *lateral lemniscus. Both nuclei are connected with the *inferior colliculus and the *medial geniculate body. Nucleus accumbens – Ganglionic component of the ventral telencephalon ventromedial to the *striatum. It is distinguished from the striatum by its cellular organization, molecular composition, and intimate connections with the *hypothalamus, *amygdala, and other regions of the limbic system. Nucleus ambiguus – Aggregate of somatic motor neurons that form a thin column in the ventrolateral medulla. Its axons innervate the muscles of the larynx and pharynx via *nerve IX.

O Occipital lobe or cortex (embryonic) – Posterior region of the developing cerebral cortex that will be the target of *visual radiation fibers from the *lateral geniculate body and the *pulvinar. Occipital NEP – Putative neuroepithelial source of the neurons and glia of the occipital lobe. It is flanked in the fetal neocortex by the occipital *subventricular zone and the *stratified transitional field. Oculomotor nerve – See Nerve III Oculomotor nuclear complex – Situated at the base of the periaqueductal *central gray, the cell columns of this complex extend from the anterior pole of the *superior colliculus rostrally to the *trochlear nucleus caudally. Its somatic motor nuclei innervate the medial rectus, inferior rectus, superior rectus and inferior oblique muscles of the eye, and are associated with the fibers of the *medial longitudinal fasciculus. Most prominent of its autonomic (preganglionic) components is the dorsally located Edinger-Westphal nucleus. Odontoid process – A tooth-like projection on the superior surface of the *axis that articulates with the *atlas. Olfactory bulb – Laminated brain structure where the first-order fibers of the *olfactory nerve terminate and the second-order fibers of the *olfactory tract orig-

569 inate. It is composed of three classes of neurons: large mitral cells, the intermediate tufted cells, and the small granule cells. Olfactory NEP – Putative source of the earlier-generated mitral and tufted cells of the olfactory bulb that lines the olfactory recess of the *telencephalic superventricle. The later-generated granule cells are supplied by the *rostral migratory stream. Olfactory nerve (embryonic) – Composed of the fine axons of bipolar cells in the olfactory epithelium that terminate in the *olfactory bulb. The nerve is recognizable in GW7.5 specimens. Olfactory tract – Large fiber bundle of second-order fibers that originate in the *olfactory bulb with two parts, the larger lateral olfactory stria and the smaller medial stria. The fibers of the lateral stria terminate in the *olfactory tubercle, the *primary olfactory cortex, and *corticomedial complex of the amygdala. Olfactory tubercle – Allocortical area in the ventral telencephalon between the *diagonal band of Broca and the *nucleus accumbens. Its input comes mainly from the lateral *olfactory tract. Optic chiasm (embryonic) – Site of crossing of fibers of the *optic nerve. Fibers from the nasal half of each retina cross here to the opposite side while those from temporal half proceed uncrossed. The earliest crossing fibers appear in GW7.5 specimens. Optic nerve – This large fiber tract contains the axons of retinal ganglion cells. Beyond the *optic chiasm it is called the *optic tract. Optic tract – Large bundle of crossed and uncrossed retinal afferent fibers. In the human brain the majority of the fibers terminate in the *lateral geniculate body; others proceed to the *superior colliculus, the *suprachiasmatic nucleus, the *pretectum, and some other structures. Orbital cortex – Ventromedial region of the *frontal lobe with afferents from the thalamic dorsomedial nucleus and efferents to the *preoptic area and the *hypothalamus. Orbitofrontal NEP – Putative source of neurons and glia of the orbitofrontal cortex. Orbitosphenoid – A cartilaginous structure in the developing skull that surrounds the *optic nerve and eventually becomes the lesser wing of the sphenoid bone.

570 P Palatal process – Part of the *maxilla that forms the hard palate in the roof of the mouth.

GLOSSARY lobe. It is flanked by the parietal *subventricular zone and *stratified transitional field.

Pallidum – See Globus pallidus

Perifascicular GEP – Fate-restricted glioepithelium, the presumed source of oligodendrocytes that surround a fiber tract, such as the *fornical GEP.

Parabrachial nucleus – Dorsolateral pontine structure with indistinct boundaries that surrounds the *superior cerebellar peduncle. Its principal input comes from the *solitary nucleus and its efferents target the *ventral posteromedial nucleus of the thalamus, the *amygdala, and the *insular cortex.

Periventricular complex (thalamus) – The thalamic region surrounding the *mesencephalic superventricle that will become partitioned as the paracentral, parafascicular, paratenial, paraventricular, and reuniens nuclei. Its principal connections are with limbic system; connections with the *neocortex are sparse.

Paracentral lobule (embryonic) – Incipient cortical region that becomes later divided by the central sulcus into the precentral gyrus and the postcentral gyrus. The term is used to distinguish this site of the presumptive motor and sensory projection areas from the *frontal lobe anteriorly and the *parietal lobe posteriorly.

Petrous temporal bone – Part of the temporal bone that contains the internal ear and semicircular canals.

Paracentral NEP – Putative neuroepithelium of the *paracentral lobule in the developing neocortex. It is flanked by the paracentral *subventricular zone and the paracentral *stratified transitional field. Parahippocampal cortex (embryonic) – Allocortical and neocortical region between the *hippocampus and the *temporal lobe that will become the parahippocampal gyrus. Its subdivisions are the *subicular complex and the *entorhinal cortex. Parahippocampal NEP – Putative source of the neurons and glia of the parahippocampal gyrus. It is flanked by the parahippocampal *subventricular zone and the parahippocampal *stratified transitional field. Paraventricular nucleus (hypothalamus) – Prominent neuroendocrine structure abutting the third ventricle with a magnocellular and a parvocellular division. The large neurons of the paraventricular nucleus are the source of oxytocin and vasopressin that reach the posterior pituitary gland by axoplasmic flow. The small neurons of the nucleus are the source of releasing hormones conveyed to the portal vessels of the median eminence. Parietal bone – A cranial bone in the skull that eventually lies over the parietal lobe of the cerebral cortex. Parietal lobe of cortex (embryonic) – Region of the developing neocortex bounded anteriorly by the *paracentral lobule and posteriorly by the *occipital lobe. Parietal NEP – Long stretch of the cortical neuroepithelium containing the neural stem cells of the *parietal

Pineal gland – Midline endocrine gland connected by its stalk to the pineal recess of the dorsal *mesencephalic superventricle. It secretes melatonin and other indoleamines. It is believed to receive indirect visual input from the retina. Piriform cortex – See Primary olfactory cortex Pituitary gland – See Anterior pituitary gland; Posterior pituitary gland Pons (embryonic) – Developing brainstem region, situated between the *isthmus and the *medulla, that surrounds the anterior part of the *rhombencephalic superventricle. It contains some early ascending, descending and decussating fiber tracts, the sensory and motor nuclei of some of the cranial nerves, and the *reticular formation. Pontine gray (embryonic) – This massive basal region of the *pons is just beginning to form as neurons of the *anterior extramural migratory stream start to settle and the earliest descending *corticofugal fibers reach the site. Corticofugal axons that collateralize here are the principal afferents of the pontine gray neurons that are, in turn, the source of the pontocerebellar fibers of the *middle cerebellar peduncle. Posterior commissure (embryonic) – Early forming decussating fiber tract in the dorsal *mesencephalon that interconnects several nuclei in the *pretectum and *tectum. Posterior complex (thalamus) – Division of the thalamus that includes the *lateral geniculate body, the *pulvinar, and the *medial geniculate body. The neurons of the lateral geniculate body and pulvinar appear to originate in a distant source and migrate from dorsal to ventral over an extended period.

GLOSSARY Posterior intramural migratory stream – Stream of young neurons that migrate inside the parenchyma from their source in the posterior *precerebellar NEP dorsally, to form the *inferior olive in the ventral medulla. Posterior extramural migratory stream – Stream of young neurons that originate in the posterior *precerebellar NEP, migrate outside the parenchyma, cross the midline ventrally, and settle on the opposite side to form the contralateral *external cuneate nucleus and *lateral reticular nucleus. Posterior pituitary gland – The posterior lobe of the pituitary gland, also known as the neurohypophysis, is the terminal and storage site of hypothalamic neurosecretory cells. Precerebellar NEP – Dorsally situated neuroepithelium that lines the *rhombencephalic superventricle in the vicinity of the ventral rhombic lip and is the source of neurons of the *precerebellar nuclei. Neurons of its rostral division migrate in the *anterior extramural migratory stream and settle in the *pontine gray and the *reticular tegmental nucleus. Neurons of its posterior division form two migratory streams, the *posterior intramural migratory stream that forms the *inferior olive, and the *posterior extramural migratory stream that crosses to the opposite side and forms the *lateral reticular nucleus and the *external cuneate nucleus. Precerebellar nuclei – A series of nuclei in the *medulla and *pons that provide massive higher-order input to the *cerebellum, including the *inferior olive, the *external cuneate nucleus, the *lateral reticular nucleus, and the *pontine gray. Premammillary area – Region with ill-defined boundaries anterior to the *mammillary body in the *hypothalamus. Preoptic area (embryonic) – Early developing midline region surrounding the preoptic recess of the *diencephalic superventricle. It is contiguous anteriorly with the ventral telencephalon and blends posteriorly with the anterior *hypothalamus. It is implicated in the regulation of sexual behavior and reproductive functions. Prepositus nucleus – Situated in the dorsomedial *medulla, it extends from the anterior part of the *hypoglossal nucleus to the posterior part of the *abducens nucleus.

571 Presubiculum – *Allocortical component of the *parahippocampal gyrus between the *subiculum and the *parasubiculum. Pretectum – Dorsal area between the posterior *thalamus and the *superior colliculus with an early forming fiber system, the *posterior commissure. Primary olfactory cortex – Allocortical region, also called the piriform lobe, where fibers of the lateral olfactory tract terminate. It is situated rostral to the *entorhinal cortex and includes the prepiriform area along the rhinal fissure and the periamygdaloid area. Primordial plexiform layer (cortical) – The first transitional layer to appear outside of the *cerebral cortical NEP that contains *Cajal-Retzius cells and *subplate neurons. The *cortical plate forms within its boundaries later on in development. Principal sensory nucleus (V) – See Trigeminal, principal sensory nucleus Pulvinar (thalamus) – Large nucleus of the thalamic *posterior complex. Its subdivisions send fibers to various regions of the *parietal lobe, *occipital lobe, *temporal lobe, and frontal lobe It has been implicated in multisensory integration. Purkinje cells (embryonic) – These neurons, which form a monolayer in the maturing cerebellar cortex, are generated in the *cerebellar NEP towards the end of the first trimester, subsequent to the production of the *cerebellar deep nuclei neurons. Hence they are initially situated beneath the layer of deep neurons adjacent to the cerebellar NEP. Later they migrate toward the surface of the formative cerebellar cortex as the *external germinal layer forms there. Putamen – Lateral component of the *striatum. It lies between the *external capsule and the *globus pallidus. It is the major source of striatal efferents to the *thalamus, *subthalamic nucleus, *substantia nigra, and *tegmentum.

R Raphe migration – Streams of cells that originate in the dorsal *medullary NEP and are later distributed in the midline of the ventral medulla. Raphe nuclear complex – Several smaller and some larger cell aggregates that extend in and near the midline from the *midbrain rostrally to the *medulla caudally. The raphe cells are the principal source of serotonincontaining fibers distributed along the entire neuraxis from the forebrain to the *spinal cord. They

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GLOSSARY are involved, as neuromodulators, in the regulation of sleep, wakefulness and emotional arousal. Red nucleus (embryonic) – A prominent nucleus in the maturing brain with a small-celled (parvocellular) and a large-celled (magnocellular) division. It is recognizable during the first trimester in the vicinity of a germinal patch, identified as the *rubral NEP. The associated fibers may be early elements of the *superior cerebellar peduncle. Reticular belt (thalamus) – Distinctive component of the thalamus; it is coextensive with the thalamic *reticular nucleus. Reticular formation – A large collection of scattered neurons, enmeshed in a complex network of fibers, in the core of the *medulla, *pons, and *mesencephalon. Reticular tegmental nucleus (embryonic) – Situated dorsal to the *pontine gray, this *precerebellar nucleus, also known as the nucleus reticularis tegmenti pontis, begins to form toward the end of the first trimester ahead of the pontine gray.

Reticular nucleus (thalamus, embryonic) – An early formong thin belt of cells and fibers between the wall of the *thalamus and the *internal capsule. Virtually all fibers that interconnect the thalamus and the cerebral cortex traverse the thalamic reticular nucleus. Rhombencephalic superventricle – The greatly inflated NEP-lined lumen of the *rhombencephalon, situated between the *isthmal canal of the *mesencephalic superventricle rostrally and the central canal of the *spinal cord caudally. Rhombencephalon (embryonic) – An extremely heterogeneous hindbrain region lining the *rhombencephalic superventricle, that includes the developing *cerebellum, *pons, and *medulla. Rostral migratory stream – A large stream of mitotic and postmitotic cells in the forebrain extending from the cerebral *subventricular zone to the *olfactory bulb. It is a source of late generated neurons and persists after the NEP has receded or disappeared. Rubral NEP – A distinctive neuroepithelial patch lining the *mesencephalic superventricle and situated between the *tectal NEP and the *tegmental NEP. It is the putative source of neurons of the early generated neurons of the *red nucleus.

S Secondary germinal matrix – Layer or field of proliferative precursors of neurons and glia abutting or some distance from the primary *neuroepithelium. These fate-restricted stem cells are progeny of the NEP and persist for varying periods postnatally (some into adulthood). Examples of secondary germinal matrices are the *external germinal layer of the cerebellum, the *subventricular zone of the neocortex, the *subgranular zone of the dentate gyrus, and the *striatal subventricular zone. Typically, the secondary germinal matrices are the source of late-generated shortaxoned interneurons, or microneurons. Sella turcica – Part of the *sphenoid bone that surrounds the pituitary gland. Septum – Midline telencephalic structure with two components, the *medial and *lateral nuclei. Its principal connections are with the *hippocampus and the *hypothalamus by way of the *fornix. The septum is a focal component of the limbic system. Sojourn zone – Transient cellular layers formed by neurons that halt their migration for varying periods before they proceed to their final destination. They have been recognized at various sites, among them the *stratified transitional field of the cerebral cortex and the *cerebellar transitional field. It is hypothesized that the sojourn zones are sites where transient or enduring connections are made as the coarse circuitry of a brain region is established. Solitary tract and nucleus (embryonic) – The solitary tract is an early forming medullary fiber system that may contain the primary sensory fibers of cranial *nerves VII, IX, and X that convey gustatory (VII and IX) and visceral-sensory information (IX and X) to the solitary nucleus. The *dorsal sensory nucleus of nerve X and the *commissural nucleus of nerve X are part of this nuclear complex. Sphenoid – The skull bone that lies mainly beneath the hypothalamus, basal telencephalon, and mesencephalon. It contains the *alisphenoid and *orbitosphenoid processes and the *sella turcica around the *pituitary gland. Spinal cord – Caudal tubular component of the central nervous system that surrounds the *central canal. Its core of gray matter (the dorsal horn, intermediate gray and ventral horn) and surrounding white matter (the dorsal, lateral and ventral funiculi) blend rostrally with the lower medulla. Spinal nucleus (V) – See Trigeminal, spinal nucleus

GLOSSARY Spinal tract (V) – See Trigeminal, spinal tract Squamous temporal bone – The flat part of the *temporal bone that covers the *temporal lobe of the cerebral cortex. Stratified transitional field (STF) – Transient component of the fetal *cerebral cortex, sandwiched between the *neuroepithelium and the *cortical plate. By the second trimester (GW13), illustrated in Volume 3, it has six layers of alternating cells and fibers (STF1 to STF6) that vary in their configuration in different lobes of the cerebral cortex. In the oldest specimens illustrated in this Volume (GW11), the STF has only two layers (STF1, 4/5) or at most three layers (STF1, 4, 5). The cell-rich STF4/5 is composed of sojourning neurons, and the cell-sparse STF1 of incoming *thalamocortical fibers with possibly some outgoing *corticofugal fibers.

573 Subcommissural organ – A highly vascularized circumventricular neuroendocrine organ located beneath the *posterior commissure in the roof of the *mesencephalon. Subgranular zone (hippocampus) – A long-persisting secondary germinal matrix beneath the *granular layer of the dentate gyrus, the source of late generated dentate granule cells. It is recognizable in incipient form by the end of the first trimester. Subicular complex – Collective term for the *parasubiculum, the *presubiculum, and the *subiculum in the *parahippocampal cortex. Subpial granular layer – Transient cellular layer between *layer I and the pia in some regions of the developing *cerebral cortex. It may be a source of cortical astrocytes.

Stria medullaris (thalamus) – Mediodorsal fiber bundle in the diencephalon coursing in an anteroposterior direction and terminating in the *habenular nuclei.

Subplate – A poorly-defined layer beneath the *cortical plate. It contains neurons that are the transient pioneer residents of the cortical plate.

Stria terminalis – Arched fiber bundle that originates in the *amygdala, courses along the medial surface of the *caudate nucleus, and terminates in the *bed nucleus of the stria terminalis, the anterior *hypothalamus, and the *preoptic area.

Substantia innominata – Extensive telencephalic area with indistinct boundaries beneath the *globus pallidus. A prominent component of the substantia innominata is the *basal nucleus of Meynert.

Striatal NEP – Primary germinal source of neurons of the *caudate nucleus, *putamen, and *globus pallidus. It has a large anterolateral and anteromedial division, also known as the lateral and medial eminences, and a small posterior division that generates the neurons of the tail of the caudate nucleus. The posterior striatal NEP is continuous with the *amygdaloid NEP Striatal subventricular zone (SVZ) – A massive *secondary germinal matrix flanking the striatal NEP. It generates the bulk of the neurons of *caudate nucleus, *putamen and *globus pallidus. It may also be the source of some cortical neurons. Striatum – Term used for two components of the *basal ganglia: the *caudate nucleus and the *putamen. Strionuclear GEP – Fate-restricted glioepithelium, the putative source of the glia of the stria terminalis, stria medullaris, and possibly other nearby fiber tracts. Strionuclear NEP – Putative neuroepithelial source of the neurons and glia of the *bed nucleus of the stria terminalis. It is situated beneath the *striatal NEP in a notch of the *lateral ventricle near the *foramen of Monro.

Substantia nigra (embryonic) – A pigmented *midbrain tegmental structure in the maturing brain at the base of the *cerebral peduncle. It has two components, the dopaminergic pars compacta, and the GABAergic pars reticulata. Subthalamic NEP – Neuroepithelial patch between the *thalamic NEP and the *hypothalamic NEP. It is also identified as the Forelian NEP to distinguish it from the *Luysian NEP. Subthalamic nucleus – Biconvex diencephalic structure, also known as corpus Luysii, situated above the substantia nigra between the *zona incerta and the base of the *internal capsule. It has extensive reciprocal connections with the *globus pallidus, hence it is considered a component of the *basal ganglia circuitry. Subthalamic lesions produce persistent choroid movements (hemiballism) in the arms, legs and face. Subthalamus (embryonic) – Diencephalic region situated between the *thalamus dorsally and the *hypothalamus ventrally. Its major components, *Forel’s fields and the *zona incerta are recognizable in late first trimester fetuses. Subthalamic nucleus NEP – See Luysian NEP

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GLOSSARY Subventricular zone (SVZ) – Secondary germinal matrix, derived from the primary *neuroepithelium. The SVZ flanks the NEP during early development and then abuts the ependyma when the NEP dissolves. The nuclei of proliferative SVZ cells, unlike the nuclei of NEP cells, do not shuttle to the lumen of the ventricle during mitosis. Prominent SVZs in the telencephalon are found in the *cerebral cortex and the *striatum. Superior cerebellar peduncle (embryonic) –A large fiber tract that originates mainly in the *dentate nucleus and *interpositus nucleus. It is present by the end of the first trimester in the formative cerebellum and appears to reach the level of the *red nucleus.

Superior colliculus (embryonic) – Anterior component of the *tectum (known in lower vertebrates as the optic lobe) is a direct target of a small complement of optic nerve fibers. Several waves of migrating cells suggest its imminent lamination by the end of the first trimester. There are indications that the entering optic fibers form a *honeycomb matrix superficially. Superior olivary complex – A group of neurons in the ventrolateral posterior *pons that receive auditory input from the dorsal and ventral *cochlear nuclei. Ipsilateral and contralateral fibers of the complex join the *lateral lemniscus and terminate in the *inferior colliculus and in the *medial geniculate body. Superventricles – The small ventricles of the mature central nervous system – known as the lateral and third ventricles in the forebrain, the aqueduct in the midbrain, the fourth ventricle in the pons and medulla, and the central canal in the spinal cord – are a continuous system of narrow channels lined by an enduring *ependyma and filled with cerebrospinal fluid. In contrast, the ventricles of the embryonic and early fetal brain are greatly inflated, balloon-like cisterns, hence the term superventricles, lined by a continuously changing germinal matrix, the *neuroepithelium and a fetal *choroid plexus that differs from its mature counterpart. Its large and variegated components are distinguished as the *telencephalic, the *diencephalic, the *mesencephalic, and the *rhombencephalic superventricles. Suprachiasmatic nucleus (hypothalamus) – Small, paired midline structure above the *optic chiasm. It is implicated in the photic entrainment of the circadian rhythm. Supramammillary area (hypothalamus) – Hypothalamic region that caps the *mammillary body. Experimental studies in animals indicate that its cells project to the *dentate gyrus of the hippocampus.

Supraoptic nucleus (hypothalamus) – Located above the optic tract lateral to the optic chiasm. The large secretory neurons of this nucleus produce arginine vasopressin and oxytocin that are conveyed by axoplasmic flow to the posterior lobe of the pituitary gland.

T Tectal NEP – Extensive mesencephalic, smooth-surfaced NEP that lines the dorsal bank of the *mesencephalic superventricle. Its larger anterior part generates the neurons and glia of the *superior colliculus, its smaller posterior part that of the *inferior colliculus. Tectum (embryonic) – Dorsal region of the *mesencephalon, consisting of the earlier developing *superior colliculus anteriorly and the later developing *inferior colliculus posteriorly. Tegmental NEP – The variegated ventral stretch of the *mesencephalic NEP that contains shorter patches that produce neurons and glia for various tegmental nuclei, such as the *substantia nigra and the *ventral tegmental area. Tegmentum (embryonic) – Ventral and ventrolateral region of the *mesencephalon and *rhombencephalon with indistinct boundaries. In addition to several brainstem nuclei, it contains many early-forming ascending, decussating, and descending fiber tracts. Some tegmental nuclei have been implicated in somatomotor and visceromotor functions. The onset of development of some components of the tegmentum appear to antedate that of the *tectum. Telencephalic superventricle – The largest component of the superventricles that begins to expand during the early first trimester and shrinks during the third trimester. It is bounded laterally, dorsally and dorsomedially by the long stretch of the *cortical NEP, and ventromedially and ventrally by the shorter *olfactory, *septal, *striatal, *hippocampal and *amygdaloid NEPs. A large portion of its lumen is occupied by the fetal telencephalic *choroid plexus. Telencephalon (embryonic) – Extensive forebrain region consisting of both cortical and subcortical components whose neurons and glia are produced by NEP stretches and patches lining the *telencephalic superventricle. Temporal bone – A cranial bone in the skull that covers the *temporal lobe of the cerebral cortex and contains the internal ear and semicircular canals.

GLOSSARY Temporal lobe or cortex (embryonic) – Lateral and ventral portion of the developing cerebral cortex that will later become separated from much of the rest of the cerebral hemisphere by the lateral fissure. Temporal NEP – Putative source of neurons and glia of the *temporal lobe. It is flanked during fetal development by the temporal *subventricular zone and the temporal *stratified transitional field. Tenia tecta – Components of the *cerebral cortex that extend into the dorsomedial *septum (dorsal tenia tecta) and medial olfactory peduncle (ventral tenia tecta). Thalamic NEP – Stretch of the *diencephalic NEP between the *epithalamic and the *hypothalamic NEPs. Its mosaic divisions are the putative source of neurons and glia of the diverse nuclei of the *thalamus. Thalamocortical fibers (embryonic) – Collective term for the large afferent tracts that proceed from relay nuclei in the thalamus, by way of the *internal capsule, to the *cerebral cortex. These nuclei include the *ventral posterolateral and *ventral posteromedial nuclei, and the *lateral geniculate and *medial geniculate bodies. Thalamus – Massive dorsal diencephalic structure with several distinct and some indistinct nuclei. As a convenience, the thalamus is divided into the following nuclear regions: the *anterior complex, the *central complex, the *dorsal complex, the *periventricular complex, the *posterior complex, the *ventral complex, and the *reticular belt. Third ventricle – See Diencephalic superventricle Thyroid cartilage – A shield-shaped cartilage in the larynx. Transpontine corticofugal tract (embryonic) – Portion of the large descending fiber tract in the maturing brain that traverses the *pontine gray and gives off collaterals there. Pioneering fibers of this tract are present by the end of the first trimester. Trapezoid body – A fiber tract extending from the ventral *cochlear nucleus to the contralateral *superior olivary complex. It contains second- and higher-order auditory fibers. Trigeminal, motor nucleus (embryonic) – Aggregate of trigeminal somatic motor neurons situated medial to the *trigeminal principal sensory nucleus. It is recognizable in late first trimester embryos.

575 Trigeminal, principal sensory nucleus (embryonic) – The second-order sensory neurons in the trigeminal system located dorsal and lateral to the incoming sensory root of cranial *nerve V. It receives topographic somatosensory input from the face and mouth, and its efferents cross the midline in the pons and proceed to the thalamic *ventral complex in close association with the *medial lemniscus. The nucleus is prominent by the late first trimester. Trigeminal, spinal nucleus (embryonic) – A continuation of the *trigeminal principal sensory nucleus that extends caudally through the *medulla to the second cervical level of the *spinal cord. It is prominent by the late first trimester. Trigeminal, spinal tract – Primary sensory fibers of the trigeminal ganglion that convey touch and pressure information from the face. The axons enter the brain in the pons and proceed caudally, forming a lateral cap around the *trigeminal spinal nucleus where they terminate in a topographic order. Trochlear nucleus – Aggregate of somatic motor neurons located posterior to the *oculomotor nuclear complex that innervate the superior oblique muscle of the eye by way of cranial *nerve IV.

V Ventral anterior nucleus (thalamus, embryonic) – The ventral anterior nucleus, to be distinguished from the *anteroventral nucleus (which is part of the *anterior complex of the thalamus) is the most rostral component of the thalamic *ventral complex. Its afferents come mostly from the *globus pallidus and the *substantia nigra, and its efferents terminate in the *paracentral lobule of the neocortex. The nucleus is recognizable during the late first trimester as a developing structure with putative migrating and sojourning neurons and sprouting fiber bundles. Ventral complex (thalamus, embryonic) – A group of structurally and functionally related ventrolateral and ventral nuclei of the thalamus, including the *ventral anterior, *ventral lateral, *ventral posterolateral, and *ventral posteromedial nuclei. The ventral thalamic complex is the principal topographically organized relay system of the direct (lemniscal) and indirect (cerebellar and striatal) somatosensory and proprioceptive input system to the sensory and motor areas of the *neocortex. Its components are recognizable during the late first trimester as formative structures with putative migrating and sojourning neurons and sprouting fiber bundles.

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GLOSSARY Ventral lateral nucleus (thalamus, embryonic) – Situated caudal to the *ventral anterior nucleus, this component of the thalamic *ventral complex is the target of input from the *superior cerebellar peduncle and the *red nucleus. Its somatotopically organized fibers terminate in the motor cortex and adjacent areas. The ventral lateral nucleus may be the principal relay from the *cerebellum to the *neocortex. The nucleus is recognizable during the late first trimester as a developing structure with putative migrating and sojourning neurons and sprouting fiber bundles. Ventral posterolateral nucleus (thalamus, embryonic) – Situated caudal to the *ventral lateral nucleus, this region of the thalamic *ventral complex is the target of fibers of the *medial lemniscus that originate in the *cuneate nucleus and the *gracile nucleus and convey somatosensory information from the trunk and the extremities. Its efferents form the somesthetic radiation that terminates in a precise topographic order in the medial part of the *postcentral gyrus. The ventral posterolateral nucleus is the principal thalamic relay of somesthetic input from the trunk and limbs to the *neocortex. The nucleus is recognizable during the late first trimester as a developing structure with putative migrating and sojourning neurons and sprouting fiber bundles.

Ventral posteromedial nucleus (thalamus, embryonic) – Situated between the *ventral posterolateral nucleus and the *centromedian nucleus, this nucleus receives afferents from the *trigeminal sensory nuclei and the *parabrachial nucleus that convey sensory information from the face, the tongue, the oral cavity, and the neck. The efferents of this nucleus terminate in a precise topographic order in the lateral part of the *postcentral gyrus. The ventral posteromedial nucleus is the principal thalamic relay of somatosensory and gustatory input from the neck, head, and mouth to the *neocortex. The nucleus is recognizable during the late first trimester as a developing structure with putative migrating and sojourning neurons and sprouting fiber bundles. Ventral rhombic lip – see Precerebellar NEP Ventral tegmental area (embryonic) – Medial area flanking the *substantia nigra and containing a high concentration of dopaminergic neurons, much like the

substantia nigra, pars compacta. It is present as a compact cell mass in the mesencephalon of late first trimester fetuses. Ventricles – See Superventricles Ventromedial nucleus (hypothalamus) – Large spherical nucleus that flanks the third ventricle and is surrounded by a fibrous shell. It has reciprocal connections with the *amygdala, the *bed nucleus of the stria terminalis, the *septum, and the *subiculum. It has been implicated in motivational functions related to feeding and sexual behavior. Vermis – See Cerebellum (vermis) Vestibular nuclear complex – A large area in the dorsal medulla, composed of the *medial, the *lateral, the *superior, and the *inferior vestibular nuclei. These nuclei get primary sensory input from the vestibular ganglion; their efferents join the *medial longitudinal fasciculus and form the vestibulospinal tract. Visual radiation (embryonic) – Thalamocortical fibers that originate in the *lateral geniculate body and terminate in the striate cortex of the *occipital lobe. The identification of *Meyer’s loop at GW11 suggests that this tract may reach the occipital lobe by the end of the first trimester.

W White matter – General term for extensive regions in the brain and spinal cord composed of myelinated fiber tracts but few or no neuronal cell bodies. In histological preparations with myelin stains, the white matter appears black. In laminated brain regions, as in the *cerebral cortex, the white matter is called the medullary layer.

Z Zygomatic bone – A facial bone in the cheek bone. Zona incerta (embryonic) – Region in the *subthalamus with uncertain boundaries with *Forel’s fields. It is a prominent area in the late first trimester *diencephalon.

An asterisk in front of a term indicates that it is a separate entry in the Glossary with additional information. Terms referring to transient developmental structures are underlined.

GLOSSARY

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