Sensory Mechanisms

PROGRESS IN B R A I N RESEARCH VO LUME 23 SENSORY MECHANISMS

PROGRESS IN BRAIN RESEARCH

ADVISORY B O A R D W. Bargmann

H. T. Chang E. De Robertis J. C. Eccles

J. D. French H. HydCn J. Ariens Kappers

S. A. Sarkisov

J. P. SchadC F. 0. Schmitt

Kiel Shanghai Buenos Aires Canberra

Los Angeles Goteborg Amsterdam Moscow Amsterdam Brookline (Mass.)

T. Tokizane

Tokyo

J. Z. Young

London

PROGRESS I N BRAIN RESEARCH V O L U M E 23

SEN S O RY M E C H AN1 S M S E D I T E D BY

Y. Z O T T E R M A N Department of Physiology, Veterinary College, Stockholm (Sweden)

ELSEVIER P U B L I S H I N G C O M P A N Y AMSTERDAM / LONDON / NEW YORK 1967

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List of Contributors

L. B. W. JONGKEES, Otorhinolaryngological Department, Wilhelmina Hospital, Amsterdam (The Netherlands). Department .of Anatomy and Embryology, University of Nijmegen, H. J. LAMMERS, Nijmegen (The Netherlands). A. H. M. LOHMAN, Department of Anatomy and Embryology, University of Nijmegen, Nijmegen (The Netherlands). R. NIEUWENHUYS, Netherlands Central Institute for Brain Research, Amsterdam (The Netherlands). D. OTTOSON, Department of Physiology, Karolinska Institutet, Stockholm (Sweden). G. M. SHEPHERD,Department of Physiology, Karolinska Jnstitutet, Stockholm (Sweden). D. STANLEY-JONES, Full Circle, Hayle, Cornwall (Great Britain). J. ZELENKA, Otorhinolaryngological Clinic, Faculty of the Medical Hygiene, Prague (Czechoslovakia). 0. ZICH,Faculty of Philosophy, Charles University, Prague (Czechoslovakia). Y. ZOTTERMAN, Veterinary College, Stockholm (Sweden).

Other volumes in this series:

Volume 1:Brain Mechanisms Specific and Unspecijic Mechanisms of Sensory Motor Integration Edited by G. MoruPi, A. Fessard and H. H. Jasper

Volume 2: Nerve, Brain and Memory Models Edited by Norbert Wienert and J. P. Schadk

Volume 3 : The Rhinencephalon and Related Structures Edited by W.Bargmann and J. P. Schad6 Volume 4: Growth and Maturation of the Brain Edited by D. P. Purpura and J. P. Schadt5

Volume 5 : Lectures on the Dieneephalon Edited by W.Bargmann and J. P. Schad6

Volume 6 : Topics in Basic Neurology Edited by W. Bargmann and J. P. Schad6 Volume 7 : Slow Electrical Processes in the Brain by N.A. Aladjalova

Volume 8: Biogenic Amines Edited by Harold E. Himwich and Williamina A. Himwich

Volume 9 : The Developing Brain Edited by Williamina A. Himwich and Harold E. Himwich

Volume 10: The Structure and Function of the Epiphysis Cerebri Edited by J. Ariens Kappers and J. P. SchadC Volume 11: Organization of the Spinal Cord Edited by J. C. Eccles and J. P. Schad6 Volume 12: Physiology of Spinal Neurons Edited by J. C. Eccles and J. P. Schad6

Volume 13 :Mechaniisms of Neural Regeneration Edited by M.Singer and J. P. s h a d 6

Volume 14: Degeneration Patterns in the Nervous System Edited by M. Singer and J. P. Schadt

Volume 1 5 : Biology of Neuroglia Edited by E. D. P. De Robertis and R. Carrea

Volume 16 : Horizons in Neuropsychopharmacology Edited by Williamina A. Himwich and J. P. Schadd

Volume 17: Cybernetics of the Nervous System Edited by Norbert Wiener? and J. P. Schad6

Volume 18: Sleep Mechanisms Edited by K. Akert, Ch. Bally and J. P. SchadC

Volume 19: Experimental Epilepsy by A. Kreindler

Volume 20: Pharmacology and Physiology of the Reticular Formation Edited by A. V. Valdman

Volume 21A: Correlative Neurosciences Part A : Fundamental Mechanisms Edited by T. Tokizane and J. P. Schadt

Volume 21B : Correlative Neurosciences Part B: Clinical Studies Edited by T. Tokizane and J. P. SchadC Volume 22 : Brain Reflexes Edited by E. A. Asratyan Volume 24 : Corbon Monoxide Poisoning Edited by H. Bow and I. McA. Ledingham Volume 25 : The Cerebellum Edited by C. A. Fox and R. S. Snider

Volume 26 : Developmental Neurology Edited by C. G. Bernhard Volume 27: Strrrcture and Function of the Limbic System Edited by W. Ross Adey and T. Tokizane

Preface

One of the subjects of the second International Summer School of Brain Research, Amsterdam, 1964, was sensory mechanisms, where anatomy, physiology and biophysics meet. A common interest in problems of sensory communication provided a meeting ground for brain scientists of man? disciplines. Instead of discussing all sensory systems, particular emphasis was given to subjects of olfaction and taste, and the vestibular system. The various chapters by eminent authorities in the field deal in great detail with the comparative anatomy and fiber connections of olfactory centers, electrophysiology of olfactory systems and neural mechanisms of taste. Emphasis is also placed on theoretical and clinical aspects of vestibular and hearing disorders. One of the main purposes of the International Summer Schools of Brain Research is that of bringing together students from various fields in a number of workshops at a high didactic level. The lectures of one of these workshops are collected in this book. Therefore it is not meant to be an exhaustive literature survey but a series of instructive lectures on various topics in the field.

THEEDITOR

Contents

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List of contributors Preface

Comparative anatomy of olfactory centres and tracts R. Nieuwenhuys (Amsterdam, The Netherlands) .

Experiments and concepts in olfactory physiology D. Ottoson and G. M. Shepherd (Stockholm, Sweden).

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83

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Mathematico-logical model of vestibular and hearing disorders 3. Zelenka and 0. Zich (Prague, Czechoslovakia) . . . . . Protopathy, paraesthesia and sensory suppressor zones D. Stanley-Jones (Hayle, Cornwall, Great Britain) .

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The examination of the vestibular organ L. B. W. Jongkees (Amsterdam, The Netherlands)

139 155

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169

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200

................................... Subject index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Author index.

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On the structure and fibre connections of the olfactory centres in mammals A. H. M. Lohman and H. J. Lammers (Nijmegen, The Netherlands) . .

The neural mechanism of taste Y. Zotterrnan (Stockholm, Sweden)

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Comparative Anatomy of Olfactory Centres and Tracts RUDOLF NIEUWENHUYS Netherlands Central Institute for Brain Research, Amsterdam (The Netherlands)

INTRODUCTION

It is the intention of this report to present a survey of the comparative anatomy of the parts of the telencephalon which are entirely or predominantly related to the sense of smell. The structures included in this so-called ‘rhinencephalon’ display a great variety in proportionate size and degree of differentiation, but nevertheless it is possible to recognize a common structural plan that underlies the morphology of this brain part in all groups of vertebrates. It seems well, especially for providing a terminological background, to start this survey with a brief sketch of this basic pattern. Reference to Fig. 1 shows that the receptive element of the olfactory apparatus is represented by slender bipolar cells, situated in the mucosa of the nasal cavity. These peripheral elements have, in addition to their receptive function, also a conductive function: they give rise to axonal offshoots which relay the sensations received directly towards the brain. Electron microscopy has revealed that these axons are extremely small in diameter and have no myelin sheath (Gasser, 1956; De Lorenzo, 1957). Because the peripheral olfactory elements combine the functions of sense cells and

cer. hem.

nasal

cov.

Fig. 1. Scheme of the organization of the peripheral and central olfactory system in vertebrates. cer.

hem. = cerebral hemisphere; glom. = glomerulus;nasal cav. = nasal cavity; olf. bulb. = olfactory bulb; prim. olf. f. = primary olfactory fibres; sec. olf. f. = secondary olfactory fibres. References p. 61-44

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R. NIEUWENHUYS

neurons they are often referred to as neurosensory cells. It is worthy of note that elements of this kind are considered the most ancient type of nervous conductors (Ariens Kappers, 1929; Ariens Kappers et al., 1936). In vertebrates, neurosensory cells outside the olfactory system are found only in the submammalian pineal organ and in the saccus vasculosus of fish. In the invertebrates on the other hand, they are numerous and widespread. It has already been mentioned that the neurites of the peripheral olfactory cells pass straight into the brain; they enter into a separate forward extension of the telencephalon known as the bulbus olfactorius. In most vertebrates the nasal cavities are closely applied to the brain surface, and the axons of the olfactory cells form a number of short fascicles,the fila olfactoria. In some groups (amphibians, most actinopterygians), however, nose and brain are further apart, and then the primary olfactory fibres collect into a pair of distinct olfactory nerves. On entering the brain the s o n s of the peripheral olfactory elements interlace in a most complex fashion and terminate by free arborizations in the superficial zone of the olfactory bulb. Here these axonal endings, together with the richly branched terminal dendritic processes of neurons situated in the bulb, constitute complexly entangled spherical plexuses named glomeruli. In these glomeruli the synaptic contacts between the olfactory neurons of the primary and the secondary series are established. The axons of the secondary olfactory neurons, or at least those of the conspicuous elements known as mitral cells, leave the bulb and enter the cerebral hemispheres. These axons form the secondary olfactory pathways, which in most vertebrates can be divided into a medial and a lateral tract. The areas which receive direct fibres from the olfactory bulb, i.e. the secondary olfactory centres, differ in the various vertebrate classes in position and extent. In cyclostomes and primitive fish almost the entire telencephalon is dominated by the olfactory organ, but in birds and certain mammals the olfactory area occupies only a very restricted part of the hemispheres. The relations found in the various vertebrate groups will be discussed below, but it is desirable to preface these special descriptions with a few general remarks on the form and morphogenesis of the cerebral hemispheres. It may be recalled that the forebrain of all vertebrates in an early embryonic stage is a simple tube-like structure, consisting of a pair of thickened side plates which dorsally, rostrally, and ventrally are connected by an epithelial membrane. During further development there occurs in most vertebrates a bulging out or evagination of the side walls which gives rise to two hemispheres, the central ventricular spaces of which are surrounded by nervous tissue (Figs. 2a, b). The dorsal parts of the hemisphere walls form the pallium, whereas the ventral parts, which comprise a ventrolateral striatal and a ventromedial septa1 region, are usually designated as the subpallium or basis. In all vertebrates the pallium as well as the basal areas contain secondary olfactory centres. We will conclude this introduction with a few words on the relation between the olfactory bulbs and the cerebral hemispheres. Fig. 2c shows that in amphibians the part of the forebrain wall which serves as the primary olfactory centre, i.e. the region in which the glomeruli and the mitral cells are found, is not represented by a separate

OLFACTORY CENTRES A N D T R A C T S

3

C

a

b

d Fig. 2. The morphogenesis of the telencephalon shown diagrammatically by horizontal sections; (a) represents the early embryonic tube-like condition; (b) shows the evagination of the telencephalic side plates; (c) and (d), the adult condition in, respectively, an amphibian (Salamandra) and a reptile (Lacerta) . Dotted parts, olfactory bulbs.

structure, but simply occupies a part of the hemisphere wall. In most other vertebrates, however, a separate evagination, starting from the rostra1 or lateral parts of the hemisphere walls, gives rise to the formation of clearly defined olfactory bulbs (cf. Nieuwenhuys, 1964; and Fig. 3). These structures may remain in close apposition to the hemispheres, but in various groups of vertebrates (Chondrichthyes, many teleosts, and most reptiles) long stalks or crura develop which connect the bulbi with the cerebral hemispheres (Figs. 2d, 3). Following these introductory notes the olfactory centres and tracts in the brain of the various groups of submammalian vertebrates will be discussed. In the final section of this paper the main results will be surveyed, and some comparisons with the mammalian olfactory system will be made*.

* For a detailed account on the mammalian olfactory system I refer to Dr. Lohman’s contribution to this volume. References p. 6 1 6 4

b. 01. hem.

A, LAMPETRA

b. 01.

E, MORMYRUS

b. 01.

F, PROTOPTERUS Fig. 3. The forebrain of a representative series of vertebrates, seen from the right side. After Jansen (B), Bing and Burckhardt (D), Franz (E), Rudebeck (F), Goldby and Gamble (J, K), and Durward (L). b. ac. = bulbus olfactorius accessorius; b. 01. = bulbus olfactorius;f. bulb. = formatio bulbaris; hem. = hemisphere; n. 01. = n e m s olfactorius; n. vom. nas. = n e m s vomeronasalis.

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O L FACT O RY CENTRES AND T R A C T S

hem.

G, NECTURUS

01.