Advances in Psychology Volume 123 Cerebral Asymmetries in Sensory and Perceptual Processing

CEREBRAL ASYMMETRIES IN SENSORY AND PERCEPTUAL PROCESSING

ADVANCES IN PSYCHOLOGY 123 editors."

G. E. STELMACH R A. VROON

ELSEVIER Amsterdam

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York

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CEREBRAL ASYMMETRIES IN SENSORY AND PERCEPTUAL PROCESSING

Edited by

Stephen CHRISTMAN Department of Psychology University of Toledo Toledo, Ohio, USA

1997

ELSEVIER Amsterdam

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- New York - Oxford.

Shannon

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NORTH-HOLLAND ELSEVIER SCIENCE B.V. Sara Burgerhartstraat 25 EO. Box 211, 1000 AE Amsterdam, The Netherlands

ISBN: 0 444 82510X 9 1997 Elsevier Science B.V. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior written permission of the publisher, Elsevier Science B.V., Copyright & Permissions Department, RO. Box 521, i 000 AM Amsterdam, The Netherlands. Special regulations for readers in the U.S.A. - This publication has been registered with the Copyright Clearance Center Inc. (CCC), 222 Rosewood Drive, Danvers, MA 01923. Information can be obtained from the CCC about conditions under which photocopies of parts of this publication may be made in the U.S.A. All other copyright questions, including photocopying outside of the U.S.A., should be referred to the copyright owner, Elsevier Science B.V., unless otherwise specified. No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. This book is printed on acid-free paper. Printed in The Netherlands

Table of Contents Preface

xi

Contributors

xviii

SECTION I: SPATIAL/TEMPORAL FREQUENCY PROCESSING

1. Hemispheric Asymmetry in the Processing of Spatial Frequency: Experiments Using Gratings and Bandpass Filtering Stephen Christman

Sinusoidal and Square-wave Stimuli 7 Compound Stimuli 12 Low-pass and Band-pass Filtered Stimuli Conclusions 23 References 26

19

2. Temporal Frequency Processing 31

Luciano Mecacci

Hemispheric Asymmetries of Spatio-temporal Interaction: Electrophysiological Evidence 35 Reading Disability and Impairment in Processing Basic Spatio-temporal Information 44 Evidence from Brain-injured Patients 46 Conclusion 49 References 49

3. Interhemispheric Transfer of Spatial and Temporal Frequency Information 55

Nicoletta Berardi and Adriana Fiorentini

Properties of Interhemispheric Commisures in Mammals Interactions between Sinusoidal Stimuli Presented in the Left or Right Visual Field 61

56

vi Discrimination of Spatial Phase in Complex Gratings Presented in the Left or Right Visual Field 67 Interhemispheric Transfer of Information on Chromatic Contrast 73 Discussion 74 References 76

SECTION II: OBJECT AND SPATIAL REPRESENTATIONS 4. Hemispheric Asymmetry for Components of Spatial Processing Joseph Hellige 83 The Categorical/Coordinate Distinction 84 The Search for Underlying Mechanisms of Hemispheric Asymmetry for Spatial Processing 88 The Speech/Attention-Shift Hypothesis 89 Are Categorical and Coordinate Spatial Relationships Processed Independently? 91 The Nature of Task-Relevant Visual Information 93 Extensions of the Categorical/Coordinate Distinction 112 Concluding Comments: More on Mechanisms and Future Directions 116 Notes 119 References 120

5. Computational Analyses and Hemispheric Asymmetries in Visual-Form Recognition Chad Marsolek and E. Darcy Burgund Visual Form Subsystems 126 Behavioral Evidence for Relatively Independent Subsystems Contradictory Internal Processing Strategies 13:5 Behavioral Evidence for Parts-based versus Holistic Processing 147 Conclusions and Implications 150 Acknowledgments 153 References 153

125

131

vii SECTION III: VISUAL ATTENTION

6. Amplification of Spatial Nonuniformities by Guided Search Mechanisms E. William Yund

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162 Visual Search and the Guided Search Model 166 Spatial Nonuniformities in Visual Search General Discussion 184 Conclusions 190 Footnotes 190 Acknowledgements 192 References 193

7. Hemispheric Coordination of Spatial Attention James Enns and Alan Kingstone

197

Hemispheric Specialization in Visual Search? 199 106 Hemifield Differences in Unilateral vs. Bilateral Visual Displays Hemifield Competition in Object Identification 216 Discussion 220 What are the Implications for Understanding Spatial Attention? 226 228 Implications for Understanding Hemispheric Specialization Acknowledgments 229 References 229

8. Asymmetries in the Flanker Compatibility Effect Frederick Kitterle, Mark Ludorf, and Jeremy Moreland Expt. 1: Left-right Asymmetries in the FCE: M and W Letter Arrays 236 Experiment 1B - FCE with H, V letter arrays 243 Experiment 2 - Effects of letter case 245 Experiment 3 - Target-Flanker Spacing 250 General Discussion 252 References 258

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viii SECTION IV: EFFECTS OF VISUAL FIELD LOCUS

9. The Relation Between Left-Right and Upper-Lower Visual Field Asymmetries Stephen Christman and Christopher Niebauer Simple Reaction Time 266 Resolution/Acuity 267 Local-Global Processing 269 Categorical/Coordinate Processing Stereopsis 272 Motion 274 Visual Search 276 Visual Attention 279 Pattern Recognition 281 Conclusions 283 References 290

263

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SECTION V: AUDITORY PROCESSING

10. Hemispheric Specialization of Human Auditory Processing: Perception of Speech and Musical Sounds Robert Zatorre Phonetic Mechanisms in Speech Perception 301 Processing of Melodic Patterns 307 Auditory Imagery 312 Morphometry of Auditory Cortex via Structural MRI References 319

11. Perceptual and Cognitive Development: Electrophysiological Correlates Dennis Molfese and Dana Narter Voice Onset Time 328 Place of Articulation 336 Vowel Sounds 341

299

316

325

ix Electrophysiological Correlates of Infant Memory 342 Electrophysiological Correlates of Early Word Acquisition Acknowledgments 374 References 374

356

12. The Ipsilateral Auditory Pathway: A Psychobiological Perspective Kendall Hutson 383 Anatomy of the Ascending Auditory System Role of Ipsilateral Pathway in Behavior 405 Evoked Potential Studies 414 Role of Ascending Pathways in Physiology of the Inferior Colliculus 415 Consequences to Cognition 439 Conclusions 441 Footnote 442 Acknowledgment 443 References 443

385

SECTION VI: TACTUAL PROCESSING

13. Role of Sensory and Post-sensory Factors in Hemispheric Asymmetries in Tactual Perception Jo~'l Fagot, Agn~s Lacreuse, and Jacques Vauclair Anatomical Bases of Tactual Perception 470 Functional Asymmetries for Elementary Tactile Discriminations 471 Tactual Discrimination of Orientations 474 Retention of Sequence of Touches 475 Tactual Discrimination of Dot Patterns 475 Tactual Maze Learning 477 Haptic Discrimination of Spatial Forms 477 Exploratory Strategies for Nonsense Shape Discrimination Haptic Perception in Nonhuman Primates 483 General Discussion 485 References 488

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478

SECTION VII: OLFACTORY PROCESSING 14. Laterality in Human Nasal Chemoreception Richard Dory, S. Bromly, P. Moberg, and T. Hummel

497

Anatomy of the Olfactory and Trigeminal Chemosensory Systems 499 Olfactory System 501 Trigeminal System 508 The Search for Anatomical Asymmetries in Brain Regions Related to Olfaction 510 The Search for Functional Asymmetry in Human Olfactory Pathways 511 Conclusions 527 Footnotes 530 Acknowledgements 531 References 531

Name Index

543

Subject Index

557

xi

Preface Since Justine Sergent (1982a) first proposed that the left versus right hemispheres were specialized for the processing of high versus low spatial frequencies, respectively, laterality researchers have increasingly come to recognize the importance of sensory and perceptual factors in determining observed patterns of hemispheric asymmetry. As Sergent and Joseph Hellige noted in a seminal 1986 paper, this growing realization mirrored comparable trends in mainstream cognitive research during the early 1970's; they quote Garner's (1970) comments: "too often has the nature of input been ignored, with the consequence of incorrect assessment of information processing at worst, or an inadequate picture at best". In important ways, laterality research was "catching up" with the rest of the field. In a similar vein, Hardyck (1986) argued that sensory and perceptual factors associated with lateral tachistoscopic presentation of input had come to "constitute a set of 'invisible effects' present in many experiments, but unanalyzable due to omnipresence across experiments" (p.226). While higher-order functions representing the end products of information processing (e.g., word and face recognition) have traditionally constituted the dominant focus of laterality research, it is apparent that a full account of cerebral lateralization needs to also consider the role of earlier information processing stages. An observer's ability to attend to, recognize, and remember material is a priori constrained by limitations in the ability to sense and perceive; sensory and perceptual processes serve as the "gateways" to higher order processing. Concerns with such lower-level factors are critical given the widespread use of lateral, tachistoscopic presentation in visual laterality work, which means that input processing is almost always data-limited, and the effects of even small hemispheric differences in sensory processing can potentially modulate the strength and direction of asymmetries in higher-level processes [the notion that small initial differences in sensory functions can "snowball" into functional asymmetries of considerable magnitude also plays a prominent role in developmental accounts of the origin of hemispheric asymmetries proposed by Kosslyn (1987) and Previc (1994)]. Thus, researchers interested specifically in higher-order processes will naturally be inclined to interpret any obtained hemispheric asymmetries in terms of precisely those higher-order processes of interest; to the extent, however, that such asymmetries are being partly or wholly determined by perceptual variables, researchers run the risk of reaching mistaken conclusions.

xii The purpose of this book is to provide a comprehensive overview of hemispheric differences in sensory and perceptual processing. Accordingly, the first section of this book deals directly with the intraand inter-hemispheric processing of spatial and temporal frequencies in the visual modality. Chapters by Christman and by Mecacci provide reviews of spatial and temporal frequency processing, respectively, while Berardi and Fiorentini describe constraints on the interhemispheric transfer of basic sensory information. The three chapters of this section may seen as an extension of two previous papers: Sergent and Hellige's 1986 paper, "Role of Input Factors in Visual-Field Asymmetries", and Christman's 1989 literature review, "Perceptual Characteristics in Visual Laterality Research" (both in the journal Brain and Cognition). These papers presented timely reviews of the influence of various visual input factors (e.g., exposure duration, size, eccentricity, luminance, etc.) on hemispheric processing. Since they were written, however, a substantial body of empirical research investigating sensory processing in the hemispheres has accumulated, providing more powerful and direct tests than could be provided by the necessarily post-hoc nature of the aforementioned review articles. While the first section focuses on the "raw" input to higher-order mechanisms, the second section addresses the initial interaction between sensory and cognitive mechanisms, dealing with how the left and right cerebral hemispheres differ in their computation and representation of sensory information: Hellige provides an overview of hemispheric differences in spatial representations, while Marsolek and Burgund present an important new theory of hemispheric differences in visual-form recognition that has roots in the distinctions between categorical and coordinate spatial representations discussed by Hellige. A key theme in both chapters is that extraction of sensory information from input is guided and constrained by perceptual goals; that is, hemispheric asymmetries are determined conjointly by the sensory information available in the input and by the types or ranges of sensory information that are required by the task at hand. The third section covers how attentional mechanisms modulate the nature of perceptual processing in the cerebral hemispheres. Processing of specific objects occurs, not in isolation, but in a rich context defined both by other objects in the environment and by internal expectations and goals on behalf of the observer. The cerebral basis for such phenomena as the attentional and grouping processes underlying local-global processing

xiii and visual search through many-element displays is addressed in the chapters by Yund and by Enns and Kingstone. In particular, Yund presents an extension of the Guided Search Model (Wolfe, 1994) to visual field differences in visual search, while Enns and Kingstone present a theory based on interhemispheric competition for limited attentional resources. Kitterle, Ludorf, and Moreland discuss a related phenomenon in the form of the "flanker" effect, reporting visual field differences in the effects of distractors on the processing of targets. Section four consists of a single chapter presenting a theme that does not fit tidily into any of the other sections. Namely, the chapter by Christman and Niebauer reviews evidence suggesting a functional linkage between upper and right visual field processing, on the one hand, and lower and left visual field processing on the other. Their chapter offers a challenege to the interpretation of lateral field differences as reflecting hemispheric differences. That is, to the extent that upper/lower field differences may not be directly interpretable in terms of retinal projection to different hemispheres, the question is raised whether the corresponding left/right differences may also reflect something beyond hemispheric differences as such. Conversely, it is also possible that upper/lower differences reflect hemispheric attentional biases along the vertical meridian; this would be consistent with previous demonstrations that manifestations of hemispheric asymmetries are not necessarily linked to retinal coordinates (e.g., Luh, Rueckert, & Levy, 1991). In any case, this chapter indicates that laterality researchers (who are interested in left-right differences) and vision researchers (who may be interested in the functional differences between near versus far vision as associated with the lower versus upper visual fields, respectively) cannot provide a complete picture without integrating their various approaches. Although vision represents the dominant sensory modality in humans, the other senses are important to consider, both in their own right and insofar as they play a role in rich, polymodal object representations. Consequently, the remaining sections cover sensory and perceptual level processing in other sensory modalities. First, the chapter by Zattore provides an overview of cerebral asymmetries in auditory processing, with special emphasis on the processing of speech and music and on auditory imagery. While research on cerebral differences in auditory processing in adults has made significant strides via the use of dichotic listening paradigms employing verbal and nonverbal material, theoretical interpretations of this work have tended to focus on higher-level cognitive

xiv mechanisms (e.g., lexical and semantic processes). Relatively less attention has been paid to the sensory and neural bases of such asymmetries, which are addressed in the chapter by Zatorre. Molfese and Narter review evoked potential studies of auditory processing, with special emphasis on research with infants and children. This focus on developmental issues is especially fitting in the context of audition, since auditory processing is more closely and exclusively linked to higher-order processes (namely, speech perception and language) than the other sensory modalities. In this sense, research on infants provides a purer picture of the sensory underpinnings of phonetic processing (e.g., without the obscuring effects of top-down influences). On a more cautionary note, Hutson's chapter reviews the neural bases for the representation of contralateral auditory hemispace in each hemisphere, with special reference to the common assumption that left versus right ear performance reflects right versus left hemisphere processing, respectively. The importance of attentional biases in overriding or obscuring structural differences in dichotic listening has been previously pointed out (e.g., Mondor & Bryden, 1992); Hutson offers evidence that even the structural linking of left ear-fight hemisphere and right ear-left hemisphere may be on tenuous ground in light of the lack of an orderly structural chiasm in the auditory system. Finally, the present book covers hemispheric processing of tactual/ haptic and olfactory stimulation; while relatively less research has been devoted to these modalities (with the exception, of course, of studies of hand dominance), their inclusion provides a breadth of treatment complementary to the depth of treatment of the visual and auditory modalities. The chapter by Fagot, Lacreuse, and V auclair provides a balanced review of processing in the tactile/haptic domain, the richness of which is often obscured by the emphasis on right-handed writing in humans; their chapter also includes data from nonhuman primate populations. Finally, Doty, Bromly, Moberg, and Hummel offer a thorough review of the neural bases for olfactory and chemosensory processing, the oldest of our senses and perhaps the most neglected in terms of research (I am aware of no previous review of cerebral asymmetries in chemoreception). The treatment of varied sensory and perceptual level asymmetries of hemispheric function in this volume is hoped to serve as a useful reference tool for laterality researchers interested in sensory level processing p e r se, as well as for those researchers focusing on higher-level processes who want to address the possible influence on such processes of

XV

lower-level asymmetries of hemispheric function. At best, it is hoped that such a compendium will shed light on possible analogs among hemispheric asymmetries in different sensory modalities; for example, some of the findings concerning asymmetries in the visual and auditory domains suggest a general hemispheric difference in processing higher versus lower resolution sensory information. In addition, a detailed consideration of sensory level asymmetries may serve to foster links between research into asymmetries in humans versus nonhumans. Functions such as language and face recognition do not exist in any directly comparable form in non-humans (with the possible exception of Great Apes); research into sensory processes in the left and right hemispheres promises to provide potentially important bridges between human and nonhuman laterality research. In the context of the preceding discussion contrasting the roles of cognitive processes versus sensory processes, it is worth noting that the distinction between higher-order and lower-order processing is somewhat artificial. That is, while at least some sensory processing must logically precede cognitive processing in the temporal domain (although there is extensive overlap), this does not necessarily entail any sharp qualitative demarcation between the contents and operations of early versus late information processing stages. There is a growing consensus among cognitive psychologists that basic principles of sensory and perceptual processing form the foundation of cognitive processes such as language, memory, and categorization. For example, Chatterjee, Maher, and Heilman (1995) argued that the assignment of thematic roles of agent versus patient (which map onto the grammatical categories of subject versus object) may be based on nonlinguistic, spatiotemporal representations. With regard to memory, Roediger, Weldon, and Challis (1989) reviewed evidence for the importance of "data-driven" processing in memory in which perceptual characteristics of both input and retrieval cues play critical roles in memory encoding and retrieval. Finally, Barsalou (1993) has developed a comprehensive model of human categorization and knowledge representation that is firmly grounded in a compositional system of perceptual symbols. It is worth noting that Barsalou's scheme in which simple perceptual symbols can be flexibly and recursively combined to form ever more elaborate representations bears more than a passing similarity to Corballis' (1991) "Generative Assembling Device".

xvi In closing, perhaps the ultimate aim of this book is to foster greater interaction and integration between neuropsychological and mainstream cognitive research. One of more attractive features of Sergent's initial formulation of the spatial frequency hypothesis was that it took a welldeveloped body of research on the visual processing of spatial frequency information and placed it in the context of laterality research; too often, laterality researchers have tended to create idiosyncratic accounts of hemispheric differences in function that lack operational definitions (e.g., the analytic-holistic dichotomy). It is hoped that a continued effort to ground laterality research in the empirical and theoretical findings gleaned from over 100 years of experimental psychology will be of benefit to both areas.

Acknowledgements I acknowledge the Department of Psychology and the College of Arts & Sciences at the University of Toledo for granting a sabbatical during which I wrote my two chapters and for providing a generous level of institutional support over the years. I would also like to thank the editors of North-Holland's Advances in Psychology series, Kees Michelson and David Hoole, for their patience and encouragement. The proofs for this book were prepared on a Power Macintosh 7100/80AV, using Microsoft Word 5. la; final preparation of figures was done using Aldus SuperPaint, v.3.0. I would like to thank Kathy Skurzewski for assistance in scanning figures. Special thanks are due my wife, Lori, for help in proofing some of the chapters and, more importantly, for putting up with my incessant work and worry. Finally, I wish to thank my children, Rayna and Sam, for tolerating (without too much rivalry) a temporary third "child" in the family in the form of this book. This book is dedicated to the memory of Justine Sergent. She published her first series of papers (e.g., Sergent, 1982a, 1982b, 1982c, 1982d) presenting the spatial frequency hypothesis the year that I entered graduate school and began pursuing her work. She was a truly exceptional source of inspiration for myself and the neuropsychology community as a whole, and she is missed. Stephen Christman Toledo, 1997

xvii References

Barsalou, L. (1993). Flexibility, structure, and linguistic vagary in concepts: Manifestations o f compositional system of perceptual symbols. In A.C. Collins, S.E. Gatlaercole, M.A. Conway, and P.E.M. Morris (Eds.), Theories of Memory. Hillsdale, NJ: Lawrence Erlbaum Assoc. Chatterjee, A., Maher, L., & Heilman, K. (1995). Spatial characteristics of thematic role representation. Neuropsychologia, 33, 643-648. Christman, S. (1989). Perceptual characteristics in visual laterality research. Brain and Cognition, 11, 238-257. Corballis, M. (1991). The Lopsided Ape: Evolution of the Generative Mind. New York: Oxford University Press. Garner, W.R. (1970). The stimulus in information processing. American Psychologist, 25, 350-358. Hardyck, C. (1986). Cerebral asymmetries and experimental parameters: Real differences and imaginary variations? Brain and Cognition, 5, 223-239. Kosslyn, S.M. (1987). Seeing and imagining in the cerebral hemispheres: A computational approach. Psychological Review, 94, 148-175. Luh, K.E., Rueckert, L.M., & Levy, J. (1991). Perceptual asymmetries for free viewing of several types of chimeric stimuli. Brain and Cognition, 16, 83-103. Mondor, T.A., & Bryden, M.P. (1992). On the relation between auditory spatial attention and auditory perceptual asymmetries. Perception & Psychophysics, 52, 393-402. Roedlger,-H., Weldon, M., & Challis, B. (1989). Explaining dissociations between implicit and explicit measures of retention: A processing account. In H. Roediger & F.I.M. Craik (Eds.), Varieties of Memory and Consciousness: Essays in Honour of Endel Tulving. Hillsdale, NJ: Lawrence Erlbaum Associates. Sergent, J. (1982a). The cerebral balance of power: Confrontation or cooperation? Journal of Experimental Psychology: Human Perception and Performance, 8, 253-272. Sergent, J. (1982b). About face: Left-hemisphere involvement in processing physiognomies. Journal of Experimental Psychology: Human Perception and Performance, 8, 1-14. Sergent, J. (1982c). Influence of luminance on hemispheric processing. Bulletin of the Psychonomic Society, 20, 221-223. Sergent, J. (1982d). Theoretical and methodological consequences of variations in exposure duration in laterality studies. Perception & Psychophysics, 3-1, 451-461. Sergent, J., & Hellige, J. (1986). Role of input factors in visual-field asymmetries. Brain and Cognition, 5, 174-199 Wolfi~, J. M. (1994). "Guided search" 2.0: A revised model of visual search. Psychonomic Bulletin & Review, 1,202-238.

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Contributors Nicoletta Berardi Istituto di Neurofisiologia C.N.R. Pisa, Italy

Frederick Kitterle Department of Psychology Northern Illinois University

Steven Bromley Department of Otorhinolaryngology Univ. of Pennsylvania Medical Center

Agnrs Lacreuse Department of Psychology University of Georgia

E. Darcy Burgund Department of Psychology University of Minnesota

Mark Ludorf Department of Psychology Stephen F. Austin State University

Stephen Christman Department of Psychology University of Toledo

Chad Marsolek Department of Psychology University of Minnesota

Richard L. Doty Department of Otorhinolaryngology Univ. of Pennsylvania Medical Center

Luciano Mecacci Universit~ degli Studi di Firenze Italy

James Enns Department of Psychology University of British Columbia

Paul Moberg Department of Otorhinolaryngology Univ. of Pennsylvania Medical Center

Jorl Fagot Center for Research in Cognitive Neuroscience, Marseille, France

Jeremy Moreland Department of Psychology Stephen F. Austin State University

Adriana Fiorentini Dipartimento di Psicologia Generale Universita' di Firenze

Dennis Molfese Department of Psychology Southern Illinois University, Carbondale

Joseph Hellige Department of Psychology University of Southern California

Christopher Niebauer Department of Psychology University of Toledo

Thomas Hummel Department of Otorhinolaryngology Univ. of Pennsylvania Medical Center

Jacques Vauclair Center for Research in Cognitive Neuroscience, Marseille, France

Kendall Hutson Department of Psychology University of Toledo

E. William Y und Department of Neurology University of California, Davis

Alan Kingstone Department of Psychology University of Alberta

Robert Zatorre Montreal Neurological Institute McGill University

SECTION I: SPATIAL/TEMPORAL FREQUENCY PROCESSING

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Cerebral Asymmetries in Sensory and Perceptual Processing S. Christman (Editor) 9 1997 Elsevier Science B.V. All rights reserved.

Chapter 1

Hemispheric Asymmetry in the Processing of Spatial Frequency: Experiments Using Gratings and Bandpass Filtering. Stephen D. Christman University of Toledo When Paul Broca first brought the existence of systematic asymmetries in language representation between the left and right cerebral hemispheres (LH and RH) to the attention of the 19th century medical community, the initial reaction was skepticism and disbelief. This was replaced within ten years by widespread acceptance (Harrington, 1987). Initial doubts centered on the prevailing assumption that bilateral symmetry was "perhaps the most general truth in all the science of animal construction" (Moxson, 1866); interestingly, however, a decade later, hemispheric asymmetry in humans was not only widely accepted, it was taken to be a hallmark of human superiority over other organisms: "Man is, of all the animals, the one whose brain in the normal state is the most asymmetrical... It is this that distinguishes us the most clearly from the animals" (Broca, 1877). While the existence of hemispheric differences has not come into serious question since, an unfortunate legacy of the 19th century viewpoint persisted until recently in the form of three implicit assumptions that guided laterality research conducted between 1880 and 1980: (i) that language and other high level cognitive functions were the only lateralized functions, (ii) that only humans

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possessed language, and (iii) that, therefore, only humans exhibited significant degrees of hemispheric asymmetry. The last two decades have seen the dispelling of all three assumptions: Stanley Glick's book Cerebral Lateralization in Nonhuman Species (1985) cleared the way for a large growth in the number of studies of hemispheric asymmetries in nonhumans, and the work of researchers such as the Gardners has at least raised the possibility of rudimentary language acquisition in nonhuman primates (e.g., Gardner, Gardner, & Van Cantfort, 1989). The theme of this chapter (and, indeed, of many chapters in this volume) is that hemispheric asymmetry is not limited to higher-order functions and can be demonstrated in a wide variety of sensory and perceptual functions. The implications of hemispheric asymmetries in lower-order functions are important elements in the recent shift in theorizing about brain laterality from emphasis on all-inclusive dichotomies (e.g., Bradshaw and Nettleton's [1981] "analytic/holistic" dichotomy) to a growing realization that behavioral asymmetries (e.g., ear and visual field advantages) are determined by a multitude of factors, some involving cerebral lateralization and some not, some involving higherorder functions and others involving lower-order functions. Hellige (1993) provides an overview of this new componential approach to hemispheric asymmetry. Hemispheric asymmetries in lower-order functions also places the study of hemispheric asymmetry in an evolutionary context. The previous view that asymmetry was confined to higher-order (and especially linguistic) functions implied a sort of evolutionary discontinuity; the current view that asymmetry is present across a wide range of both species and functions places human asymmetry in a richer comparative context, allowing the potential use of animal models in studies of human asymmetry, and helping foster a reevaluation of the neural basis of higher-order asymmetries (c.f., the growing acknowledgment of the importance of non-cortical brain asymmetries). This chapter focuses on hemispheric differences in processing different ranges of spatial frequency content of visual input. Before discussing the relevant literature, however, it is useful to provide background on the role of spatial frequency in visual processing. The modem era in the visual sciences can be traced back to the seminal work of researchers such as Hubel and Wiesel (1962), who helped refine the use of single-cell recording techniques in the study of the neural basis

Spatial Frequency

5

of visual processing. Models of visual processing initially derived from this work posited the existence of various neuronal cell types selectively responding to specific visual features. For example, Hubel and Wiesel (1962, 1965) proposed three important types of cells in striate cortex: (i) simple cells, which respond best to lines, bar, or edges at particular orientations; (ii)complex cells, which respond best to bars or edges moving in specific directions in particular orientations; and (iii) hypercomplex cells, which respond not only to the orientation and direction of motion of stimuli, but also to specific stimulus sizes, lengths, and widths. More extreme versions of this approach have gone so far as to postulate the existence of "pontifical" or "grandfather" cells: cells that fire only when presented with a visual representation of some specific, complex object such as a face or hand (e.g., Barlow, 1972). The 1960s saw an alternative approach emerge which more or less replaced the single-cell feature detection framework. Campbell and Robson (1968) first proposed the existence of discrete pathways in the visual system, each sensitive to a limited range of spatial frequency components. These various pathways or channels were hypothesized to carry out a two-dimensional Fourier analysis of the visual scene, in which complex patterns are broken down into simple, sinusoidal components. Spatial frequency components can be described in terms of a number of dimensions. First, they consist of sinusoidal variations in luminance across space, with higher spatial frequencies involving more numerous cycles per unit distance (the spatial frequency of stimuli is typically described in terms of cycles per degree [cpd] of visual angle; high versus low frequency grating stimuli consist of thinner versus wider bars). Phenomenologically, high frequencies carry information about fine details, while low frequencies carry information about more global aspects of the visual scene. Second, they possess a specific orientation that is perpendicular to the axis of luminance variation. Third, they have some specific contrast, defined by the luminance difference between the lightest and darkest portions of the stimulus divided by the sum the luminances of the lightest and darkest portions of the stimulus. Finally, they have a specific phase, referring to the absolute position in space of the light and dark bars relative to some referent. For a more thorough coverage of the spatial frequency approach, the interested reader is directed to I)eValois and DeValois (1988); a concise but effective overview is provided in Hams (1980).

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Thus, in the spatial frequency approach, the fundamental units of visual analysis are not discrete features, but spatially distributed sinusoidal frequency components. The spatial frequency approach has enjoyed great success, and is now a dominant approach to modeling visual processes. A nice example of the utility of the spatial frequency approach over the feature detection approach can be found in a study by DeValois, DeValois, and Yund (1979), who examined single-cell responses to gratings and checkerboard patterns. Checkerboards afford a dissociation between the predictions of the two approaches. Namely, the orientations of the explicit features (i.e., the edges) of a checkerboard are 0 ~ and 90 ~ while the orientations of the fundamental spatial frequency components are • 45 ~ Their procedure involved first identifying cells that produced optimal responding to a sinusoidal grating of some specific orientation (e.g., 0~ According to the feature detection approach, such a cell should exhibit optimal responding to a checkerboard pattern that contains edges oriented at 0 ~ while the spatial frequency approach would predict that such a cell would exhibit no response to such a checkerboard. Rather, that cell would respond optimally to a checkerboard whose edges were oriented at 45 ~ but whose fundamental Fourier component is at 0 ~ Their results confirmed the predictions of the spatial frequency approach: cells tuned to gratings at 0 ~ responded optimally to diagonally oriented checkerboard patterns. Additional evidence was reported concerning similar dissociations involving higher harmonic components and contrast. The ascending dominance of the spatial frequency approach in models of vision during the 1970s led to the first studies of visual field differences in spatial frequency processing, which will be discussed later (e.g., Blake & Mills, 1979; Rao, Rourke, & Whitman, 1981; Rijsdik, Kroon, & van der Wildt, 1980; Rovamo & Virsu, 1979). However, it was Justine Sergent who first formally proposed a model of cerebral hemispheric asymmetry in spatial frequency processing. She came to this hypothesis not through an interest in sensory psychophysics per se, but rather as an outgrowth of an interest in the cerebral bases for facial processing. In a thorough review of the literature, Sergent and Bindra (1981) proposed that perceptual characteristics of facial stimuli play an important role in determining which hemisphere exhibited superior performance. For example, experiments using faces consisting of line drawings and/or in which different faces differed by a single feature tended to yield LH advantages; photographs of faces and/or facial

Spatial Frequency

7

stimuli which differed on many features, on the other hand, tended to yield RH advantages. This led Sergent to the conclusion that a complete understanding of hemispheric differences in facial processing (and, more generally, in any higher-order type of process) required an understanding of potential hemispheric differences at lower .. sensory levels. More specifically, based on the fact that the facial studies that yielded LH versus RH advantages were biased towards the processing of fine versus coarse details, respectively, Sergent (1982) went on to propose that the LH versus RH were specialized for the processing of higher versus lower ranges of spatial frequency content of input. Initial tests of the spatial frequency hypothesis focused on indirect manipulations of the frequency content of input, with increases in size and retinal eccentricity, blurring, and decreases in luminance and exposure duration all attenuating the availability of high, relative to low, spatial frequencies; such manipulations were hypothesized to result in greater relative impairment of LH processing. Christman (1989) reviewed the relevant literature and concluded that there was moderate support for the spatial frequency hypothesis; however, he concluded that more definitive tests of the spatial frequency hypothesis would require the use of simpler grating stimuli or band-pass filtered stimuli. In the eight years since Christman's review was published, a substantial number of such studies have appeared, and are the focus of this chapter (the interested reader is also directed to a recent review by Grabowska and Nowicka [1996] that covers studies employing indirect manipulations of frequency content and/or electrophysiological measures that are beyond the scope of this chapter). Three domains will be reviewed: (i) studies employing single component stimuli, (ii) studies employing compound stimuli containing two or more components, and (iii) studies employing blurred or digitally filtered versions of more complex, naturalistic stimuli (e.g., letters, faces). The chapter will conclude with an evaluation of the current state of the spatial frequency hypothesis, along with recommended directions for future research.

I. Sinusoidal and Square-wave Stimuli A. Contrast Sensitivity/Detection The earliest studies of hemispheric processing of spatial frequency focused on contrast sensitivity, which refers to the threshold contrast

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Christman

necessary to detect a spatial frequency component. In general, human contrast sensitivity for foveal vision peaks at about 2-4 cpd; the peak shifts to lower frequencies with increasing retinal eccentricity. A number of studies appeared in the late 1970s and early 1980s examining contrast sensitivity functions in the left and right visual fields. The prevailing trend was a finding of hemispheric symmetry in the processing of spatial frequency. Blake and Mills (1979) reported no hemiretinal or hemispheric differences in contrast thresholds for 2 and 6 cpd stimuli. Rao, Rourke, and Whitman (1981) reported an overall LVF superiority in sensitivity to non-flickering gratings that did not interact with spatial frequency (all visual field interactions in their study were confined to effects of temporal frequency, with 0-2 Hz vs. 4-16 Hz being associated with LVF vs. RVF advantages, respectively). Beaton and Blakemore (1981) reported no hemispheric differences in contrast sensitivity for a 3 cpd test grating. Fiorentini and Berardi (1984) reported no hemispheric differences in contrast sensitivity across the range of 0.7 to 7.0 cpd. Kitterle and Kaye (1985) reported hemispheric symmetry in contrast sensitivity, employing a procedural variation in which, rather than determining the lowest contrast at which a given frequency is visible, they determined the highest resolvable frequency at a given contrast level. Peterzell, Harvey, and Hardyck (1989) reported no hemispheric differences in contrast sensitivity functions with gratings ranging from 0.5 to 12 cpd. Finally, Kitterle, Christman, and Hellige (1990) also reported hemispheric symmetry in contrast sensitivity over a range from 0.75 to 12.0 cpd, although they did report a marginal overall LVF advantage in RT that did not interact with frequency. The above studies all involved detection of gratings at threshold, and none indicated hemispheric ~differences as a function of spatial frequency (although two studies, Rao et al. [1979] and Kitterle et al. [1990] reported overall LVF advantages, possibly reflecting a LVF advantage in simple RT; see Christman and Niebauer, this volume). Kitterle et al. (1990) pointed out that the lack of hemispheric asymmetry may have arisen from (i) the threshold contrast levels, and/or (ii) the use of detection tasks; accordingly, they examined suprathreshold detection and also reported no hemispheric differences (although they once again found an overall LVF advantage for RT). Thus, research examining hemispheric differences in contrast sensitivity and spatial frequency detection yields no evidence of hemispheric differences as a function of spatial frequency for threshold or suprathreshold stimuli.

Spatial Frequency

9

B. Discrimination

Discrimination of spatial frequency in the LVF vs RVF has also been examined. Berardi and Fiorentini (1984) examined discrimination performance for successively presented gratings in which one stimulus was fixed at 1.0 cpd and found no visual field differences. Szelag, Budhoska, and Koltuska (1987) employed square-wave gratings (which consist of a fundamental component of frequency f, along with the odd frequency harmonics, i.e., 3f, 5f, 7f, etc.) in a successive same/different task (with "different" trials involving a one octave difference in frequency) and reported no interaction between visual field and spatial frequency. Boles and Morelli (1988) also employed square-wave gratings in a successive same/different task and found no visual field differences (it is not clear from their methods section what ranges of frequency differences were tested). Grabowska, Semenza, Denes, and Testa (1989) used square-wave gratings of low, intermediate, and high frequencies in a successive discrimination task with left- versus rightbrain damaged patients; although the right-brain damaged patients exhibited greater overall impairment, this effect did not interact with frequency. Kitterle and Selig (1991) had subjects decide whether the second of two successively presented sinusoidal gratings was higher or lower in frequency than the first; they reported LVF vs. RVF advantages in the low (1-2 cpd) vs. high (4-12) frequency ranges. Finally, Niebauer and Christman (1997), using the same basic task as Kitterle and Selig (1991), manipulated the interstimulus interval (ISI; 100 vs. 3600 msec) and frequency difference (0.125 vs 1.0 octave) in a discrimination task employing sinusoidal gratings; they found LVF advantages for low frequency stimuli (1.0 cpd) across both ISis and both frequency differences; the complementary RVF advantages for higher frequencies (4.0 cpd) were found for all conditions except the 0.125 octave difference, 100 msec ISI condition. The results for discrimination tasks are somewhat mixed. However, there are potential problems with a number of the studies reporting no visual field differences. For example, the studies by Grabowska et al. (1989) and Szelag et al. (1987) used a constant phase for their gratings, which meant that Ss could have based responses on local luminance cues, and not the frequency of input as such. The two studies reporting visual field X frequency interactions (Kitterle & Selig, 1991; Niebauer & Christman, 1997) randomly varied the phase of the stimuli. Similarly,

10 Christman the procedures of Grabowska et al. (1989), Szelag et al. (1987), and Boles and Morelli (1987) involved uncontrolled luminance changes upon stimulus presentation; given evidence that such luminance changes can have complex and differential masking effects on different ranges of spatial frequency (e.g., Kitterle, Beasley, & Berta, 1984; Green, 1981), it is not clear how to evaluate their results. Again, the studies by Kitterle and Selig (1991) and Niebauer and Christman (1997) kept display luminance constant. Finally, with the exception of the study by Fiorentini and Berardi (1984), all studies reporting no visual field differences employed square-wave gratings, which contain broad ranges of frequency components and are therefore less than ideal for testing hemispheric differences in the processing of narrow and specific ranges of frequency. Thus, the evidence suggests that when sinusoidal stimuli are used and the procedures force Ss to base their responses on the frequency of input as such, there are RVF versus LVF advantages in discriminating stimuli of higher versus lower frequency, respectively. C. Identification

Few studies involving identification of spatial frequency have been conducted. Indeed, the author knows of only one relevant paper. Kitterle, Christman, and Hellige (1990) examined threshold and suprathreshold identification of spatial frequency as a function of visual field. Threshold data indicate that hemispheric differences depend on criteria used to define threshold. Their data indicate that visual field X spatial frequency interactions do not emerge until performance is at or above approximately 80% correct (this is close to the 75% criterion commonly used in psychophysical studies of threshold processing). Furthermore, they found that the visual field X frequency interaction reflected no hemispheric differences at lower frequencies and RVF advantages at higher frequencies. RT data yielded a trend towards a comparable visual field X frequency interaction (p, 0

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generally discarded during the Seventies (see relative reviews in Benton, 1975; Vellutino, 1979). However, in the early '80s, Lovegrove and coworkers proposed that a high percentage of specifically-disabled readers was affected by a low-level visual deficit, in particular in the transient system (after the paper in Science by Lovegrove, Bowling, Badcock, & Blackwood, 1980, many other works were published; see a first review in Lovegrove, Martin, & Slaghuis, 1986). Psychophysical data showed that disabled readers had a specific impairment in processing low SF and high TF. Considering that transient system has a crucial role in the integration of information from successive fixations (such as in reading: Breitmeyer, 1983), Lovegrove suggested that an abnormal functioning of the transient system might be one of the main cause of reading disability. Abnormalities of VEPs for gratings at low SF were recorded in children with reading disability (May, Lovegrove, Martin, & Nelson, 1991), supporting the hypothesis of a deficit in the transient system.

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Also differences in VEPs for checkerboards of different check size were found between controls and poor readers by Mecacci, Sechi, & Levi (1983), and were interpreted as evidence of basic visual impairments in reading disability (the results are discussed also in the framework of their hypothesis by Lovegrove et al., 1986, pp. 255-256). The question was updated in terms of the distinction between the magnocellular and parvocellular pathways. In the work by Livingstone, Rosen, Drislane, and Galaburda (1991) on VEPs in dyslexic individuals, abnormalities of VEPs were found for checkerboards at high TF, low luminance and low contrast. Results were interpreted as the correlate of a loss of magnocellular neurons and the main cause of reading disability. This hypothesis was tested by Victor, Conte, Burton, and Nass (1993) recording transient and steady-state VEPs in dyslexics, patient controls, and normals. Contrast, luminance and TF of checkerboards were varied. However the results by Livingstone et al. (1991) were not confirmed. The hypothesis of an impairment of the magnocellular pathway in specific reading disability requires further investigation, using more adequate psychophysical or electrophysiological procedures to differentiate the contributions of the parvocellular vs. magnocellular visual pathways (see the work by Spinelli, Angelelli, De Luca, & Burr, 1996).

Evidence from brain-injured patients Impairment of SF and TF processing has been frequently shown in several cases of individuals affected by brain lesions. Some investigations were carried out by means of psychophysical methods, other works have been conducted by means of VEP recording (on the use of EP technique in neuropsychological research, see Viggiano, 1996). Spatial contrast sensitivity was found to be seriously reduced in patients with lesions in the visual cortex (Bodis-Wollner, 1976; Bodis-Wollner & Diamond, 1976; a review of these results in Regan, 1989). If a general impairment in the processing of spatial and temporal parameters of basic visual information may be expected, the effect of damaged hemisphere (left or right) on the type and severity degree of deficit remains an open question. In the work by Hess, Zihl, Pointer, and Schmidt (1990), contrast sensitivity for sine-wave gratings of different spatial frequencies was tested in 62 patients. No relation was found between the side of lesion and the range of SF (low or high) for which a deficit in contrast sensitivity was ascertained. Other works have found a

Temporal Frequency

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special impairment of spatial contrast sensitivity in patients with RH than LH lesions. In the work by Kobayashi, Mukuno, Ishikawa, and Tasaki (1985) on 23 patients with unilateral lesions, the contrast sensitivity impairment was more serious in patients with right parieto-occipital lesions and hemispatial agnosia syndrome than in patients with lesion to the same areas of left hemisphere. In the work by Grabowska, Semenza, Denes, and Testa (1989), the performance in a discrimination test (subjects had to judge whether the SF of the second square-wave grating was the same as that for the first one presented 2 sec before for a 300msec duration) was more impaired in patients with fight lesions (N=19) than in patients with left lesions (N=24), and in control subjects (N=28). Another group of investigations focused on the impairment of contrast sensitivity and processing of SF and TF in patients affected by unilateral spatial neglect syndrome (briefly, hemineglect). Hemineglect is generally associated with lesions of right parietal areas, in particular the cortex of the right inferior parietal lobe. These patients ignore stimuli presented in the left part of visual field and do not explore this side of the space by means of eye movements. Although hemineglect syndrome is now generally explained by deficit at higher levels of information processing, some works have tried to verify the hypothesis that a basic sensory-perceptual deficit is the main cause of this neuropsychological impairment (for a review, Bisiach & Vallar, 1988). To test whether basic visual information is impaired in hemineglect patients, a series of investigations was carried out by Spinelli and her coworkers. In a first study (Spinelli, Guariglia, Massironi, Pizzamiglio, & Zoccolotti, 1990), contrast sensitivity and performance in a discrimination test (subjects had to judge whether the bars in the upper and lower parts of the stimulus - divided in two equal parts - were equal or different) were tested in 26 patients with lesions to right hemisphere (15 patients with hemineglect syndrome). A general impairment in contrast sensitivity, especially in the range of low SF, was found in brain-injured patients, but no special deficit was shown by hemineglect patients. In a second study (Spinelli & Zoccolotti, 1992), the contrast sensitivity for stationary and moving sine-wave gratings was psychophysically tested in 17 patients (5 with hemineglect) and 5 control subjects. Both the impairment of contrast sensitivity for low SF in patients and the absence of special deficit in hemineglect patients were confirmed. However the question remained whether impairments might be found in relation to TF processing interacting with SF analysis. A systematic investigation on

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VEPs by checkerboards varying in both check size (range: 12-72 min of arc)and TF (phase-reversal mode; range: 1.96-16.6 Hz), was carried out in 20 patients (10 fight-damaged with hemineglect, 4 right-damaged without neglect, 6 left-damaged) and 6 controls (Viggiano, Spinelli, & Mecacci, 1995). In the condition of peripheral stimulation, no significant difference was found between patients and controls. In hemineglect patients, VEPs by stimuli presented to left (neglected) hemifield had smaller amplitudes compared to VEPs by stimuli to right hemifield, but the difference did not reach the statistical significance (p=0.08). In the condition of central stimulation, VEPs recorded in patients had smaller amplitudes than in controls (p

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whole range. In comparison with unilateral displays, accuracy on bilateral displays was better for left field targets and worse for right field targets. This confirms that the two hemispheres were competing for something they both needed when searching in bilateral displays, even when displays were brief and response time was not at issue. As in the response time version of the task, the right hemisphere won the competition. The results for a split brain observer (JW) are shown in Figure 9. There are two differences from the data of normal observers that are immediately apparent. First, the interaction of hemifield and type of display seen for normal observers was not evident here. The left hemisphere showed a tendency for more accurate search in both unilateral and bilateral displays, especially as display size was increased. This replicated the RT task in showing that the competition seen normally between hemispheres during visual search on bilateral displays does not occur when the corpus callosum is sectioned. A second difference from the search data of normal observers was the markedly steeper search slopes in bilateral than in unilateral displays. Over the small display sizes (2 to 6 items) the search slopes were similar (5% per item for unilateral and 7% per item for bilateral). For larger display sizes, however, the search slope was almost flat for unilateral displays (0% per item), yet it decreased 1.5% per item for bilateral displays. This finding points to an important competition between the hemispheres of a split brain observer that is not evident in normal observers. Note too that this finding runs completely counter to the implication derived from Luck et al (1989, 1994), and replicated in our RT task for small display sizes (Figure 8), that the separated hemispheres of split brain observers have independent systems for visual search. On the contrary, these data indicate that the separated hemispheres of split brain observers draw on a common system of attention in a visual search task. These experiments therefore point to two different aspects of hemispheric coordination in the visual search task. First, there is an apparent competition between the hemispheres for visual search mechanisms that is only evident when the connections between hemispheres are intact. Faced with bilateral displays, the right hemisphere searched more efficiently and the left hemisphere less efficiently than they did when presented with the same items in a unilateral display. Disconnecting the hemispheres by sectioning the

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corpus callosum eliminated this form of competition, allowing visual search in each hemisphere of the split brain observer to be largely unaffected by these display differences. Second, there is a competition between the hemispheres for subcortical mechanisms necessary for visual search. This competition can only be seen following callosotomy. It is glaringly apparent in visual search performed by split brain observers when large display sizes are compared under unilateral and bilateral conditions. The split brain observer become very inaccurate when searching through large numbers of items that were distributed across both visual fields. Note that the large number of items are not at issue. Search by JW through the same number of items was much more accurate when the items were presented to only one hemisphere. In fact, in these displays each hemisphere was actually viewing twice the number of items, yet performing more accurately. The brief exposure duration was also not at issue for a similar reason: accuracy was much better for the same number of items, provided they were all presented in the same visual field. Finally, these results could not be explained by any simple form of hemispheric specialization. JW showed the same tendency for a left brain advantage when searching in either unilateral or bilateral displays. We were therefore compelled to conclude that there must be subcortical mechanisms, important to visual search, that are in demand by each hemisphere in the split brain observer. When the corpus callosum is intact, these mechanisms are presumably used by both hemispheres in a coordinated fashion. Any competition is resolved before it has the opportunity to express itself in behavior. It is only when the hemispheres lose the ability to communicate directly, that an overt competition for these mechanisms is observed.

Hemifield competition in object identification How general is the finding that the hemispheres compete for subcortical structures in tasks involving spatial attention? We addressed this question with a divided attention task that was much simpler than visual search (Duncan, 1980, 1984, in press). In this task, only one or two items are presented briefly on each trial and the observer is asked to identify one of them by indicating whether or not it corresponds to a subsequent probe item. The general result is that accuracy in this task is consistently lower (and correct response times are slower) when two

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items have been presented than when only one is shown. This effect is often referred to as a two-object cost. In the present study we asked whether the two-object cost was any different for unilateral and bilateral visual displays. Examples of the stimulus displays are shown in Figure 10. Each trial began with a view of four sets of location markers, at the comers of an imaginary square 3 degrees from fixation, showing where display items would be presented. Four shapes (vertical or horizontal bars) were then flashed briefly (60, 100, or 150 ms). One or two of the shapes were black, the remainder were white. Observers were told to attend only to the black shapes and were asked to indicate the shape of one of them immediately following a brief mask (180 ms) at each of the four locations. The probe, a black shape that was either the same or opposite to the target, stayed on view until the observer responded or until 2 s had elapsed. Observers pressed a left-hand key if a match was detected on the left side of the display and they pressed a fight-hand key if a match was detected on the fight side. Displays were evenly divided between one-target, two-target unilateral (targets in the same field), and two-target bilateral (targets in different fields). The key factor in this experiment was whether the two targets were presented unilaterally or bilaterally. If the two connected hemispheres could each perform object identification separately, then the two-object cost should be reduced or eliminated in normal observers viewing bilateral displays. If each of the hemispheres were capable of identifying the items independently, but only when direct connections between hemispheres were severed, then the two-object cost should be reduced in split brain observers viewing bilateral displays. This would be consistent with the proposal of independent attention systems (Luck et al., 1989, 1994). Finally, if the two hemispheres drew on shared subcortical structures, there should be an increased two-object cost in one hemisphere in the split brain observer (in the hemisphere losing the competition), along with a reduced two-object cost in his other hemisphere (in the hemisphere winning the competition). This would be consistent with the proposal of a shared subcortical system as seen in the previous visual search study. Results for two groups of normal college-age observers are shown in Figure 11. Each observer contributed 320 trials. One group was tested with a stronger mask than the other group (random black and white shapes) in order to examine the accuracy pattern at two different levels

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of difficulty. This had no effect on the results other than changing the overall level of task difficulty. In each case, a two-object cost was obtained to approximately the s a m e degree in both unilateral and bilateral displays. The visual field of the item to be reported had no additional influence on accuracy. The results for JW are shown in Figure 12, averaged over 640 trials of testing. Averaged over visual field, the pattern of results was identical to that for the normal observers: a similar two-object cost was observed

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in unilateral and bilateral displays. However, there was also a large interaction with visual field. The fight hemisphere (left field) showed no significant two-object cost on bilateral displays, whereas the left h e m i s p h e r e (right field) showed a two-obJect cost that was approximately twice as large on bilateral than on unilateral displays. This finding is consistent with the proposal of a shared subcortical system for spatial attention tasks.

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Discussion In this section we discuss various aspects of the results from our three studies, examining threads common to all of them, as well as pointing out important differences between the studies. We do this by attempting to answer four questions that emerge quite naturally from the results of these studies. Why did normal observers demonstrate hemispheric competition when performing visual search on bilateral displays? Visual search was most efficient for normal observers on bilateral displays when the target was presented to the right hemisphere. This result stood in sharp contrast to their search in unilateral displays, where targets were detected in a very similar way in both visual fields. It also stood in contrast to the results of a split brain observer, who performed visual search for left and right targets in very much the same way on unilateral and bilateral displays. A scanning bias? One possibility that must be considered before loftier theoretical speculations arc made is that this result was the consequence of a strategic decision by normal observers. Perhaps normal observers adopted a left-to-right scanning strategy, thereby giving targets in the left visual field an advantage over those in the right field. This would explain an advantage for targets on the left in bilateral

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displays. However, it encounters difficulties with several other aspects of the data. First, this account predicts a left field advantage that should grow along with display size, since an increasing number of left field items would have to be inspected before the right field items could be inspected. This prediction was not supported by either the response time task (Figure 6) or the brief exposure task (Figure 8). In both cases, the advantage for left side targets on bilateral displays remained fairly constant across display size, and in some cases performance actually converged with display size for targets in the two visual fields. Second, there were strong hints of nonlinearities in the way performance changed with display size for left side targets. Such nonlinearities are also not predicted by a scanning bias explanation. Consider the slopes from display size 2-8 and then again from display size 8-24 in the two tasks (Figures 6 and 8). In each case, slopes are relatively shallow in the small range and then much steeper in the larger range, to the extent that target detection is similar on both sides at the largest display sizes. This points to a qualitative difference, rather than merely a quantitative difference, between search by the right hemisphere in unilateral versus bilateral displays. Third, a scanning strategy that produced a general left-side advantage should have been evident in normal observers performing the global-local search task (Figure 2), in a split brain observer performing visual search tasks (Figures 3 and 7), and in normal and split brain observers performing the object identification task (Figures 11 and 12). This feature was clearly not a general one of spatial attention tasks, and as such, it strengthens our confidence in its importance to visual search for these specific items. Fourth, a left-to-right scanning strategy should have produced results that were similar for unilateral displays and for targets on the left side in bilateral displays. This hypothesis was examined by comparing he average performance on unilateral displays with that on bilateral displays for the corresponding display sizes. This is shown in Figure 13. Note that in this comparison, a unilateral display size of 12 corresponds to a bilateral display size of 24, a unilateral display of 8 corresponds to a bilateral display size of 16 items, etc. These are the comparable conditions for someone scanning the displays from left to right. The comparison given in Figure 13 shows that this hypothesis was not supported. Except for left side targets in the smallest three display

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sizes, search for both left and fight side targets was consistently less efficient than for the comparable display sizes in unilateral displays. This points to a competition between the hemispheres that goes well beyond a scanning bias. A competition for mechanisms of feature integration? T h e hemispheric competition was observed in only one task for normal observers, the visual search task patterned after Luck et al (1989, 1994). It was not observed in the global-local visual search task, nor in the object identification task. What distinguished this task from the others? Although there are many differences that could be considered, one theoretically important one is that of feature conjunction. Only the Luck-style task involved search for targets defined solely by the spatial relations among identical elements (white and black squares). This is equivalent to a conjunction of brightness level and relative location (see Figure 5). The global-local search task and the object identification task, on the other hand, involved search for targets defined by the simple feature of item orientation. It is true that in the global-local task, item

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orientation had to be determined on the basis of dots that were nonabutting and sometimes of different levels of brightness. Nonetheless, it is likely that the resulting signal concerning item orientation is simpler than the signal for the conjunction of brightness and relative location. Perhaps feature integration involves communication between the hemispheres, at least in observers with an intact corpus callosum. This possibility will clearly have to await additional tests before it can be fully accepted. However, we think it warrants some consideration, in particular, concerning the question of why feature integration may be susceptible to hemispheric competition. If nothing else, such speculation will help guide future experiments that disconfirm the hypotheses. One possibility, therefore, is that the intact brain is organized to permit conjunctions of features to emerge into consciousness for only one location or object at a time. Such an organization would promote unified and coherent action to objects in the visual environment. There is also growing support for such a view among researchers studying the neuropsychological conditions of neglect and extinction (Baylis, Driver, & Rafal, 1993; Cohen & Rafal, 1991; Cohen, Ivry, Rafal, & Kohn, 1995). In the split brain observer, these constraints would no longer be at work and so feature conjunction might be able to proceed independently in the two hemispheres. Another possibility is that visual search for targets defined by feature conjunctions involves more than one attention system: a cortical and a subcortical one. Neurophysiological research suggests that feature integration is performed by mechanisms in the temporal lobe of the cortex. Receptive fields of neurons in this brain region are large in size, often crossing the vertical meridian, and are sensitive to complex combinations of features (Laberge, 1995; Moran & Desimone, 1985). The mechanisms important to search, on the other hand, have large subcortical components. Eye movements to various locations in a display, as well as covert movements of the mind's eye, involve mechanisms in the superior colliculus. The engagement of attention on a new item is governed by mechanisms in the pulvinar nucleus of the thalamus (Laberge, 1995; Posner & Raichle, 1993). The competition seen in visual search by normal observers may therefore be an interaction between these two systems. Search for conjunction-defined targets may activate a competition for activity in temporal lobe neurons, as well as a competition for control of neurons in the thalamus and superior colliculus. Severing the direct connections between the hemispheres, as

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in the split brain observer, may therefore eliminate the cortical aspect of this competition. The loser-wins? One form of hemispheric competition that may be playing itself out in visual search is that between bottom-up (data driven) and top-down (strategic or intentional) mechanisms. As discussed in the introduction to these experiments, visual search is guided by a combination of data driven mechanisms that include spatially-parallel operations for rapid grouping and segmentation, and strategic mechanisms which control the locus of the attentional gaze. It is also strongly possible that one hemisphere is more adept in the use of one of these mechanisms than the other. On the basis of past research on visual search by split-brain observers (Kingstone et al, 1995; Luck et al, 1989, 1994), one might suspect that the left hemisphere was most adept, or at least most dominant, in assuming strategic control over the voluntary locus of attention. Finally, the present results from the splitbrain observer in visual search and object identification tasks indicates that the division of attention between the hemispheres involves a competition for a common mechanisms. Armed with these premises, the following scenario can be considered. In an effort to control visual search on bilateral displays, the left hemisphere searches diligently through the items on the fight side of the display. Control of attention by the left hemisphere in this way leaves little, if any, of the voluntary control mechanisms for use by the fight hemisphere. As such, fight hemisphere search is conducted, at least in the small range of display sizes, by the bottom-up mechanisms of rapid grouping and segmentation. Such mechanisms might indeed be able to point to a target when the display size is small, or when the target is highly distinctive (Pashler, 1987; Treisman, 1982). However, they will also fail at some point, when the relative salience of the target is too low relative to the distractors. From that point on, controlled visual search will be required for targets on the left side as well. This account provides a reason for the nonlinearities seen in the search slopes for targets on the left side in bilateral displays. Slopes should be shallow for small display sizes, reflecting the operation of bottom-up mechanisms in the right hemisphere. The finding that these shallow search slopes were also associated with response times and accuracy levels that were better, in absolute terms, than the performance levels associated with voluntary control of attention, is not predicted explicitly by this account. However, it does fit reasonably well with the

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rest of the account, given the slower time course of endogenous versus exogenous orienting (Cheal & Lyon, 1991). The hemispheric competition, in this view, is thus for brain structures important for the voluntary control of attention. This competition is "won" by the left hemisphere, which is often dominant in these matters. This has the unintended consequence of permitting the right hemisphere to perform search primarily with bottom-up mechanisms. These are actually more efficient than voluntary control mechanisms, at least for small display sizes, and so the hemisphere which "loses" the hemispheric competition actually "wins" the behavioral race. The finding that the split-brain observer failed to show this form of competition points further to a competition that involves interhemispheric communication. Why did the split-brain observer show hemispheric competition when performing visual search and item identification on bilateral displays? The split-brain observer was at a large disadvantage in searching through bilateral displays, in comparison to search through the same number of items in unilateral displays. This was true both for targets presented to the left hemisphere, which was generally more adept at search, and for targets presented to the fight hemisphere. This observer also showed a large interaction between visual field and type of display in the object identification study. In this case, his right hemisphere showed an advantage in bilateral displays, showing no interference from the item displayed to the left hemisphere, whereas the left hemisphere suffered noticeably in object identification when another item was presented to the right hemisphere on bilateral displays. What are the subcortical mechanisms that are shared between the disconnected hemispheres in these spatial attention tasks? Posner and Raichle (1993) point to two systems that are each relevant to these tasks. The first is a midbrain structure known as the superior colliculus. Neurons in this structure are not only highly active during the initiation and execution of eye movements, but are also active when the mind's eye moves covertly from one scene location to another (Holtzman, 1984, Wurtz, 1996). When the superior colliculus is damaged in animals, eye movement responses to cues become delayed. A disease in humans known as progressive supranuclear palsy causes selective damage to this brain region, dramatically slowing both eye movements and covert shifts of attention (Rafal, Posner, Friedman, Inhoff & Bernstein, 1988). Finally, studies of covert orienting in split brain observers confirm that cues presented to one visual field can produce orienting responses to

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targets in the other visual field (Holtzman et al., 1981; Holtzman, 1984). This indicates that information is being passed between hemispheres in a spatial attention task involving the superior colliculus, but that the route of communication cannot be cortical. A second relevant subcortical structure is the thalamus. It has long been assigned an important role in the selection of information from multiple sources (Crick, 1984). More recently, PET studies have provided direct evidence of its importance in a visual filtering task (Laberge & Buchsbaum, 1990). During the time an observer was selectively attending to a target item surrounded by distractors, neuronal activity increased in the pulvinar nucleus of the thalamus, but not in other regions of the thalamus, or in cortical visual regions. The functions supported by each of these subcortical structures were important in the efficient performance of the tasks in our studies. Visual search and bilateral object identification both require controlled shifts of attention between items in a visual display; they also require that some items be filtered out from further consideration (i.e., distractors in visual search; the white items in object identification). Our findings therefore indicate that these subcortical functions cannot be performed independently for each of the two hemispheres at the same time. In unilateral displays, the entire system can be devoted to a single hemisphere because of the absence of competition. However, in bilateral displays, one hemisphere gains control over the system, causing a direct detriment in performance for the other hemisphere.

What are implications for understanding spatial attention? The larger point made by these patterns of hemispheric competition is that the performance of complex tasks involves the coordination of activity in a number of specialized brain regions (Zeki, 1995). Tasks involving spatial attention are no exception. Multiple specialized brain regions are involved and so speeded and accurate responses require the coordination of a network of distributed systems (Posner & Raichle, 1993). One unique contribution of the present s t u d i e s is the demonstration that some of these issues can be studied in normal observers. Previous to this study, one form of hemispheric coordination had been studied in patients with damage to the parietal lobes. Damage to this region, especially if it is on the right side, often results in various

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forms of neglect of the opposite (left) side of visual space (Kinsbourne, 1977; Rafal, 1994). These patients often fail to notice objects on the left side of the vertical meridian, sometimes they neglect only the left side of objects wherever they appear in the visual field, and sometimes they neglect the left side of their own bodies. It is as though the damaged fight parietal lobe no longer competes with the left lobe for control over attentional mechanisms. A more subtle form of visual neglect, termed visual extinction, is observed in some patients, who tend to show contralateral field neglect only when the ipsilateral visual field is also stimulated (Baylis, Driver and Rafal, 1993; Bradshaw & Mattingly, 1995; Valler, Rusconi, Bignamini, Geminiani, & Perani, 1995). In some cases, even this extinction is modulated by the visual similarity and perceptual coherence of the items in the two visual fields (Ward & Goodrich, 1996). Extinction is strongest when the item in the "good" visual field is most similar to that in the damaged field; extinction is weakened if the items in the two fields are grouped into a single object via connectedness or other Gestalt principles. This clinical phenomenon is therefore additional evidence for hemispheric competition when one region of the brain has been damaged. We are aware of only one previous study of hemispheric competition in normal observers (Reuter-Lorenz, Kinsbourne, & Moscovitch, 1990). In that study, observers were given a line bisection task in conjunction with a stimulus that selectively activated one or the other hemisphere. Errors in line bisection were biased by the hemisphere activation stimulus, such that a longer line segment was perceived in the visual field contralateral to the activated hemisphere. In addition, a rightward orienting bias (left hemisphere dominance) was observed when the two hemispheres were placed into direct competition. These results were interpreted within the framework of the activation-orienting hypothesis (Kinsbourne, 1977), which proposes that control over attentional orienting is governed by a dynamic balance between opponentprocesses in the two hemispheres. These processes are ordinarily in rough balance, with a slight tendency to favor the right side of space. However, selective injury to either side of the brain will result in an imbalance, producing the clinical conditions of hemifield neglect and extinction. From this perspective, the present evidence of hemispheric competition in the visual search task points to yet another behavioral domain in

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which hemispheric coordination can be studied in normal observers. We suspect that other domains will be found. It appears that the key ingredient to observing it in our study was the comparison between performance on unilateral and bilateral displays. Informal anecdotes we have begun collecting from other researchers suggest that this may not be an unusual occurrence. For example, judgments of the direction of coherent motion in a random-dot display are severely compromised by the presence of an irrelevant motion pattern in the opposite visual field (Jane Raymond, personal communication). Competition between the two hemispheres of normal observers will perhaps be seen in any situation in which the two hemispheres are unequal in their abilities, or at least unequal in their demand for preeminence. The challenge for researchers will be to design behavioral tasks that allow the competition to be visible in performance.

Implications for understanding hemispheric specialization Most of the emphasis in past research on hemispheric differences has been on specialization. The guiding questions have been "What tasks are each hemisphere best equipped to perform?" and "What kinds of specialized equipment does each hemisphere bring to a task?" Implicit in this approach is the assumption that specializations are hard-wired, or least very well-established in their home hemisphere as a result of experience and maturation. We are calling for a different emphasis. Instead of viewing evidence of specialization as a direct reflection of the resident equipment of that hemisphere, one should view specialization as the outcome of a competition for control over the network of distributed resources required to perform the task. That is, specialization may not reflect a difference in hemispheric circuitry or algorithms so much as hemispheric dominance in the competition. One reason we propose this view of specialization is because of the diverse pattern of hemispheric specialization seen in split brain observers. Consider JW, without a doubt the most thoroughly studied of these observers. His left hemisphere consistently outperforms his right hemisphere in the Luck-style search task (Luck et al, 1989, 1994; present study), yet his right hemisphere is dominant over the left in the object identification task. Both of these tasks place a heavy demand on the division of attention between spatially separated items; yet the story

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on "specialization" is different. We think that there is no reason to expect a uniform pattern of hemisphere dominance if the dominance reflects the outcome of a competition for distributed resources rather than inherent differences in processing. Instead, one might expect dominance to vary a great deal with the task, since each task uses these distributed resources in a slightly different way. Perhaps the most vivid example of this view of specialization comes from JW's visual search performance when a conjunction-defined target is placed among an imbalanced ratio of distractors. An intelligent search strategy would be to search among the smaller of the two subsets of distractors that share a feature with the target. Although normal observers employ this "guided search" strategy for targets in either visual field, JW and one other split brain observer did so for targets on the right side (Kingstone et al, 1995). It therefore appeared that the left hemisphere was specialized for guided search. However, subsequent testing has revealed that JW can perform guided search with his right hemisphere (left field displays), provided that these displays occur in a block of trials in which the left hemisphere is not presented with an imbalanced ratio of distractors (Kingstone & Enns, unpublished). We conclude that the apparent specialization of the left hemisphere for guided search should more correctly be seen as a dominance of the left hemisphere when placed in competition with the right hemisphere for task-relevant mechanisms. How should questions of specialization be distinguished from issues of hemispheric coordination in future research? One of the necessary first steps is to design experiments that systematically vary the degree of competition between hemispheres. The traditional approach of specialization studies involves comparisons of unilateral left and right field displays, or comparisons of bilateral displays in which the target item is in the left or the fight field. This does not manipulate the level of competition. It is only when unilateral and bilateral displays are compared for the same visual field that competition can be studied. Our studies, involving a simple comparison of this kind, represent only the beginning of what is possible with this methodology. In future studies we plan to systematically vary the nature of the stimulus in the competing visual field, in a similar way to how this has been done in studies of extinction following parietal lobe damage (Baylis, et al, 1993; Ward & Goodrich, 1996).

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Acknowledgments The research described in this chapter was supported by grants from the Natural Science and Engineering Research Council of Canada to both authors and by a grant from the Alberta Heritage Foundation to A. Kingstone.

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Duncan, .L, & Humphreys, G. W. (1989). Visual search and stimulus similarity. Psychological Review, 96, 433-458. Enns, J. T. & Kingstone, A. (1995). Access to global and local properties in visual search for compound stimuli. Psychological Science, 6, 283-291. Holtzman, J. D. (1984). Interactions between cortical and subcortical visual areas: Evidence from human commissurotomy patients. Vision Research, 24, 801-813. Holtzman, J. D., Sidtis, J. J., Vol~, B. T., Wilson, D. H., & Gazzan!ga, M. S. (1981). Dissociation of spatial information Ior stimulus localization and the control of attention. Brain, 104,861-872. Hughes, H. C., Fendrich, R., & Reuter-Lorenz, P. A. (1990). Global versus local processing in the absence of low spatial frequencies. Journal of Cognitive Neuroscience, 2, 272-282.

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Jane Raymond (personal communication). Department of Psychology. University of North Wales, Bangor, Wales. Kinchla, R. A., & Wolfe, J. M. (1979). The order of visual processing: "top-down", bottom-up" or "middle out". Perception & Psychophysics, 25, 225-231. Kingstone & Enns, unpublished. The lateralization of guided search: "Hardware" versus "software". Kingstone, A., Enns, J. T., Mangun, G. R., & Gazzaniga, M. S. (1995). Guided visual search is a left-hemisphere process in split-brain patients. Psychological Science, 6, 118-121. Kinsbourne, M. (1977). Hemi-inattention and hemispheric rivalry. In E. A. Weinstein & R. P. Freidland (Eds.), ttemi-attention and hemispheric specialization: Vol. 18. Advances in Neurology (pp. 4149). New York: Raven Press. Kitterle, F. L., Christman, S., & Conesa, J. (1993). Hemispheric differences in the interference among components of compound gratings. Perception & Psychophysics, 54, 785-793. Laberge, D., & Buchsbaum, M. S. (1990). Positron emission tomographic measurements of pulvinar activity during an attention task. Journal of Neuroscience, 10, 613-619. Laberge, D. (1995). Computational and anatomical models of selective attention in object identification. In M. S. Gazzaniga (Ed.), The cognitive neurosciences (pp. 649-663). Cambridge, MA: MIT Press. Lamb, M. R., & Robertson, "I5. C. (1990). The effect of visual angle on global and local reaction times depends on the set of visual angles presented. Perception & Psychophysics, 47, 489-4%. Lamb, M. R., Robertson, L. C., & Kni.ght, R. T. (1990). Component mechanisms underlying the processing of hierarchically organized patterns: Inferences from patients with unilateral cortical lesions.

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Luck, S., Hillyard, S. A., Mangun, G. R. & Gazzaniga, M. S. (1989). Independent hemispheric attentional systems mediate visual search in split-brain patients. Nature, 342, 543-545. Luck, S. J., Hillyard, S. A., Mangun, G. R., & Gazzaniga, M. S. (1994). Independent attentional scanning in the separated hemispheres of split-brain patients. Journal of Cognitive Neuroscience, 6, 84-91. Martin, M. (1979). Local and global processing: The role of sparsity. Memory & Cognition, 7, 476-484. Moran, J., Desimone, R. (August, 1985). Selective attention gates visual processing in the extrastriate cortex. Science, 229, 782-784. Navon, D. (1983). How many trees does it take to make a forest? Perception, 12, 239-254. Pashler, H. (1987). Detecting conjunctions of color and form: Reassessing the serial search hypothesis. Perception & Psychophysics, 41, 191-201. Posner, M. I., & Raichle, M. E. (1993). Images of mind. NY: Scientific American Library. Rafal, R. (1994). Neglect. Current Opinion in Neurobiology, 4, 231-236.

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Rafal, R. D., Posner, M. I., Friedman, J. H., Inhoff, A. W., & Bernstein, E. (1988). Orienting of visual attention in progressive supranuclear palsy. Brain, 111, 267-280. Raymond, J. (personal communication). Department of Psychology. University of North Wales, Bangor, Wales. Reuter-Lorenz, P. A., Kinsbourne, M., & Moscovitch, M. (1990). Hemispheric control of spatial attention. Brain & Cognition, 12, 240266. Robertson, L. C., & Lamb, M. R. (1991). Neuropsychological contributions to theories of part/whole organization. Cognitive Psychology, 23, 299-330. Treisman, A. (1982). Perceptual grouping and attention in visual search for features and for objects. Journal of Experimental Psychology: Human Perception & Performance, 8, 194-214. Treisman, A., & Gelade, G. (1980). A feature integration theory of attention. Cognitive Psychology, 12, 97-136. Valler, G. Rusconi, M. L., Bignamini, L., Geminiani, G. & Perani, D. (1995). Anatomical correlates of visual and tactile extinction in humans: A clinical CT scan study. Journal of Neurology, Neurosurgery, & Psychiatry, 57, 464-70. Ward, R, & Goodrich, S. (1996). Differences between objects and nonobjects in visual extinction: A competition for attention. Psychological Science, 7, 177-180. Wolfe, J. M., Cave, K. R., & Franzel, S. L. (1988). Guided search: An alternative to the feature integration model for visual search. Journal

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419-433. Wurtz, R. H. (19%). Vision for the control of movement. Investigative Ophthalmology and Visual Science, 37, 2131-2145. Zeki, S. (1995). A vision of the brain. Boston, MA: Blackwell.

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Asymmetries in the Flanker Compatibility Effect Frederick Kitterle Northern Illinois University Mark R. Ludorf & Jeremy Moreland Stephen F. Austin State University One issue of concern in studies of selective visual attention is degree to which attention can be narrowly focused on a given spatial location such that stimuli falling within this region are fully processed, whereas those falling outside the focal region are excluded from processing. Several studies indicate that the ability to do this is limited. That is, stimuli that fall outside the zone of attention, which are irrelevant to the task, in fact may interfere with the efficient performance of the task, cannot be ignored and thus, influence the processing of stimuli within the focal region. For example, Eriksen and Eriksen (1974) found that when a target letter that was associated with a given response was flanked by letters that were associated with the same response (response compatible condition), time to identify the target was somewhat faster (although not consistently so) than if flanked by letters that has no assigned response (response neutral condition). On the other hand when the target was surrounded by letters that were associated with a different response (response incompatible condition), reaction time to identify the target was considerably longer than the response neutral condition. The difference in reaction time between the incompatible and the compatible

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conditions reflects the degree to which the flankers influence reaction time to the target. This is referred to as the flanker compatibility effect (FCE; see Eriksen, 1995 for a review). Thus, even though the task explicitly requires identifying the central target letter in a string of three letters and ignoring the flanking letters, the FCE indicates that the flanking letters cannot be ignored; rather they are also identified and influence RT to the central target letter. Thus, there appears to be a limit on the degree to which attention can be narrowed. Several studies have addressed the issue of where in the information processing stream that limit is set, that is, whether the FCE reflects an early or late selection process. Early selection processes (e.g., Treisman, 1964) hypothesize that the processing of stimuli outside of the focus of attention is confined to rudimentary physical properties whereas, for late selection theories (e.g., Deutsch & Deutsch, 1963), stimuli outside the focus of attention are fully identified. Eriksen and Eriksen (1974) found that the magnitude of the FCE decreased with spatial separation. Nevertheless, the effect is quite robust; it is still present at large spatial separations (e.g., Miller, 1991). Eriksen and Eriksen (1974) have interpreted this as evidence for an imperfect late selection process, which reflects response competition and is driven by the spatial allocation of attention. Other research supports the view of a late selection response competition interpretation. For example Coles, Gratton, Bashore, Eriksen, and Donchin (1985) demonstrated this physiologically. Miller (1987) has shown that neutral letters that are correlated with a particular response act as congruent stimuli for this response. However, early selection processes also play a role in the flanker effect. Studies have shown that the physical characteristics of the flankers also contribute to the FCE. Response neutral flankers that are similar to response incompatible flankers cause a slower response than response neutral flankers that are similar to response compatible flankers (Eriksen & Eriksen, 1974). Flankers that are response compatible and identical to the target produce faster reaction times that flankers that are only response compatible (Eriksen & Eriksen, 1979; Eriksen & Schultz, 1979). Yeh and Eriksen (1984) found that physical similarity between target and flanker (e.g., both upper case) has a greater effect than name similarity (e.g., target upper case and flankers lower case). LaBerge, Brown, Carter, Bash, and Hartley (1991) have shown that the effect of flankers could be reduced by manipulating the focus of attention. They presented in the same spatial location a digit

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prior to presenting a target flanker array and required that subjects identify both the preceding digit and the target letter. LaBerge et al. (1991) manipulated the focus of attention by shortening the duration of the first target. They assumed that, with shorter durations, the focus of attention would be narrowed and carried over to the target-flanker presentation. They showed that shorter durations of the digit target reduced the influence of the flankers and with slight increases in spatial separation between the letters, the effects of the flankers was virtually eliminated. These results suggest that there is an early selection spatial component to the FCE in addition to any response selection components because the focus of attention was set prior to the onset of the targetflanker display. Baylis and Driver (1992) demonstrated that the FCE decreases when the target and flankers are different colors. These results complement other work which indicates that perceptual grouping principles influence the magnitude of the FCE (Harms & Bundesen, 1983; Kramer & Jacobson, 1991). The fact that the impact of flankers varies with distance from the target is consistent with spotlight or zoom lens models of selective attention (Eriksen & Eriksen, 1974; Posner, 1980). That is, flankers falling within the attentional beam are processed, whereas those falling outside are not. For most experiments, the flanker to the left and to the fight of the target are both consistent, both inconsistent, or both neutral. An important question which this study addresses is whether the magnitude of interference from each flanker is equal or whether interference with target processing is asymmetrical and depends upon the spatial position of the flanker. This question is motivated by recent work showing that target identification in multielement arrays is influenced by spatial position. For example, Efron, Yund, and Nichols (1990) proposed a serial scanning mechanism which is biased to begin scanning at the top and right of a display. An implication of this hypothesis for the FCE is that in horizontal displays - the fight flanker will have a greater effect than the left. In vertically oriented displays, the top flanker will have a greater effect than the bottom. Also, research on hemispheric differences in information processing suggests the possibility of differences in the effectiveness of the left and right flanker because in the three element display, the left and fight flankers fall in different visual fields. Although differences in the relative effectiveness of flankers are not predicted by either the zoom lens or spotlight models, there is evidence,

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which suggests a greater influence on target processing from the left flanker. This is based upon the studies indicating a left side advantage in the processing of letter like strings (Posner, Snyder, & Davidson, 1980; Pashler, 1984). On the other hand other research has found right side advantages in the shifting of attention (Posner et al., 1980; Laberge & Brown, 1986; 1989). Dowling and Pinker (1985) found that the distribution of attention was asymmetric, the right visual field showing an advantage in facilitating responses and in the detection of a luminance increment (Hughes & Zimba, 1985). These results suggest that flanker on the fight should have a greater effect on the processing of a central target than those on the left. However, Hommel (1995) has argued that in strings that closely approximate words, asymmetries resulting from the automatic initiation of reading-like habits may also account for the fact that the left flanker has a considerably greater effect on the FCE than the fight flanker. Preliminary research on the FCE indicates complex relationship in which the effectiveness of the left or the fight flanker depends upon stimulus characteristics (Hommel, 1995). For example, with letter strings, flankers to the left of the target letter produce greater response compatibility and incompatibility effects than those on the fight (Beach, 1995; Harms & Bundesen, 1983; Hommel, 1995). However, other research has found fight-side flanker effects with mirror-image letters and with geometrical forms (Hommel, 1995). In summary, regardless of which flanker may be dominant in the FCE, it is important to note that neither the spotlight nor the zoom lens model assumes asymmetries in the relative effectiveness of the left or right flanker (that is, of course assuming that the center of the distribution of attention is focused at the center of the target letter). Thus, the purpose of this study is to determine further those factors leading to asymmetries in the FCE.

Expt. 1: Left-right asymmetries in the FCE: M and W letter arrays As indicated earlier, research indicates the existence of left-right asymmetries. However, the flanker that is most effective appears to depend upon stimulus characteristics (Hommel, 1995). For example, with letter strings flankers to the left of the target letter produce greater response compatibility and incompatibility effects than those on the right (Beach, 1995; Harms & Bundesen, 1983; Hommel, 1995). In

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contrast to these data, Kitterle and Ludorf (1993) reported preliminary data indicating flanker asymmetries in which the right flanker produced a greater compatibility effect than the left. In that study, the letters M and W were used as targets and the flankers. In their study there were eight stimulus conditions that resulted from orthogonally varying the left and right flankers and factorally combining them. It should be noted that the letters M and W have component line segments that are highly similar in contrast to the letters used by others (e.g., Beach, 1995; Harms & Bundesen, 1983; Hommel, 1995). It might be argued that identification of these letters is more critically dependent upon discriminating local features. Given research on hemispheric differences in the processing of local and global stimuli, a fight visual field/left hemisphere difference might be expected. In light of these apparent discrepancies, this experiment is designed to determine the direction of flanker asymmetries using the same letters as in Kitterle and Ludorf (1993). In their study, Kitterle and Ludorf (1993) made the general assumption that the effects of two incompatible flankers on the FCE was greater than a display with only one incompatible flanker. Consequently, when one flanker was response compatible (C) and the other response incompatible (I), then reactions time (RT) for left incompatible/right compatible, RT(I-C), or left compatible/right incompatible, RT (C-I), should fall between the RTs when both flankers were compatible, RT(C-C), or when both were incompatible, RT(I-I). Kitterle and Ludorf (1993) also proposed the following specific hypotheses: Hypothesis 1: Under the assumption that both flankers exert equal interference and one incompatible flanker produces less interference than two [left compatible-right incompatible (C-I) or left incompatiblefight compatible (I-C)], then RT (C-I) = RT (I-C) and RT(C-C) < RT(C-I or I-C) < RT (I-I). Hypothesis 2: Flanker interference is asymmetrical, one incompatible flanker produces less interference than two, then RT (I-C) RT (C-I)and RT(C-C) < RT(C-I) < RT(I-C) < RT (I-I) or RT(C-C) < RT(I-C) < RT(C-I) < RT (I-I).

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Hypothesis 3: Interference is asymmetrical, one flanker totally accounts for interference, then RT (I-C) ~ RT (C-I) and RT(C-C) < RT(C-I) < RT(I-C) = RT (I-I) or RT(C-C) < RT(I-C) < RT(C-I) = RT (I-I). The present experiment tests these hypotheses as well as considering experimental conditions in which the stimulus display contains one response incompatible flanker and one response neutral (N) flanker (that is, displays in which there is no response assigned to one of the flanker letters). Thus, we also test conditions for flanker asymmetries of the form RT(I-N) vs. RT(N-I) as well as RT(C-N) vs. RT (N-C). As noted earlier, the left and the right flankers project to the right and left hemisphere, respectively. Given the fact that the FCE reflects, in part, response competition, it is of interest to examine how hand of response and flanker position interact to determine the magnitude of the FCE. For example, it might be assumed that in the letter array WMM (or WMN), the magnitude of the FCE might be larger with the left hand responding to the target letter M (ML) and the right hand to the target letter W (We,) than vice versa. The basis for this assumption is that if the left flanker has a greater effect on the FCE because of an automatic left to right scanning process (Hommel, 1995), then the left flanker should prime the hemisphere that controls response, namely the right hemisphere. In this case, more inhibition may be needed to suppress the primed response "W" if the correct response "M" is to be made. On the other hand when the "W" projects to the hemisphere that controls the response "M", there is less priming of the "W" response and consequently less inhibition with a resulting smaller FCE effect. Subjects. Forty undergraduates participated in this experiment and received extra credit for participation. Subjects had normal or correctedto-normal vision and were naive about the purpose of this study. Apparatus and stimuli. PC-compatible computer workstations were used to present stimuli and collect responses and latencies. Subjects were seated at a work station 54 cm from the monitor (14" SVGA color monitor), which was positioned at eye level. A standard keyboard in front of and below the monitor was used to record responses and latencies. Subjects responded to the target stimuli using the "z" and "/"

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keys located on the bottom left and right sides of the keyboard, respectively. Mapping of targets to response keys was counterbalanced. The stimuli consisted of three-letter arrays that were horizontally oriented with the central letter falling in the fovea. The letters were upper case with a width of 15 min. and height of 30 min. The distance between each letter was 5.4 min. The central target letter (M or W) was flanked on the left and right of the array by one of four letters randomly chosen letters from the set (M, W, E, or G). A second neutral letter was chosen so that the total number of neutral letters equaled the number of target letters. Thus, for the left and right flankers there were four conditions: response compatible and response incompatible plus two response neutral conditions. The left and right flankers were orthogonally varied and crossed with each other to produce 8 arrays (e. g., MWM, WMM, EWW, GWM, etc.). Procedure. Subjects performed a block of 32 practice trials followed by a block of 128 experimental trials. On each trial, a fixation cross was presented for 1000 msec, followed by a 500 msec warning tone. After a variable ISI of 700 to 1200 msec. the fixation cross was extinguished and a three letter array was presented for 500 reset. Subjects were instructed to identify as quickly and accurately as possible whether the central target letter was an 'M' or a 'W' by using the "z" key or "/" key as response input, respectively. Subjects were given a total of 2500 msec. to respond. For half of the subjects the target letter M was responded to with their left hand and the target letter W with the right hand and for the other half this was reversed (i.e., MLWR vs. MR WE, respectively). Results. Preliminary analyses of the data indicate that there were no significant differences between the neutral conditions. Consequently, they were collapsed. The data, which are shown in Table 1, presents correct mean reaction times as a function of stimulus condition. These data were analyzed by means of a 2 Hand of Response (between group factor: MLWR, MRWL) X 3 Left Flanker (compatible, incompatible, neutral) X 2 Target Name (M or W) X 3 Right Flanker (compatible, incompatible, neutral) split-plot ANOVA. There were significant main effects of Left Flanker [F(2,76)= 69.40, p< .0000001] and Right Flanker [F(2,76)= 30.25, pRH over parietal sites

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Table 1, cont'd. Vowel Sounds Electrode Study Molfese & T3, T4 Searock, 1986 Reference= linked ears. 12-month-old infants, n= 16.

Infants divided into 2 groups, High and Low Groups, based on Median Split of McCarthy Verbal Scores at 3-years-of age.

Task Auditory ERPs.

3 Vowel sounds, I, ae, au, and their nonspeech controls matched to the center frequencies of each vowel. Presented in random order with equal probabilities of occurrence.

Results P60 RH discriminated I from au.

N200 High Group discriminated nonspeech control I from ae and ae from au. P300 High Group RH discriminated speech vowels I from ae, RH discriminated nonspeech vowels I from ae and I from au. LH discriminated ae from au. Low Group RH discriminated ae from an.

Although the right-hemisphere discrimination of the VOT cue appears paradoxical in light of arguments that language processes are carried out primarily by the left hemisphere, the fact that identical responses are elicited by both speech and nonspeech sounds which contain the same temporal cues suggests that it may be the temporal quality of the sounds, not their speech-like quality, which in fact triggers the right hemisphere response. Furthermore, studies of clinical populations suggest that the V OT cue is discriminated, if not exclusively, then at least in part, by brain mechanisms restricted to the right hemisphere (for a review of this literature, see Molfese, Molfese, & Parsons, 1983, or Simos, Molfese, & Brenden, 1997). For example, Miceli, Caltagirone, Gianotti, and Payer-Rigo (1978), using a nondichotic pair presentation task, noted that the left-brain-damaged aphasic group made fewest errors with stimuli differing in voicing but not place of articulation. Blumstein, Baker, and Goodglass (1977) also

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noted fewer errors for voicing contrasts than for place contrasts with left hemisphere damaged Wemicke aphasics. Finally, Perecman and Kellar (1981), based on their own findings that left-hemisphere-damaged patients continue to match sounds on the basis of voicing but not place, speculated that voicing could be processed by either hemisphere but that the POA cue was more likely to be processed by only the left hemisphere. Three general findings have emerged from this series of temporal discrimination studies involving VOT and TOT. First, the discrimination of the temporal delay cue common to voiced and voiceless stop consonants can be detected by ERPs recorded from electrodes placed on the scalp over the two hemispheres. Second, from at least 2 months of age, if not before, the infant's brain appears capable of discriminating voiced from voiceless stop consonants in a categorical manner. That is, the ERPs appear to discriminate stimuli in one phonetic category from those with VOT values which characterize a second phonetic category. At the same time, these ERPs can not discriminate between different VOT stimuli that come from the same phonetic category. Third, categorical discrimination across different ages appears to be carried out first by bilaterally represented mechanisms within both hemispheres and then, somewhat later in time, by right-hemisphere lateralized mechanisms. The bilateral effects appear to be reflected with some consistency in the negative peak that occurs with a latency of approximately 530 ms in infants from birth onward. The lateralized effect, when noted in the infant ERPs, has a markedly longer latency. The presence of several different peaks with markedly different latencies which are responsive to the same temporal cues may signal that multiple regions of the brain are responsive to and perhaps process differently these voicing or temporal contrasts.

Place of Articulation (POA) In addition to studies of VOT, a second speech cue, place of articulation or POA, has been investigated in a number of studies with infants and adults (Molfese, 1978a, 1980b, 1984; Molfese, Buhrke, & Wang, 1985; Molfese, Linnville, Wetzel, & Leicht, 1985; Molfese & Schmidt, 1983, Molfese & Molfese, 1979b, 1980, 1985). As in the case of the VOT temporal cue, these studies of the POA cue identified both lateralized and bilateral hemisphere responses that discriminated

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between different consonant sounds. However, unlike the discrimination abilities for VOT, the ability to discriminate the POA cue consistently appeared to be present from birth. There were some important differences, however, both in the development of ERP responses to the POA cue and in the character of the lateralized responses which distinguished the perception of this cue from that for VOT. Molfese (1978a) first attempted to study POA in adults in order to obtain some reference for studying these abilities in infants. For the most part, this research focused on attempts to isolate the neuroelectrical correlates of the second formant transition, the cue to which listeners attend in order to discriminate between different consonant sounds which are formed in different portions or places within the vocal tract. In this study, Molfese presented a series of consonant-vowel syllables in which the stop consonants varied in POA, formant structure, and phonetic transition characteristics. Changes in the POA cue (i.e., changes in the second formant transition) signaled either the consonants b or g. The formant structure variable referred to two sets of sounds, one set of which consisted of nonspeech sounds that contained formants composed of sinewaves 1 Hz in bandwidth whereas a second set of speech sounds contained formants with speech-like formant bandwidths of 60, 90, and 120 Hz for formants 1 through 3, respectively. The phonetic transition cue referred to two stimulus properties in which one stimulus set contained formant transitions that normally characterize human speech patterns while the second set contained an unusual pattern not found in the initial consonant position in human speech patterns. Auditory ERP responses were recorded from the left and right temporal regions of 10 adults in response to randomly ordered series of CV syllables that varied in consonant place of articulation, bandwidth, and phonetic transition quality. Two regions of the auditory ERP that peaked at 70 and 300 ms following stimulus onset discriminated the phonetic transition and POA cues only over the left-hemisphere temporal electrode site. As in the case of Molfese (1978b) who also used only a single left-hemisphere temporal site, no bilateral place discrimination was noted. Similar left hemisphere POA discrimination effects were noted by Molfese (1980b), Molfese and Schmidt (1983), Molfese (1984), and Gelfer (1987) with the exception that, with the inclusion of auditory ERP data collected from more electrode recording sites over each hemisphere, consistent discrimination of the place cues were also noted to occur at the same time over both hemispheres (bilateral effects).

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Several general findings have emerged from these adult POA studies. First, when multiple electrode sites are employed, bilateral stimulus discrimination effects are usually found in addition to left hemisphere lateralized ones. Second, these bilateral effects invariably occur early in the waveform and prior to the onset of the left hemisphere lateralized POA discrimination responses. This temporal relationship between bilateral and lateralized effects was noted earlier in our review of the VOT studies. Third, in addition to stimulus related hemisphere effects, portions of the ERPs also vary between hemispheres that are unrelated to stimulus, task, or subject features. Apparently, during the discrimination of these auditory tokens, both hemispheres initially discriminate between POA and VOT/TOT stimuli at the same time in adults, somewhere approximately 100 ms following stimulus onset. Shortly afterwards, at approximately 300 ms following stimulus onset, the left hemisphere discriminates between differences in the POA cue, while the right hemisphere at approximately 400 ms discriminates the VOT or temporal offset cue. Finally, throughout this time period and afterwards there are brief periods of ERP activity during which the two hemispheres appear to be doing quite different things, which may be unrelated to the discrimination of the stimuli. In an extension of these POA findings to younger populations, Molfese and Molfese (1979b) noted similar patterns of lateralized and bilateral responses with newborn and young infants. Unlike findings for VOT, however, POA discrimination were consistently found to be present at birth. In this study, ERPs were recorded from the left and fight temporal regions (T3 and T4) referred to linked ear references of 16 full term newborn human infants within 2 days of birth. These data were recorded while the infants were presented series of consonantvowel syllables that differed in the second formant transition (F2, which signaled POA information), and formant bandwidth. As with adults, one auditory ERP component that appeared only over the left-hemisphere recording site discriminated between the two consonant sounds when they contained normal speech formant characteristics (peak latency = 192 ms). A second region of the auditory ERP varied systematically over both hemispheres and also discriminated between the two speechlike consonant sounds (peak latency = 630 ms). Notably, these latencies were markedly shorter than those found for VOT and TOT in young infants.

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In a subsequent replication and extension of this work, Molfese and Molfese (1985) presented a series of consonant-vowel syllables that varied in POA and formant structure. Two different consonant sounds, b, g, combined with three different vowel sounds were presented with speech or nonspeech formant structures. ERPs were again recorded from the left and right temporal regions (T3, T4). As in the case of Molfese and Molfese (1979b), analyses identified two regions of the auditory ERP that discriminated POA differences. One region, with a peak latency of 168 ms, was detected only over the left-hemisphere site as discriminating between the two different consonant sounds; a second region with a peak latency of 664 ms, discriminated this POA difference and was detected by electrodes placed over both hemispheres. The lateralized effect noted for infants in the Molfese series of infant studies for the POA cue occurred prior to that for the bilateral effect, a finding opposite to that noted when adults were studied. However, the reversal of the temporal relationship between the bilateral and lateralized responses appears to be a legitimate one, given that virtually identical results were found by Molfese and Molfese (1985) and Molfese and Molfese (1979b) with different populations of infants and somewhat different stimulus sets which contained the POA variable. A replication and extension of this work which involved recorded ERPs from 6 scalp locations of 38 newborn infants to a somewhat different stimulus set reported comparable effects at similar latencies (Molfese, BurgerJudisch, & Hans, 1992). This temporal pattern of initial lateralized responses followed by bilateral responses is also opposite to that noted previously for VOT cues for adults as well as that found for infants exposed to changes in the VOT temporal cue. Clearly, such differences in the ERP effects suggest that different mechanisms subserve the perception and discrimination of the different speech related cues. The relationship between lateralized and bilateral responses is not clear at this time. It does appear, however, that bilateral responses may develop after the lateralized ones for POA, both ontogenetically as well as phylogenetically. For example, Molfese and Molfese (1980) noted only the presence of left-hemisphere lateralized responses in 11 preterm infants born on average 35.9 weeks postconception. Stimuli identical to those employed in Molfese (1978b) with adults were presented to these infants while ERPs were recorded from the left- (T3) and righthemisphere (T4) temporal regions. As was found with full-term infants (Molfese & Molfese, 1979b), a portion of the auditory ERP recorded

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from over the left hemisphere with a peak latency at 848 ms discriminated between speech stimuli containing different consonant transition cues. An additional left-hemisphere component with a peak latency of 608 ms differentiated only between the nonphonetic consonants, a finding similar to that reported by Molfese (1978b) with adults, with the exception that adults were sensitive to both phonetic and nonphonetic contrasts. While most studies of POA in infants involve newborns, one study by Dehaene-Lambert and Dehaene (1994) noted a POA effect in older infants at 3 months of age. They tested a group of 16 infants, recording ERP activity from a series of 58 scalp electrodes to ba and ga syllables. Two conditions were used: a repeated trials condition in which a standard sound was presented five times and a deviant trial condition in which the standard was repeated four times, followed by one instance of a different syllable. Consonant discrimination changes were noted at one ERP peak, at 390 ms, which declined in amplitude as the standard stimulus was presented and then increased in amplitude with the presentation of the different syllable. Thus, the ERPs detected a difference in the speech sounds and recovered in amplitude in contrast to repetitions of the same stimulus which resulted in further decreases in amplitude. They also noted a moderate LH asymmetry for this peak over posterior electrode sites. While this study is consistent with the neonatal research in reporting LH lateralized effects in young infants, the latency of the response differs from that reported by Molfese and colleagues. In addition, there is no report of a bilateral effect. However it is difficult to determine whether such differences result from the different paradigms used, the differences in the ages of the infants sampled across the studies, or other factors. It is clear that much more research is needed to fill in the missing gaps in our knowledge of the neuroelectrical correlates of POA from early infancy into the late adolescent years. In summary, unlike the VOT studies, the POA cue evokes a relatively stable pattern of lateralized and bilateral responses from infancy into adulthood (Gelfer, 1987; Molfese, 1978b, 1980b; Molfese, Buhrke, & Wang, 1985; Molfese, Linnville, Wetzel, & Leicht, 1985; Molfese & Schmidt, 1983; Molfese & Molfese, 1979b, 1980, 1985). These effects appear to replicate well across laboratories (Gelfer, 1987; Segalowitz & Cohen, 1989), although a great deal more research is needed to characterize the changes in both the neuroelectrical correlates of VOT and POA through the infant and child years.

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Vowel Sounds

There is one published study investigating vowel discrimination abilities in one-year old infants (Molfese & Searock, 1986). They recorded auditory ERPs from 16 Caucasian infants tested within two weeks of their one-year birthdate. The infants heard three vowel sounds, 300 ms in duration, with normal speech formant characteristics (i,ae,au) and three nonspeech controls which contained one-hertz sinewave formant bandwidths instead of the normal speech formant bandwidths of 60, 90, and 120 Hz for formants l, 2, and 3, respectively. Auditory stimuli were presented randomly at 80 dB SPL(A) and ERPs were collected from scalp electrodes placed at the left and right temporal areas, T3 and T4, referred to linked ears (Jasper, 1958). Upon completion of the testing, the infants were divided using a median split into two groups based on their McCarthy verbal scores at three years of age. The High Group had a mean McCarthy verbal score of 77.25 (s.d.=15.5) and the Low Group had a mean McCarthy score of 20.5 (s.d.=12.6). Three regions of the ERP changed following presentation of the vowel sounds. An initial positive component (P60) changed systematically over the RH of both groups to the vowel sounds, i and au. A second region of the waveform, the N190, which characterized a negative peak at 190 ms post vowel sound onset, only changed systematically for the High Group at the RH temporal site and discriminated the nonspeech control sounds, i from ae and ae from au. Finally, a positive peak at 340 ms discriminated at the RH site the Vowel speech sounds, i from ae, and the nonspeech sounds, i from ae and i from au. The only LH discrimination of sounds for the High Group occurred in response to the nonspeech control sounds for ae versus au. Only one discrimination over the RH was noted for the Low Group, ae from au. On the basis of these electrophysiological data, it appears that brain responses to speech materials from infancy into adulthood are multidimensional and that they develop in a dynamic fashion. First, it is clear that discrimination of different speech cues emerge at different times in early development. This is true from both the standpoint of behavioral research (Eimas, et al., 1971) as well as ERP research (Molfese & Molfese, 1979a, 1979b, 1985, 1997). Relatively stable and reliable ERP correlates of consonant place of articulation (POA) discrimination have been noted in newborns. At the same time, however, discrimination of a different speech cue, voice onset time (VOT), does

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not appear to develop until sometime after birth, at least in the majority of the population (Molfese & Molfese, 1979a; Simos & Molfese, 1997). Second, different regions of the auditory ERP elicited by the different auditory stimuli appear to lateralize differently, depending on the evoking stimuli. The temporal cue, VOT, elicits a differential righthemisphere response, while the POA cue elicits a differential lefthemisphere response. Third, the scalp distributions for ERP effects in relation to speech sound discrimination change with development. Thus, for example, Molfese and Molfese (1979a) note temporal lobe lateralized effects in newborn infants, while more pronounced temporalparietal effects are noted in children (Molfese & Molfese, 1988) and adults (Molfese, 1978a). The fourth point is that different portions of the ERP waveform appear sensitive to phonetic speech sound contrasts at different developmental stages. Thus, shortly after birth, speech sound discriminations are noted to occur at relatively long latencies (520 - 920 ms, see Molfese & Molfese, 1979b; Simos & Molfese, 1997), while these effects shift forward in the ERP wave to 180 - 400 ms for one-year-olds (Molfese & Searock, 1986) and for preschoolers (Molfese & Hess, 1978; Molfese & Molfese, 1988), and from 50 to 350 ms for elementary school children and adults (Molfese, 1978a, 1978b, 1980a, 1980b). Fifth, and finally, at some point during the auditory ERP to virtually all stimuli tested to date using this procedure, the two hemispheres, in both infants and adults, respond differently to all stimuli. This general hemisphere difference seems most pronounced in the preterm infants, with many different regions of the ERP varying between the two hemispheres (Molfese & Molfese, 1980). However, this difference is also present in newborn (Molfese & Molfese, 1979b, 1985), one-year-old infants (Molfese & Searock, 1986), preschool age children (Molfese & Hess, 1978; Molfese & Molfese, 1988), and adults (Molfese, 1978a, 1978b, 1980a, 1980b, 1984; Molfese & Schmidt, 1983). Electrophysiological correlates of Infant memory.

While our knowledge of infants' speech perception has expanded rapidly over the past two decades as noted above (Eimas, Siqueland, Jusczyk, & Vigorito, 1971; Kuhl, 1985; Morse, 1974; Morse & Snowdon, 1975: Molfese & Molfese, 1979b; 1980b; 1985), little is known concerning how particular speech sound patterns come to be

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recognized and discriminated as a function of the differential experience that eventually accompanies early word acquisition. Additionally, little is known regarding the role that the brain plays in the early discrimination of these novel and familiar events. The next section of this paper focuses on one aspect of this process, infant short and long term memory. A series of papers both with human and non-human primates demonstrate that long term memory is present and measurable from an early age (Gunderson & Sackett, 1984; Gunderson & Swartz, 1985; 1986). In one such study, Gunderson and Sackett (1984) examined the development of pattern recognition in 31 infant pigtailed macaques using the familiarization-novelty technique. Following a familiarization period with 2 identical black and white patterns, the infants were tested on the familiar and novel patterns. A novelty preference clearly emerged with increasing age. Younger infants (mean age 178 days postconception) did not show a reliable visual preference for either the novel or the familiar patterns while older infants (by approximately 25 days) attended longer to novel than familiar patterns. However, by 200 days postconception, infant macaques could remember some aspects of previously exposed stimuli and consistently preferred a novel stimulus. Cowan, Suomi, and Morse (1982) noted that such memory also occurs for speech sounds. Using a modification of an adult masking paradigm and a non-nutritive sucking discrimination procedure, Cowan et al. investigated preperceptual auditory storage in 8 and 9 wk old infants. Fifty-four infants and 10 adults listened to repeating pairs of brief vowels with a stimulus onset asynchrony (SOA) of 50 msec. Within each series, either the first vowel in a pair changed (backward masking), the second vowel changed (forward masking), or neither vowel changed (control). Discrimination of the change occurred only in the forwardmasking condition. In Experiment 3, with 30 infants and 10 adults, discrimination occurred in a backward-masking condition with an SOA of 400 msec, but not with an SOA of 250 msec or in a control condition. Cowan et al. interpreted their results as suggesting that echoic storage contributes to auditory perception in infancy, as in adulthood, but that the useful lifetime of an echoic trace may be longer in infancy. In an early study of more long term memory using human infants, Sullivan, Rovee-Collier, and Tynes (1979) provided some of the earliest indications of long term memory in young human infants 3-months of age, who were trained in a conjugate reinforcement paradigm in which

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footkicks produced conjugate activation of an overhead crib mobile. Following two training sessions, retention as measured by savings during cued recall was assessed cross-sectionally in a third session scheduled after intervals that varied from 2 to 14 days. No evidence of forgetting was observed for up to 8 days following original training, suggesting that these memories persisted for at least this long. These types of studies provide clear indications of different types of short and long term memory in infants early in development. Another area of early infant memory research that has begun to receive more extensive treatment in recent years concerns the neuropsychology of infant memory. There exists an extensive set of electrophysiological studies investigating memory functions in young infants. Most often, these studies utilize a paradigm commonly used with adults - the "odd-ball" technique. In this procedure, two different visual or auditory stimuli are presented for differing numbers of times. For example, a picture of one face is randomly presented on 80% of the trials while another face occurs on 20% of the trials (i.e., the "odd-ball" trials). Typically, in an adult study, a positive peak with a latency of approximately 300 ms is noted to occur when adults attend to the infrequent stimulus while no such peak or a greatly reduced peak occurs for the frequent stimulus. Studies which range from involving infants as young as 4-weeks of age (Karrer & Monti, 1995) to those testing 12-month-olds (Nelson & Karrer, 1992; Nelson & deRegnier, 1992) have noted ERP differences in response to such frequent versus infrequent occurrences. For the most part, these memory effects appear to produce changes in specific peak portions of the ERP that range from those occurring prior to 500 ms following stimulus onset such as the Nc (Hoffman, Salapatek, & Kuskowski, 1981; Karrer & Monti, 1995) to the late positive components (LPC) that occur as late as 1700 ms (Nelson & Karrer, 1992; Nelson & deRegnier, 1992). Usually midline frontal or occipital ERP effects occur in response to these frequent and infrequent events. However, it is important to note that these it is only these response sites which are usually selected for study across virtually all infant memory studies. Given the widespread use of midline electrode sites, it is not surprising that relatively few studies which have investigated hemisphere effects (DeHaan & Nelson, 1997; Molfese, 1989; Molfese & Wetzel, 1992). A summary of the infant memory studies which have utilized the ERP procedure is presented in Table 2.

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Table 2. Studies Using Event-Related Potential (ERP) Procedures To Study Infant Memory. Study/Ss Karrer & Monti (1995)

Electrode Fz, Cz, Pz, Oz, C3, C4

Task Visual ERPs oddball task

4-7-week old infants, n=20

Reference= linked ears

80% and 20% probabilities Stimuli: highcontrast contours contained in a black and white checkerboard or in a set of 4 solid geometric shapes of different colors.

Hoffman, Salapatek, & Kuskowski, (1981)

Oz, Opz Reference= left mastoid.

3-month old infants, n= 13

Courchesne, Ganz, & Norcia

(I~I)

4-7-month old infants, n= 10

Fz, Pz Reference= fight mastoid

Results Latency of a frontally predominant Nc (5001000 ms) and magnitude of an NSW (100-500 ms)changed as a function of stimulus experience. Nc latencies faster and NSW magnitude larger to oddball (infrequen0 stimulus than to frequent stimulus. Latency of N378 component over occipital scalp faster to oddball stimulus.

Visual ERPs: Familiarization: Pre-exposure for 40 trails to 80% stimulus. Testing: 80% of trials a 500 ms a vertical squarewave grating with one spectral frequency while on 20% viewed stimulus with different spectral frequency.

Late positive component (300-600 ms) only to novel (20%) at Oz and Opz.

Visual ERPs: One female face on 88% trials, second face on 12% of trials

Negative Nc (latency = 700 ms) amplitudes larger, latencies longer for infrequent faces at both Fz and Pz

Also occurred when used vertical vs. horizontal gratings matched in spectral frequency.

Effects maximal at Fz

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Table 2: cont'd Study/Ss Hoffman, Salapatek, & Kuskowski, (1981)

Electrode Oz, Cz, Pz

Reference= left mastoid.

3-month old infants, n= 16

Karrer & Ackles (1988)

Fz, Cz, Pz, Oz, C3, C4.

6-week, 6-, 12-, and 18-month old infants

Reference= linked ears.

Nelson & Collins (1992) 4(n=14) & 8 (n= 17) month old infants

Task Visual ERPs: Familiarization: Pure tone paired with vertical squarewave grating. Testing: on 20% of trials changes made in either: 1) auditory 2) visual 3) auditory + visual.

Results Visual change: Late positive component (300-600 ms) only to novel at Oz, Cz and Pz. Auditory- visual change: Late positive component (300-600 ms) only to novel (20%) at Oz and Pz. Auditory change: No effect.

Visual ERPs

Large negative slow wave (NSW) complex and Nc negative component (latency=770 - 800 ms)

80% and 20% probabilities; 6 week: random shapes and checketl~atds, 6 month: 2 female faces; 12-, 18-month: stuffed animals and furniture.

Fz, Cz, Pz, Oz. Reference = linked ears.

Visual ERPs Experiment had 20 familiarization trials (10 each) with 2 alternating faces for 500 ms. Remaining design identical to Nelson & Collins (1991a).

Larger at Cz to infrequent events for only 6 month olds,

Familiarization trials: No differences between familiar and novel. 4 month olds: No effects. 8 month olds: Responses similar to Frequent-Familiar and Infrequent-Familiar Infrequem-Novd produced sustained negative slow wave after 400 ms.

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Table 2: cont'd Study/Ss Nelson, Ellis, Collins, & Lang, (1990)

6-month old infants, n= 11

Thomas & Lykins (1995) 5-month-old infants. Expt. 1:n=24 Expt. 2:n=24

Electrode Fz, Cz, Pz, Oz.

Reference = linked ears.

Electro-cap International. Cz, Fz, T3. Reference= linked ears.

Nikkel & Karrer (1994)

Fz, Cz, Pz, Oz, C3, C4

6-month old infants, n=28

Reference= linkedears

Task Visual ERPs

On 80% trials a 100 ms presentation of doll face; On 20% of trials no face presented.

Audi tory ERPs. Tones (100ms, 400 Hz), dicks (5 ms burst) Expt 1: Day 1 Tones and dicks presented for 100 trials. On Day 2, 50 old stimuli presented along with 50 new stimuli. Expt 2:Two tones presented as in Experiment 1. Visual ERPs 80 trials of two female face pictures, presentedat 80%/20% probabilities, was divided into 3 blocks.

Results Differences between 80% and 20% trials at 100-150 ms, 600-700 ms, and a sustained positive slow wave (1100-1700 ms) to the next presented familiar (doll face) stimulus after deleted face trial. Effect at Fz (maximal) and Cz.

Experiment 1: Familiar stimuli produced larger N350 (N2) on Day 2. Experiment 2: N350 replicates Experiment 1. P200 larger in amplitude and faster for familiar stimuli on Day 2.

Nc amplitude decreased across blocks at all central and anterior scalp sites but significantly decreased only at Cz. Pb increased in amplitude at all sites across blocks but was significant only at C4. No changes in NSW, Pz, or Oz at any sight.

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Table 2: cont'd Study/Ss Karrer, Wojtascek, & Davis (1995)

Electrode Fz, Cz, Pz, Oz, C3, C4

6-month old infants,

Reference= linked ears

23 with Down syndrome

Task Modified combination of an oddball task and a habituation-novelty task using faces; 80 trials 80% with frequent stimulus and 20% for oddball.

18 without Down syndrome

Nelson & Collins (1991)

Fz, Cz, Pz, Oz.

6-month old infants, n - 12

Reference = linked ears.

Visual ERPs: 20 familiarization trials (10 each) with two alternating faces for 500 ms. Testing involved 3 conditions: Frequent-Familiar 1 face 60% InfrequentFamiliar: 2nd face on 20% of trials Infrequent-Novel: one of 12 faces seen on 20% of trials.

Results Same ERP morphology for both groups. Chronometry of information processing by infant with Down syndrome similar to or faster than that of infants without Down syndrome, depending on component. Amplitude differences between groups may implicate frontal attention processes in Down syndrome as opposed to more posterior processes. Infants with Down syndrome had an amplitude decrement in Nc over the central but not frontal cortex. Familiarization trials: No differences between familiar and novel. Infrequent-Familiar produced a LPC after 400 ms at Cz. Infrequent-Novel produced sustained negative slow wave after 400 ms.

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Table 2: cont'd

Study/Ss Nelson & Salapatek (1986)

Electrode

Task

Results

Fz, Cz, Oz.

Visual ERPs

Reference=

Experiments 1 and 2 had 40 familiarization trials with one face for lOOms.

Experiment 1: Negative component at Cz between 550-700 ms discriminated between novel event and stimulus presented during initial familiarization;

right 6-month old infants

mastoid.

Experiment 1 n=16

Experiment 1" Familiar face on 80% of trials.

Experiment 2 n=15

Experiment 2: Familiar face on 50% of trials.

Experiment 3 n=16

Experiment 3" No familiarization, novel and familiar faces presented randomly with equal frequency.

LPC between 8501000 ms did discriminate between novel and familiar during test at Cz and Fz. Experiment 2: Negative component at Cz between 550-700 ms discriminated between novel event and stimulus presented during initial familiarization. Experiment 3: No effects.

Molfese (1989) 14-month old infants, n= 10

F L , FR T3, T4 P L , PR Referencelinked ears.

Auditory ERPs Experiment 2: Familiarization: 6 exposures for 15 min. each over 2 days. Test: 60 presentations of the novel and 60 of the familiar syllable

Large positive component at 360 ms over FL and FR for only the familiar stimulus while a large negativity occurred for the novel stimulus.

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Table 2: cont'd Study/Ss De Haan& Nelson (1997) 6-month old infants Experiment 1 n=22

Electrode Fz, Cz, Pz, Oz. T3, T4, TS, T6 Reference = linked ears.

Experiment 2 n=22

Task Visual ERPs

Results

Color digitized images of mother and stranger's faces which were similar or dissimilar to mother's face. Experiment 1: Infant saw own motherand stranger

Experiment 3 n=22

Experiment 2: Infant saw another mother and stranger

Experiment 4 n=22

Experiment 3: Infant saw own motherand stranger who looked similar to mother. Experiment 4: Infant saw another motherand stranger who looked similar to mother. Faces presented with equal probability. Nelson & Karrer (1992) 12- month old infants, n=24

Oz, Pz, Cz, Fz

Visual ERPs

Reference= linked ears

~ures identical to Nelson & Collins ( 1991 )

Infrequem-Familiar proOuceOa LPC between 750-1250 and between 1250-1700 ms at Fz

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Table 2: cont'd Study/Ss Nelson, Henschel, & Collins (1993). 8-month old infants, n=58

Electrode Fz, Cz, Pz, Oz Reference = linked ears.

Task Visual ERPs following Haptic familiarization. Familiarization: 60 Sec. 3-D object placedin hand. Condition 1: 20 500 ms trials of color slide of object Then 30 slide trials of familiar object and 30 of novel. Condition 2: 20 500-ms trials of color slide of novel object; Then 30 slide trials of familiar object and 30 of novel. Condition 3: 2 10-see trials of novel and familiar object Then 30 slide trials of familiar object and 30 of novel. Condition 4: 30 slide trials of familiar object and 30 of novel.

Results Condition 1: LPC to novel stimulus. Condition 2: No effects. Condition 3: No ERP effects. I_xmking times greater to novel than to familiar stimuli. Condition 4: LPC to novel stimulus.

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Table 2: cont'd Study/Ss

Electrode

Task

Results

Nelson & deRegnier (1992)

Fz, Cz, Pz, Oz.

Visual ERPs.

Infrequent-Familiar produced a LPC between 750-1250 and between 1250-1700 ms at Fz.

12-month old infants, n=24 Molfese & Wetzel (1992) 14-month old infants, n=9

Reference= linked ears. F L , FR T3, T4 P L , PR Reference = linked ears.

Procgdures identical to Nelson & Collins ( 1991). Auditory ERPs: Familiarization: 6 exposures for 15 min. each over 2 days. Test 1 on day 3: 60 presentations of the novel and 60 of the familiar syllable Retest - day 10: All infants retested 1 wk later. 60 presentations of the novel and 60 of the familiar syllable

Test 1: Large positive component at 370 ms over FL and FR for only the familiar stimulus while a large negativity occurred for the novel stimulus. Retest: Large negative peak at 280 ms over F L and FR for only the familiar stimulus while a large negativity occurred for the novel stimulus. Large negative peak at 550 ms at T3 and PL sites for familiar stimuli.

LPC = Late Positive Component (Wave); NSW = Negative Slow Wave (Component) In a study conducted with the youngest group of infants to study memory, Karrer and Monti (1995) tested a group of 20 infants, four to seven weeks of age. They placed electrodes over midline positions from front to back (Fz - the midline frontal position, Cz - the midline central position, P z - the midline posterior parietal site, and Oz - the midline occipital position, see Jasper, 1958) as well as over left and right hemisphere central positions (approximately midway between the top, center of the head at Cz and the left and fight ear meatus at C3 and C4, respectively. All electrodes were referred to linked ears. The stimuli consisted of slides of high-contrast contours contained in a black and white checkerboard or in a set of four solid geometric shapes of

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different colors (i.e., circle, cloverleaf, triangle, inverted T). Karrer and Monti used a modified oddball task in which stimuli were presented in an 80-trial sequence with an occurrence probability of 80% for the frequent stimulus and 20% for the oddball. Two second epochs beginning with a baseline period 390 ms before stimulus onset were collected. No differences in ERPs were noted based on which specific stimulus was frequent or not, so the data were combined in all subsequent analyses across stimuli. Karrer and Monti noted that the Nc negative area between 500-1000 ms at Fz was larger than at Cz. There was a significant effect of stimulus probability (frequency) on Nc latency with a later Nc peak for frequent than for oddball stimuli. Nc latency at C3 and C4 was significantly later for frequent than for oddball stimuli. The NSW area, a negative area between 100 and 500 ms preceding Nc, at Fz was significantly larger than at Cz. NSW had significantly larger areas at C3 and C4 for novel trials than for familiar trials. Finally, the latency of N378 at Oz was significantly faster for oddball trials than for frequent trials. Karrer and Monti concluded on the basis of these findings that Nc latency and the magnitude of the NSW demonstrated that these two c o m p o n e n t s are functionally independent and most predominant over anterior and right central scalp areas overlying brain regions known to be associated with attentional processes. They felt that the latencies of these ERP components permitted them to gain some insight into the infant's ability to process information. Infants from 4 to 7 weeks of age require about 40 ms (N378 latency differences) to perceive the physical difference between stimuli, 800 ms (Nc latency) to search memory to encode simple visual stimuli, and about 80 ms (Nc latency differences) to search memory to discriminate between them. In a related study with somewhat older infants, Hoffman, Salapatek, and Kuskowski (1981) noted that when an infrequent or unexpected stimulus is presented to an adult, a characteristic enhancement of the late positive component (LPC) of the averaged evoked cortical potential is observed. To test whether this effect occurs during early infancy, they presented low and high probability visual stimuli to 29 infants 3-months of age in a series of two experiments, Initially, infants viewed a single visual stimulus for 40 trials. Next, during testing, the pre-exposed stimulus was presented for 500 ms each time on 80% of the trials. Visual ERPs recorded from posterior parietal (Pz), and occipital (Oz) scalp sites contained a clear LPC effect between 300 and 600 ms following the

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onset of the infrequent stimulus that was presented on 20% of the trials. Hofmann et al. interpreted these findings as a demonstration that the LPC effect in infants reflects cognitive processing involving memory. A similar visual ERP effect in terms of polarity and latency was noted with another group of 3 month olds by Hoffman and Salapatek (1981) at Cz, Pz, and Oz, as well as by Nelson and Collins (1991) at the Cz site with 6 month olds. In a related study, Nelson and Salapatek (1986) noted that visual ERPs recorded over a midline electrode position (Cz) to a novel face were significantly more positive than responses to a familiar face during the interval between 551 and 700 msec following stimulus onset. Negative peak effects have also been found to index differences in familiar and novel events. Karrer and Ackles (1987) recorded visual ERPs from 6-month olds in response to two different female faces that were presented on 80% and 20% of the trails. They noted that what they labeled as the Nc component was larger at Cz to the infrequently presented face. Nelson and Salapatek (1986) also noted a negative component at Cz between 500 and 700 ms that discriminated between a novel face and one that had earlier been presented during the initial familiarization trials. Nelson and Collins (1991), in a study with 6 month olds, reported a sustained negative slow wave after 400 ms that discriminated between an infrequently presented face and a familiar face as did Nelson and Collins (1992) 8 month olds. While most of these ERP studies have focused on infants at 6 months of age or younger, there are a growing number of studies conducted with older infants between 8 and 14 months of age as illustrated in Table 2 that indicate such effects continue and even elaborate further during later infancy (Nelson & Collins, 1992; Nelson, Henschel, & Collins, 1991; Nelson & deRegnier, 1992; Molfese, 1989; Molfese & Wetzel, 1992). Only two studies investigating infant memory have been conducted using auditory stimuli (Molfese, 1989; Molfese & Wetzel, 1992). Interestingly, these were the only two studies to also include more than a single pair of lateralized electrode placements which permitted some examination of hemisphere related differences. While scientists have speculated that the left hemisphere plays a major role in early sound discrimination (Molfese, Freeman, & Palermo, 1975; Molfese & Molfese, 1979b; 1980; 1985; Molfese & Betz, 1988), few studies directly assessed early memory for these speech sounds in infants which might indicate the role that different areas of the brain play in the recognition of familiar versus novel speech sounds at this stage of

Cognitive Development 355 development. Molfese (1989) recorded auditory ERPs from frontal, temporal, and parietal scalp locations over the left and right hemispheres of 10 infants, 14 months in age, who listened to a series of repeated consonant-vowel-consonant-vowel (CVCV) syllables over a 2 day period prior to testing. On the third day, when ERPs were recorded to the familiar CVCV and to a novel one, differences in the ERPs were noted only over the left and right frontal electrode sites. These effects were most marked at approximately 360 ms following stimulus onset and were characterized by a large positive peak at this latency over both the left and right frontal regions for the familiar CVCVs but not for the novel CVCVs. Molfese and Wetzel (1992), in a follow-up to this study, replicated these effects and also noted that after one week, a retest showed in the ERPs both a large bilaterally distributed frontal negative peak (N 1) 280 ms after onset of the novel stimulus and a subsequent larger bilaterally distributed frontal positive peak (P2) for the familiar stimulus as well as larger left hemisphere lateralized temporal and parietal responses at approximately 550 ms for familiar stimuli. Thus, the memory effects noted in much younger infants appear to become more complex in that they are reflected in both lateralized and bilateral responses with varying peak latencies after some period of time. In a related study using visual stimuli, Thomas and Lykins (1995) conducted two experiments using ERPs to investigate 24-hour recognition memory in infants. ERPs were recorded to 100 identical stimuli in 5-month old infants. After 24 hours, 50 of these familiar stimuli and 50 novel stimuli were then presented. The amplitude of a large negative peak (N2; approximate latency = 350 msec) of the auditory ERP was larger on Day 2 for the familiar stimuli compared with ERPs for both Day 1familiar stimuli and Day 2-novel stimuli. Trial-to-trial latency variability of N2 decreased from Day 1 to Day 2 for the familiar stimuli. A second experiment replicated the results of Experiment 1 and also noted an additional effect, an earlier positive peak (P2; approximate latency = 200 msec) characterized by larger amplitudes and smaller latency variability to the familiar stimulus on Day 2. All of these infant memory studies have produced results supporting the suggestion that infants respond differently to two stimulus sets if one is made familiar by first exposing the infant to this stimulus set prior to the novel-familiar comparison test or else indicating that infants can discriminate between frequent and infrequent events. Consequently, it

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appears that these infants are able to respond to events or stimuli that are through experience differentially encoded in memory.

Electrophysiologicai correlates of Infant word acquisition While our knowledge of infants' speech perception has expanded rapidly over the past decade (Eimas, et al., 1971; Kuhl, 1985; Morse, 1974; Molfese & Molfese, 1979b; 1980; 1985), little remains known about the infant's beginning comprehension of "names" for objects/ events (Bates, 1979). While some investigations have documented and catalogued the words first comprehended by infants, beginning around 8 months of age (Benedict, 1975; Kamhi, 1986; Miller, & Chapman, 1981; Macnamara, 1982), only recently have investigations probed the nature of the older infant's early word meanings (Bloom, Lahey, Hood, Lifter, & Fiess, 1980; Clark, 1983; Snyder, Bates, & Bretherton, 1981; Retherford, Schwartz, & Chapman, 1981) and to study the very beginning stages of the infant's ability to perceive and remember the names for objects and events (Bates, Benigni, Bretherton, Camaioni, & Volterra, 1979; Bates,Bretherton, Snyder, Shore, & Volterra, 1980; Golinkoff, Hirsh-Pasek, Cauley, & Gordon, 1987; Hirsh-Pasek & Golinkoff, 1996; Kamhi, 1986). Moreover, virtually nothing is known about the role that the brain plays in the early acquisition of such word meanings (Molfese, 1989, 1990; Molfese, Morse, & Peters, 1990). Furthermore, while scientists have speculated that the left hemisphere plays a major role in early language acquisition (Best, 1988; Lenneberg, 1967), little actual work has been conducted to address this issue. Indeed, five recent papers indicate that such procedures can be successfully used to study the developmental neuropsychology of early word comprehension in infants from 12- to 20-months of age (Mills, Coffey-Corina, & Neville, 1993, Molfese, 1989, 1990; Molfese, Morse, & Peters, 1990; Molfese, Wetzel, & Gill, 1993). The youngest group of infants to be studied using ERPs was a population of 12-month-old infants (Molfese, Wetzel, & Gill, 1993). This study represented a direct attempt to determine whether ERPs recorded from 12-month-old infants could discriminate between words thought by infants' parents to be known to these young infants from those words that parents strongly believed were not known to the infant. It was hoped that multiple electrode sites over various areas of each hemisphere would provide more information concerning the involve-

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ment of different brain regions in early word discrimination. Because details of this study are relevant to subsequent studies to be reviewed here, this review of Molfese et al. (1993) will be more extensive. A group of nine infants, three females and six males, (mean age = 12.2, s.d. = .36) were tested. Initial screening indicated that each of the parents were strongly fight handed as indicated by their responses to the Edinburgh Handedness Inventory (Oldfield, 1971) which yielded a mean Laterality Quotient greater than +0.7. Unique stimulus tapes were constructed for each infant, based upon the parental ratings obtained during a telephone interview during which parents were asked to identify all of the words from the original list of ten (i.e., "bottle," "book," "cookie," "key," "kitty," "ball," "dog," "baby," "duck," and "cat.") which they believed that their infant understood. Next, they were asked to rate their confidence in their identification using a five-point scale. Parents were told that a rating of "5" indicated that they were "very confident" that the infant did or did not know the word, while a rating of "1" signified that the parents were "not confident at all" about their decision. Following the interview, parent ratings were converted to a range from "1" to "10", with "1" signifying high confidence that the infant did not know the word, and "10" signifying high confidence that the infant knew the word. The stimuli which were used as the "known" words in the present study had a mean rating of 9.7 out of 10.0 (s.d. = .4). For the "unknown" words, there was a mean rating of 1.9 (s.d. = .5). Each tape contained stimulus repetitions of two spoken words produced by an adult male speaker using flat intonation. Each word began with a voiced, stop consonant to minimize E R P variations due to acoustic factors such as voicing or rise time. One of the two words was identified by that infant's parent as known to the infant while a second word was believed by the parent to be unknown to the infant. The known and unknown words were arranged on the tape in a block random order, with 54 occurrences of each and a randomly varied interstimulus interval. Six silver cup scalp electrodes were placed over the left and right sides of each infant's head. These placements included two electrodes placed respectively over the left (T3) and fight (T4) temporal areas of the Ten-Twenty System (Jasper, 1958); a third electrode placed a t FL, a point midway between the external meatus of the left ear and Fz; a fourth electrode placed at FR, a position midway between the right external meatus and Fz; a fifth electrode placed at PL, a point midway

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between the left external meatas and Pz; and a sixth electrode placed at PR, a point on the fight side of the head midway between the right ear's external meatus and Pz. These electrode placements were positioned on the scalp over the left frontal (FL), temporal (T3), and parietal (PL) areas of the brain and the corresponding areas of the fight hemisphere (FR, T4, and PR, respectively). Such placements, it was hoped, would provide information concerning not only left versus right hemisphere responses to the known and unknown words, but in addition, information within each hemisphere concerning general language perception areas commonly thought to be localized to the left temporal and parietal language receptive regions of the brain as well as the language production areas of the frontal lobe. The electrical activity recorded from these scalp electrodes was obtained in response to a randomly arranged series of words matched in duration and peak intensity levels. As in previous studies by Molfese and his collaborators, scalp electrodes were referred to electrodes placed on each earlobe and linked together (A1, A2). The words were presented auditorily through a speaker positioned approximately one meter over the midline of the infant's head at 80 dB SPL (A) as measured at the infant's ears and occurred while the infant was in a quiet awake state. Continuous monitoring of the infant's ongoing EEG and EMG, as well as behavioral observation, were used to determine when stimulus presentation should occur. During periods of motor activity, stimulus presentation was suspended and the infant was shown various toys and pictures until quieting. Testing was resumed when the infant's motor activity declined to an acceptable level. Data reduction and analysis procedures first involved digitizing 70 data points over a 700 ms period beginning at stimulus onset for each electrode site, stimulus event, and infant. Next, the ERPs were subjected to artifact rejection for each electrode to eliminate from further analyses those contaminated by motor or eye movements. This resulted in rejecting less than 10% of the trials for each infant. Rejection rates were comparable across the two stimulus conditions. Following artifact rejection, the single trial data were then averaged separately for each electrode site and stimulus condition. Thus, 12 averages were obtained for each infant,. These included averages for the known and unknown words for each of the six scalp electrode sites. As in the case of the speech perception studies, the average ERPs then were submitted to a two step analysis procedure (Brown, Marsh, & Smith, 1979; Chapman,

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McCrary, Bragdon, & Chapman, 1979; Donchin, Teuting, Ritter, Kutas, & Heffley, 1975; Gelfer, 1987; Molfese, 1978a, 1978b; Molfese & Molfese, 1979b, 1980, 1985; Ruchkin, Sutton, Munson, Silver, & Macar, 1981; Segalowitz & Cohen, 1989). This procedure first involved the use of a Principal Components Analysis (PCA) and then an Analysis of Variance. Factor scores or weights were generated by the PCA for each of the 108 averaged ERPs for each of the six rotated factors accounting for 77.84% of the total variance. The ANOVAs were based on the design of Subjects (9) X Word Understanding (2) X Electrode Sites Within Hemispheres (3)X Hemispheres (2). These were conducted to determine if any of the regions of the ERPs identified by the six factors varied systematically as a function of the specific levels of the independent variables in this study. Two ERP regions were noted to vary as a function of whether parents believed that the infant could recognize the meaning of a word or not. The first region which reflected variations in the initial portion of the waveform until approximately 140 ms following stimulus onset indicated that ERP activity recorded from over all left hemisphere sites discriminated the known from the unknown words. However, only electrical activity from the frontal and temporal regions of the right hemisphere made similar discriminations. The ERPs elicited by the known words were characterized by a larger negative (or downward) peak prior to 140 ms while a markedly smaller negative peak characterized the ERPs evoked by the unknown words. Thus, the vertical amplitude appears larger for the known words than the unknown words. A second region of the averaged ERPs between 210 and 300 ms post stimulus onset also varied systematically as a function of whether the word was thought to be understood by the infant. This effect was reflected by amplitude differences in the second major negative component of the ERP where the overall negative peak-to-peak amplitude in the region between 210 and 300 ms was generally larger for ERPs elicited by the known than by the unknown words. These results were interpreted by Molfese and colleagues to indicate that auditory evoked ERPs successfully discriminated between words that parents believed their 12-month-old infants knew from those that the infants were thought not to understand. Moreover, Molfese et al. noted that even at this young age the process of word comprehension appeared to be dynamic in that different regions of the brain responded differently over time following the onset of the word that was known to

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the infant. Initially, differential electrical activity was generated early in the waveform for approximately 200 ms over the entire left hemisphere and most of the right hemisphere except the right parietal area Such early responses suggest that the infant may begin to process words as meaningful from virtually the time they begin to hear the auditory signal. This initial response period then was followed for a 100 ms period by a spreading of the discrimination to all ERP scalp regions. Thus, the differential response of the ERPs to words appears to continue through much of the time that the infant hears the word, although it appears to be carried out by different brain regions. In Experiment 1 of a study with older infants, Molfese (1989) recorded auditory evoked responses from frontal, temporal, and parietal scalp locations over the left and right hemispheres of 10 infants, 14 months in age, who also listened to a series of words, half of which were determined to be known to the infants (based on behavioral testing and parental report) and half of which were believed not to be known to the infant. A behavioral test was used to confirm the parents' ratings of their infant's word comprehension. As in the case of the 12-month infant study (Molfese, et al., 1993), parents rated words from a list as either words the infant knew or words they did not know. In addition, however, each infant received four behavioral trials, with two independent observers rating whether or not the infant knew the word presented. In order to assess the infant's comprehension, a specially constructed cabinet was used. The cabinet was 1 meter in height and contained four shelves, each .4 meters in length, with two shelves to the left and two shelves to the fight of midline. The object representing the known or the unknown word (as appropriate) was placed in one of the four compartments of a test cabinet. Two compartments of the test box each contained distracter items randomly selected for each trial from a sack of toys while the fourth compartment remained empty. The parent then instructed the infant to look at or retrieve various toys using instructions to the infant such as, "Go get the book." or "Look at the duck." The compartments that contained the test object, the empty space, and the distracters were randomized for each trial for each infant based on a randomly generated list derived by computer prior to the test session. On each trial the raters independently determined whether they believed that the infant responded to the instructions correctly and recorded their confidence in these judgments on a 5-point scale identical to that previously used by the parents. For the children in this study, both the

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parents (across the two interviews) and the raters reliably rated the words they believed were known to the infant as different from those that they believed the infant did not understand. Analyses of the ERP data isolated three regions of the evoked potential waveform that discriminated known from unknown words in this population. Initially, ERP activity across both hemispheres (with the exception of the fight parietal region) between 30 and 220 ms following stimulus onset discriminated known from unknown words. This effect appeared as a positive peak for the known words and a negative peak in this same region for the unknown words. This activity was followed shortly by a large positive to negative shift in the waveform between 270 and 380 ms across all electrode sites for both the left and right hemispheres that was larger for the known than for the unknown words. Finally, a late negative peak between 380 and 500 ms that was detected only by electrodes placed over the left and right parietal regions was larger for the known than for the unknown words. In Experiment 2 of this study, Molfese attempted to determine whether familiarity with speech stimuli produced brain responses similar to those found for the known vs. unknown word materials. In this procedure, a different set of ten 14-month-old infants first listened to a nonsense bisyllable (CVCV)over a 2 day period. Parents encouraged their infant to play with a box on which a large orange Frisbee was mounted and connected to a series of switches. Infants played with the device for three times on each of the 2 days designated for training, with 15 minutes allowed for each of the six play sessions. Five infants heard "toto" during the familiarization process while five children heard "gigi" to decrease the likelihood that any experimental effects were due to acoustic differences between the stimuli instead of due to differences in amount of previous exposure to the different stimuli. On the third day, ERPs were recorded to this now familiar CVCV and to the novel CVCV. Electrode placements were identical to those used in Experiment 1. If the latencies and scalp distributions of the brain responses found in this study were identical to those found in the known - unknown word study, it was felt that the familiarity hypothesis could not be rejected. In fact, however, results indicated that only the brain responses recorded over both the left- and right-hemisphere frontal areas discriminated between the familiar and nonfamiliar CVCVs. In addition, the major peak in the ERP that discriminated these differences occurred at 360 ms, not at the 630 ms previously found for the known - unknown word distinction.

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Consequently, Molfese concluded that the earlier ERP findings discussed in the first experiment did indeed reflect meaning differences and not differences in familiarity. A study with 16-month-old infants (Molfese, 1990) which utilized procedures similar to those employed by Molfese, Wetzel, and Gill (1993) and Expt. 1 of Molfese (1989), found comparable differences in response to known and unknown words. Molfese tested 18 infants (9 females, 9 males with a mean age of 16.57 mo. (s.d.=.6, range=15.417.5). As in his previous studies, parent handedness was measured and found to indicate strong right hand preferences across parents. In addition, parents were asked to rate a set of 10 words during a telephone interview and a subsequent lab visit in order to identify at least one word that parents confidently believed their infant knew and another word they believed the infant did not know. As in the case of Experiment 1 of Molfese (1989), two independent raters evaluated infants' word knowledge using the four shelf cabinet. Only infants were tested whose parents and raters agreed on the same set of known and unknown words, and who displayed high confidence that the infant did or did not know specific words. Following these rating procedures, electrodes were applied to six electrode sites, three over each hemisphere using the same scalp locations and references used previously by Molfese in this series of studies. ERP testing then commenced with 54 repetitions of each of the two words presented auditorily in random order, separated from each other by a varied ISI random (2.5-4 Sec.). A principal components analysis of the averaged ERPs yielded five factors (scree) accounting for 74.33% of the total variance. Two factors identified ERP regions which varied as a function of the KNOWN vs. UNKNOWN distinction. The first region, between 180 and 340 ms with a peak latency of 270 ms contained a larger N180 - P340 complex for UNKNOWN words at only the T3 site for females while the left and fight frontal regions as well as T3 showed a similar effect for males. A second region, between 580 and 700, with a peak latency of 650 ms, also discriminated KNOWN vs. UNKNOWN words for females but this time at all LH sites while for males, both the LH and RH sites discriminated KNOWN vs. UNKNOWN words. In all cases, this discrimination was reflected by larger negative shifts for UNKNOWN words. A fourth study by Molfese, Morse, and Peters (1990) also investigated aspects of the infant's early word comprehension, but this time in a training situation. Fourteen infants, seven females and seven

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males, at 14 month of age (mean = 14.72 months, s.d. = .63) participated in a training study in which specific CVCV nonsense syllables were systematically paired with specific objects of specific shapes and colors over a five day training period. Handedness questionnaires administered to all parents (Edinburgh Inventory, Oldfield, 1971) indicated that both parents of each infant were strongly fight handed (group mean Laterality Quotient = .67, s.d. = . 19). On the day before the training period, infants first were tested in a Match Mismatch task in which on half of the trials each object was paired with its CVCV label (i.e., the label that the infant would later learn during the training period was the "name" of that object) while on the other half of the trials the objects were mispaired with the CVCV "names" of other objects. The parents and infants then returned home for 5 days of training. On the sixth day and immediately prior to the post-training session, parent were asked to indicate whether or not their infants knew the name of the object in question and then to rate their own confidence in that judgment using a 5 point scale with "1" as "completely not confident" and "5" as " very confident". The confidence ratings were then used to transform parents' ratings from a "1" of "confidently unknown" to a "unknown but completely not confident" rating of "5" to a "known but completely not confident" rating of "6" to a "confidently known" rating of "10". Using this rating system all parent rated the terms as "known" by the infant with a mean confidence rating for "bidu" at 8.71 (s.d. = .88) and for "gibu at 8.79 (s.d. = .94), indicating that the parents as a group were confident that their infants understood which terms labeled which objects. Next, during the post-training test, infants again were tested in a Match - Mismatch task in which on half of the trials each object was paired with its CVCV label (Match condition) while on the other half of the trials the objects were mispaired with the CVCV "names" of other objects (Mismatch condition). The electrophysiological techniques used during this phase were identical to those employed during the pretest phase of this study. Using artifact rejection and analysis procedures comparable to those employed in the earlier studies conducted by Molfese and colleagues, the ERPs were averaged separately for the pre- and post-training tests for each of the six electrode sites and each of the two stimulus conditions (match vs. mismatch). Twelve averages were obtained for each data set for each infant. Each average was based on 80 samples

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combining responses to "bidu" and "gibu" for the Match condition and 80 samples across "bidu" and "gibu" for the Mismatch condition. Two regions of the ERP waveform reliably reflected Match related effects during this task - an early component of the ERP which changed bilaterally over the frontal regions of both hemispheres and a late occurring lateralized response which was restricted to only the left hemisphere electrode sites. The first, which occurred between 30 and 120 ms post stimulus onset, was characterized by a marked negativity for the Mismatch condition. A second region, which began 520 ms after stimulus onset, reached its peak at 580 ms, and then diminished by 600 ms, produced a positive going wave for the Mismatch condition over all of the left hemisphere electrode sites. Since no such Match or Mismatch effects were noted in the pretraining ERP session, it is clear that the ERPs detected changes which occurred as a function of training. When a correct match occurred between the auditorily presented word and the object that the infant held, both the left and right frontal regions of the brain emitted brain responses which contained an initial positive deflection or peak between 20 and 100 ms following the auditory onset of the object name. If a mismatch occurred, however, this early positive deflection inverted 180 degrees and became a negative deflection. Later in time, between 520 and 600 ms, just before the conclusion of the ERP, a large positive going wave occurred over only the three left hemisphere electrode sites when the infant listened to a stimulus which did not name the object that the infant held. Given the short latency of the initial changes in the ERP waveshape across the frontal regions, it appears that the young infant must recognize almost immediately if there is agreement between something that it hears and something that it sees and touches. These early word acquisition studies are summarized in Table 3. Perception of Coartieulated Cues: While the early ERP response during the first 100 ms following stimulus onset might superficially appear to have occurred before the infant could process the acoustic information of the CVCVs, such early discrimination is not without precedence. Both behavioral and electrophysiological investigations have indicated that coarticulated speech cues can lead to comprehension long before the entire word or phrase has been articulated by the speaker and heard by the listener (Ali, Gallagher, Goldstein, & Daniloff, 1971; Daniloff & Moll, 1968; MacNeilage & DeClerk, 1969; Molfese,

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Table 3. Studies Using Event-Related Potential (ERP) Procedures To Study Infant Word Acquisition. Study/Ss Molfese (1990) 14-month old infants, n= 16 (8 males, 8 females)

Electrode F L , FR T3, T4 P L , PR Reference= linked ears.

Task Auditory ERPs Experiment 1" Randomly ordered words rated as known to the infants and words rated as unknown. Equal number of known and unknown words.

Molfese, Wetzel, & Gill (1994) 12-month old infants, n= 12

Molfese (1989) 14-month old infants, n= 14

F L , FR T3, T4 P L , PR Reference= linked ears.

F L , FR T3, T4 P L , PR Reference = linked ears.

Auditory ERPs Randomly ordered words rated as known to the infants and words rated as unknown.

Results Known vs. Unknown word effects: Females: T3 Males: FL,T3, FR 180-340 ms. Females: LH frontal, temporal, parietal Males: All electrode sites. 580-700 ms. Known vs. Unknown word effects: LH frontal, temporal, parietal RH frontal, temporal 210-300 ms.

Equal number of known and unknown words.

All electrode sites. 210-300 ms.

Auditory ERPs

Known vs. Unknown word effects:

Experiment 1: Randomly ordered words rated as known to the infants and words rated as unknown. Equal number of known and unknown words.

LH frontal, temporal, parietal RH frontal, temporal 30 - 220 ms. All electrode sites 270-380 ms. LH and RH parietal 380-500 ms.

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Table 3: cont'd Study/Ss Mills, CoffeyCorina, & Neville (1993) 20.5-month old infants, n=24 (16 females, 8 males)

Electrode F7, F8, 33% distance from T3/4 to C3/4, 50% of distance from T3/4 to P3/4, O1, 02. Reference= linked mastoids.

Task AuditoryERPs Ten known words, unknown words, andbackward presented words All presented 6 times each for total of 180 trials.

Results N200: 90% showed larger N200 known vs. unknown words at LH temporal & parietal sites. 80% showed known > unknown words at LH frontal and RH temporal & parietal sites. Known: Temporal, parietal > frontal, occipital Unknown: RH amplitude > LH. Larger to known than backward at frontal, temporal & parietal sites. Larger to unknown than backward at RH sites. Backward ERPs more positive over LH anterior than LH posterior sites. N350 latency: Known < backward (by 20 ms). N350 amplitude: Known > unknown at LH temporal & parietal sites. Known > backward at LH sites. Unknown > backward at RH sites. Unknown larger for RH than LH sites. N600-900: For all stimuli, anterior RH>LH. No sex related effects.

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T a b l e 3: cont'd

Study/Ss Molfese, Morse, & Peters (1990) 14-month old infants, n= 14

Electrode

Task

Results

F L , FR T3, T4 P L , PR

Auditory ERPs

Pretraining test: No ERP differences for Match vs. Mismatch

Reference= linked ears.

Pretraining test: ERPs to meaningless CVCVs. 5 days training, 2 blocks of 15 minutes per day training one CVCV to one novel object and another CVCV to another novel

Post training test: Match vs. Mismatch wordeffects: LH and RH frontal 30 - 120 ms.

LH frontal, temporal, parietal 530-600 ms

object. Post training test: Parents rate training effectiveness; ERPs to same CVCV s used in pretraining test. RH = Right hemisphere LH = Left hemisphere

1979). It is possible that infants used such information to discriminate between the Match and Mismatch conditions of the Molfese, Morse, and Peters (1990) study as well as the known versus unknown discrimination studies of Molfese (1989, 1990). Coarticulation refers to the finding that the shape of the vocal tract during the production of a speech sound will be altered by the place and manner of articulation for later speech sounds. MacNeilage and DeClerk, in one study, made cineflurograms and electromyograms of individuals producing a series of 36 CVC syllables and found that the articulation of the initial consonant sounds changed as a function of the identify of the following sounds. Ali, et al. noted a perceptual counterpart of coarticulation. They constructed series

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of CVC and CVVC syllables in which final sounds were either nasal [m, n] or non-nasal consonants. After the final vowel-consonant and consonant transitions were removed, the resulting CV and CVV syllables were presented to a group of adults who were able to discriminate between the nasal and non-nasal sequences at well above chance levels. Ali et al. and others have argued that such coarticulated information allows the listener to perceive and process some or all of the utterance at a more rapid pace and before it has been completely articulated. In fact, there appears to be an neuroelectrical correlate of perception for coarticulated cues. Molfese (1979) in a study with adults recorded ERPs to duration matched CVC words and nonsense syllables which differed from each other only in the final consonant sound. Adults listened to each CVC and then after a brief delay pressed one of two keys to indicate whether they had heard a word or a nonsense syllable. Three regions of the ERP, including one that peaked 60 ms following stimulus onset, changed systematically as a function of the meaningfulness of the CVC syllables. Molfese interpreted this component as well as later negative peaks at 260 and 400 ms as sensitive to the coarticulated speech cues which carried information concerning the later occurring (after 650 ms) final consonant sound. In the Molfese, Morse, and Peters (1990) study, given that the consonant burst and frequency transition information that discriminated one C V C V from the other occurred during approximately the first 50 ms of each stimulus (MacNeilage & DeClerk, 1969), it is possible that infants utilized this coarticulated perceptual information to rapidly identify and discriminate early in time between the auditory tokens that matched or failed to match the object the infant was holding throughout a block of trials. If infants can indeed process such acoustic (and consequently linguistic) information this rapidly so early in development, it would seem quite likely that we have been underestimating significantly the infant early language processing abilities. Such findings suggest that ERP studies with young infants can be used to both successfully study early word acquisition and the processes they use to acquire and recognize words. Mills, Coffey-Corina, and Neville (1993), in a more recent study of early infant word perception, recorded auditory ERPs from 24 children, 16 females and 8 males (mean age = 20.5 mo.) to a series of 10 comprehended (known), unknown, and backward presented words. A language assessment test, the Early Language Inventory (ELI), was administered one week before ERP testing. Parents rated 120 words on

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1-4 scale of confidence that child did or did not comprehend word. Also a Comprehension Book with 50 object names, 9 verbs and modifiers was presented to the child who then pointed to each picture verbalized by experimenter. The child's language production was tested separately. These procedures allowed investigators to identify stimuli for the ERP test. For the electrophysiological part of the study, each child was seated in a parent's lap, opposite an audio speaker which was positioned behind hand puppets used to focus the child's attention. ERPs were collected to 10 known, unknown, and backward words presented 6 times each for 180 trials. An electrode cap was used with electrodes placed at F7, F8, 33% distance from T3 to C3 and from T4 to C4, 50% of distance from T3 to P3, and from T4 to P4, O1, 02, all referenced to linked mastoids. Prior to analyses the children were divided into two groups based on whether their ELI was above or below the 50th percentile. Subsequent tests then confirmed that these groups differed on productive vocabulary and comprehension. In general, Mills et al reported larger temporal and parietal responses than for frontal or occipital sites for known words, while there were larger RH responses overall to unknown words. A number of known vs. unknown word effects were noted. For the N200 region (the most negative point between 125-250 ms) 90% of the children produced a larger N200 to known versus unknown words at LH temporal and parietal sites while 80% showed a larger N200 to known versus unknown words at LH frontal and RH temporal and parietal sites. When comparisons included backward speech, larger responses were noted to known and unknown words than to backward speech, with generally more positive responses over LH anterior than LH posterior sites. At the next major peak measured (N350 - the most negative point between 275 and 450 ms), the known words elicited a faster N350 than backward speech (by 20 ms). Amplitude measures of this peak found larger responses to known than unknown words at LH temporal and parietal sites. Unknown words overall elicited larger responses over RH than LH sites. Finally, responses to known words were larger than to backward stimuli at LH sites while unknown words elicited larger responses than backward stimuli at RH sites. Measures of the negative wave in the region between 600 and 900 ms noted that all stimuli elicited larger anterior RH than LH responses.

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When ERP sensitivity to language abilities was compared between the two language groups, a number of additional effects were noted. Overall, the N200 amplitude was greater for Low language producers for both known and unknown words. N350 latency was fastest to known words for the High production group (by 28 ms). Additionally, High production group had larger N350 amplitudes at LH temporal and parietal sites. Other later effects were also noted within the 600-900 region (mean negative amplitude between 600-900 ms). The negative amplitude was largest for known words for the High production group at RH frontal site, and the Low production group at bilateral anterior sites. Known words also produced larger responses for the Low than High producers at LH temporal and parietal sites while the unknown words produced larger responses for the Low than for the High producers at RH parietal site. Unlike Molfese (1990), who tested 16-month-olds, they did not note any sex effects. Summary of early word acquisition studies. Based on this review, it is clear that electrophysiological measures involving the auditory event related potential can be used successfully to discriminate between ERPs elicited by words thought to be known to an infant versus words identified as unknown. As argued elsewhere, such procedures open up a number of possibilities, both for exploring further the semantic development of the young infant and for detecting developmental problems in children who are slow in acquiring their first words. There are remarkably similarities in terms of scalp electrode effects and k n o w n - unknown word discrimination effects across studies. For example, Molfese (1989, Experiment 1) noted that three regions of the ERP waveform discriminated known from unknown words. Initially, ERP activity across both hemispheres (with the exception of the right parietal region) between 30 and 220 ms following stimulus onset discriminated between known and unknown words. Thus, in two different ages of infants, 12-month-olds and 14-month-olds, similar regions of the ERP waveform distributed over the same electrode recording areas discriminated known from unknown words. A similar effect was also reported by Molfese, Morse, and Peters (1990). Furthermore, in all three studies, this activity was followed shortly by a large positive to negative change in amplitude across all electrode sites for both the left and right hemispheres that was larger for known than for unknown words or match versus mismatched labels. Molfese (1989) reported that this effect

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occurred between 270 and 380 ms while Molfese et al. (1990) identified this area between 210 and 300 ms. These studies differ, however, in that Molfese (1989) reported a third, late negative peak between 380 and 500 ms, that was detected only by electrodes placed over the left and fight parietal regions, an effect which was larger for the known than for the unknown words. No such effect was noted by Molfese et al. The absence of such a late effect in the ERP responses of 12-month-old infants could reflect differences in the developmental stages between the younger infants tested by Molfese, Wetzel, and Gill (1993) and the older infants tested by Molfese (1989, 1990). Molfese, Wetzel, and Gill (1993), as in the case of both Molfese (1989) and Molfese, Morse, and Peters (1990), observed an effect in the initial portion of the ERP that discriminated known from unknown words. Given other behavioral and electrophysiological investigations of coarticulated speech cues as noted above (Ali, Gallagher, Goldstein, & Daniloff, 197 l, Daniloff & Moll, 1968; MacNeilage & DeClerk, 1969; Molfese, 1979), it is possible that the infants can use acoustic correlates of articulatory information in the initial portion of words to identify words. If so, this suggests that such perceptual strategies are mastered by the infant at a very early stage of the language learning process. It is interesting to note that, although a general belief exists that language perception is carried out by mechanisms within the left hemisphere (Lenneberg, 1967), none of the known versus unknown word related effects were exclusively restricted to only the left hemisphere electrode sites in infants younger than 16 months of age. Even the Mills et al. study with 20+ month-old infants indicate that a large percentage of children (80%) showed larger N200 responses to known than unknown words at both LH frontal and RH temporal and parietal sites. The N350 latency difference between known and unknown words also occurred across both hemispheres, rather than for only LH sites. These data can be used to argue that, at least in the early stages of language acquisition, both hemispheres of the brain are dynamically involved in the process of learning to relate word speech sound sequences to word meanings. If this is indeed the case, then perhaps the reason that young infants experiencing left hemisphere brain damage during the initial stages of language acquisition are able to recover language skills more quickly than those injured later may be due to the duplicated mechanisms subserving language abilities of the right hemisphere at that stage. Consequently, after the loss of the left

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hemisphere, the infant's language functions may continue to be served by these fight hemisphere mechanisms. If, on the other hand, the child experiences left hemisphere damage later in development, the outcome could be quite different. Either due to changes in brain plasticity or further specialization of the brain with development, the ability of the non-language specialized hemisphere in the normally developing child becomes more restricted with age. Consequently, following injury to the left hemisphere at this later stage of development, there may not be a right hemisphere that is capable of performing these functions and therefore language performance would be impaired because the right hemisphere is unable to continue this process in the absence of a fully functioning left hemisphere. Instead, the right hemisphere would only have residual abilities that reflected its involvement at a much earlier stage of development. The initial tenet of this review was to discern whether similar mechanisms might underlay different cognitive areas in infancy. A working hypothesis was that similarities in peak latency, amplitude, and scalp distribution effects across different cognitive domains would suggest that these different cognitive domains depend at some level on similar mechanisms. Alternatively, if one accepts Karrer and Monti's (1995) argument that differences in latency and response pattern must argue for different mechanisms which generate these differences, one is struck by marked differences between these different cognitive domains. Infant speech perception responses generally appear to occur at approximately 200, 530, and 900 ms post stimulus onset for VOT and at approximately 200, 400, 630, and 850 ms for POA. The major discrepancy between studies for these two cues appears to be centered on variations in the ERP's middle latencies between 400 and 630 ms, as well as the scalp distributions for these effects. This suggests that different mechanisms must subserve these two different speech cues. With age, responses to both speech cues appear to occur earlier in time as indicated by shorter latency responses in the ERP waveforms. In addition, ERPs to speech materials appear to generate multiple responses in the infant waveform with an earlier ERP peak varying bilaterally while a second, later peak occurs in a lateralized fashion. Across both speech cues bilateral responses appear to occur with similar latencies. The lateralized responses for these two cues, however, show much more variability. POA and VOT thus elicit different lateral patterns with

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different latencies. This is a further indication that different mechanisms must underlay these two different speech cues. Studies of infant memory, on the other hand, report many bilateral effects, often restricted to frontal areas. Latencies for these responses initially appear to occur between 100 - 500 ms and between 500 - 1000 ms. A later response beyond 1000 ms appears to emerge by 6-months of age (Nelson, Ellis, Collins, & Lang, 1990) while the response prior to 500 ms is less well noted. Finally, word related effects appear even at the earliest ages tested (12 months of age) to elicit both left and right hemisphere responses throughout the first 500 ms of the wave. Even with older infants at 16 and 22 months of age, discrimination of known from unknown words continues to occur between 200 and nearly 700 ms following the onset of the word. Thus, there is a marked pattern of overlap between ERP components which (1) signal the reception of acoustic and visual information with (2) those components which indicate recognition and recall, to (3) those peak changes which reflect the understanding of word meanings. Instead of the simplistic serial model of processing described at the outset of this chapter, the infant brain appears to process different types of information (i.e., speech sounds, memory, and meaning) in an overlapping fashion and not necessarily in the expected temporal order. There are, of course, some marked differences in the ages of the infants tested for each cognitive domain and such differences could contribute to the overlapping latency results. Younger infants might simply produce longer latency responses regardless of the cognitive area of test because of their more immature nervous system and the additional time needed for information to travel along incompletely myelinated pathways to dendritic trees which are still relatively early in their developmental life. The bulk of the infant speech perception studies focus on infants from birth through 5 months of age while the memory studies report findings from infants ranging in age from four weeks to 12 months of age. The earliest work with word discrimination appears to be have the least overlap in subject ages tested with these other cognitive areas since testing did not commence until 12 months of age (Molfese, Wetzel, & Gill, 1993)and then extended upwards to 20 months of age (Mills et al, 1993). Nevertheless, from the existing data with vowel perception (Molfese & Searock, 1986), memory (Nelson & Karrer, 1992; Nelson & deRegnier, 1992; Molfese, 1989, Molfese & Wetzel, 1992), and word discrimination studies (Molfese, 1989, 1990,

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Molfese, Morse, & Peters, 1990; Molfese, Wetzel, & Gill, 1993) we can still discern that by one-year of age some speech discrimination effects occur slightly earlier in time than some word related effects, which all occur earlier than the memory effects reported for older infants. The one question we started out with at the beginning of this chapter now becomes many questions. Are the memory studies which produce such late responses relative to these other domains measuring factors which simply are unrelated to speech perception and word meaning? Are speech perception and word discrimination more automated at this stage and consequently require less time for processing or are there some innately specified mechanisms which subserve at least some aspects of speech perception which contribute to those faster response times? Does the infant's early knowledge of perception for coarticulated speech information tap such mechanisms and consequently results in such faster processing time for word discrimination? It is obvious from this review that there are a large number of gaps in our knowledge about each of these three domains of infant cognition. In fact, we still know very little about the neurophysiological development of mechanisms underlying not only speech perception, but memory, and early language development as well. Clearly, there is a great deal of work that still needs to be done before questions concerning the integration of infant cognition can be adequately addressed.

Acknowledgements Support for this work was provided by the National Science Foundation (BNS8004429, BNS 8210846), and the National Institutes of Health (R01-HD 17860).

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Molfese, D. L. (1978b). Left and right hemispheric involvement in the speech perception: Electrophysiological correlates. Perception and Psychophysics, 23, 237-243. Molfese, D. L. (1979). Cortical and subcortical involvement in the processing of coarticulated cues. Brain and Language, 7, 86-100. Molfese, D. L. (1980a). Hemispheric specialization for temporal information: Implications for the processing of voicing cues during speech perception. Brain and Language, 11, 285-300. Molfese, D. L. (1980b). The phoneme and the engram: Electrophysiological evidence for the acoustic invariant in stop consonants. Brain and Language, 9, 372-376. Molfese, D. L. (1983). Event related potentials and language processes. In A.W.K. Gaillard & W. Ritter (Eds.), Tutorials in ERP Research: Endogenous Components, (pp 345-368). The Netherlands: North Holland Publishing Co. Molfese, D. L. (1984). Left hemisphere sensitivity to consonant sounds not displayed by the right hemisphere: Electrophysiological correlates. Brain and Language, 22, 109-127. Molfese, D. L. (1989). Electrophysiological correlates of word meanings in 14-month-old human infants. Developmental Neuropsychology, 5, 79-103. Molfese, D. L. (1990). Auditory evoked responses recorded from 16month-old human infants to words they did and did not know. Brain and Language, 38, 345-363. Molfese, D. L. & Betz, J. C. (1988). Electrophysiological indices of the early development of lateralization for language and cognition and their implications for predicting later development. In D.L. Molfese and S.J. Segalowitz (Eds.), Developmental Implications of Brain Lateralization, (pp. 171-190). New York: Guilford Press. Molfese, D. L. & Hess, R. M. (1978). Speech perception in nursery school age children" Sex and hemispheric differences. Journal of Experimental Child Psychology, 26, 71-84. Molfese, D. L. & Molfese, V. J. (1979a). Infant speech perception: Learned or innate. In H. A. Whitaker and H. Whitaker (Eds.), Advances in Neurolinguistics, Vol. 4. New York: Academic Press. Molfese, D. L. & Molfese, V. J. (1979b). Hemisphere and stimulus differences as reflected in the cortical responses of newborn infants to speech stimuli. Developmental Psychology, 15, 505-511. Molfese, D. L. & Molfese, V. J. (1980). Cortical responses of preterm infants to phonetic and nonphonetic speech stimuli. Developmental Psychology, 16, 574- 581. Molfese, D. L. & Molfese, V. J. (1997). Discrimination of language skills at five years of age using event related potentials recorded at birth. Developmental Neuropsychology,13, 135-156. Molfese, D. L. & Molfese, V. J. (1985). Electrophysiological indices of auditory discrimination in newborn infants: The basis for predicting

Cognitive Development 379 later language development. Infant Behavior and Development, 8, 197-211. Molfese, D. L. & Molfese, V. J. (1988). Right hemisphere responses from preschool children to temporal cues contained in speech and nonspeech materials: Electrophysiological correlates. Brain and Language, 33, 245-259. Molfese, D. L. & Schmidt, A. L. (1983). An auditory evoked potential study of consonant perception. Brain and Language, 18, 57-70. Molfese, D. L. & Searock, K. (1986). The use of auditory evoked responses at one year of age to predict language skills at 3 years. Australian Journal of Communication Disorders, 14, 35-46. Molfese, D. L. & Wetzel, W. F. (1992). Short and long term memory in 14 month old infants: Electrophysiological correlates. Developmental

Neuropsychology, 8, 135-160. Molfese, D. L., Buhrke, R. A., & Wang, S. L. (1985). The right hemisphere and temporal processing of consonant transition durations" Electrophysiological correlates. Brain and Language, 26, 289-299. Molfese, D. L., Burger-Judisch, L. M., & Hans, L. L. (1991). Consonant discrimination by newborn infants: Electrophysiological differences. Developmental Neuropsychology, 7, 177-195. Molfese, D. L., Freeman, R. B., Jr., & Palermo, D. S. (1975). The ontogeny of lateralization for speech and nonspeech stimuli. Brain

and Language, 2, 356- 368. Molfese, D. L., Linnville, S. E., Wetzel, W. F., & Leicht, D. (1985). Electrophysiological correlates of handedness and speech perception contrasts. Neuropsychologia, 23, 77-86. Molfese, D. L., Morse, P. A., & Peters, C. J. (1990). Auditory evoked responses from infants to names for different objects: Cross modal processing as a basis for early language acquisition. Developmental Psycho logy, 26, 780-795. Molfese, D. L., Wetzel, W. F., & Gill, L. A. (1993). Known versus unknown word discrimination in 12-month-old human infants: Electrophysiological correlates. Developmental Neuropsychology, 34, 241-258. Molfese, V. J., Molfese, D. L., & Parsons, C. (1983). Hemispheric involvement in phonological perception. In S. Segalowitz (Ed.), Language Functions and Brain Organization, (pp. 29-50). New York: Academic Press. Morse, P. A. (1974). Infant speech perception: A preliminary model and review of the literature. In R. Schiefelbusch and L. Lloyd (Eds.),

Language perspectives: Acquisition, retardation, and intervention, (pp. 19-53). Baltimore: University Park Press. Morse, P. A. & Snowdon, C. (1975). An investigation of categorical speech discrimination by rhesus monkeys. Perception &

Psychophysics, 17, 9-16.

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Nelson, C. A. & Collins, P. (1991). An event related potential and looking time analysis of infants' responses to familiar and novel events" Implications for visual recognition memory. Developmental Psychology, 27, 50-58. Nelson, C. A. & Collins, P. (1992). Neural and behavioral correlates of recognition memory in 4- and 8-month olds infants. Brain and Cognition, 19, 105-121. Nelson, C. A. & deRegnier, R. (1992). Neural correlates of attention and memory in the first year of life. Developmental Neuropsychology, 8, 119-134. Nelson, C. A. & Salapatek, P. (1986). Electrophysiological correlates Of infant recognition memory. Child Development, 57, 1483-1497. Nelson, C. A., Ellis, A., Collins, P., & Lang, S. (1990). Infants' neuroelectric responses to missing stimuli: Can the missing stimuli be novel stimuli? Developmental Neuropsychology, 6, 339-349. Nelson, C. A., Henschel, M. & Collins, P. (1993). Neural correlates of cross-modal recognition memory in 8-month-old infants.

Developmental Psychology,. Nikkel, L., & Karrer, R. (1994). Differential effects of experience on the ERP and behavior of 6-month-old infants: Trends during repeated stimulus presentations. Developmental Neuropsychology, 10, 1-11. Oldfield, R. L. (1971). The assessment of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97-113. Perecman, E., & Kellar, L. (1981). The effect of voice and place among aphasic, nonaphasic right-damaged and normal subjects on a metalinguistic task. Brain and Language, 12, 213-223. Pisoni, D. B. (1977). Identification and discrimination of the relative onset time of two component tones" Implications for voicing perception in stops. Journal of the Acoustical Society of America, 61, 1352-1361. Retherford, K. S., Schwartz, B. C., & Chapman, R. S. (1981). Semantic roles and residual grammatical categories in mother and child speech. Journal of Child Language, 8, 583-608. Rockstroh, B., Elbert, T., Birbaumer, N., & Lutzenberger, W. (1982). Slow brain potentials and behavior. Baltimore: Urban & Schwarzenberg. Ruchkin, D., Sutton, S., Munson, R., Silver, K., & Macar, F. (1981). P300 and feedback provided by absence of the stimulus. Psychophysiology, 18, 271-282. Segalowitz, S. J. & Cohen, H. (1989). Right hemisphere EEG sensitivity to speech. Brain and Language, 37, 220-231. Simos, P. G., & Molfese, D. L. (1997). Electrophysiological responses from a temporal order continuum in the newborn infant. Neuropsychologia, 35, 89-98.

Cognitive Development 381 Simos, P. G., Molfese, D. L., Brenden, R. A. (1997). Behavioral and electrophysiological indices of voicing cue discrimination: Laterality patterns and development. Brain and Cognition, Snyder, L., Bates, E., and Bretherton, I. (1981). Content and context in early lexical development. Journal of Child Language, 8, 565-582. Streeter, L. A. (1976). Language perception of two-month-old infants shows effects of both innate mechanisms and experience. Nature, 259, 39-41. Sullivan, M., Rovee-Collier, C., Tynes, D. (1979). A conditioning analysis of infant long-term memory. Child Development, 50, 152-162. Thomas, D. G. and Lykins, M. S. (1995). Event-related potential measures of 24-hour retention in 5-month-old infants. Developmental Psychology, 31,946-957.

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Chapter 12

The lpsilateral Auditory Pathway: A Psychobiological Perspective. Kendall A. Hutson University of Toledo

Since the time of Ferrier (1876a, 1890) the ascending auditory system has been viewed as "contralateralized". That is, auditory information arriving at one cochlea traverses the central auditory pathways destined for the contralateral auditory cortex. For nearly a century, the pathway ultimately responsible for "hearing" was thought to be the projection of the dorsal cochlear nucleus to the contralateral medial geniculate body of the thalamus and from there to the auditory cortex (e.g., Winkler, 1911, 1921). Not all investigators agreed with the conclusion that only pathways from the dorsal cochlear nucleus subserved heating. Indeed, the view of a contralateralized auditory system was not universally accepted. One of the earliest investigations into the function of auditory cortex was conducted by Luciani (1884). From his studies, Luciani provided some very important insights as to the function of the ascending auditory system. He noted that subsequent to unilateral ablation of auditory cortex, an animals behavior could only be explained by "each ear having connections with both auditory spheres [cortex] ... In fact, every unilateral extirpation of sufficient extent in the province of the auditory sphere causes a bilateral disorder of hearing, more marked on the opposite side." He concluded that in the auditory system, as in the visual system "we must distinguish a crossed and a direct fasciculus."

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Thompson (1878) had expressed a similar view, and further stated the true nature of the problem: "to account for a blending of the sensations [derived from the two ears] ... this point deserves the attention of anatomists and physiologists." By the turn of the century, the anatomical bilaterality of the central auditory pathways had been well documented (e.g., Bechterew, 1885; Baginski, 1886, 1890; Monakow, 1887, 1890; Bumm, 1889; Held, 1891, 1893; Kolliker, 1896; Ferrier & Turner, 1898; Tschermak, 1899). Indeed, the findings of these Continental anatomists had even made their way into American textbooks, e.g., Gordinier (1899). Physiological evidence for a functional ipsilateral component of the ascending auditory pathway was provided by Kreidl (1914). Here, after section of the decussating contralateral pathways experimental animals "showed no difference in hearing ability from normal control animals." Thus, it seemed an inescapable conclusion that the ascending auditory system was composed of both ipsilateral and contralateral pathways. Unfortunately, as noted by Rosenzweig (1961), "After these early achievements, progress not only lagged but some of the findings were even forgotten by workers in the field. Thus, for example, it was taken as surprising in 1928 when removal of one hemisphere of a patient did not destroy hearing in the opposite ear." Again the view of a contralateralized auditory system prevailed, and over the years the notion of a functional ipsilateral pathway was subjected to relative obscurity. Textbook descriptions of the central auditory system referred only vaguely to the existence of ipsilateral components of the system "which is known more on a clinical and physiological than an anatomical basis" (Fulton, 1946; Ranson & Clark, 1947). Further, the underlying pathway for heating was once again reduced only to the contralateral projections of the dorsal cochlear nucleus (e.g., Strong & Elwyn, 1953). From the results of modern investigations of the central auditory system, the concept of a functional ipsilateral pathway has re-emerged. Moreover, it is clear that ipsilateral pathways have an important role in the so-called "acoustic chiasm" of Glendenning and Masterton (1983). Therefore, it seems timely to re-evaluate the nature of the ipsilateral auditory system and its role in audition. The general outline of this paper will be to discuss evidence favoring a functional ipsilateral auditory pathway. Results from anatomical, physiological, and behavioral investigations will be introduced as they pertain to the question of the potential significance of ipsilateral

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pathways. Particular attention will be paid to physiological mechanisms of the auditory system in which a functional ipsilateral pathway may help to explain.

I. Anatomy of the Ascending Auditory System Briefly, the ascending central auditory system begins with the termination of the eighth nerve onto the secondary sensory neurons of the cochlear nuclear complex. The cochlear nuclei then give rise to three separate, yet not completely isolated central pathways known as the acoustic striae. The striae traverse the brainstem sending axons, in various amounts, to the superior olivary complex, the nuclei of the lateral lemniscus, and the inferior colliculus. Neurons of the superior olivary complex send their axons to the nuclei of the lateral lemniscus and to the inferior colliculus. The nuclei of the lateral lemniscus project mainly to the inferior colliculus. The inferior colliculus then originates fibers destined for the medial geniculate body, which in turn issues fibers of the auditory radiations to innervate the auditory cortex. Various commissural systems exist which interconnect the right and the left halves of the central pathways. In the sections that follow, details of the central auditory system will be presented. These will be concerned primarily with the pathways from the cochlear nucleus to the inferior colliculus, accepting the established fact that projections from inferior colliculus through auditory cortex remain, for all practical purposes, on the same or homolateral side of the brain (see Hutson, 1988; Hutson et al., 1991; 1993). Therefore, above the level of the inferior colliculus there is no need to distinguish a substantial ipsilateral versus contralateral fiber pathway.

Nuclei of the Central Auditory System Cochlear Nucleus. This complex of cells is composed of two major divisions, one dorsal (dorsal cochlear nucleus, DCN), the other ventral (ventral cochlear nucleus, VCN). The entering eighth nerve further subdivides the VCN into an anterior portion (anterior ventral cochlear nucleus, AVCN) and a posterior portion (posterior ventral cochlear nucleus, PVCN). Having entered the cochlear nucleus, the eighth nerve bifurcates giving rise to an ascending branch and a descending branch. The ascending branch terminates in the AVCN, while the descending

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branch innervates both the PVCN and the DCN (Ramon y Cajal, 1909; Lorente De No, 1933; Rose, 1960; Jones et al., 1992, Ryugo and Rouiller, 1988). Although the cochlear nucleus is made up of at least 14 different cell types based on Golgi material (e.g., Lorente De No, 1933; Brawer et al., 1974), the most useful cell classifications are those of Osen (1969a), Warr (1982), and Morest et al., (1990) which are based on Nissl preparations. Following this scheme, there are five major cell types in the cochlear nucleus. Three of these cell types are unique to one of the three divisions of the cochlear nucleus: pyramidal (or fusiform) cells in the DCN; spherical cells in the AVCN; and octopus cells in the PVCN. The remaining two cell types, globular and multipolar, are distributed around the entrance of the eighth nerve and therefore lie in both the AVCN and PVCN. The VCN can then be visualized as having spherical cells rostral, globular and multipolar cells in middle regions, and octopus cells caudally (Osen, 1969a). Along its margins, the cochlear nucleus is surrounded or encapsulated by a small cell shell or cap, composed predominantly of granule cells (Mugnaini et al., 1980; Hutson and Morest, 1996). Superior Olivary Complex. The superior olivary complex consists of four major sub-nuclei, all of which are embedded in the fibers of the trapezoid body. These are the lateral superior olive (LSO), the medial superior olive (MSO), the medial nucleus of the trapezoid body (MTB), and a group of cells collectively termed the peri-olivary nuclei. The peri-olivary nuclei are cell groups which surround the LSO, MSO, and MTB (Morest, 1968), and for the most part participate in descending connections of the auditory system (though some exceptions may exist, e.g., see Adams, 1983; Spangler et al., 1985, Schofield & Cant, 1992; Ostapoff, et al., 1997; Warr & Beck, 1996). Since the peri-olivary nuclei probably do not contribute greatly to the ascending auditory system, they will not be discussed in detail. Lateral Superior Olive. The predominant cell type of the LSO is fusiform in shape, possessing large polar dendrites extending toward the margins of the nucleus. The distinguishing characteristic of the LSO is its convoluted shape. Typically the nuclear contour follows an S-shape, as seen in the cat, although there are some species differences (e.g., West, 1970; Moore, 1987; Heffner & Masterton, 1990). Despite species variation in shape, the neurons and their appendages always orient themselves in such a way to be approximately perpendicular to the

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margins of the nucleus (Held, 1893; Hofmann, 1908; Stotler, 1953; Scheibel & Scheibel, 1974; Cant, 1984; Helfert & Schwartz, 1987). Medial Superior Olive. The MSO has certain striking morphological qualities that make it easily discernible from other nuclei of the superior olivary complex. It is composed of a cluster of cells arranged in a dorsal-ventral stack or column, (often appearing comma-shaped as in the cat), bounded laterally by the LSO and medially by the MTB. Individual cells of MSO are quite unique in that radiating from their cell bodies are two large diametrically opposed dendrites, one pointing laterally the other medially. These singular properties of MSO have been well documented across a wide variety of mammals (La Villa, 1898; Hofmann, 1908, Ramon y Cajal, 1909; Shaner, 1934; Stotler, 1953; Verhaart, 1970; Moore & Moore, 1971, Harrison & Howe, 1974; Willard & Martin, 1983; Henkel & Brunso-Bechtold, 1990). Medial Nucleus of the Trapezoid Body. This nucleus resides ventrally in the medulla within the fibers of the trapezoid body, located between the MSO laterally and the exiting sixth nerve medially. The nucleus generally appears roughly triangular in shape, although it's cells do not conform to any distinctive geometric outline as do cells of the LSO and MSO. The main cellular component of MTB is the principal cell which is large and round to ovoid in shape (e.g., Morest, 1968; Harrison & Feldman, 1970; Willard & Martin, 1983; Kuwabara & Zook, 1991). Nuclei of the Lateral Lemniscus. The nuclei of the lateral lemniscus lie among the fiber fascicles of the lateral lemniscus, collectively bridging the pons between the medullary superior olivary complex and the inferior colliculus at midbrain levels. Nuclei of the lateral lemniscus have classically been divided into two divisions, one ventral (ventral nucleus of the lateral lemniscus, VLL) the other dorsal (dorsal nucleus of the lateral lemniscus, DLL). The VLL is the larger of the two, and can be divided further into three zones, ventral, middle, and dorsal. Recently, the dorsal region of VLL has been referred to as the intermediate nucleus of the lateral lemniscus (ILL; e.g., Glendenning et al., 1981; Zook & Casseday, 1982a; Willard & Ryugo, 1983; Hutson et al., 1991). The VLL is composed of several cell types, with multipolar cells scattered throughout its length. There is a ventro-dorsal gradient of distinguishing cell types. Ventrally, large oval cells give way to a higher density of elongate cells in the middle zone, which become less packed in the dorsal zone (Whitley & Henkel, 1984). The DLL also contains a

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variety of cell types, the most distinguishing of which are elongate cells with their dendrites oriented horizontally (Kane & Barone, 1980). Inferior Colliculus. In Nissl preparations, the inferior colliculus is divisible into four sub-nuclei: the central nucleus, the dorsomedial nucleus, the pericentral nucleus, and the external nucleus. With respect to the ascending auditory system, the central nucleus of the inferior colliculus is of primary importance. The central nucleus is encapsulated by the pericentral nucleus (dorsally and caudally), the external nucleus (laterally), the dorsomedial nucleus (dorsomedially, as the name implies), and the peri-aquaductal grey (ventromedially, see Rockel & Jones, 1973a; Harrison, 1978). Further subdivision is possible in Golgi stained material (e.g., Morest & Oliver, 1984). Two cell types characterize the central nucleus of the inferior colliculus, primary cells with disc shaped dendritic fields and multipolar or stellate cells with spherical dendritic fields (Rockel & Jones, 1973a; Oliver & Morest, 1984; Oliver et al., 1991). For simplicity, in the remaining sections of this paper the term IC will be used to denote the central nucleus of the inferior colliculus.

Basic Physiological Properties There are three basic physiological characteristics that define the neurons of the auditory brainstem: the unit discharge properties, the binaural response classification, and the tonotopic arrangement within the individual nuclei. Unit Discharge. Neurons below the level of the inferior colliculus have, as a general characteristic, unit discharge patterns that are tonic in nature. Although variations in discharge patterns have been observed (i.e. "choppers" or "primary-notch" or "complex") all have the common characteristic of a maintained discharge throughout the stimulus period (e.g., Goldberg & Brown, 1968; Boudreau & Tsuchitani, 1970; Aitkin et a1.,1970, 1981; Guinan et al., 1972a; Tsuchitani, 1977; Brugge & Geisler, 1978; Feng et al., 1994). At the IC, the situation is quite different. Here, the tonic or sustained discharge type unit response is seen, but the much more prevalent response type is that of a phasic or "onset" type of discharge (e.g., Erulkar, 1959, 197.5; Rose et al., 1963). Binaural Response Classification. Within the central auditory system, neurons can be classified based on their response to stimuli presented to both ears (e.g., Goldberg & Brown, 1968). For example,

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(P C

F i g u r e 1. Tonotopic organization in auditory brainstem nuclei of the cat. Note the preservation of the arrangement of frequencies (H, high; L, low) in each nucleus. A similar arrangement is present in all other auditory structures. Also shown are the unique neuronal and dendritic arrangements which characterize the medial superior olive (MSO) and the lateral superior olive (LSO). AVCN, anterior ventral cochlear nucleus; DCN, dorsal cochlear nucleus; DLL, dorsal nucleus of the lateral lemniscus; IC, inferior colliculus; MTB, medial nucleus of the trapezoid body; PVCN, posterior ventral cochlear nucleus; VLL, ventral nucleus of the lateral lemniscus. Based on Stotler, 1953; Rose et al., 1959; Aitldn et al., 1970; Guinan et al., 1972b; Merzenich & Reid, 1974.

neurons of the LSO respond to acoustic stimuli presented to either ear, typically stimulation of the ear ipsilateral to LSO causes excitation while stimulation of the contralateral ear results in inhibition (e.g., Goldberg et al., 1963). Thus, LSO units may be classified binaurally as El, (meaning ipsilateral = Excitatory, contralateral = Inhibitory; Goldberg & Brown, 1968; Tsuchitani, 1977; Caird & Klinke, 1983)1. Similarly MSO can be classified as binaurally excitatory, or EE; in contrast, MTB is classified as OE meaning no response to ipsilateral ear stimulation but

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Right SOC MSO

MTB

Figure 2. Details of tonotopic organization of the right superior olivary complex (SOC) of the cat. Numbers reflect range of best frequencies in kHz of units located within the SOC. Note that high frequencies are represented medially in the medial nucleus of the trapezoid body (MTB), ventrally in the medial superior olive (MSO), and medially (medial "limb") in the lateral superior olive (LSO). Low frequencies are represemed laterally in MTB, dorsally in MSO, and laterally (lateral "limb") in LSO. Also note that both MTB and LSO have a larger cross-sectional area devoted to the representation of higher frequencies (e.g., greater than 4 kHz) while MSO has a larger cross-sectional area devoted to the representation of lower frequencies (e.g., less than 4 kHz). Adapted from Boudreau and Tsuchitani, 1970; Guinan et al., 1972b.

excited by contralateral ear stimulation (Goldberg & Brown, 1968; Guinan et al., 1972a; Caird & Klinke, 1983; Spitzer & Semple, 1995). Units within VLL are OE; while the DLL appears to have two types of binaural units, EE cells are found dorsally in DLL and IE cells ventrally in DLL (Aitkin et al., 1970; Brugge et al., 1970; Markovitz and Pollak, 1994). The IC has a mixed population of binaurally classified cells, most of which are IE, with EE and OE units also being quite common (e.g., Roth et al., 1978; Semple & Aitkin, 1979; Aitkin & Martin, 1987). Tonotopicity. A common organizational feature amongst the various auditory nuclei is that they are arranged in an orderly tonotopic sequence. Within the cochlea, moving from the apical to basal turns,

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there is an orderly progression of sensitivity from low to high frequencies. This orderly progression is followed through the eighth nerve onto the cochlear nucleus (e.g., Rose, 1960; Arnesen & Osen, 1978). Electrophysiological studies have reported that within each auditory nucleus a similar orderly progression of frequency sensitivity can be demonstrated (e.g., Rose et al., 1959, 1963; Rose, 1960; Boudreau & Tsuchitani, 1970; Aitkin et al., 1970; Guinan et al., 1972b; Merzenich & Reid, 1974; Bourk et al., 1981; Clarey et al., 1992). Thus, there is a tonotopic or more correctly a cochleotopic, organization topograghically mapped onto each auditory nucleus (see Figure 1). Particular attention has been given to demonstrating the frequency distribution within the superior olivary complex (Figure 2). The LSO and MTB appear to have more nuclear volume devoted to the representation of middle to high range frequencies, whereas MSO has most of its nuclear mass devoted to low to middle range frequencies (Boudreau & Tsuchitani, 1970, 1973; Guinan et al., 1972b; Tsuchitani, 1977, 1982; Yin & C h a n , 1990). Other auditory nuclei do not show such a distinct frequency specificity, rather they show a more even representation of frequency sensitivity (e.g., Rose, 1960; Merzenich & Reid, 1974).

The Central Auditory Pathways The central auditory pathways will first be described in terms of an integrated system, in which both crossed (contralateral) and uncrossed (ipsilateral) connections will be included. A discussion of the crossed pathway is necessary for arguments that will be made in later sections of this paper. The final anatomy section will detail the ipsilateral pathway. Connections of the Cochlear Nucleus. Neurons of the cochlear nucleus give rise to all second order auditory afferent fibers, which are collectively termed the acoustic striae. The acoustic striae compose, in part, the medullary decussation of the auditory system and were well known to the Classical anatomists (e.g., Flechsig, 1876; Monakow, 1890; Held, 1891, 1893; Kolliker, 1896; Van Gehuchten, 1902, 1903; Ramon y Cajal, 1909). The striae can be divided into three major pathways: the dorsal acoustic stria of Monakow (DAS); the intermediate acoustic stria of Held (IAS); and the ventral acoustic stria of Flechsig, better known as the trapezoid body. Axons of the three stria distribute themselves to the superior olivary complex, the nuclei of the lateral lemniscus, and the inferior colliculus in various quantities.

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The Dorsal Acoustic Stria contains fibers that originate primarily from the fusiform (or pyramidal) cells of the DCN. From the DCN axons pass dorsally over the restiform body, then sweep ventrally to cross the midline just dorsal to the superior olivary complex, where the fibers enter the medial aspects of the contralateral lateral lemniscus (Fernandez & Karapas, 1967; Van Noort, 1969). During their course through the brainstem fibers of the DAS may give off collaterals to the VLL, however virtually all of these fibers terminate throughout the contralateral IC (Osen, 1972, Adams & Warr, 1976; Beyerl, 1978; Adams, 1979; Brunso-Bechtold et al., 1981; Nordeen et al., 1983; Willard & Martin, 1983, Oliver, 1984). The Intermediate Acoustic Stria originates primarily from the octopus cells of the PVCN (though some fusiform cells of DCN may contribute axons to this pathway as well). Fibers of the IAS pass dorsally over the restiform body in association with the DAS. At this point the IAS separates and descends medial to the restiform body to a level just above the ipsilateral superior olivary complex where the fibers turn medially to pass through the nuclei and tract of the spinal trigeminal complex. The IAS then continues on a medial course just above the trapezoid body, crossing the midline and joining with the DAS to enter the medial aspects of the contralateral lateral lemniscus. Fibers of the IAS terminate primarily in the contralateral VLL, though contributing a scant projection to the ipsilateral LSO and contralateral IC (Fernandez and Karapas, 1967; Oliver, 1984). Unless specifically referred to by name (dorsal or intermediate acoustic stria), these two pathways will collectively be designated as the dorsal striae (DS; see Figure 3). The Trapezoid Body contains fibers originating from every cell group of the VCN (e.g., Warr, 1982), and is by far the largest fiber component of the medullary auditory system. Trapezoid body fibers exit the VCN ventral to the restiform body and course medially to innervate the ipsilateral superior olivary complex, the contralateral superior olivary complex, and then continue within the lateral aspects of the lateral lemniscus to reach the contralateral nuclei of the lateral lemniscus and IC (e.g., Flechsig, 1876; Held, 1891, 1893; Sabin, 1897; Ferrier & Turner, 1898; Van Gehuchten, 1902, 1903; Ramon y Cajal, 1909; Fuse, 1919; Poljak, 192.5; Barnes et al., 1943; Warr, 1966, 1969, 1972, 1982; Van Noort, 1969; Browner & Webster, 1975; Strominger et al., 1977; Brunso-Bechtold et al., 1981; Glendenning et al., 1981, 1985, Thompson & Thompson, 1991).

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ClC

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I

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Figure 3. Schematic diagram summarizing the major connections of auditory brainstem nuclei. Note that this is a simplified diagram, and each projection shown has a "mirror-image" on the opposite side of the midline. Solid lines major pathways, dashed lines minor pathways. Also for convenience the dorsal and intermediate acoustic striae have been depicted simply as the dorsal striae (DS). See text for details of connections. CIC, commissure of inferior colliculus; CPr, commissure of Probst; DCN; dorsal cochlear nucleus; DLL, dorsal nucleus of the lateral lemniscus; IC, inferior colliculus; LL, lateral lemniscus; LSO, lateral superior olive; MSO, medial superior olive; MTB, medial nucleus of the trapezoid body; TB, trapezoid body; VCN, ventral cochlear nucleus; VLL, ventral nucleus of the lateral lemniscus.

In addition to the three striae just described, axons of cells from all divisions of the cochlear nucleus enter the ipsilateral lateral lemniscus directly, ascending to the ipsilateral nuclei of the lateral lemniscus and ipsilateral IC. Although in terms of the number of cells involved, these ipsilateral cochlear nucleus projections are not as large as the contralateral projections, they do exist, as demonstrated by a variety of anato-

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mical 1902, 1982; 1979;

techniques (e.g., Baginski, 1886; Held, 1893; Van Gehuchten, 1903; Poljak, 1925; Woollard & Harpman, 1940; Warr, 1972, Brunso-Bechtold & Thompson, 1976; Roth et al, 1978; Adams, Glendenning et al, 1981; Nordeen et al., 1983; Oliver, 1987).

Connections of the Superior Olivary Complex The Medial Nucleus of the Trapezoid Body. One of the most salient characteristics of the MTB is in the mode of termination of its afferent supply. Since before the turn of the century it was known that each principal cell of MTB received a large nerve ending, the calyx of Held (Held, 1893; Ramon y Cajal, 1896; Meyer, 1896; Kolliker, 1896; La Villa, 1898; Turner & Hunter, 1899; Vincenzi, 1900; Veratti, 1900). It was assumed, on the basis of histological inspection of normal material, that it was the contralateral VCN which originated the fibers ending in calyces on MTB cells (e.g., Held, 1893), but the connection was proven by degeneration studies (e.g., Lewy, 1909). Ablation of the cochlear nucleus causes dense degeneration within the contralateral MTB, demonstrable by degeneration stains or by the loss of calyces in normal stains (Barnes et al., 1943; Stotler, 1953; Harrison & Warr, 1962; Powell & Erulkar, 1962; Warr, 1972; Jean-Baptiste & Morest, 1975). While unilateral cochlear nucleus destruction only affects the contralateral MTB, bilateral destruction of the cochlear nucleus or section of the trapezoid body near the midline causes total loss of calyces in the MTB of both sides, therefore the evidence is quite substantial that the source of afferent innervation to MTB is the contralateral cochlear nucleus (Tschermak, 1899; Fuse, 1916, 1919; Stotler, 1953; Harrison & Warr, 1962; Harrison & Irving, 1964). More recent investigations using restricted lesion placement, anterograde or retrograde axonal transport methods have demonstrated that it is the globular cells of the contralateral VCN, whose large axons traverse the trapezoid body, that terminate in calyces on MTB principal cells (e.g., Warr, 1972, 1982; Tolbert et al., 1982; Glendenning et al., 1985, Spirou et al., 1990; Smith et al., 1991; Kuwabara et al., 1991). The principal cells of MTB send their axons to three major sites, all of which are located homolateral to MTB; these are the LSO, the nuclei of the lateral lemniscus, and the IC. Axons of these cells pass over, under, and through MSO to reach their targets in LSO. Other axons, or more likely, collaterals enter the lateral aspects of the lateral lemniscus

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ascending primarily to the ILL, and to a much lesser extent to VLL, DLL and IC (Browner & Webster, 1975; Brunso-Bechtold & Thompson, 1976; Elverland, 1978; Glendenning et al., 1981, 1985; Held, 1893; Lewy, 1909; Ramon y Cajal, 1909; Rasmussen, 1946, 1967; Spangler et al., 1985; Van Noort, 1969). In summary, the MTB is a monaural nucleus receiving afferents from the contralateral cochlear nucleus, and distributing its axons to other auditory nuclei of the same side. The Medial Superior Olive. In contrast to MTB, the MSO is a binaural nucleus, receiving its primary afferent supply from the cochlear nucleus of both sides of the brain (Ferrier & Turner, 1898; Poljak, 1925; Stotler, 1949, 1953; Warr, 1966; Glendenning et al, 1985). Afferents to MSO terminate in a unique and specific manner. Destruction of one cochlea or cochlear nucleus will cause the loss of terminals or degeneration in MSO on both sides of the brain, but only on one dendrite, i.e., if the left cochlear nucleus is destroyed, degeneration will be seen on the laterally directed dendrites of the left (ipsilateral) MSO and on the medially directed dendrites of the fight (contralateral) MSO (Stotler, 1953). Thus, the medial dendrites receive afferents from the contralateral cochlear nucleus, while the lateral dendrites receive afferents from the ipsilateral cochlear nucleus. That afferents to MSO travel within the trapezoid body can be demonstrated by the various tract-tracing methods of degeneration (Lewy, 1909; Poljak, 1925; Woollard & Harpman, 1940; Warr, 1966; Harrison & Irving, 1966; Goldberg & Brown, 1968; Van Noort, 1969; Strominger & Strominger, 1971; Glendenning et al., 1981, 1985), or axoplasmic transport (e.g., Glendenning et al., 1985; Zook & Casseday, 1985; Smith et al., 1993). More specifically, section of the trapezoid body at the midline results in afferent degeneration on the medial dendrites of MSO on both sides of the brain, while section of the trapezoid body as it exits the V CN produces the same degeneration pattern as cochlear nucleus ablation (Stotler, 1953; Harrison & Warr, 1962). Restricted lesions of V CN, or axonal transport studies reveal that the cells of origin of MSO afferents are the spherical cells of the AVCN (Warr, 1966; Kiss & Majorossy, 1983; Zook & Casseday, 1985; Cant & Casseday, 1986; Smith et al., 1993). The MSO also receives indirect inputs from both cochlear nuclei via collateral innervation from other cell groups of the ipsilateral superior olivary complex. Fibers from MTB occasionally send collaterals to MSO while en route to other structures, and thus indirectly supply information from the contralateral cochlear nucleus, while some

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indirect information from the ipsilateral cochlear nucleus is provided by one of the peri-olivary nuclei, i.e., the lateral nucleus of the trapezoid body (e.g., Spangler et al., 1985; Banks & Smith, 1992; Cant & Hyson, 1992; Smith, 1995). Axons of MSO cells project within the medial aspects of the ipsilateral lateral lemniscus to terminate in the ipsilateral DLL (Rasmussen, 1946; Niemer & Cheng, 1949; Van Noort, 1969; Elverland, 1978; Glendenning et al., 1981; Henkel & Spangler, 1983) and ipsilateral IC (Monakow, 1890; Fuse, 1911; Niemer & Cheng, 1949; Roth et al., 1978; Adams, 1979; Brunso-Bechtold et al., 1981; Zook & Casseday, 1982b; Henkel & Spangler, 1983). Minor projection targets of MSO may include the ipsilateral VLL (Browner & Webster, 1975) and possibly the contralateral IC (Rasmussen, 1946; Adams, 1979; BrunsoBechtold et al., 1981; Kudo et al., 1988). However, the ipsilateral DLL and ipsilateral IC are by far the principal efferent targets of MSO. Thus, the MSO receives direct bilateral afferent innervation, while axons of its constituent cells ascend almost exclusively to the ipsilateral DLL and IC. The Lateral Superior Olive. Afferents to LSO are derived from two sources, the ipsilateral cochlear nucleus and the ipsilateral MTB. The origin of LSO's afferent innervation was a puzzle for quite some time. The projection from the ipsilateral cochlear nucleus was known quite early (e.g., Held, 1893; Ferrier & Turner, 1898), but the projection of MTB to LSO though suspected (Held, 1893), remained elusive until much later (Rasmussen, 1967). It could easily be demonstrated that destruction of one cochlear nucleus would result in massive degeneration throughout the ipsilateral LSO (e.g., Ferrier & Turner, 1898; Van Gehuchten, 1902; Woollard & Harpman, 1940), yet electrophysiologists could also demonstrate that LSO neurons responded to stimulation of both ears (e.g., Goldberg et al., 1963). Therefore, there must be a functional connection from the contralateral cochlear nucleus. Evidence of a functional connection came from Rasmussen's (1967) studies of trapezoid body transections. Selective sectioning of the trapezoid body medial to the MTB produced degeneration in MTB and MSO as expected, while cuts that included MTB produced degeneration in MSO and LSO. This was the proof needed to substantiate not only the previous Golgi observations (Held, 1893), but also his own experimental results (Rasmussen, 1946). It also proved correct the suspicions of Harrison and Warr (1962) who found that sectioning the trapezoid body immediately below LSO resulted in

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retrograde chromatolysis of principal cells in MTB. Thus the LSO receives binaural afferent innervation directly from the ipsilateral cochlear nucleus and in a two-step manner from the contralateral cochlear nucleus via the MTB. There are some details about the afferent innervation of LSO that warrant further discussion. The excitatory ipsilateral supply to LSO has been found to originate from the spherical cells of the AVCN (Harrison & Warr, 1962; Harrison & Irving, 1966; Osen, 1969b; Rouiller & Ryugo, 1984f Glendenning et al., 1985; Shneiderman & Henkel, 1987, Cant & Casseday, 1986), and are distributed to the LSO in a precise tonotopic arrangement (e.g., Warr, 1966, 1982). The MTB also projects to LSO in a precise tonotopic manner (Glendenning et al., 1985; Spangler et al., 1985), yet this innervation of LSO by MTB is not equally distributed to all parts of LSO. Electrophysiologically, the ipsilateral innervation of LSO is excitatory throughout the nucleus, while the contralateral inhibition (via the inhibitory interneurons of MTB) does not extend throughout the nucleus. Although the excitatory and inhibitory inputs to the same area of LSO are well matched in terms of best-frequency (e.g., Boudreau & Tsuchitani, 1968; Guinan et al., 1972b; Banks & Smith, 1992), low frequency LSO neurons, i.e., those of the lateral limb responding to 2000 Hz or less, are not inhibited by contralateral stimulation (Boudreau & Tsuchitani, 1968, 1970; Tsuchitani & Boudreau, 1969; Tsuchitani, 1977, 1982). This same point has been demonstrated anatomically in that MTB lesions result in anterograde degeneration that is more dense in the medial limb of LSO (high frequency) and very sparse degeneration in the lateral limb of LSO (low frequency; Goldberg, 1975; Glendenning et al., 1985). This graded projection of MTB to LSO has been verified by anterograde transport studies and by 14C-2deoxyglucose techniques (e.g., Glendenning et al., 1985). Thus the entire LSO receives direct excitatory innervation from the ipsilateral AVCN, and an indirect inhibitory innervation from the contralateral VCN via synapse in the MTB which ultimately exerts its influence more on high frequency units and then grades down to no influence on low frequency units. Two other lines of investigation directly address the point of MTB inhibition of LSO. Microiontophoretic application of glycine, a potent inhibitory neurotransmitter, effectively mimics the action of MTB on LSO neurons actively responding to stimulation of the ipsilateral ear. More importantly strychnine, a specific glycine receptor antagonist,

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blocks the inhibitory effects of binaural stimulation. Thus glycine is most likely the neurotransmitter used by MTB to inhibit neuronal activity in LSO (Moore & Caspary, 1983). Even more striking was the demonstration that 3H-strychnine (which specifically binds to glycine receptors) marked a receptor distribution gradient in LSO essentially identical to what would be predicted from the anatomical results, i.e., highest concentration of receptors in the medial limb and lowest concentration of receptors in the lateral limb (Sanes et al., 1985). Thus there is ample reason to believe that MTB inhibits LSO non-uniformly across the nucleus, and that the neurotransmitter acting at the MTB-LSO synapse is probably glycine (Wenthold et al., 1987; Glendenning & Baker, 1988; Bledsoe et al., 1990; Wu & Kelly, 1992). However, the low frequency lateral limb of LSO is not totally devoid of inhibitory inputs (Brownell et al., 1979; Wu & Kelly, 1994). The source of these inputs appear to arise from the ipsilateral lateral nucleus of the trapezoid body or from the ipsilateral cochlear nucleus itself (Glendenning et al., 1991). Neurons of LSO project axons into the lateral lemniscus of both sides in approximately equal numbers (Monakow, 1890; Yoshida, 1925; Poljak, 1925; Papez, 1930; Ohnisi, 1932; Niemer & Cheng, 1949; Stotler, 1953; Glendenning & Masterton, 1983). Efferent axons of LSO terminate predominantly in the IC (Roth et al., 1978; Brunso-Bechtold et al., 1981; Glendenning & Masterton, 1983; Casseday & Covey, 1983; Shneiderman & Henkel, 1987; Hutson, 1988; Vater et al., 1995), in DLL (Elverland, 1978; Glendenning et al., 1981; Shneiderman et al., 1988; Hutson, 1988; Vater et al., 1995), and only meagerly in VLL (Browner and Webster, 1975). An important feature of the efferent projections of LSO is that they are not random, instead specific portions of LSO project either ipsilaterally or contralaterally. The high frequency medial limb projects contralaterally, crossing the midline above the trapezoid body to enter the contralateral lateral lemniscus medially, while the low frequency lateral limb projects to the ipsilateral lateral lemniscus ascending in both its medial and lateral aspects (Van Noort, 1969; Glendenning et al., 1981). Cells of LSO representing intermediate frequencies project to either lateral lemniscus, but very few project bilaterally (Glendenning & Masterton, 1983). Nuclei of the Lateral Lemniscus. The VLL receives its afferent supply almost exclusively from the contralateral VCN (Glendenning et al., 1981; Warr, 1982; Vater & Feng, 1990). One exception to this is a small area of the ventral division of VLL that receives, apparently

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exclusive, innervation from the ipsilateral VCN (Glendenning et al., 1981; Warr, 1972). Other minor projections to VLL arise from both the ipsilateral and contralateral superior olivary complex, the most substantial of these originate from the ipsilateral MTB (Lewy, 1909; Zook & Casseday, 1979, Glendenning et al., 1981, Spangler et al., 1985). The ILL (or dorsal division of VLL), while receiving its major afferent supply from the contralateral VCN, also receives a substantial projection from the ipsilateral MTB. This is the heaviest MTB projection to any structure other than LSO (Glendenning et al., 1981; Spangler et al., 1985). When the ILL is injected with retrogradely transported tracer substances, the majority of principal cells of MTB are labeled throughout its rostro-caudal length. Therefore it would seem likely that the same MTB cells that innervate the LSO also send a collateral to ILL or at least some portion of the VLL (Spangler et al., 1985). Despite small projections from LSO and MSO, the VLL and ILL can be collectively considered as monaural nuclei under the influence of the contralateral cochlear nucleus directly or indirectly via the MTB. The only exception is a very small area of the ventral VLL that is innervated exclusively by the ipsilateral VCN, and therefore also monaural in nature (Warr, 1982, Glendenning et al., 1985, Spangler et al., 1985). Neurons of VLL, together with ILL, project principally to the IC (Zook & Casseday, 1979, 1982b; Brunso-Bechtold et al., 1981, Whitley & Henkel, 1984; Hutson, 1988; Glendenning et al., 1990; Hutson et al., 1991), though there are some meager VLL fiber terminations in the ILL and DLL, again probably collaterals of fibers en route to IC (Kudo, 1981; Whitley & Henkel, 1984). A tiny, yet demonstrable projection of ILL is to the medial division of the ipsilateral and contralateral medial geniculate body (Papez, 1929a,b; Kudo, 1981; Whitley & Henkel, 1984; Aitkin & Phillips, 1984a, Hutson, 1988; Hutson et al., 1991). These few axons that bypass the IC have been termed the central acoustic tract and travel medial to the brachium of the inferior colliculus (Ramon y Cajal, 1909; Papez, 1929a,b; Whitley & Henkel, 1984, Hutson et al., 1991). In contrast to VLL, the DLL receives bilateral innervation through the convergence of a variety of inputs, many of which are presumed to be collaterals of fibers destined for IC (Warr, 1966; Glcndenning et al., 1981). The most meager of the afferents to DLL arise from the ipsilateral MTB and the cochlear nucleus of both sides (Held, 1893; Kolliker, 1896; Fernandez & Karapas, 1967; Glendenning et al., 1981; Van Noort, 1969, Shneiderman et al., 1988). The few fibers from the

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contralateral DCN enter DLL medially (Fernandez & Karapas, 1967), while those of the ipsilateral and contralateral ventral cochlear nucleus enter DLL from its lateral edge (Warr, 1966; Van Noort, 1969; Browner & Webster, 1975). The contribution from the contralateral ventral cochlear nucleus is somewhat more substantial than the ipsilateral VCN (Glendenning et al., 1981; Shneiderman et al., 1988). The major afferents to DLL originate in the ipsilateral LSO and MSO, contralateral LSO and DLL (Monakow, 1890; Held, 1893; Glendenning et al., 1981; Woollard & Harpman, 1940; Barnes et al., 1943; Elverland, 1978; Zook & Casseday, 1979; Shneiderman & Henkel, 1987; Hutson, 1988; Hutson et al., 1991). Of all the afferents to DLL, the most prominent arise from the ipsilateral superior olivary complex (Glendenning et al., 1981). The principal efferent targets of DLL are the ipsilateral IC, contralateral IC and DLL (Kolliker, 1896; Woollard & Harpman, 1940; Kudo, 1981; Brunso-Bechtold et al., 1981; Shneiderman et al., 1988; Hutson, 1988; Hutson et al., 1991). To reach the ipsilateral IC, DLL efferent fibers ascend directly within the lateral lemniscus, while efferent fibers destined to innervate contralateral structures course through the commissure of Probst (Probst, 1902) bound for the opposite DLL and the contralateral IC (Held, 1893; Van Gehuchten, 1903; Stokes, 1912; Castaldi, 1926; Ariens Kappers et al., 1936; Woollard & Harpman, 1940; Goldberg & Moore, 1967; Brunso-Bechtold et al., 1981; Glendenning et al., 1981; Kudo, 1981; Whitley & Henkel, 1984; Hutson et al., 1991). The Inferior Colliculus. As mentioned above, very few fibers of the ascending auditory system bypass the IC, and as such the IC may be considered an obligatory synapse for all ascending afferents (Ferrier & Turner, 1898; Aitkin & Phillips, 1984a; Rouiller & Ribaupierre, 1985; Hutson et al., 1991; Hutson et al., 1993). The discussion so far has revealed the multitude of projections to the IC, therefore a brief list of these afferents should suffice. The major afferents originate in the contralateral cochlear nucleus, contralateral and ipsilateral LSO, ipsilateral MSO, ipsilateral VLL, ipsilateral and contralateral DLL (e.g., Adams, 1979; Brunso-Bechtold et al., 1981). Lesser afferents arise from the ipsilateral cochlear nucleus, and ipsilateral MTB (Brunso-Bechtold & Thompson, 1976; Adams, 1979; Brunso-Bechtold et al., 1981; Warr, 1982; Spangler et al, 1985).

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Neurons of the IC have two major efferent routes, the brachium of the inferior colliculus and the commissure of the inferior colliculus. The main efferent pathway of the IC is through its brachium to reach the ipsilateral medial geniculate body (MG). Terminals of IC fibers can be found in all divisions of the MG, but they are most concentrated in the ventral division of MG, which in turn projects to primary auditory cortex (Monakow, 1895; Woollard & Harpman, 1940; Anderson et al., 1980; Moore & Goldberg, 1963; Winer et al., 1977; Kudo & Niimi, 1978, 1980; Ravizza & Belmore, 1978; Morel & Imig, 1987; Hutson, 1988; Hutson et al., 1991, 1993). Axons projecting through the commissure of the inferior colliculus terminate in the dorsomedial division of the contralateral inferior colliculus, probably to participate in the descending system, though a modest number of fibers continue on to reach the MG of the opposite side (Diamond et al., 1969; Kudo & Niimi, 1980; Aitkin & Phillips, 1984b; Hutson, 1988; Hutson et al., 1991, 1993). Commissures. In the preceding sections the various commissural fibers of the auditory system were discussed. Since these are the points where the two sides of the auditory system interconnect, i.e., the points of decussation, they are of obvious importance in any attempt to separate the ipsilateral pathways from the contralateral pathways. To reiterate, the major commissures are the three acoustic striae, the commissure of Probst, and the commissure of the IC (see Hutson et al., 1991). There is of course, the corpus callosum, interconnecting the auditory cortices of the two hemispheres (e.g., Diamond et al., 1968; Imig & Brugge, 1978; Code &Winer, 1986).

The Ipsilateral Auditory Pathway From the preceding discussion it can be seen that there are many routes ipsilateral information can travel. This can be direct, e.g., cochlear nucleus to ipsilateral IC, or indirect, e.g., cochlear nucleus to contralateral DLL and then back to ipsilateral IC through the commissure of Probst. For the remaining discussion of ipsilateral pathways, emphasis will be given to those pathways that are of direct origin. That is to say, nuclei whose afferent innervation and efferent projections do not cross the midline. This will be presented in terms of how the ascending auditory system would be affected by severing the decussating (contralateral) pathways at the midline (see Figure 4).

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The Cochlear Nucleus. Degeneration and axonal transport studies have reported a direct ipsilateral projection from DCN to IC, yet each commented on the sparsity of the pathway (Baginski, 1886; Strominger, 1973; Roth et al., 1978; Adams, 1979; Brunso-Bechtold et al., 1981; Nordeen et al., 1983). Therefore it is the VCN that gives rise to major afferents of the ascending ipsilateral auditory system. The VCN distributes its fibers to directly innervate the ipsilateral (laterally directed) dendrites of MSO, the entire LSO, a small portion of ventral VLL, the DLL, and finally the IC (e.g., Ferrier & Turner, 1898; Woollard & Harpman, 1940; Warr, 1966, 1969, 1972, 1982; Van Noort, 1969; Strominger & Strominger, 1971; Harrison & Howe, 1974; Strominger et al., 1977; Brunso-Bechtold et al., 1981; Glendenning et al., 1981, 1985, 1991, 1992; Ryugo et al., 1981; Moore & Kitzes, 1985; Cant & Casseday, 1986; Oliver, 1987). Although cochlear nucleus projections to the ipsilateral superior olivary complex arise from all regions of the VCN (high, middle, and low frequency), the projections to the ipsilateral IC originate primarily, though not exclusively, from ventral (low frequency) regions of both the DCN and VCN (Nordeen et al., 1983; Oliver, 1984, 1987). Therefore, the cochlear nucleus projections to the ipsilateral IC may have a bias toward low frequencies. The Superior Olivary Complex. It is important to note here that the influence of MTB would be completely eliminated, due to its exclusive innervation by the contralateral VCN. Carrying this one step further, MTB's efferents to ipsilateral nuclei (LSO, IC, and nuclei of the lateral lemniscus) would also be eliminated from consideration in the ipsilateral pathway. Therefore, although MTB projections are to ipsilatera! structures, its own afferent source lies in the contralateral VCN. By the restriction posed above (no axons crossing midline), the MTB is for all practical purposes de-afferented and a non-participant in the ascending ipsilateral system. The MSO and LSO would continue to be innervated by the spherical cells of AVCN, but both MSO and LSO would function without their contralateral inputs. MSO would lack innervation of its medially directed dendrites, LSO would lack contralateral inhibitory innervation. MSO would retain all of its efferent projections, i.e., a tiny projection to VLL, and huge projections to DLL and IC. In contrast LSO, under the no crossing the midline restriction, would have its efferents as well as afferents reduced by one-half. Thus, neurons medially located in LSO

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IC

! !

I

,

VLL

ti

VCN

Figure 4. Summary diagram of the major connections of the ipsilateral auditory pathway. See text for details. Abbreviations as in Figure 3.

(high frequency, and projecting across the midline) would be eliminated, though neurons located laterally in LSO (low frequency) would

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still participate in the ascending ipsilateral pathway. LSO, like MSO, would continue to supply a sparse projection to the VLL, and more substantial projections to DLL and IC. In terms of frequency representation, the ipsilateral pathways ascending from the superior olivary complex originate chiefly from neurons which respond best at middle to low frequency stimulation (i.e., MSO, lateral LSO). High frequency ipsilateral projections from the superior olivary complex would then originate primarily from neurons located ventrally in MSO (see Figure 2). The Nuclei of the Lateral Lemniscus. The major afferent sources of VLL and ILL are the contralateral cochlear nucleus and ipsilateral MTB, but as concerns the ipsilateral system, these nuclei would be almost totally eliminated following the same argument as for MTB. The only exception would be the relatively small ipsilateral VCN projection to ventral VLL, the remaining ipsilateral afferents from MSO and LSO being almost negligible by comparison (Browner & Webster, 1975, Glendenning et al., 1981). The VLL would have a minor, essentially nonexistent, role in the ipsilateral pathway contributing only its minute projections to DLL and IC from the small area of ventral VLL which receives ipsilateral cochlear nucleus inputs. On the other hand, DLL would still retain many of its afferent connections, i.e. from the cochlear nucleus, MSO, and LSO. It would lose afferents from the contralateral cochlear nucleus and contralateral DLL, but more importantly it would lose inputs from the contralateral LSO. Thus DLL would remain a highly innervated structure, receiving direct afferents from the cochlear nucleus and also from the superior olivary complex. DLL efferents would be reduced to its projections to the ipsilateral IC. The Inferior Colliculus. As can be seen, the IC would be devoid of all inputs derived from contralateral sources both directly, i.e. cochlear nucleus, and indirectly, e.g., ipsilateral MTB, VLL, contralateral LSO and DLL. It would receive those afferents of the ipsilateral pathway described above. The major efferents of IC would be, as always, to the ventral division of the MG. The connections through the commissure of the IC would be eliminated, even though these are normally probably not of great importance to the ascending auditory system. Thus, the connections above the IC, while lacking contralaterally derived information, would not be significantly reduced in terms of their projection

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fiber compliment since there are no more opportunities for their axons to cross over to the opposite side of the brain until reaching cortex. In summary, the most substantial ipsilateral pathways remaining after a midline section of the brainstem would be as shown in Figure 4. The largest components being cochlear nucleus to MSO, LSO, DLL, and IC; MSO and LSO to DLL and IC; and DLL to IC. Minor components being cochlear nucleus to VLL, and VLL to DLL and IC. Having now reviewed properties of the ascending auditory system and defined the ipsilateral components, the following sections of this paper will discuss the evidence in support of potential functions of this ipsilateral pathway. II. Role of Ipsilateral Pathway in Behavior Clearly, the essential connections of the auditory system had been described by the turn of the century (see Flechsig, 1876; Monakow, 1890; Held, 1891; Van Gehuchten, 1902, 1903; Ramon y Cajal, 1909). In particular, anatomists knew of the decussations that take place in the medulla (the acoustic striae and contralateral projections of LSO), as well as those at pontine levels (commissure of Probst and commissure of the inferior colliculus). Further, it had been shown that the medullary decussations were the primary source of any contralateral projections to higher nervous structures. The anatomical course of the auditory pathway was known to originate in the cochlear nucleus and ultimately connect with the auditory cortex of the temporal lobe. However, the physiological properties of auditory elements, other than the cochlea and auditory cortex were not known (e.g., Ferrier, 1890). This lack of physiological information did not last long, and again prior to the turn of the century physiologists were well underway into investigating the properties of the deep seated auditory structures. Some of the earliest attempts to experimentally derive the functional importance of the different auditory pathways were conducted by Hammerschlag (1899, 1901). On the basis of the following types of experiment, Hammerschlag concluded that the dorsal pathways (dorsal striae) differed from the ventral pathways (trapezoid body). Cuts were made at various positions in the medulla of cats or dogs, and the immediate effects on the tensor tympany muscle noted. From this it was concluded that only cuts of the ventral pathways had an effect on this reflex, and therefore the "hearing" pathway was located in the ventral bundle of the trapezoid body. Furthermore, it was claimed that this

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trigeminal reflex was mediated through the MSO. Even though this line of evidence is reflexive in nature and not a true test of "heating" per se, it was probably the first attempt to delineate the possible functions of the acoustic pathways. The question of the relative contributions of the medullary decussations to hearing was re-opened by Winkler (1911), who found that severing the dorsally decussating pathways (dorsal striae) rendered his two experimental cats unresponsive to sound. On this evidence, Winkler concluded that the dorsal decussations carried the largest number of auditory impulses, and therefore it was the secondary fibers arising from DCN that are ultimately responsible for the transmission of auditory information to cortex. This interpretation achieved wide acceptance, and can be found in textbooks well into the mid-1950's (e.g., Strong & Elwyn, 1953). Contrary to Winkler's findings were those of Kreidl (1914). Kreidl's experiments were important for two reasons, they were the first experimental demonstration of a functional ipsilateral auditory system and they were the only clear cut demonstration of the ipsilateral auditory system for 30 years, enduring into the mid-1940's as the only accepted evidence for the "possible" existence of ipsilateral pathways (e.g., Ranson & Clark, 1947). Unfortunately, reference to Kreidl's contribution to our knowledge of the auditory system disappeared after the late-1940's (e.g., Ranson & Clark, 1947). For historical reasons, and for the fact that they still remain a very convincing example of a functioning ipsilateral auditory system, Kreidl's experiments will be outlined in some detail. Prior to publication of Winkler's (1911) results, Kreidl had been involved in experiments on auditory cortex and medullary respiratory centers. During his respiratory research, he had divided the dorsal medulla mid-sagittally in two animals (dogs) and found it convenient to simultaneously test the hearing capacity of these animals. The animals survived 3 and 7 weeks respectively, and "in the time between surgery and death they reacted to being called by name and showed no difference in heating ability from normal control animals." The brainstem of these animals, subjected to Marchi staining, revealed that the medulla had been divided at the midline to about 1/3 of its normal thickness and that the dorsal striae were degenerated, while the trapezoid body was undamaged. Noting the difference between his casual observations and those of Winkler (1911), and being of the opinion that the dorsal

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pathways were not the important pathways for audition, he undertook a more systematic investigation of the secondary auditory pathways. From a dorsal exposure, mid-sagittal sections of the medulla were made in six more dogs. One dog again received a cut that only sectioned the dorsal striae, leaving the trapezoid body intact. One received a section that left the caudal-most fibers of the trapezoid body intact while severing the middle and rostral trapezoid body and the entire dorsal striae. The remaining four dogs had the dorsal striae and trapezoid body completely transected. In each case, the animals "hearing hardly differs from a normal hearing dog", e.g., "reacts to sounds, barks when hears other dogs barking, wags tail and approaches when called by name, when lying down raises head when called by name." Clearly, these forms of observational evaluations are subjective at best and are far from being well controlled auditory tasks. Indeed no description of the testing situation is given. Yet these results are hard to dismiss even on the grounds of being uncontrolled observations. Moreover, their credibility is enhanced by the results from an additional experiment. In this case, following a 14 day post-operative survival period, a dog demonstrated "hearing" reactions similar to those described above. In addition, this dog was tested in a Pavlovian' type experiment. Here, when put in a room, a knock on the door from the outside would initiate barking in this animal. Thus a crude unconditioned stimulus, the knock, would elicit an unconditioned response, barking. Histological examination of this animals brainstem revealed that it had received the most extensive longitudinal cut of all the animals. The cut not only completely severed the dorsal striae and trapezoid body, but also a large part of the commissure of Probst. Thus, despite complete transection of the secondary auditory pathways that cross the midline, these animals were not rendered deaf or unresponsive to sounds. Since the anatomical pathways are essentially identical in dogs and cats, Kreidl attributes the discrepancy between his results and Winkler's as being due to post-surgical trauma. Winkler's cats survived only 5 and 8 days, whereas Kreidl found that it required 5-8 days of post-operative recovery before he could elicit clear reactions to sound, suggesting that if the cats had survived longer they could have been shown capable of hearing. During the initial post-operative recovery period there was no reaction to sound, but hearing returned over time. This observation gives further credence to Kreidl's results.

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Kreidl also completely transected both the dorsal striae and the trapezoid body in one Rhesus monkey. Again, in this animal hearing returned after approximately one week. In conclusion, Kreidl states: "One can cut the entire dorsal and ventral paths at the midline and find no difference from normal animals. The anatomy agrees that there are secondary crossed and uncrossed paths...behavior shows the uncrossed paths are important for heating. Under normal conditions crossed and uncrossed paths are used for transmitting hearing impulses. But in what way these pathways differ needs more experimentation." Even though these conclusions predict the course of over 80 years of auditory research, Kreidl's contributions have unfortunately been overlooked. The question of the relative importance of the ipsilateral (uncrossed) pathways versus the contralateral (crossed) pathways was re-examined with more quantitative methods by Brogden et al., (1936). The rationale for the experiment was as follows. Information derived from each cochlea eventually courses through the central pathways to be distributed to the MG of both sides, and from there to auditory cortex. Thus, information from the left cochlea will reach both the left and right auditory cortex. Employing a conditioned response paradigm, absolute auditory thresholds were obtained from cats at three test frequencies of 125, 1000, and 8000 Hz. The experimental procedure (outlined in Figure 5), consisted of systematic destruction of either the cochlea or auditory cortex to isolate the crossed or uncrossed pathways. Thus the degree of hearing loss, resulting from interruption of various components of the auditory system, could be determined. Destruction of one cochlea produced an average hearing loss of 3-4 dB at each test frequency, destruction of both cochleas producing total deafness (e.g., no response to tones 125 dB above pre-operative threshold). Unilateral ablation of cortex resulted in a threshold increase of 3-5 dB (or 3-5 dB hearing loss), similar to unilateral cochlea destruction. To ascertain the relative contribution of the crossed vs. uncrossed pathways, unilateral cortex ablation was combined with either ipsilateral or contralateral cochlear destruction. Contralateral cochlear destruction (eliminating uncrossed pathways) increased thresholds an average of 15 dB, and ipsilateral cochlear destruction (eliminating crossed pathways) increased thresholds an average of 13-14 dB. It was concluded that, at least for absolute thresholds, the ipsilateral pathways were functionally equivalent to contralateral pathways. Similar results were obtained for dogs (Mettler et al., 1934).

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AC Ablation

,

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A Threshold 3-4dB

MG 1+2

IC

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2+3

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Figure 5. Summary diagram of the experimental paradigm employed by Brogden et al., (1936) to demonstrate the functional equivalence of ipsilateral and contralateral pathways to auditory cortex (AC). Absolute auditory thresholds were obtained before and after selective ablation of auditory structures. Note that following ablation 1+3 hearing was dependent upon an ipsilateral pathway, while after ablation 2+3 hearing was dependent upon a contralateral pathway. In either case hearing loss, as measured by change in absolute threshold (A threshold), was minor and essentially equivalent for the two pathways. Coch, cochlea; IC, inferior colliculus; MG, medial geniculate body.

A more intensive investigation, again using a conditioned response paradigm to test absolute intensity thresholds was conducted by Kryter and Ades (1943). Absolute thresholds were obtained for cats at test frequencies of 125, 1000, and 8000 Hz. By pairing a unilateral lateral lemniscus section with destruction of the cochlea on the same side, a single ipsilateral pathway could effectively be isolated, and in this case thresholds remained within normal limits. Isolation of a single contralateral pathway by pairing a lateral lemniscus section with destruction of the contralateral cochlea produced a slight hearing loss on the order of 11 dB. Interestingly, this loss was much greater for low frequencies than for high frequencies (e.g., 125 Hz, 18.7 dB; 1000 Hz, 10 dB; 8000 Hz, 5.6 dB). This experiment shows the conditioned

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response to be resilient to any manipulation that reduces the auditory pathway to only its ipsilateral or contralateral components. Bilateral destruction of the cochleas resulted in a permanent loss of the conditioned response. Similarly, Dixon (1973) also isolated a single ipsilateral or contralateral pathway by combined lateral lemniscus section and cochlear destruction, and measured absolute pure-tone thresholds for 250, 1000, 4000, 16000, and 32000 Hz. Again the ipsilateral pathway was equally sensitive as the contralateral pathway. Neither manipulation resulted in significant changes in pure-tone thresholds, although bilateral section of the lateral lemniscus did cause an increase in threshold of 80 dB or more. Masterton et al. (1992) repeated these experiments (unilateral cochlear destruction combined with ipsilateral or contralateral lateral lemniscus section) using a conditioned avoidance procedure and a battery of 26 auditory detection tasks. Again, in no case was heating or the conditioned response abolished for any task, regardless of whether the ascending system was reduced to a single ipsilateral or a single contralateral pathway. Although the results suggest that on 24 of the 26 tasks, the ipsilateral pathway makes no unique contribution to the ascending auditory system, the results do suggest that the ipsilateral pathway has an advantage over the contralateral pathway for detection of low frequency tones (below 4000 Hz) where thresholds remain near normal, and also for detection of a low frequency amplitude modulated tone (500 Hz). When only a contralateral pathway remained the average hearing loss, across all frequencies tested, was 18 dB. When only an ipsilateral pathway remained, the loss in sensitivity for frequencies above 4000 Hz averaged 17 dB. Surprisingly similar results have been reported for humans after surgical transection of one lateral lemniscus (e.g., Walker, 1942; Drake & McKenzie, 1953). A udiograms from these patients show a diminished ability to detect high frequency tones delivered to the contralateral ear, i.e., to the intact ipsilateral pathway. Even at the level of auditory cortex, unilateral ablation results in a significantly elevated threshold for detecting high frequency tones in the ear contralateral to the ablation, that is, the ear ipsilateral to the undamaged cortex (Heffner & Heffner, 1989). Thus there is relatively good agreement across studies that the ipsilateral pathway has a lower threshold for detecting low frequency tones, while deficient for detection of high frequency tones.

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Changing the behavioral task from absolute threshold detection to active conditioned avoidance of an auditory stimulus, cats can still maintain avoidance behavior with a single, isolated ipsilateral pathway (Jane et al., 1965). For example, in one case despite total transection of the medullary decussations (DAS, IAS, trapezoid body, contralateral projections from LSO) and the commissure of Probst, plus interruption of one lateral lemniscus and partial transection of the commissure of the inferior colliculus, this animal did not lose the learned avoidance response. Further, this manipulation also caused no detectable decrement in threshold to a 300 Hz tone. This one example shows that a single functional ipsilateral pathway can maintain not only normal thresholds, but also avoidance behavior. The behavioral studies reviewed above essentially dealt with the question of whether or not can you hear with your ipsilateral pathways. The answer is obviously you can. Further, it can be stated that not only can ipsilateral pathways maintain hearing, but also conditioned responses to auditory stimuli, conditioned avoidance to auditory stimuli, and intensity thresholds. Given that the ipsilateral pathway can maintain these fundamental aspects of audition, the question now arises as to whether it is capable of supporting more demanding auditory tasks. In other words, is there anything that the ipsilateral pathways can n o t do? Investigations e x a m i n i n g the contributions of the auditory commissures to sound localization discovered that ipsilateral pathways alone can not sustain an animals ability to localize sounds in space (e.g., Moore et al, 1974; Casseday & Neff, 197:5). While transection of the corpus callosum or the commissure of the inferior colliculus have no effect on sound localization (Moore et al, 1974), section of the medullary decussations (dorsal striae, trapezoid body, decussating fibers from the LSO) produces a profound deficit in sound localization (Moore et al, 1974; Casseday & Neff, 1975). Furthermore, transection of the medullary decussations not only destroys the pre-operative localization habit, but also renders these animals unable to re-acquire the habit despite massive training. Nonetheless, these animals displayed normal intensity thresholds (at 250, 1000, and 8000 Hz) and were capable of learning auditory pattern discriminations (Casseday & Neff, 1975). Thus ipsilateral pathways alone are sufficient to sustain a great many auditory functions, but sound localization is not one of them. Accepting this conclusion, one would reasonably suspect that sound localization is a function that relies upon the contralateral pathways.

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Turning to the sound localization literature to verify this suspicion leads to quite a different conclusion. This is a difficult question to answer directly, owing to the paucity of investigations specifically addressing this question (e.g., Neff & Casseday, 1977). However, many points concerning the role of contralateral pathways may be abstracted from the sound localization literature. To begin, subtotal transection of the medullary decussations (i.e., experiments severing only the trapezoid body or that destroy the region of the superior olivary complex) which leave the dorsal decussations intact (dorsal striae) produce deficits in sound localization equal in magnitude to total transection of all the medullary decussations. Therefore the contralateral pathways via the DAS and IAS apparently can not maintain sound localization behaviors, even in the presence of intact ipsilateral pathways (Masterton et al, 1967; Moore et al, 1974; Casseday & Neff, 1975). Thus, by elimination this leaves only the pathways originating in the VCN (which decussate in the trapezoid body) as the source of information usable for sound localization. Fibers emanating from VCN cross the midline to innervate the contralateral superior olivary complex, or continue on to enter the lateral lemniscus and terminate in the contralateral IC. Behavioral experiments manipulating this pathway demonstrate that these fibers, while necessary for accurate sound localization are not sufficient in and of themselves. Evidence for this conclusion results from unilateral ablations at various levels of the auditory system. Recall that once past the medulla (i.e. at the level of the lateral lemniscus) the central auditory pathways are essentially ipsilateral (lateral lemniscus to IC to MG to auditory cortex), though composed of fiber tracts transmitting information derived from bilateral, and therefore binaural, sources. Unilateral ablation of auditory structures anywhere from the lateral lemniscus to auditory cortex result in localization deficits confined to the contralateral auditory hemifield (Penfield & Evans, 1934; Wortis & Pfeffer, 1948; Sanchez-Longo & Forster, 1958; Strominger, 1969; Strominger & Oesterreich, 1970; Neff et al, 1975; Masterton et al, 1981; Jenkins & Masterton, 1982; Jenkins & Merzenich, 1984; Kavanagh & Kelly, 1987; Heffner et al., 1992; Poirier et al., 1994). In contrast, ablation of the auditory system anywhere from cochlea to superior olivary complex results in localization deficits within the ipsilateral auditory hemifield, or deficits in both the ipsilateral and contralateral hemifields (Masterton et al, 1967; Casseday & Neff, 1975;

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Casseday & Smoak, 1981; Jenkins & Masterton, 1982; Kavanagh & Kelly, 1992). Specifically, destruction of the ventral cochlear nucleus results in localization deficits ipsilateral to the side of the lesion (e.g., Casseday & Smoak, 1981) while ablation of the superior olivary complex results in predominantly bilateral localization deficits (e.g., Jenkins & Masterton, 1982; Kavanagh & Kelly, 1992). On the basis of these and other studies it is apparent that VCN fibers crossing the midline are necessary, but not sufficient for sound localization. Also implicated as vital for sound localization are the nuclei of the superior olivary complex, the point where fibers from both the ipsilateral and contralateral VCN first converge (Masterton et al., 1981; Jenkins & Masterton, 1982; Phillips & Brugge, 1985). Indeed, subtotal transection of the trapezoid body sparing the anterodorsal region (the area through which VCN fibers course to reach the contralateral MSO; Wart, 1966, 1982) results in sound localization deficits that are less severe or non-existent in comparison to total trapezoid body section (Casseday & Neff, 1975). From this it can be concluded that although the contralateral pathways coursing through the trapezoid body are of comparatively greater value than the ipsilateral pathways in terms of sound localization, ipsilateral pathways most certainly participate in sound localization. That accurate localization of sounds in space requires both ears is a recognized tenet of audiology (e.g., Rosenzweig, 1961; Phillips & Brugge, 1985). Interaction of information derived from the two ears can occur at many places along the central auditory pathway from cochlear nucleus to auditory cortex. The studies previously cited demonstrate the importance of the trapezoid body as a commissure interconnecting the ipsilateral with the contralateral pathways. Ablation of other potential sites of commissural interconnections, i.e., commissure of the inferior colliculus, or the corpus callosum, have no measurable effect on sound localization (Neff & Diamond, 1958; Moore et al, 1974), however, isolated transection of the commissure of Probst in rats does result in reduced localization acuity near the midline (Ito et al., 1995). Thus, the primary points of convergence between the ipsilateral and contralateral systems occur from the level of the superior olivary complex through the inferior colliculus. Ascending beyond the inferior colliculus, there is no evidence for binaural convergence taking place in any other structure (e.g., Phillips & Brugge, 1985).

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The results from the behavioral investigations of sound localization, taken together show that: (1) midline sections that reduce fibers ascending in the lateral lemniscus to only ipsilateral pathways or ipsilateral pathways plus the dorsal striae, can not support sound localization; (2) destruction of one lateral lemniscus, leaving the other lateral lemniscus intact (with its complement of ipsilateral and contralateral pathway fibers), can maintain sound localization at least in the hemifield opposite the intact lateral lemniscus; (3) unilateral ablation of structures above the lateral lemniscus results in the same syndrome; and (4) on the basis of anatomy and physiology the IC is the last point where clearly separable ipsilateral and contralateral pathways interact. III. Evoked Potential Studies

Another line of inquiry that is useful in supporting the functional importance of the ipsilateral pathways comes from evoked potential studies. Early evoked potential studies demonstrated that fibers coursing through the lateral lemniscus were responsive to stimulation of either the ipsilateral or the contralateral ear (Davis & Saul, 1931, Saul & Davis, 1932). Subsequent investigations used the evoked potential method to trace functional auditory pathways through the brain by an "ablationevoked potential" paradigm (e.g., Ades, 1944; Ades & Brookhart, 1950; Jungert, 1958; Fullerton & Kiang, 1990; Kelly & Li, 1997). Two experiments performed by Ades and Brookhart (1950) are of particular interest in terms of verifying the anatomical and behavioral results. In the first experiment electrodes were placed over both the right and the left auditory cortex of cats, and potentials recorded in response to click stimulation. Then the left auditory nerve was severed, without obvious effect to either cortical evoked potential. A second cut transecting the commissure of the inferior colliculus also had little or no effect on either cortical evoked potential. Finally, section of the decussating fibers in the medulla (dorsal striae, trapezoid body, decussating fibers of LSO) totally eliminated the left cortical evoked potential, while the right cortical evoked potential was only reduced in amplitude. In this experiment after transecting the left auditory nerve, the commissure of the inferior colliculus, and the medullary decussations, only the ipsilateral pathways from the right cochlear nucleus to right auditory cortex remained and they were capable of eliciting a strong cortical evoked potential.

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The second experiment was similar to the one just described except that the recording electrodes were placed on the two inferior colliculi. Section of the left auditory nerve and commissure of the inferior colliculus produced only minor changes in the evoked potentials, whereas medullary transection eliminated the left evoked potential, and again only reduced the amplitude of the right evoked potential. Thus ipsilateral pathways alone can elicit a strong collicular evoked potential. Other auditory evoked potential investigations demonstrated the ipsilateral and contralateral pathways to be of approximately equal value, and that binaural interactions occur at the superior olivary complex, the nuclei of the lateral lemniscus, and the IC (Ades, 1944; Rosenzweig & Amon, 1955; Rosenzweig & Sutton, 1958; Galambos et al., 1959; Kelly & Li, 1997). Further, transection of the commissure of the inferior colliculus does not eliminate or in any way interfere with the interactions (Rosenzweig & Wyers, 1955). From all the lines of evidence discussed thus far, there is certainly abundant grounds for accepting not only the existence of ipsilateral pathways but also their functional significance. Ablation-behavior experiments indicate that ipsilateral and contralateral pathways can operate alone, although they normally interact with one another. This interaction appears to be necessary for accurate localization of sounds in space. The following section of this paper will explore some of the of the physiological properties of the ipsilateral (and contralateral) pathways at the last place where they can be separately distinguished, the IC. IV. Role of Ascending Pathways in the Physiology of the IC Before drawing conclusions as to the nature of the ipsilateral pathways, this section will discuss the physiological influence of the ascending pathways on neurons of the IC. The IC is not only a major relay center for the ascending auditory system but it is also the last opportunity for direct binaural interactions to occur (Ferrier & Turner, 1898; Semple & Aitkin, 1981; Aitkin & Phillips, 1984a; Phillips & Brugge, 1985; Hutson et al, 1991). The IC integrates acoustic information arising from the cochlear nucleus, superior olivary complex, and nuclei of the lateral lemniscus. Although the IC receives pre-processed binaural information from the superior olivary complex and DLL, there is clear anatomical, electrophysiological, and behavioral evidence indicating further binaural processing at the IC (Chan & Y in, 1984;

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Kuwada et al., 1984; Phillips & Brugge, 1985; Carney & Yin, 1989; Yin & Chart, 1990; Batra et al., 1993; Covey et al., 1996). Since the basic physiological responses have been addressed in a previous section, the aim here will be to focus on synaptic mechanisms and synaptic relationships among the ipsilateral and contralateral inputs to IC neurons. Briefly, it will be recalled that IC neuronal responses may be typed as EE, IE, and OE based on their binaural response properties, which reflects their laterality preference from afferent inputs (e.g., Semple & Aitkin, 1979). Additional descriptive terms for IC unit discharge characteristics include "onset" or phasic and "sustained" or tonic (e.g., Erulkar, 1959; Rose et al., 1963, 1966; Hind et al., 1963; Kuwada et al., 1984). Units displaying an onset response show spike activity at the initiation of the stimulus with no further response, while sustained type units respond throughout the stimulus presentation. Onset type neurons predominate over sustained response units, and have been described as the result of intricate excitatory-inhibitory events (Hind et al., 1963). Onset type responses are of particular interest since they are found in greater numbers at the IC and higher levels, while at lower levels, e.g., cochlear nucleus or superior olivary complex, sustained responses predominate (e.g., Rose et al., 1963). The remainder of this section will be devoted to the examination of the excitatory-inhibitory interplay at the IC. Inhibition of IC Neurons. Intracellular recordings from IC neurons by Nelson and Erulkar (1963) demonstrated that acoustic stimulation could elicit depolarization, hyperpolarization, or both in combination. Furthermore, these experiments revealed the probable synaptic mechanisms underlying the onset type of response. Many IC neurons respond to auditory stimulation with an initial depolarizing excitatory potential eliciting spike discharges which are followed by a powerful inhibitory input cessating the discharge. Additional experiments were undertaken to examine the properties of the inhibitory inputs by current injection through the recording electrode in the presence or absence of acoustic stimuli. The results suggest that active inhibition may come about by two synaptic mechanisms. The most convincing evidence is for post-synaptic inhibition, arising either directly from the ascending pathways or perhaps mediated by local inhibitory interneurons. The other form of observed inhibition appeared to act by a reduction of background excitation (i.e., reduced excitatory post-synaptic potentials), evidence suggestive of the involvement of pre-synaptic mechanisms.

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Ultrastructural evidence from normal material supports the interpretation of post-synaptic mechanisms. Electron microscopic studies have demonstrated the presence, in significant numbers, of terminal boutons containing flattened vesicles apposed to IC neurons, indicative of inhibitory synapses (Rockel & Jones, 1973b). Unfortunately, these authors could not determine the origin of these boutons, but suggested the possibility that they could arise intrinsically from multipolar cells. Although not specifically discussed, this same electron microscopic study also yields some ultrastructural evidence for considering the presence of pre-synaptic inhibition. Examining the photomicrographs, one is struck by the abundance of terminals apposed to IC cell bodies and dendrites. In many instances astrocytic "fingers" can be seen separating the boutons, but in many other cases no such "fingers" are visible, in addition there appears to be thickening of the terminal membranes when they are in close proximity. Furthermore, apparent "stacking" of terminals can be seen, all of which are suggestive of, but certainly not proof of pre-synaptic interactions or synaptic modulation. Neurochemical and pharmacological studies have also addressed the question of inhibitory processes occurring at the level of the IC, again evidence obtained by these methods indicate that both pre- and postsynaptic inhibitory mechanisms are characteristic of inputs to the IC. Of the long list of putative neurotransmitter substances, GABA (gammaaminobutyric acid) and glycine are considered to be the best candidates as inhibitory neurotransmitters (e.g., Curtis, 1968; Johnston, 1976; McGeer & McGeer, 1981; Fagg & Foster, 1983; Davidoff & Hackman, 1985). Moreover, GABA has been associated with inhibitory mechanisms presumably pre-synaptic in nature, while glycine has been considered as the best candidate for post-synaptic mechanisms (e.g., McGeer & McGeer, 1981; Moore & Caspary, 1983; Davidoff & Hackman, 1985; Caspary et al., 1985; Bormann, 1988; Gage, 1992). Microinjection or iontophoretic application of these compounds or their antagonists have potent inhibitory or disinhibitory actions respectively on IC neurons (Watanabe & Simada, 1971, 1973; Faingold et al., 1989a, 1991). Both GABA and glycine depress spontaneous activity and stimulus-induced responses (Watanabe & Simada, 1973; Faingold et al., 1991). Furthermore, receptor binding studies have demonstrated that the auditory system is characterized by high levels of inhibition. The evidence here is based on the relative abundance of sites marked by various ligands used to probe for inhibitory neurotransmitter receptors

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(e.g., Baker et al., 1986; Glendenning & Baker, 1988; Glendenning et al., 1991, 1992) Considerable evidence supporting GABA as an inhibitory neurotransmitter at the IC has accumulated from pharmacological and neurochemical studies. When GABA is exogenously applied to IC neurons the inhibition produced is rapid in onset and rapid in offset. Benzodiazapine, which acts at GABA receptor sites, and nipecotic acid, a GABA reuptake inhibitor, both inhibit IC neuronal discharge and augment the action of GABA applied simultaneously. Bicuculline, a GABA antagonist, blocks inhibitory effects of exogenously applied GABA and blocks binaural inhibition at the IC. Baclofen, a possible GABA agonist, inhibits IC neuronal firing but its temporal action does not follow the same time course as GABA (Watanabe & Simada, 1973; Johnston, 1976; McGeer & McGeer, 1981; Faingold et al., 1989a, 1991; Klug et al., 1995). Experiments using the GABA antagonist picrotoxin as an inhibitory probe show that the phasic onset-type response of IC neurons to an acoustic stimulus can be converted to a tonic sustained-type discharge by application of picrotoxin. The abolition of synaptic inhibition by picrotoxin is most pronounced during the initial period of stimulation, lasting 40-80 msec. In contrast, picrotoxin had very minor effects on tonic units of the IC only slightly increasing their number of discharges (Watanabe & Simada, 1971, 1973). (This effective disinhibition by picrotoxin further supports the belief of GABA as a pre-synaptic inhibitor, as picrotoxin reverses pre-synaptic inhibition of spinal motorneurons; Eccles et al., 1%3). Neurochemical observations show that there are high concentrations of glutamic acid decarboxylase (GAD), the enzyme responsible for GABA synthesis, within the IC. GABAergic terminals can be labeled in the IC by GAD-immunocytochemistry or by antibodies to GABA itself (Adams & Wenthold, 1979; Thompson et al., 1985; Moore & Moore, 1987; Roberts & Ribak, 1987; Hutson, 1988; Glendenning et al., 1992). Evidence of synaptic terminals in IC visualized by GABA antibodies show that these terminals are found predominately along dendrites, rarely contacting the cell soma (e.g., Oliver & Bekius, 1992). Furthermore, it has been observed that GABA terminals are slightly elevated from the neuron perikaryon, suggestive of pre-synaptic inhibition via axo-axonic synapse (e.g., Thompson et al., 1985). Taken together, there is structural evidence for GABA terminals contacting IC

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neurons directly (possible post-synaptic mechanism), and indirectly (possible pre-synaptic mechanism). Similar methods of investigation have been employed to assess the possibility of glycine as an inhibitory neurotransmitter in the IC, though these experiments have not been as extensive as the GABA studies. Exogenously applied glycine has a powerful inhibitory effect on phasic neurons of the IC, acting with rapid onset and offset (Watanabe & Simada, 1971, 1973; Faingold et al., 1989a). Strychnine sulfate, a glycine antagonist has no disinhibitory effects on the phasic onset-type IC neurons, though in many cases there was a temporal depression of spike discharge (Watanabe & Simada, 1971, 1973). However, other investigations aimed at evaluating the role of glycinergic inhibition of IC neurons found that strychnine can block binaural interactions, that is, disinhibit an IE neuron (Faingold et al., 1989a; Klug et al., 1995). Glycine receptors have been demonstrated autoradiographically in the IC (Baker et al., 1986; Glendenning & Baker, 1988; Glendenning et al., 1992), and electron microscopic studies show that monoclonal antibodies to glycine receptors are found apposed to synaptic terminals containing flattened vesicles (Wenthold et al., 1988), supporting the view that glycine acts as the neurotransmitter for post-synaptic inhibition. In summary, there appears to be reasonably good evidence for GABA and glycine acting as inhibitory neurotransmitters in the IC. Excitation of IC Neurons. Recordings from electrodes placed intracellularly or extracellularly show that neurons can be excited by acoustic stimuli presented to either the ipsilateral or the contralateral ear (e.g., Nelson & Erulkar, 1963; Aitkin et al., 1981). However, the neurotransmitter mechanisms for excitation at the IC are poorly understood. The best candidates for excitatory neurotransmitters are acetylcholine, glutamate, and aspartate. The evidence for any of these putative neurotransmitters acting at the IC is not overwhelming, although glutamate is currently the most likely candidate based on neurochemical and receptor binding studies (e.g., Glendenning et al., 1992). Unfortunately, in many instances the results of pharmacological studies contradict one another (e.g., Curtis & Koizumi, 1961; Watanabe & Simada, 1973; Farley et al., 1983, Faingold et al., 1989b). About the only conclusive statement that can be made is that excitation probably involves glutamate as the neurotransmitter (Glendenning et al., 1992), that glutamate is associated with terminals containing round synaptic vesicles (Helfert et al., 1992), and this type of terminal morphology has

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long been believed as excitatory in the auditory system (e.g., Rockel & Jones, 1973b; Oliver, 1984, 1985, 1987).

Role of the Ipsilateral Pathway At the present time the evidence from electrophysiological studies suggests that inhibition of IC neurons is the result of activation of ipsilateral pathways (e.g., Roth et al., 1978; Semple & Aitkin, 1979; Semple & Kitzes, 1985; Aitkin & Martin, 1987; Carney & Yin, 1989). While the electrophysiology does show that units in IC can be classified by their response to afferent inputs (e.g., IE or EE), these responses are either net excitatory or net inhibitory, yielding no direct information as to the exact source or pathways by which excitation or inhibition reach the IC. To date, most experiments combining electrophysiological recording and tract-tracing methods have focused on tonotopic or topographic projections to IC from sub-collicular levels having little to offer about excitatory or inhibitory routes of innervation (e.g., Roth et a1.,1978; Aitkin & Schuck, 1985). The relative strength of the ipsilateral inhibition is most striking in autoradiographs obtained by the 14C-2-deoxyglucose method. In these experiments, white noise was presented to one ear and a tone to the other ear. As expected the IC contralateral to the tone stimulus displayed a band of increased activity, while the IC ipsilateral to the tone showed a band of reduced activity against a background of white noise induced activity (Webster et al., 1984, 1985). These authors argue that the reduced band of activity present in the IC ipsilateral to the tone corresponds to an inhibitory contour band, though again no information can be extracted as to the inhibitory pathway other than it originates from the tone stimulated ear. These electrophysiological and 14C-2-deoxyglucose findings together support the prevalent view that the acoustic information arriving at the IC from the ipsilateral ear is predominantly inhibitory. Before proceeding to evaluate the potential sources of the ipsilateral inhibitory pathway, it should first be acknowledged that the ipsilateral pathways are also responsible for excitation of the IC. A brief examination of this excitatory component of the ipsilateral pathway is warranted here for two reasons, first it enables one to estimate the relative size of the ipsilateral excitatory vs. inhibitory pathways and second, by analysis of the probable sites of origin of the excitatory

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pathway, they can be eliminated confidently from consideration in the inhibitory pathway. The common finding among all electrophysiological investigations of IC neurons is that the majority of cells examined could be excited by stimulation of the contralateral ear, while only about 25% are excited by stimulation of the ipsilateral ear (e.g., Roth et al., 1978; Semple & Aitkin, 1979, 1981; Kuwada et al., 1984; Moore et al., 1984; Semple & Kitzes, 1985). Thus on the basis of excitatory inputs, the ipsilateral pathways are about one-fourth the magnitude of contralateral pathways. But, given the evidence that the ipsilateral pathways also contain an inhibitory component raises the relative magnitude of the overall ipsilateral projection. One can obtain a rough estimate of the magnitude of the ipsilateral inhibitory pathway by deduction from the electrophysiological studies. Of the population of inferior collicular neurons studied electrophysiologically, approximately 20% respond only to contralateral stimulation (OE cells; e.g., Semple & Aitkin, 1979), leaving 80% of the original population being influenced to some degree by the ipsilateral pathways. From this 80%, an additional 25% can be subtracted as being excitable by ipsilateral pathways. Thus, at least 55% of the neurons sampled are capable of being influenced by the ipsilateral pathway in a non-excitatory manner. Granted such a deduction leaves many details unconsidered, yet it does convey the impression that the ipsilateral pathway is characterized by an inhibitory component that is by no means insignificant. As the origin of all ascending auditory pathways, the cochlear nucleus would be the first structure to examine as the origin of the excitatory and inhibitory components of the ipsilateral pathway. It will be recalled that the cochlear nucleus (both DCN and V CN) project to the IC of both sides (e.g., Adams, 1979; Brunso-Bechtold et al., 1981; Nordeen et al., 1983; Oliver, 1985, 1987). Of particular interest here are the studies which utilized the anterograde transport of 3H-leucine from the cochlear nucleus to label terminals in the IC (e.g., Oliver, 1984, 1987). From these injections dense terminal labeling appears in both the ipsilateral and contralateral IC, contralateral being somewhat heavier. Nevertheless, examination of both IC's at the electron microscopic level reveals that all terminals labeled by anterograde transport contained small round synaptic vesicles, with morphology of the terminals in the ipsilateral IC being indistinguishable from those of the contralateral IC. Furthermore these terminals formed asymmetric synaptic contacts

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primarily upon dendrites of IC neurons. The sum of these observations lead one to believe that the cochlear nucleus provides excitatory synapses in both the ipsilateral and contralateral IC. Finally, it is probably safe to conclude that although there may be other sources of ipsilateral excitation in the IC, the cochlear nucleus is probably n o t a direct source of the inhibition seen in the ipsilateral IC. Having eliminated the cochlear nucleus as a direct source of inhibition to the ipsilateral IC, the next most logical consideration would be the possibility of inhibitory interneurons in the IC (Rockel & Jones, 1973b). For this to be a plausible mechanism, excitatory ipsilateral inputs would contact the interneurons which in turn would inhibit other IC neurons. However, the electrophysiological evidence does not tend to support this mechanism. As suggested by Semple and Kitzes (1985), ipsilaterally excited neurons are seen too infrequently to account for the amount of inhibition produced, yet they concede the possibility that electrodes could simply be failing to record from these interneurons. This seems unlikely due to the size of neurons found in the IC, on the order of 17-30/am cell body diameter in cats (Oliver & Morest, 1984). Given the observation that the cochlear nucleus probably does not give rise to inhibitory projections to the ipsilateral IC and that evidence in support of the inhibitory interneuron theory is not particularly convincing, the number of alternative sources of ipsilateral inhibitory input to IC would seem to be reduced to the superior olivary complex and the nuclei of the lateral lemniscus. Further, given the high probability that the inhibitory neurotransmitters operating at the IC are GABA and glycine, one might reasonably suspect two categories of ipsilateral inhibitory pathways. Namely, a GABAergic pathway and a glycinergic pathway. The notion that the superior olivary complex or the nuclei of the lateral lemniscus may be the source of ipsilateral inhibition to IC is not novel, each has previously been suspected to play such a role (e.g., Semple & Aitkin, 1980; Adams & Mugnaini, 1984; Semple & Kitzes, 1985). One additional piece of information makes this point more salient. The ipsilateral superior olivary complex should provide (on the basis of their discharge characteristics) massive excitatory inputs to the IC. Both LSO and MSO receive excitatory inputs from the ipsilateral cochlear nucleus and themselves respond with excitation. However, as stated previously the incidence of ipsilaterally excitable cells in the IC is low, but as noted by Semple and Kitzes (1985) a large ipsilaterally evoked field potential is seen. This

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observation was puzzling to them, since it is suggestive of a vigorous volley of activity which is reduced to "relative feebleness" at the IC. However, such an observation is exactly what one would expect for an inhibitory pathway. These superior olivary complex neurons would respond to ipsilateral stimulation with action potentials producing a wave of activity that would n o t be replicated at the IC, due to the release of inhibitory rather than excitatory neurotransmitter substance. The only flaw in this explanation is that the recordings were made in anesthetized preparations, which had very low rates of spontaneous activity, so they could not directly observe the strength (or mechanism) of inhibition (Semple & Kitzes, 1985; Kitzes & Semple, 1985). Fortunately, there is reasonably good neurochemical evidence to support many of the known ipsilateral projecting nuclei as falling into one or the other (GABA or glycine) neurochemical pathway. Evidence for a GABAergic pathway begins with the localization of GABA positive neurons within these suspect nuclei. Using GABA antibodies, labeled neurons were found in LSO, DLL, and VLL (Thompson et al., 1985; Hutson, 1988; Helfert et al., 1989; Hutson et al., 1991). Other studies using GAD as a probe found labeled cells in DLL, and few in the dorsal division of VLL, and in LSO (Adams & Mugnaini, 1984; Moore & Moore, 1987). All of these are strong candidates for being the neural substrate for an ascending GABAergic pathway, with the exception of LSO. Many GABA positive cells are reported in LSO of rodents (e.g., Helfert et al., 1989), but only a few in cats (e.g., Glen-denning et al., 1992); however none of the cells had the morphology of LSO principal cells that give rise to ascending projections. This species difference may reflect the role LSO plays in descending projections of the superior olivary complex to the cochlea. A portion of this descending pathway originates from cells within LSO of rodents (e.g., White & Warr, 1983), but not in carnivores or primates (e.g., Warr, 1975; Thompson & Thompson, 1986). Furthermore, it appears to be the GABA positive cells within the rodent LSO that give rise to this descending projection (Vetter et al., 1991; Ostapoff et al., 1997). This leaves nuclei of the lateral lemniscus as the major source of ascending GABAergic inputs to the IC. Although GABA positive cells are found in DLL, VLL (and ILL), DLL contains the highest concentration (Adams & Mugnaini, 1984; Hutson, 1988; Glendenning et al., 1992).

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Perhaps the most convincing evidence in support of the nuclei of the lateral lemniscus being the source of GABAergic projections to the IC is the retrograde transport of radioactively labeled GABA (3H-GABA). When 3H-GABA is injected into the IC, it is rapidly incorporated by axon terminals and transported back to their cells of origin. In cat, this method selectively marks very few cells in VLL and ILL and only on the side ipsilateral to the injection, while many cells are marked in DLL both ipsilateral and contralateral to the injection (Hutson, 1988; Glendenning et al., 1992). Within the medullary auditory nuclei, n o cells were labeled in the cochlear nucleus of either side, none in MTB, MSO, or LSO of either side, with only a meager number of peri-olivary cells marked on the same side as the injection (Hutson, 1988; Glendenning et al., 1992). Other evidence for DLL as the origin of a significant bilateral inhibitory projection to the IC has come from electron microscopic studies of DLL axon terminals, demonstrating these terminals to contain pleomorphic shaped vesicles (Shneiderman & Oliver, 1989), and terminals containing pleomorphic vesicles are associated with GABAergic synapses in the auditory system (Oliver and Bekius, 1992; Helfert et al., 1992). Furthermore, ablation of DLL reduces the amount of induced GABA release in the IC (Shneiderman et al., 1993). Thus from the nuclei of the lateral lemniscus, only DLL appears to be a significant source of an ascending GABAergic projection to the IC. Before leaving this discussion of sources of GABA inputs to the IC, one additional source must be considered, and that is the IC itself. Previously in this paper, the notion of inhibitory interneurons within the IC was dismissed for lack of evidence. However, an inhibitory interneuron does not have to conform to the classic Golgi type II classification (i.e., a small neuron whose axon does not leave its parent nucleus). A projection neuron, with recurrent axon collaterals could serve the same purpose. Evidence for this possibly occuring in the IC comes from the observation that the IC contains a large population GABA positive neurons (e.g., Moore & Moore, 1987; Hutson, 1988; Glendenning et al, 1992; Oliver et al., 1994). Furthermore, if 3H-GABA is injected into the MG, a vast number of IC neurons are vividly marked by retrograde transport (Hutson et al., 1993). Thus, the IC gives rise to a significant ascending inhibitory projection to the MG. In addition, these large projection neurons often give off extensive axon collaterals before leaving the IC en route to MG (Oliver et al., 1991). These studies

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demonstrate that the IC is capable of supplying its own source of inhibition, yet the arguments against the possibility of interneurons being responsible for ipsilateral inhibition still hold true, few IC neurons are excited by stimulation of the ipsilateral ear. As for an ascending glycinergic pathway providing inhibition at the IC, the evidence is somewhat more compelling. The observations in favor of a glycinergic pathway include the previously noted presence of glycine receptors in the IC, and these receptors are most likely apposed to terminals containing flattened vesicles (Wenthold et al., 1988). Although there are no glycine positive cells in IC as measured by antibodies directed against glycine, there are abundant glycine positive fibers and puncta within IC (e.g., Glendenning et al., 1992), and glycine immunoreactive puncta have been demonstrated to be axon terminals that typically contain flattened vesicles (Helfert et al., 1992). A second line of investigation is, however, a most powerful demonstration of a glycinergic pathway and is based upon the retrograde transport of 3Hglycine itself. When 3H-glycine is injected into the IC of a cat, retrogradely labeled neurons are found in the ipsilateral VLL and ipsilateral LSO (Hutson, 1986; Hutson, et al., 1987; Hutson, 1988; Glendenning et al., 1992). Beyond this, it is important to note that retrogradely labeled neurons were n o t seen in other nuclei that would also be marked by transport of a non-specific tract-tracing substance (e.g., horseradish peroxidase) from an IC injection, these include the contralateral IC, ipsilateral and contralateral DLL, the cochlear nucleus of both sides, the contralateral LSO, and in particular the ipsilateral MSO. Similar results have been reported using retrograde transport of 3H-glycine in chinchillas (Saint Marie & Baker, 1990). Thus the possibility of specific glycinergic pathways appears quite likely, and the same electrophysiological argument used above (based on Semple and Kitzes, 1985) for ascending inhibition at the IC would hold here, with glycine most likely participating in a post-synaptic inhibitory process. It is equally important to point out that not all neurons of LSO retrogradely transport 3H-glycine after its injection into IC. Those that do transport glycine appear to represent a subpopulation of LSO principal cells (the remaining principal cells are candidates for an excitatory projection to the contalateral IC, see below; Glendenning et al., 1992). Furthermore, even though many VLL neurons retrogradely transport glycine, and only on the same side as the injection, they can not account for the observed inhibition of IC neurons resulting from

426

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stimulation of the ipsilateral ear. Recall that VLL receives almost exclusive afferent innervation from the contralateral cochlear nucleus, and since VLL gives rise to an ascending glycinergic projection it would be expected to have an inhibitory influence on IC neurons, but only after stimulation of the contralateral ear. Nonetheless, the evidence is reasonably convincing that both GABA and glycine are important inhibitory neurotransmitters in the central auditory system, and both are major components of the ipsilateral auditory pathway. This is interesting in view of pharmacological and electrophysiological findings. Pharmacological studies show that picrotoxin disinhibits IC neurons for up to 80 msec (Watanabe & Simada, 1971), while electrophysiological records show IC units can be silenced for up to 120 msec following initial excitation (Erulkar, 1959). These two results have led to the suggestion that the phasic response of IC neurons may be shaped by both pre- and post-synaptic inhibitory events (Erulkar, 1975). Therefore, LSO and DLL appear to be equipped with the necessary connections and neurotransmitters to carry out both pre- and post-synaptic inhibition at the level of the IC subsequent to stimulation of the ipsilateral ear. The observation of LSO neurons containing an inhibitory neurotransmitter (glycine), and that glycine has potent effects at the level of the IC can explain some long perplexing electrophysiolgical observations. Since most IC neurons are excited by contralateral ear stimulation (e.g., Moore et al., 1984; Semple & Kitzes, 1985), and the medial portions of LSO project contralaterally (Glendenning & Masterton, 1983), it would not be surprising to find a subpopulation of LSO neurons located in the medial limb of LSO containing an excitatory neurotransmitter, and indeed there is such a population. Glendenning et al., (1992) demonstrated the contralaterally projecting cells of LSO contain glutamate, and thus are a source of excitation at the IC. Similarly, the lateral portions of LSO project ipsilaterally (Glendenning & Masterton, 1983)and neurons retrogradely labeled by 3H-glycine are found in the lateral portions of LSO (Hutson, 1986; Hutson et al., 1987; Glendenning et al., 1992). Many units in the IC display response types that are IE (ipsilateral inhibitory, contralateral excitatory) and appear to be remarkably similar in their response characteristics to the contralateral LSO (e.g., Roth et al., 1978; Semple & Aitkin, 1979). This can be explained simply by the axons of LSO cells, which are EI in character, crossing the midline and terminating in the contralateral IC at which point they would now be characterized as

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427

IE (Glendenning & Masterton, 1983). However, there is a paucity of IC neurons displaying El characteristics which would reflect inputs from the ipsilateral (El) LSO (e.g., Semple & Aitkin, 1979). This has been the perplexing observation, why are there no (or very few) IC units that are "ipsi LSO-like"? Previous explanations of this quandary have been to assume the 'EI'-ness of the ipsilateral LSO projections are lost or masked by convergence and integration of other afferent types, obscuring any ipsilateral LSO-like characteristics (e.g., Roth et al., 1978; Semple & Aitkin, 1979; Glendenning & Masterton, 1983). In light of the findings presented above, that the ipsilateral LSO projections are inhibitory, an alternative explanation could be put forth. Consider for the moment one IC, say the right IC, receiving inputs from ipsilateral and contralateral LSO. Each LSO receiving excitatory inputs from its ipsilateral cochlear nucleus and inhibitory inputs from it contralateral cochlear nucleus via MTB. The left LSO projecting (by its medial portions) to the right IC and having excitatory terminals on IC neurons (see Figure 6). In this figure, one can easily see how El properties of the left LSO would be transformed into IE properties at the right IC. Now attend to the situation as it occurs in the right LSO, still El in character, but projecting inhibitory terminals to the right IC. Here, stimulation of the right ear (ipsilateral) excites the right LSO, however the right LSO, due to the action of the neurotransmitter released by its terminals, does not excite the fight IC but rather inhibits it. On the other hand, stimulation of the left ear (contralateral) would inhibit the right LSO and by doing so would promote a "disinhibitory" effect at the fight IC and appear as net excitation. In this manner, the ipsilateral LSO, while E1 itself, would not project El properties to the IC. Rather, the effect would be more IE-like in nature, and there would be no reason to expect EI or ipsilateral LSO-like unit response properties in the IC. In fact, by overlapping with OE and EE inputs (e.g., Semple & Aitkin, 1979) the ipsilateral LSO inputs would be enhanced further to appear as IE. For example, contralateral ear stimulation would excite an area of overlap by OE or EE cells, which would be potentiated by the withdrawal of inhibition by the ipsilateral LSO (i.e., contralateral stimulation would inhibit the inhibitory ipsilateral LSO projection thus promoting "disinhibition"). Likewise, stimulation of the ipsilateral ear would provide inhibition to the area of overlap.

428

Hutson

Response at right IC

Ear stimulated contra

ipsi o o

E O

~V - I

=E

-I

=E

= increased

firing

IC

o 0 O3 ~-, C G)


RH LH>RH ns. ns.

LH>RH LH>RH ns. LH>RH ns.

1990; Verjat, 1988) on both normal subjects (Hatta, 1978; Cohen & Levy, 1986, 1988; Dodds, 1978; Flanery & Bailing, 1979; Riege, Metter & Williams, 1980; Streitfeld, 1985), and brain damaged patients (e.g., Milner & Taylor, 1972; Nebes, 1971). It should be noted, however, that this effect has not always been obtained (e. g., Y amamoto & Hatta, 1980; Webster & Thurber, 1978), while a very limited number of studies (e.g., Cranney & Ashton, 1982; Yandell & Elias, 1983) showed a rightinstead of left-hand superiority for meaningless shape recognition. Our studies also revealed that lateralization may emerge during the initial learning phase, but may disappear during the recognition phase. For instance, whatever the experiment, the left hand was found to touch a greater surface of the stimulus than the right, but this effect was present during the learning phase only (see Table 1). Because the same stimulus set was used for learning and recognition, this phase difference cannot be accounted for by physical characteristics of the input. It could rather be attributed to cognitive factors, such as the knowledge of the shape which provided a frame in the search for form features. In a different perspective, some authors have suggested that monohaptic situations are inadequate to reveal manual perceptive asymmetries

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and proposed, instead, to use dichhaptic tasks (e.g., Witelson, 1974). Results reported in Table 1 are in agreement with this position, because score asymmetries were observed in dichhaptic testing conditions only. The question remains, however, to understand why the dichhaptic task is more appropriate for unveiling asymmetries. In an attempt to address this question, Witelson (1974) argued that the dichhaptic task produces a competition in the neural system for the required cognitive processing in the two hemispheres. According to Witelson (1974), this competition gives a leading role to the specialized hemisphere which will thus control haptic information processing. We conducted an experiment which addressed this hypothesis in an indirect way. This study (Fagot, Hopkins & Vauclair, 1993) used the apparatus depicted in Figure 1, and subjects were requested to touch two objects simultaneously, and then to recognize one of them on a visual array. In the analysis, we wanted to verify if the two hands would work in synchrony during the dichhaptic exploration. For that purpose, we distinguished two types of exploration strategies. The first one involved a simultaneous displacement of both hands on the shape. The second one involved contacts of both hands with the shape, but one hand at least was not moving for a minimum of 500 ms. The percentage of time spent with both hands active is represented in Figure 2. On average for the group, 20 percent of the exploration time only was devoted to a simultaneous exploration of the two objects. During the other 80 percent, one hand only was active at a time, and the other one remained in a fixed position, with an intermittent alternation in the function of each hand. A similar division of labor between the two hands was observed in blind people reading Braille (Millar, 1987). If the dichhaptic procedure involved so few simultaneous explorations, why did it reveal asymmetries that the monohaptic procedure was unable to elicit? Rather than referring to a process of inter-hemispheric competition (i.e., Witelson, 1974), we propose that dichhaptic exploration introduces more cognitive constraints than the monohaptic exploration, for instance in terms of attention sharing and memory load, which is favorable for lateralization effects to emerge. It is also likely that the instruction to simultaneously explore the two objects made the linguistic encoding difficult, thus enhancing the spatial component of the task. In brief, it occurs that lateralization exists for tactual form discrimination, but that the left hand bias emerging from somato-spatial

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100

80

60

40

20

1

2

3

4

5

6

7

8

9

1 0 11

12

13

14

Figure 2: Percentage of exploration time spent using bimanual versus unimanual strategy (solid: bimanual search; stippled: unimanual search).

tasks may be masked, or may even be reversed, under the influence of several possible factors. Among these factors are the complexity of the form (e.g., Franco & Sperry, 1977), the subjects' previous knowledge or expectancies (Fagot et al., 1994), the instruction to process haptic information in a given way (Webster & Thurber, 1978) and the need to process several forms in parallel (see Table 1). Of particular importance, the reference to verbal codes for form processing may cancel asymmetries in favor of the left hand, and may even induce a bias in the opposite direction (e.g., Cioffi & Kandel, 1979). In this context, it is relevant to verify if the closest relatives of humans (monkeys and apes) share the same lateralization patterns as humans, as nonhuman primates have no human-like language p e r s e (Vauclair, 1996).

Haptic Perception in nonhuman primates Very few studies investigated lateralization in somatosensory discrimination tasks with nonhuman primates, and most of them focused

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on the existence of a preference for either hand rather than on asymmetries in performance. Consequently, this approach limits the possibility to strictly compare human and nonhuman primates, because the available human literature bears on performance measures. Nevertheless, experimental evidence suggest that nonhuman primates exhibit a left hand preference for haptic tasks, even though the neural mechanisms underlying this asymmetry remain unknown (Garcha, Ettlinger, MacCabe, 1982). As a first support for this hypothesis, a series of experiments showed in macaques a trend (though not significant) for preferring the left-hand in haptic form discrimination (Ettlinger, 1961; Ettlinger & Moffet, 1964; Milner, 1969; Brown & Ettlinger, 1983). In these studies, however, the sample size was small and left/right differences were not significant. In a larger group, Hoerster and Ettlinger (1985) showed that 77 rhesus who predominantly used their left hand learned haptic discrimination faster than did 78 monkeys who preferred their right hand. Other evidence for group asymmetry in haptic tasks derives from Fagot, Dr6a and Wallen (1991) whose findings on rhesus macaques were later replicated in cebus monkeys by Parr, Hopkins & de Waal (in press) and Lacreuse & Fragaszy (1996). In this study, rhesus monkeys had to climb a wire netting and to maintain a vertical three point posture while they introduced one hand in an opaque box in order to discriminate peanuts mixed with sand and stones of different sizes. There was for the group (n=29) a significant left hand preference for haptic search. A similar left bias occurred for haptic reach in a sitting position, showing that the posture was not critical for the emergence of the left hand preference. When a visual version of this task was proposed, the left hand bias again emerged, but the frequency of left hand usage was significantly lower than in the tactile version (Fagot et al., 1991). To our knowledge, one study only (Lacreuse & Fragaszy, in press) addressed the relation between performance and preference for haptic task in monkeys. This study showed a left hand preference for obtaining out of view food items fixed on the side surface of three dimensional objects, but detailed analyses of hand movements during haptic exploration failed to reveal hand asymmetries in search strategies. In short, findings resulting from nonhuman primate studies are consistent with the human picture, in that asymmetries for haptic perception are generally in favor of the left hand. The problem, however, is that this left bias in monkeys was inferred from measures

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different from those employed in human studies. The existence of a left hand bias in monkeys suggests that the previously reported human left hand right-hemisphere advantage has a long phylogenetic history, and certainly predates cerebral lateralization for linguistic processing. General discussion

The general picture that emerges from this overview of the literature is presented in a condensed way in Table 2. This table reports, for each task, the presence or absence of hand biases as inferred from the literature and provides additional general comments on these effects. Elementary discrimination tasks are presented in the upper part of Table 2 and complex discrimination tasks are listed in the lower part. When the effects are very consistent in the literature, Table 2 refers to a "hand bias". The wording "hand tendency" is used in Table 2 when effects were repeatedly reported, but several studies failed to replicate them. A quick look at Table 2 indicates a general tendency for a left hand (right hemisphere) advantage for somato-sensory discriminations. With the possible exception of the pressure and vibration sensitivity tasks, it must be remarked that tasks used in the assessment of haptic lateralization have in general a high spatial load. Hence, it is not unreasonable to propose that the left-hand biases reported in Table 2 reflect a fight hemisphere advantage for spatial processing. As the fight hemisphere advantage was also observed for visuo-spatial tasks (e.g., Hellige, 1993), this advantage might not be tied to the tactual modality, but might reflect a supramodal ability to process spatial information. The tasks listed in Table 2 have sensory as well as post-sensory components, since subjects had to feel the stimuli and to report what they felt. Also, given the varying complexity of the tactile input, these tasks differ in terms of cognitive load. Thus, it is likely that comparing the findings on the basis of the demands of the task will shed light on the respective role of sensory and post-sensory factors on brain lateralization. Regarding the possible role of early factors, Table 2 suggests that a distinction must be made between kinesthetic and cutaneous inputs. For kinesthesis, asymmetries emerged and were consistently in favor of the left side. They were described for thumb, arm and feet movements, but it must be acknowledged that the literature in this domain remains limited, which prevents any definitive conclusion but rather calls for an in depth investigation of this possibility. For

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T a b l e 2: Summary of tactual studies on hand/hemisphere specialization.

TASK

EFFECT

COMMENTS

Pressure/vibration sensitivity

left tendency

possible attentional effects

Point localization

no asymmetry

too few studies

Two-point discrimination

no asymmetry

too few studies

Roughness discrimination

no asymmetry

too few studies

Weight discrimination

no clear trend

too few studies

Sense position

left bias

reported for thumb, arm, and feet

Orientation discrimination

left hand bias

found with different populations

Retention of sequences

left/fight hand advantage

depends on processing mode

left tendency

too few studies/depends on spatial distribution

left tendency

interference between spatial and linguistic codings apparently robust

Dot pattems -numbers -Braille Tactual maze

left hand bias

Nonsense form discrimination

left tendency

depends on presentation mode (dichhaptic or not) depends on encoding mode (linguistic or not)

Haptic search in monkeys

left hand preference

too few studies on hand performance

cutaneous inputs, only the pressure/vibration sensitivity tasks provided some arguments for lateralization. Lateralization was in this case in favor of the left hand, but the obtained effects, possibly affected by attentional factors, were not systematic, although no studies reported a right hand advantage. Other tasks involving the simple cutaneous stimuli showed either no clear trend for a lateral bias (e.g., roughness discrimination) or no asymmetry at all (e.g., two-point discrimination). The necessary

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conclusion is thus that there is no definitive evidence for a sensory lateralization related to the cutaneous sense p e r se. A t best, the literature indicates some tendencies for a left hand advantage (i.e., for pressure/ vibration sensibility tasks), but the left hand advantage hypothesis awaits further investigations to be validated. Turning now to the discrimination of more complex tactual stimuli, the lower part of Table 2 strongly suggests that tactual lateralization exists, and is most of the time in favor of the left side. Note, however, that laterality biases depend on a series of subject (e.g., handedness) and stimulus related factors (e.g., verbal codability and presentation mode of the stimulus). It happens that the most convincing left hand advantage concerns line orientation discrimination, as this effect was obtained in normal subjects, patients and children. At least three aspects of the literature suggests that the left hand advantage for line orientation was determined by post-sensory factors. Firstly, Honda (1977) demonstrated that the left hand advantage occurred even though the task required the discrimination of imaginary lines, because only the two extreme points of the line, instead of the whole line, were physically applied on the skin. Secondly, right hemispheric advantages for line orientation were repeatedly found in visual studies (e.g., Atkinson & Egeth, 1973; Benton, Hannay & Varney, 1975), suggesting that this asymmetry is not linked to a specific sensorial modality. Thirdly, Oscar-Berman et al. (1978) showed a left hand advantage only when the left hand responded after the right, suggesting that tactual laterality effects for line orientation may emerge after some delay in short-term memory. The largest literature on haptic lateralization concerns nonsense form discrimination. Again, when an asymmetry was found in this domain, it was mostly in favor of the left hand, but the left hand bias was not always robust (see Table 2). However, it is noticeable that this literature used the score and occasionally response times as the unique dependent variables. As the score variable appears to be less sensitive to laterality effects than hand exploratory strategies (e.g., Fagot, Lacreuse & Vauclair, 1993), it is suggested that the inconsistencies in hand biases mainly rest on a restricted selection of the measures, and it is thus presumed that a clear-cut picture would emerge if strategies are more systematically considered. As already stated above, the analysis of hand exploratory strategies has the additional advantage to provide information on the processing mode adopted by each hemisphere (e.g., global vs analytic treatments).

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In 1990, Summers and Lederman concluded from their review of the literature that "somatosensory perceptual asymmetries are not robust, although hand superiorities are in the predicted direction when they do occur" (page 221). Our own review of the literature is in agreement with this position, but expands it by allowing conclusions regarding the respective role of early and late factors. In this perspective, if we can suspect that early somato-sensory factors affect lateralization, with the possible exception of kinesthetic tasks, this involvement has not yet been firmly established. Haptic lateralization, however, appears to be affected in a major way by a series of cognitive factors, and in particular, by the spatial and verbal dimension of the task. In this respect, the nonhuman primate model, for which there are already evidence of left hand haptic lateralization, might be informative and is worth developing. References

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S E C T I O N VII: OLFACTORY PROCESSING

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Chapter 14

Laterality in Human Nasal Chemoreception.

Richard L. Doty, Steven M. Bromley, Paul J. Moberg & Thomas Hummel Smell and Taste Center and Department of Otorhinolaryngology: Head and Neck Surgery University of Pennsylvania Medical Center

As we interact with the environment, airborne chemicals and other volatile agents enter our noses and bombard the olfactory receptors. These finely-tuned microscopic structures determine, to a large degree, the flavors of foods and beverages, and warn us of such environmental hazards as leaking natural gas, spoiled food, and polluted air. Just as in the case of our two eyes and two ears, evolution has provided us with two separate nasal passages, each of which harbors a receptor-bearing olfactory epithelium. What is the physiological significance, if any, of this duality with regard to sensory lateralization? Is there a physiological advantage to this anatomical arrangement, other than providing redundancy? Although these questions have been debated for many years, considerable controversy still continues to exist as to whether asymmetries in olfactory function are, in fact, present at all.

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A major reason for investigating lateralization in olfactory function becomes apparent when one considers the atypical anatomy of this system. Among the senses, olfaction is unique in that second order neurons (whose cell bodies lie within the olfactory bulb) send information directly, with primarily ipsilateral projections, to the older portions of the telencephalon before reaching the thalamus and the neocortex (Gordon & Sperry, 1969; Youngentob et al., 1982; Hummel et al., 1995). However, some contralateral afferent and efferent connections exist between the two sides of the olfactory system via the anterior commissure, the corpus callosum, and conceivably the poorly understood hippocampal commissure. Although such connections are believed to be comparatively minor, they clearly exist in humans and other mammals. A classic example of the role of the anterior commissure in mediating cross-hemispheric exchange of information can be found in studies of infant rats conditioned to move toward an odor when only one naris is open. These rats are then tested with opposite (previously occluded) naris open to see if the conditioning transferred to the contralateral side. When six-day-old rats, who lack a mature anterior commissure, are trained in this manner, no transfer of training to the opposite side occurs. In contrast, 12-day-old rats with a mature anterior commissure demonstrate recall of information on the contralateral side. If the anterior commissure is sectioned prior to training of such rats, recall is confined to the side of training, just as occurs in 6-day-old rats (Kucharski & Hall, 1987, 1988). Such a phenomenon is seen using a number of behavioral paradigms, including those of odor aversion and habituation (King & Hall, 1990; Kucharski, Arnold & Hall, 1995). Most information related to laterality of human nasal chemoreception comes from the study of six types of subjects: (i) epileptic patients whose epileptogenic foci are lateralized to one or the other side of the brain; (ii) stroke patients with damage localized to one side of the brain; (iii) epileptic patients whose corpora callosa have been sectioned to prevent seizure activity from spreading contralaterally (so-called "split-brain" patients); (iv) epileptic patients who have received unilateral frontal and/or temporal lobe resection to mitigate their seizure activity; (v) patients with hemiparkinsonism whose dopaminergic deficits are asymmetrical; and (vi) normal subjects. Variation in the quality or type of olfactory testing, size and location of the epileptogenic focus, and, in the case of resection studies, the amount and location of the tissue removed, unfortunately complicate comparisons of results among a

Laterality and Olfaction 499 number of these studies. Nevertheless, the bulk of the research, including "split-brain" experiments, suggests that left and right hemispheres can function quite independently and that there may be some differences in the representation and processing of olfactory information by the two hemispheres. This occurs in despite the fact that odor detection, identification, and discrimination can apparently be performed by each hemisphere independently. In this chapter, we provide an overview of what is presently known about the anatomy of major nasochemosensory systems and the degree to which these systems exhibit laterality, drawing upon anatomical, psychophysical, imaging, and electrophysiological studies. This review attempts to shed light on the degree to which the two sides of the nose provide independent information to higher brain structures and how these structures filter, integrate, interpret, and retrieve such information. ANATOMY OF THE O L F A C T O R Y AND T R I G E M I N A L CHEMOSENSORY SYSTEMS Odorants enter the nose during both active (e.g., sniffing) and passive inhalation; most have the propensity to stimulate both olfactory receptors (CN I) located in the upper recesses of the nasal vault, and free nerve endings of the ophthalmic and maxillary divisions of the trigeminal nerve (CN V), distributed throughout the nasal mucosa and the olfactory neuroepithelium (Figure 1). 1 Sensations derived from CN I stimulation are those of odors (e.g., flowers, lemon, grass, fish, etc.), although at low concentrations minute sensations that lack qualitative character, "something more than nothing," can be perceived. Sensations derived from CN V stimulation are somatosensory, and include tactile sensations, burning, cooling, tickling, warming, and the perception of atmospheric humidity, "thickness," or "fullness." Difficult-to-describe "feelings" can also be perceived from low concentrations of CN V stimulants. It is important to realize that a variety of odorants differentially stimulate these two systems, and that CN I and CN V differ in terms of their central projections and the degree to which their pathways project contralaterally and ipsilaterally. The weight of the evidence suggests that CN I stimulants presented to one nasal chamber cannot be localized to that chamber; however, this is not the case with CN V stimulants (von Skramlik, 1925; Schneider & Schmidt, 1967; Ehrlichman, 1986; Kobal, van Toiler & Hummel, 1989).

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