COMPARATIVE VERTEBRATE
NEUROANATOMY
Evolution and Adaptation
Second Edition
ANN B. BUTLER
Professor
Krasnow Institute for Advanced Study and Department of Psychology
George Mason University
Fairfax, Virginia
WILLIAM HODOS
Distinguished University Professor
Department of Psychology
University of Maryland
College Park, Maryland
A JOHN WILEY & SONS, INC., PUBLICATION

COMPARATIVE VERTEBRATE
NEUROANATOMY

COMPARATIVE VERTEBRATE
NEUROANATOMY
Evolution and Adaptation
Second Edition
ANN B. BUTLER
Professor
Krasnow Institute for Advanced Study and Department of Psychology
George Mason University
Fairfax, Virginia
WILLIAM HODOS
Distinguished University Professor

Department of Psychology
University of Maryland
College Park, Maryland
A JOHN WILEY & SONS, INC., PUBLICATION
Copyright © 2005 by John Wiley & Sons, Inc. All rights reserved.
Published by John Wiley & Sons, Inc., Hoboken, New Jersey.
Published simultaneously in Canada.
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, scanning, or otherwise, except as permitted under Section 107 or 108 of
the 1976 United States Copyright Act, without either the prior written permission of
the Publisher, or authorization through payment of the appropriate per-copy fee to
the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923,
the Publisher for permission should be addressed to the Permissions Department,
John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, (201) 748-6011,
fax (201) 748-6008.
Limit of Liability/Disclaimer of Warranty: While the publisher and author have used
their best efforts in preparing this book, they make no representations or warranties
with respect to the accuracy or completeness of the contents of this book and
specifically disclaim any implied warranties of merchantability or fitness for a
particular purpose. No warranty may be created or extended by sales representatives
or written sales materials. The advice and strategies contained herein may not be
suitable for your situation. You should consult with a professional where appropriate.
Neither the publisher nor author shall be liable for any loss of profit or any other
commercial damages, including but not limited to special, incidental, consequential,
or other damages.
For general information on our other products and services please contact our
Customer Care Department within the U.S. at 877-762-2974, outside the U.S. at
317-572-3993 or fax 317-572-4002.
Wiley also publishes its books in a variety of electronic formats. Some content that

appears in print, however, may not be available in electronic format.
Library of Congress Cataloging-in-Publication Data:
Butler, Ann B.
Comparative vertebrate neuroanatomy : evolution and adaptation / Ann B. Butler,
William Hodos.
p. cm.
Includes bibliographical references and index.
ISBN 0471210056 (alk. paper)
1. Neuroanatomy. 2. Vertebrates—Anatomy. 3. Nervous system—Evolution.
4. Anatomy, Comparative. 5. Nervous system—Adaptation. I. Hodos, William.
II. Title.
QM451.B895 1996
596¢.048—dc20 95-49380
CIP
Printed in the United States of America
10987654321
978-750-8400, fax 978-646-8600, or on the web at www.copyright.com. Requests to
This dedication is in four parts: to those special friends,
mentors, and family members who are now deceased, to
those special persons still living who have taught and guided
us in our careers, to a special friend of the field, and to our
families.
In recognition of those special persons who are now
deceased, Ann Butler dedicates her contribution to this work
to the memory of Alexander and Ethel Benedict Gutman,
Raymond C.Truex, and B. Raj Bhussry;William Hodos dedicates
his contribution to the memory of his parents, Morris and
Dorothy Hodos, and Walle J. H. Nauta.
In recognition of those special persons in our lives who
have been teachers and mentors as well as friends and col-

leagues, we also dedicate this book to Warren F. Walker, Jr.,
Theodore J. Voneida, R. Glenn Northcutt, Ford F. Ebner, Sven
O. E. Ebbesson, C. Boyd Campbell, and Harvey J. Karten. Addi-
tionally, we dedicate this work to Harold J. Morowitz, James L.
Olds, Robert F. Smith, and William S. Hall in acknowledgement
of their outstanding support and encouragement.
We also dedicate this book to Dr.Thomas Karger in appre-
ciation of his generous and steadfast support of the field of
comparative neurobiology, as particularly evinced by his
sponsorship of the J. B. Johnston Club and its yearly Karger
Symposium. His beneficence has substantially promoted the
dissemination of new data and theories in the field and thus
materially aided the preparation of this second edition.
Finally, we dedicate this book to our families, Thomas and
Whitney Butler and Nira, Gilya, and Tamar Hodos, who have
always given us their loyal support, their patience, and their
ceaseless encouragement.
Dedication

Preface xv
Acknowledgments xix
List of Boxes xxi
Part One
EVOLUTION AND THE
ORGANIZATION OF THE
CENTRAL NERVOUS SYSTEM
1 Evolution and Variation 3
Introduction, 3
Diversity Over Time, 4
Evolutionary Mechanisms, 5

Genetic Factors, 5
Natural Selection, 5
Evolution of the Vertebrate Central Nervous
System, 7
Sameness and Its Biological Significance, 8
Analogy, 8
Historical Homology, 8
Homoplasy, 9
Biological Homology, 11
Generative Homology or Syngeny, 12
Analysis of Variation, 13
Cladistic Analysis, 13
Parsimony, 14
Tests of Homology, 15
A Word of Caution, 15
Reconstructing Evolution, 16
2 Neurons and Sensory Receptors 19
Introduction, 19
The Nervous System, 19
Neurons and Sensory Receptors, 20
Transport Within Neurons, 21
Classification of Neurons, 21
Somata, 21
Dendrites, 21
Axons, 23
Synapses, 23
Chemical Synapses, 23
Neuroactive Substances, 24
Electrical Synapses, 26
Volume Transmission, 26

Neuronal Populations, 26
Golgi Type I and II Cells, 26
Nuclei and Planes of Section, 27
Techniques for Tracing Connections Between
Nuclei, 27
Receptors and Senses, 28
How Many Senses? 29
Receptors and Awareness, 29
Sensory Experience as a Private Mental Event, 30
Sensory Adaptation, 30
Receptor Types, 30
Mechanoreceptors, 31
Radiant-Energy Receptors, 34
Chemoreceptors, 37
Nervus Terminalis: An Unclassified Receptor, 41
Electroreceptors, 41
Nociceptors, 42
Magnetoreceptors, 43
Topographic Organization, 43
Receptive Fields, 46
The Senses and Evolution of the Central Nervous
System, 46
3 The Vertebrate Central Nervous System 49
Introduction, 49
Development of the Brain, 49
Segmental Development of the Vertebrate
Brain, 50
Neurogenesis and Migration of Neurons, 54
Cortices and Nuclei, 55
Differing Patterns of Development, 57

Ontogeny and Recapitulation, 60
Contents
vii
viii CONTENTS
The Brain and Spinal Cord, 61
Cellular Organization of the Central Nervous
System, 61
Regional Organization of the Nervous System, 63
The Spinal Cord, 63
The Brain, 63
The Meninges and the Ventricular System, 66
Major Systems of the Brain, 67
Sensory Systems, 68
Motor Systems, 68
Nomenclature of the Brain, 69
4 Vertebrate Phylogeny and Diversity in
Brain Organization 73
Introduction, 73
Vertebrate Phylogeny, 74
Chordate Relationships, 74
Jawless Vertebrates, 74
Chrondrichthyes, 76
Actinopterygii, 76
Sarcopterygii, 76
The Big Picture of Vertebrate Evolution, 84
Two Types of Brain Organization, 84
Laminar Brains (Group I), 86
Elaborated Brains (Group II), 87
Glia and Brain Elaboration, 89
Laminar and Elaborated Brains across

Evolution, 89
5 Evolution and Adaptation of the Brain,
Behavior, and Intelligence 93
Phylogeny and Adaptation, 93
Phyletic Studies, 93
Adaptation Studies, 94
The Phylogenetic Scale, 95
The Phylogenetic Tree, 95
Complexity and Evolution, 96
Anagenesis, 97
Grades of Evolutionary Advancement, 99
Evolutionary Change, 99
Brain Evolution and Behavioral Adaptation, 100
Brain Size and Brain Allometry, 100
Brain Size and Behavioral Adaptation, 105
Brain Size and Intelligence, 106
What Is Intelligence? 108
Summary and Conclusions, 109
6 Theories of Brain Evolution 113
Introduction, 113
Some Common Assumptions, 113
Previous Theories of Vertebrate Brain Evolution:
Addition of Structures or Areas, 114
MacLean, 114
Flechsig and Campbell, 114
Sanides, 115
Previous Theories of Vertebrate Brain Organization:
New Formation and Reorganization of Circuits, 115
Herrick, 115
Bishop, 115

Ariëns Kappers, 115
Bowsher, 115
Diamond and Hall, 116
Critique of Previous Theories of Vertebrate Brain
Evolution, 116
Parcellation Theory, 117
Ebbesson, 117
Deacon, 117
Current Theories of Forebrain Evolution, 117
Forebrain Evolution: Experimental
Foundations, 117
Karten: Equivalent Cell Hypothesis, 118
Other Theories of Pallial Evolution, 119
Perspective, 121
Part Two
THE SPINAL CORD AND HINDBRAIN
7 Overview of Spinal Cord and Hindbrain 127
Overview of the Spinal Cord, 127
Segmentation Within the Spinal Cord, 127
Roots and Ganglia, 128
Columns of the Spinal Cord, 129
Pathways Within the Spinal Cord, 130
Reflexes, 131
Spinal Autonomy, 133
Rhythmic Movements and Central Pattern
Generators, 133
Overview of the Hindbrain, 133
The Obex and the Fourth Ventricle, 135
The Pontine Nuclei, 135
Ganglia of the Cranial Nerves, 135

Organization of the Cranial Nerves, 135
Embryology of the Hindbrain and a New
Classification of Cranial Nerves, 135
Efferent Axons in Afferent Nerves, 136
Evolutionary Perspectives on the Spinal Cord and
Hindbrain, 136
The Transition to Land, 136
Tetrapod Locomotor Patterns, 137
CONTENTS ix
8 The Spinal Cord 139
Muscles and Locomotion, 139
Cell and Fiber Columns, 139
Giant Axons and Escape, 141
Electromotor Neurons, 144
The Curious Spinal Cords of Sharks, 144
Ascending and Descending Pathways, 144
Reissner’s Fiber, 145
The Organization of the Tetrapod Spinal Cord, 145
Locomotor Patterns and Spinal Cord
Organization, 145
The Curious Spinal Cords of Birds, 146
Segmental Organization, 147
Lamination, 147
Intrinsic Spinal Neurons, 148
Somatotopic Organization of the Ventral Horns, 148
Renshaw Cells, 149
Axon Columns and Cell Columns, 149
Marginal Cells, 150
Accessory Lobes, 150
Ascending Spinal Pathways, 150

Descending Spinal Pathways, 150
Tetrapod Central Pattern Generators, 152
Evolutionary Perspective, 152
9 Segmental Organization of the Head,
Brain, and Cranial Nerves 157
“Twelve” Cranial Nerves, 157
The Vertebrate Head: Segmental Organization, 158
Head Skeleton, 159
The Striated Musculature of the Head, 159
Neural Crest and Placodes, 162
Segmentation of the Head, 164
Theoretical Head Segments, 165
Segmental Organization of the Individual Cranial
Nerves, 166
The Forebrain, 168
The First Head Segment, 168
The Second Head Segment, 169
The Third Head Segment, 169
The Fourth Head Segment, 169
The Fifth Head Segment, 170
10 Functional Organization of the Cranial
Nerves 173
Introduction, 173
The Cranial Nerves and the Spinal Cord, 173
The Organization of Sensory and Motor Columns of the
Caudal Brainstem, 176
Afferent Columns of the Brainstem, 177
Efferent Columns of the Brainstem, 179
Five Cranial Nerves Rostral to the Brainstem, 180
General Considerations, 181

11 Sensory Cranial Nerves of the Brainstem 183
Introduction, 183
Dorsal Cranial Nerves: Sensory Components for General
Somatosensory Sensation, 183
Somatosensory Innervation of the Head, 184
Central Terminations of the Trigeminal Nerve, 185
The Mesencephalic Division of the Trigeminal
System, 185
Secondary Connections of the Trigeminal Nuclei, 186
Ventrolateral Placodal Cranial Nerves: Taste, 189
The Gustatory System, 190
The Gustatory Nerves and the Nucleus Solitarius, 190
Secondary Connections of the Gustatory
Nucleus and Nucleus Solitarius, 190
Cyprinid and Silurid Gustatory Specializations, 192
Dorsolateral Cranial Nerves: Lateral Line and Octaval
Systems, 194
The Lateral Line System, 195
The Octaval System, 196
12 Motor Cranial Nerves 205
Introduction, 205
Feeding and Swallowing, 207
The Neural Control of Feeding and Swallowing, 209
The Communication Systems of Fishes, 211
The Acoustic Reflex, 213
Motor Control of Eye Muscles, 214
The Extraocular Muscles in Jawless Vertebrates, 214
The Extraocular Muscles in Jawled Vertebrates, 214
The Intraocular Muscles, 215
Central Control of the Eye Muscles, 215

The Oculomotor Complex, 217
Coordination of Eye Muscle Action, 218
Evolutionary Perspective on the Hindbrain and
Midbrain Cranial Nerves, 218
13 The Reticular Formation 221
Introduction, 221
The Organization of the Reticular Formation, 222
Neurons of the Reticular Formation, 222
Giant Reticulospinal Neurons, 223
Nomenclature of the Reticular Formation, 224
The Reticular Formation of the Medulla, Pons, and
Midbrain, 225
The Reticular Formation of the Diencephalon, 228
Pathways of the Reticular Formation, 230
Chemical Pathways of the Reticular Formation, 232
The Spinal Cords of Nontetrapods, 139
x CONTENTS
The Reticular Formation and Sleep, 234
Evolutionary Perspective on the Reticular
Formation, 236
14 The Cerebellum 241
Introduction, 241
Overview of the Cerebellum, 241
Cerebellar Size, 242
The Various Forms of the Cerebellum, 243
Corpus Cerebelli, 243
Electroreception and the Cerebellum, 244
The Cerebellar Auricle, 245
Phyletic Development of the Form of the
Cerebellum, 245

The Cerebella of Tetrapods, 246
The Cerebella of Nontetrapods, 246
Agnathans and Cartilaginous Fishes, 246
Ray-Finned Fishes, 246
The Cerebellar Cortex, 247
The Purkinje Cell Layer, 247
The Granule Cell Layer, 249
The Molecular Layer, 253
Afferent Inputs to the Cerebellar Cortex, 253
Interconnections Within the Cerebellar Cortex, 255
The Precerebellar Nuclei, 256
Cerebelloid Structures Associated With the
Fishes, 259
Cerebellar Efferents and the Deep Cerebellar
Nuclei, 260
Evolutionary Perspective, 262
Functions of the Cerebellum, 262
Part Three
THE MIDBRAIN
15 Overview of the Midbrain 267
Introduction, 267
The Isthmus, 268
The Tegmentum, 273
The Tectum, 273
16 Isthmus 275
Introduction, 275
Nuclei of the Raphe, 275
Group I, 275
Group II, 275
Evolutionary Perspective, 277

Locus Coeruleus, 277
Group I, 277
Group II, 277
Evolutionary Perspective, 278
Nucleus Isthmi, 281
Group I, 281
Group II, 281
Evolutionary Perspective, 283
Isthmo-Optic Nucleus, 283
Group I, 283
Group II, 283
Evolutionary Perspective, 284
Midbrain Locomotor Region and Pedunculopontine
Tegmental Nucleus, 284
Group I, 284
Group II, 284
Evolutionary Perspective, 285
Interpeduncular Nucleus, 285
Group I, 285
Group II, 285
Evolutionary Perspective, 285
17 Tegmentum and Tori 289
Introduction, 289
Mesencephalic Nucleus of the Trigeminal Nerve, 289
Group I, 289
Group II, 290
Evolutionary Perspective, 290
Red Nucleus and Related Nuclei, 290
Group I, 290
Group II, 290

Evolutionary Perspective, 292
Substantia Nigra and Ventral Tegmental Area, 292
Group I, 293
Group II, 294
Evolutionary Perspective, 303
Torus Lateralis, 304
Group I, 304
Group II, 304
Evolutionary Perspective, 304
Torus Semicircularis, 304
Group I, 304
Group II, 305
Evolutionary Perspective, 306
18 Optic Tectum 311
Introduction, 311
Overview of Tectal Organization, 311
Overview of Tectal Connections, 312
The Optic Tectum in Group I Vertebrates, 315
257
The Exceptional Cerebella of Weakly Electric
Cerebellum in

Nontetrapods,
CONTENTS xi
Lampreys, 315
Squalomorph Sharks and Ratfishes, 316
Nonteleost Ray-Finned Fishes, 316
Amphibians, 319
The Optic Tectum in Group II Vertebrates, 321
Hagfishes, 321

Galeomorph Sharks, Skates, and Rays, 322
Teleosts, 322
Amniotes, 325
Evolutionary Perspective, 334
Part Four
THE FOREBRAIN: DIENCEPHALON
19 Overview of the Forebrain 343
Introduction, 343
Nomenclature of the Forebrain in Amniotes, 344
The Diencephalon, 344
Pretectum, 344
Posterior Tuberculum, 344
Epithalamus, 345
Dorsal Thalamus, 346
Ventral Thalamus, 347
Hypothalamus and Preoptic Area, 352
The Telencephalon: Pallium, 352
The Telencephalic Pallium of Mammals, 353
The Telencephalic Pallium of Nonmammalian
Amniotes, 361
The Telencephalon: Subpallium, 364
The Ventrolateral Telencephalon of Anamniotes, 364
The Ventrolateral Telencephalon of Mammals, 364
The Ventrolateral Telencephalon of Nonmammalian
Vertebrates, 368
The Septum, 369
20 Pretectum, Accessory Optic System, and
Migrated Posterior Tuberculum 373
Introduction, 373
Pretectum, 373

Group I, 374
Group II, 375
Accessory Optic System, 389
Group I, 391
Group II, 392
Evolutionary Perspective, 394
Migrated Posterior Tuberculum, 396
Group I, 396
Group II, 396
Evolutionary Perspective, 399
21 Epithalamus 407
Introduction, 407
Epiphysis, 407
Habenula, 409
Evolutionary Perspective, 414
22 Dorsal Thalamus 417
Introduction, 417
Collothalamic Auditory System, 418
Group I, 418
Group IIA, 418
Group IIB, 420
Collothalamic Visual and Somatosensory Systems, 426
Group I, 427
Group IIA, 430
Group IIB, 430
Lemnothalamus, 432
Group I, 432
Group IIA, 434
Group IIB, 434
Evolutionary Perspective, 437

Collothalamus, 437
Lemnothalamus, 437
A New Definition of the Dorsal Thalamus in
Vertebrates, 439
23 The Visceral Brain: The Hypothalamus
and the Autonomic Nervous System 445
Introduction, 445
The Hypothalamus, 445
The Hypothalamus and the Endocrine System, 446
Circumventricular Organs, 449
Biological Rhythms, the Epiphysis, and the
Hypothalamus, 449
The Hypothalamus and the Limbic System, 450
The Preoptic Area, 450
The Hypothalamus in Anamniotes, 451
Jawless Fishes, 451
Cartilaginous Fishes, 451
Actinopterygians, 451
Sarcopterygians, 455
The Hypothalamus in Amniotes, 455
Connections of the Hypothalamus in Reptiles and
Birds, 456
Connections of the Hypothalamus in Mammals, 457
Functions of the Hypothalamus, 460
The Autonomic Nervous System, 460
Autonomic Neurochemistry, 462
Amniotes, 462
Anamniotes, 462
Evolutionary Perspective, 462
xii CONTENTS

Part Five
THE FOREBRAIN: TELENCEPHALON
24 Basal Telencephalon 471
Introduction, 471
The Striatopallidal Complexes, 472
Group I, 472
Group IIA, 476
Group IIB, 477
The Striatal Amygdala, 487
Cholinergic Neuronal Populations of the Basal
Telencephalon, 488
Evolutionary Perspective, 489
25 Nonlimbic Pallium 495
Introduction, 495
The Nonlimbic Pallium in Group I Vertebrates, 496
The Nonlimbic Pallium in Group IIA Vertebrates, 498
Neuroanatomical Organization, 498
Behavioral Issues, 501
The Nonlimbic Pallium in Amniotes, 501
Mammals: Neocortex, 501
Mammals: Claustrum-Endopiriform Formation and
Frontotemporal Amygdala, 504
Reptiles and Birds, 504
Ascending Sensory Pathways to the Pallium in
Amniotes, 507
Pallial Evolution and Persistent Questions of
Homologies, 510
26 Visual Forebrain in Amniotes 523
Introduction, 523
Ipsilateral Retinal Pathways and Stereoscopic

Vision, 524
Visual Pathways to the Telencephalon in Mammals, 524
Lemnothalamic Visual Forebrain, 524
Collothalamic Visual Forebrain, 536
Pathways to the Visual Telencephalon in Reptiles and
Birds, 537
Lemnothalamic Visual Pathways, 538
Collothalamic Visual Pathways, 540
Evolutionary Trends in the Visual System of
Amniotes, 540
27 Somatosensory and Motor Forebrain in
Amniotes 547
Introduction, 547
The Somatosensory and Motor Forebrain of
Mammals, 547
The Ventral Tier Nuclei of the Dorsal Thalamus, 548
Somatosensory Lemnothalamus, 548
Somatosensory Collothalamus, 548
Motor Lemnothalamus, 548
Afferents to Somatosensory Cortex, 549
Efferents of Somatosensory Cortex, 549
Pain Pathways, 549
Somatotopic Organization, 552
Motor Cortex, 557
Multiple Motor Representations of the Body, 558
The Cortical Eye Fields, 558
Afferents and Efferents of the Motor Cortex, 558
The Somatosensory and Motor Forebrain of
Nonmammalian Amniotes, 559
Somatosensory System, 559

Motor System, 564
Evolutionary Perspective, 566
28 Auditory and Vocal Forebrain in Amniotes 571
Introduction, 571
Location of Sound Sources, 571
Echolocation, 572
Auditory Channels for Time and Intensity, 573
Design Features of the Auditory System, 574
Topographic Organization, 574
Bilateral Interaction in the Auditory Pathway, 574
Descending Auditory Pathways, 574
Auditory Pathways in Tetrapods, 574
Auditory Telencephalon, 577
Columnar Organization, 577
Mammals, 577
Reptiles and Birds, 579
Vocal Telencephalon, 580
Vocalization and Hearing, 581
Anurans, 582
Reptiles and Birds, 583
Mammals, 587
Evolutionary Perspective, 589
29 Terminal Nerve and Olfactory Forebrain 593
Introduction, 593
Olfactory System, 593
Group I, 594
Group II, 595
Vomeronasal System, 601
Terminal Nerve, 605
Evolutionary Perspective, 606

30 Limbic Telencephalon 611
Introduction, 611
The Limbic Pallium in Anamniotes, 612
CONTENTS xiii
Group I, 612
Group IIA, 613
The Limbic Pallium in Amniotes (Group IIB), 617
Limbic Pallium of Mammals, 619
Limbic Pallium in Nonmammalian Amniotes, 623
Limbic Subpallium: Septum, 628
Evolutionary Perspective, 629
Part Six
CONCLUSION
31 Evolution of Brains: A Bilaterian View 637
Introduction, 637
Invertebrate Brains and the Inversion Hypothesis, 638
Insect Brain Organization, 639
Urbilateria and the Ancestral Condition of Bilaterian
Brains, 641
Deuterostomes and Dorsoventral Inversion, 641
Brain Evolution within Chordates, 644
The Origin of Vertebrates, 649
Haikouella, 650
Sensory System Evolution in the Vertebrate
Lineage, 652
Organization of the Vertebrate Brain, 653
The Advent of Jaws, 655
Onto the Land and Into the Air, 656
Theories of Vertebrate Brain Evolution, 657
How Vertebrate Brains Evolve, 657

Appendix: Terms Used in Neuroanatomy 665
Introduction, 665
Direction and Location Terms, 665
Planes of Section, 666
Neuroanatomical Names, 668
Derivation of Terms, 668
Glossary 671
Index 679

What Is This Book About?
This book is about the central nervous system of those
animals that possess backbones—the vertebrates—and how
evolution has shaped and molded their bodies and their
nervous systems, allowing them to thrive in their particular
environments or to take advantage of new environmental
opportunities.Thus, it is a book about the relationship between
structure and function and about survival through effective
design. It is a book about the past as well as the present and
about the history of vertebrate nervous system evolution, to
the extent that we can read that history from the present state
of these animals.
Who Is This Book For?
This book has been written first and foremost for neuro-
science students at the graduate or advanced undergraduate
level. We have presumed that the reader will have taken one
or more introductory undergraduate biology courses or other-
wise be familiar with this material. In a more general sense, this
book is also for anyone who is interested in the anatomy of the
nervous system and how it is related to the way that an animal
functions in its world, both internal and external.

This book is intended as an introductory work rather than
as a handbook or reference work that scientists might refer to
in their professional writing. We have modeled this book on
several textbooks designed for advanced undergraduate to
graduate levels: Functional Anatomy of the Vertebrates: An
Evolutionary Perspective (Second Edition) by W. F. Walker, Jr.
and K. F. Liem (Saunders College Publishing, Fort Worth, TX,
1994); Hyman’s Comparative Vertebrate Anatomy edited by
M. H. Wake (The University of Chicago Press, 1979); The
Human Brain and Spinal Cord by L. Heimer (Springer-Verlag,
New York, 1983); Core Text of Neuroanatomy by M. B.
Carpenter (Williams and Wilkins, Baltimore, 1991); An Intro-
duction to Molecular Neurobiology by Z. W. Hall (Sinauer
Associates, Sunderland, MA, 1992); and Principles of Neuro-
science (Third Edition) by E. R. Kandel, J. H. Schwartz, and T.
M. Jessell (Appleton and Lange, Norwalk, CT, 1991). In keeping
with the format of these texts, we have not cited references in
the body of the text, but at the end of each chapter we have
listed the references from which we drew material and addi-
tional papers that may interest the reader. Our aim has been to
introduce the reader to the field and to synthesize information
into a coherent overview, rather than to present an extensive
catalog of individual data.
In keeping with the introductory nature of this work, we
largely have omitted details on whether and/or where particu-
lar projections cross the midline of the nervous system. In
some cases, where this information is of particular importance,
we have included it. However, in most cases, we leave it to the
interested reader to glean such details from other sources.
This is a book that we hope will be of interest to the

general scientific reader and the nature enthusiast, as well as
to advanced undergraduate or beginning graduate students in
the neurosciences. Physicians and others with knowledge of
the human central nervous system should also find much of
interest here. To our colleagues who are specialists in the field
of comparative neuroanatomy, we say that this is not the book
that you might write; this is the book that students should read
to give them the background to read your book and other
scholarly publications in neuroanatomy and brain evolution.
Apropos of this aim and since the time of the first edition
of this textbook, a truly remarkable contribution to the lit-
erature of comparative neuroanatomy was made by Rudolf
Nieuwenhuys, Hans ten Donkelaar, and Charles Nicholson with
the publication of their comprehensive and encyclopedic set
of three volumes on The Central Nervous System of Verte-
brates (1998, Springer-Verlag, Berlin).These volumes cover the
subject and the literature in far greater depth and breadth than
could or should be included in a textbook. We have benefited
greatly from the material in these volumes in writing the
second edition of this book. In updating material, there is
the constant temptation to add more and more detail, and in
the process, forsake the original purpose. We thus have endeav-
ored to tread a fine line between updating and maintaining the
introductory level. We hope that this book will continue to fill
its intended role as an introductory work, allowing the reader
to then delve into the Nieuwenhuys et al. volumes as well as
the primary literature for much more extensive and detailed
treatments of a multitude of topics.
What Can Be Learned About the Human
Brain From a Book About the Brains of Many

Different Vertebrates?
During the past four decades, a great explosion of infor-
mation about the anatomy of the brains of nonhuman and espe-
cially nonmammalian vertebrates has taken place. One of the
lessons to emerge from this wealth of new data has been the
reversal of the nineteenth century view that a dramatic change
in brain evolution occurred with the evolution of mammals in
Preface
xv
xvi PREFACE
general and humans in particular. In other words, once the
powerful tools of modern neuroanatomy were applied to the
brains of birds, fishes, reptiles, and amphibians, many of
the same patterns of cell groups and their interconnections that
were known to be present in mammals (including primates)
were found to be present in nonmammalian vertebrates as well.
Thus, comparative neuroanatomists came to recognize that the
evolution of the vertebrate central nervous system had been
far more conservative than earlier investigators had realized.
To be sure, great differences in specialization of the brain
exist between animals that have become adapted to very dif-
ferent modes of existence. Indeed, those differences in form
and function are what make the study of comparative neu-
roanatomy and brain evolution so fascinating—a fascination
that we hope to share with you. In spite of these differences,
however, all vertebrate central nervous systems share a
common organizational scheme so that someone who is famil-
iar with the brain of any vertebrate will also be on familiar
ground when first encountering the brain of any other species.
Someone who has read this book and retained the general

principles of brain anatomy and organization that it presents
will have little difficulty reading a medical school textbook of
human neuroanatomy because much of it will be familiar both
in overall conception and in many of the details.
What Is New in This Book and How Does It
Differ from Other Texts?
The first edition of this book incorporated several new
approaches to the subject matter of comparative neuroanatomy
and the orientation with which we study it. These new
approaches, which have been maintained and/or further
developed in this second edition, include
• A recent reevaluation of the cranial nerves of vertebrates
and their derivation and organization
• A new organizational approach to the various groups of
vertebrates based on the degree of elaboration in their
central nervous systems rather than the traditional, scala
naturae-like ranking
• New insights into the organization and evolution of the
dorsal thalamus and dorsal pallium in the forebrain
• A new and comprehensive overview of brain evolution in
vertebrates that encompasses many of the evolutionary
and developmental topics covered in the rest of the text
The first of these new approaches is based on the work of
Northcutt, Baker, Noden, and others, on the organization of the
cranial nerves. While constituting a radical departure from the
established, traditional list of twelve cranial nerves with their
functional components, we feel that this new approach is a
marked improvement for two reasons: First, it takes into
account additional cranial nerves, both long known and newly
recognized ones, that are found in many vertebrates but are not

included in the “traditional twelve.” Second, it is based on
embryological development, including gene expression pat-
terns, and thus provides a coherent accounting of the seg-
mentation of the head itself and of its component parts,
including both the brain and other tissues (particularly the
neural crest, epithelial placodes, and paraxial mesoderm).
Chapter 9 on the embryology of the cranial nerves in relation
to head segmentation covers this newly developed approach
to cranial nerve organization and is crucial to understanding
the subsequent chapters on the cranial nerves themselves.
The second departure from tradition that we took in the
first edition and have retained here is the order in which
various groups of vertebrates are considered in the chapters on
the various regions of the nervous system. This approach is
based on the range of variation in brain structure within each
of the major groups of vertebrates. It is intended to overcome
the erroneous but culturally ingrained idea of a single, simple-
to-complex, linear series of evolutionary stages leading from
fish to frog to rat to cat to monkey to human, i.e., the myth of
a scala naturae. Chapter 4 specifically addresses this issue.
A great diversity in brain organization has been achieved
independently at least four separate times within four separate
radiations of vertebrates; our approach is designed to highlight
both the diversity itself and its multiple, independent devel-
opment. Thus, in a number of the chapters on brain regions
and systems, particularly in the midbrain and forebrain, we first
consider and compare those species within each radiation in
which the brain has relatively simple cellular organization, as
for example, lampreys, dogfish sharks, gars, and frogs. We then
consider and compare those species within each radiation in

which the brain has relatively complex cellular organization, as
for example, hagfishes, skates, teleost fishes, and amniotes
(mammals, reptiles, and birds).We hope to convince the reader
that the development of a more complex brain has been
accomplished not just once for the “ascent of man,” but multi-
ple times. Moreover, we will show that mammals (including
primates) do not always have the most sophisticated brain
systems.
In line with this point, other chapters, including “Evolu-
tion and Variation,” “Evolution and Adaptation of the Brain,
Behavior, and Intelligence,” and “Theories of Brain Evolution,”
seek to dispel further the myth of scala naturae and to deal
with the actual range of variation in line with the known facts
and processes involved. In this context, we hope that the
reader will come to understand that, whereas some vertebrates
have simpler brains than others, all living vertebrates are
equally successful in that they are alive and adapted to their
environments.
A third new approach taken for the first edition and main-
tained here concerns the evolution of two major parts of the
forebrain, the dorsal thalamus and the dorsal pallium, particu-
larly in amniote vertebrates. Two fundamentally different divi-
sions of the dorsal thalamus recently have been recognized in
all jawed vertebrates: one that predominantly receives direct,
lemniscal sensory and related inputs, called the lemnothala-
mus, and one that predominantly receives sensory inputs
relayed to it via the roof of the midbrain, called the collothala-
mus. These lemnothalamic and collothalamic divisions of the
dorsal thalamus have recently gained validation from differen-
tial patterns of gene expression during development. Corre-

spondingly, two major divisions of the pallium in amniote
vertebrates that receive their respective inputs predominantly
from the lemnothalamic and collothalamic divisions of the
dorsal thalamus have been recognized as well. The way in
which a number of the chapters on the forebrain have been
PREFACE xvii
organized and the material presented in them are based to
some extent on these new concepts of forebrain evolution.
Finally, new insights into the evolution of the brain, not just in
vertebrates but among some of the invertebrate chordates as
well, are presented in the last chapter of this book. Recent find-
ings on genetic patterning of central nervous system structure
and on the anatomy of the brain and head region in the
cephalochordate Branchiostoma, as well as anatomical evi-
dence from the recently found fossils of the chordate Haik-
ouella, allow for some of the features of the brain in the earliest
vertebrates to be identified. A new survey of brain evolution is
presented. For context, brain organization in some inverte-
brates is surveyed, particularly in terms of gene expression pat-
terns, which are strikingly similar to those in vertebrates.Then
vertebrate brain evolution is discussed, beginning with a few
but significant features that can be identified in the common
ancestors of cephalochordates and vertebrates, identifying
additional features that were present in the earliest vertebrates,
including two novel tissues of the head (neural crest and pla-
codes) and a number of cranial nerves associated with them,
and then tracing the separate evolutionary histories of the brain
in the major radiations of extant vertebrates.
For the second edition, a recently proposed model of the
transition to vertebrates that specifies the gain of paired eyes

and elaboration of the diencephalon and hindbrain before most
of the elaboration of neural crest and placodal tissues occurred
to produce the peripheral nervous system has been included.
This model was recently given strong support by newly dis-
covered fossil evidence from the chordate Haikouella. Also,
the striking similarities of patterning gene expression across all
bilaterally symmetrical animals studied, from mice to fruit flies,
and their implications for the evolution of rostrocaudally
and dorsoventrally organized central nervous systems are
discussed.

A number of our colleagues have read portions of the first
and/or second editions for us or have discussed a variety of the
topics with us.They also sustained us with their enthusiasm for
this project. We owe a large debt of gratitude to Philip Zeigler,
who served as editor of the first edition and provided us with
detailed and thoughtful commentary on all of the chapters.The
book was greatly improved as a result of his efforts. We thank
Andrew Bass, Steven Brauth, Catherine Carr,William Cruce, the
late William Dingwall, Joseph Fetcho, Michael Fine, Katherine
Fite, Jon Kaas, Harvey Karten, Darcy Kelley, Wayne Kuenzel,
Harry Jerison,Thurston Lacalli, Michael Lannoo, Rodolfo Llinás,
Paul Manger, Gloria Meredith, Donald Newman, Rudolf
Nieuwenhuys, Glenn Northcutt, Mary Ann Ottinger, Michael
Pritz, Luis Puelles, Anton Reiner, Daphne Soares, Charles
Sternheim, Mario Wullimann, David Yager, and several anony-
mous reviewers for their comments and suggestions on
various chapters for the first and/or second edition. We are
grateful to them for their advice and suggestions and for inter-
cepting various errors. We accept full responsibility for any

errors that remain despite our best efforts. We also thank Wally
Welker for providing several photomicrographs of raccoon
brain sections. We owe a special debt of gratitude to R. Glenn
Northcutt for providing original negatives of Nissl-stained sec-
tions for use in some of the revised figures for the second
edition.
A number of publishers and individuals granted us gratis
permission for the use of material adapted from their publica-
tions. These include Elsevier, W. H. Freeman and Company, S.
Karger AG, Basel, The Johns Hopkins University Press, The Uni-
versity of Chicago Press Ms. Elizabeth Rugh Downs, Dr. Daphne
Soares, McGraw-Hill, Akademie Verlag, The Royal Society of
London, The Cambridge University Press, Thomson Learning,
and John Wiley & Sons. We thank them for their generosity and
the support of scholarly endeavors that it demonstrates.
We offer our special thanks to several additional people,
who are both friends and colleagues, and who had important
influences on various aspects of the writing of this book. The
first is Trev Leger, formerly of John Wiley & Sons, who played
a major role in the inception of the first edition many years ago.
We also thank the several editors at Wiley-Liss—Kelly Franklin,
Ginger Berman, Fiona Stevens, Luna Han, Thomas Moore, and
Danielle Lacourciere—who have helped and encouraged us
over the years. We also wish to thank Dean Gonzalez for his
excellent work on the figure reproductions. Next, our friend
and colleague, Boyd Campbell, who also contributed to the
inception of the book, advised us on many occasions, and
offered numerous valuable suggestions about the overall con-
ception and scope of the work. Arthur Popper, another friend
and colleague, was instrumental in forming the partnership

between us for the task of writing the book. His seemingly
modest proposal had major consequences. Ann Butler espe-
cially acknowledges and thanks Harold Morowitz, James Olds,
and Robert Smith for their unflagging encouragement and
support at the Krasnow Institute for Advanced Study and the
Department of Psychology at George Mason University. Like-
wise, William Hodos acknowledges and thanks William S. Hall
for his generous support and encouragement in the Depart-
ment of Psychology at the University of Maryland. Finally, each
of us also wishes to thank the other—for much intellectual
stimulation, for mutual support, and, most important, for man-
aging to remain friends, even through two editions of this
book!
Acknowledgments
xix