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COMPARATIVE VERTEBRATE NEUROANATOMY: EVOLUTION AND ANATOMY, 2nd Edition

By: Ann B. Butler and William Hoods
Jon Wiley & Sons, Inc.

FROM THE PUBLISHER
The Second Edition of this landmark text presents a broad survey of comparative vertebrate neuroanatomy at the introductory level, representing a unique contribution to the field of evolutionary neurobiology. It has been extensively revised and updated, with substantially improved figures and diagrams that are used generously throughout the text. Through analysis of the variation in brain structure and function between major groups of vertebrates, readers can gain insight into the evolutionary history of the nervous system. The text is divided into three sections:
1) Introduction to evolution and variation, including a survey of cell structure, embryological development, and anatomical organization of the central nervous system; phylogeny and diversity of brain structures; and an overview of various theories of brain evolution, 2) Systematic, comprehensive survey of comparative neuroanatomy across all major groups of vertebrates, 3) Overview of vertebrate brain evolution, which integrates the complete text, highlights diversity and common themes, broadens perspective by a comparison with brain structure and evolution of invertebrate brains, and considers recent data and theories of the evolutionary origin of the brain in the earliest vertebrates, including a recently proposed model of the origin of the brain in the earliest vertebrates that has received strong support from newly discovered fossil evidence

Ample material drawn from the latest research has been integrated into the text and highlighted in special feature boxes, including recent views on homology, cranial nerve organization and evolution, the relatively large and elaborate brains of birds in correlation with their complex cognitive abilities, and the current debate on forebrain evolution across reptiles, birds, and mammals.

Comparative Vertebrate Neuroanatomy is geared to upper-level undergraduate and graduate students in neuroanatomy, but anyone interested in the anatomy of the nervous system and how it corresponds to the way that animals function in the world will find this text fascinating.

ABOUT THE AUTHORS
Ann B. Butler, Professor
Kranow 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




CONTENTS

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

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 forTracing 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, 3 I

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

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

lawless Vertebrates, 74

Chrondrichthyes, 76

Actinopterygii, 76

Sarcopterygii, 76

The Big Picture of Vertebrate Evolution, 84

Two Types of Brain Organization, 84

Laminar Brains (Group 1), 86

Elaborated Brains (Group 11), 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

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

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

Ariens 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



8 The Spinal Cord, 139

The Spinal Cords of Nontetrapods, 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 lawless Vertebrates, 214

The Extraocular Muscles in ]awled 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 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 Cerebellum in

Nontretapods, 257

The Exceptional Cerebella of Weakly Electric 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 ofTectal Connections, 312

The Optic Tectum in Group I Vertebrates, 315

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



Part Five

THE FOREBRAIN: TELENCEPHALON



24 Basal Telencephalon, 471

Introduction, 471

The Striatopallidal Complexes, 472

Group I, 472

Group IIA, 476

Group lIB, 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

Group I, 612

Group IIA, 6 I3

The Limbic Pallium in Amniotes (Group lIB), 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 WHERE TO ORDER ISBN number 0471210056 ($125.00 hardcover) John Wiley & Sons, Inc. 111 River Street Hoboken, NJ 07030 Website: http://www.wiley.com/WileyCDA/ Direct link to catalog entry: http://www.wiley.com/WileyCDA/WileyTitle/productCd-0471210056.html Posted Date: 10/26/05