FrontMatter.qxd 30/9/03 4:08 PM Page i

THE HUMAN NERVOUS SYSTEM

SECOND EDITION FrontMatter.qxd 30/9/03 4:08 PM Page iii

THE HUMAN NERVOUS SYSTEM

SECOND EDITION

Edited by

GEORGE PAXINOS Prince of Wales Medical Research Institute The University of New South Wales Sydney, Australia

JÜRGEN K. MAI Institute of Neuroanatomy Heinrich-Heine University of Düsseldorf Düsseldorf, Germany

Amsterdam Boston Heidelberg London New York Oxford Paris San Diego San Francisco Singapore Sydney Tokyo FrontMatter.qxd 30/9/03 4:08 PM Page iv

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Cover image: Figure 17.12, Panel A: illustrates the mixing of neurons that stain with antiserum against ORX (brown) and with a digoxygenin-labeled probe for MCH mRNA (blue) in the perifornical region of a rat. Although the two types of neurons cluster closely with one another around the edge of the fornix, there is virtually no colocalization within individual neurons. Modified from Elias, C.F., Saper, C.B., Maratos-Flier, E., Tritos, N.A., Lee, C., Kelly, J., Tatro, J.B., Hoffman, G.E., Ollmann, M.M., Barsh, G.S., Sakurai, T., Yanagisawa, M., and Elmquist, J.K. (1998b). Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J. Comp. Neurol. 402, 442–459.

Library of Congress Catalog Card Number: 2003107471

International Standard Book Number: 0-12-547626-4

For information on all Academic Press publications visit our website at www.academicpress.com

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To Alexi and Benigna FrontMatter.qxd 30/9/03 4:08 PM Page vii

Contents

Contributors xiii 3. Fetal Development of the Central Preface xvii Nervous System JÜRGEN K. MAI AND KEN W. S. ASHWELL Cerebral cortex 49 Deep Telencephalic Nuclei 57 I Diencephalon 69 Midbrain 76 EVOLUTION AND DEVELOPMENT Cerebellum and Precerebellar Nuclei 78 Pons and Medulla 81 1. Brain Evolution Spinal Cord 84 GEORG F. STRIEDTER Acknowledgment 86 Historical Pattern of Vertebrate Brain Evolution 4 References 86 Developmental Mechanisms Underlying Brain Evolution 9 4. Development of the Peripheral Evolution of Uniquely Human Brains 13 Nervous System Conclusions 16 KEN W. S. ASHWELL AND PHIL M. E. WAITE References 16 Cranial Nerves 95 Somatic Peripheral Nervous System 102 2. Embryonic Development Automatic and Enteric Nervous System 104 of the Central References 107 Nervous System FABIOLA MÜLLER AND RONAN O’RAHILLY Developmental Stages and Ages 23 II Areas with Special Inductive Influence 23 PERIPHERAL NERVOUS SYSTEM Neurulation 24 AND SPINAL CORD Neurocytogenesis 26 Development of the Neural Plate and Groove 28 5. Peripheral Motor System The Brain from 4 to 6 Postfertilizational Weeks 29 SIMON C. GANDEVIA AND DAVID BURKE Some Individual Regions of the Brain 30 Ventricles, Choroid Plexuses, and Circumventricular Composition of Muscle Nerves 113 Organs 43 Muscle Receptors 115 The Cerebral Arteries 44 Features of Muscle 122 Measurements 44 Muscle Units and Motor Units 126 Summary 45 Acknowledgment 129 References 46 References 129

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6. Peripheral Autonomic Pathways Cranial Motor Nuclei 308 IAN GIBBINS Somatosensory System 309 Vestibular Nuclei 312 General Organization of Autonomic Pathways 134 Auditory System 312 Cranial Autonomic Pathways 138 Visual System 314 Sympathetic Pathways 152 Precerebellar Nuclei and Red Nucleus 314 Pelvic Autonomic Pathways 162 Conclusion 316 Enteric Plexuses 167 References 317 Adrenal Medulla and Paraganglia 170 Concluding Remarks 171 11. Cerebellum and Precerebellar Nuclei Acknowledgments 171 References 171 JAN VOOGD External Form, Development, and Subdivision of 7. Spinal Cord: Cyto- the Human Cerebellum 322 and Chemoarchitecture Cerebellar Nuclei 331 JEAN SCHOENEN AND RICHARD L. M. FAULL Cerebellar Peduncles: Topography of Pathways from the Human Cerebellar Nuclei 336 Cyto- and Dendroarchitecture 190 Afferent Fiber Systems 355 Chemoarchitecture 209 The Vestibulocerebellum 374 Myeloarchitecture 224 Longitudinal Zonation of the Cerebellum 375 Acknowledgments 227 Acknowledgments 382 References 228 References 382 8. Spinal Cord: Connections 12. Periaqueductal Gray JEAN SCHOENEN AND GUNNAR GRANT PASCAL CARRIVE AND MICHAEL M. MORGAN Propriospinal Pathways 233 External Boundaries of the Periaqueductal Afferent Pathways 235 Gray 393 Efferent Pathways 243 Internal boundaries of the Periaqueductal References 247 Gray 394 9. Spinal Cord in Relation to Chemoarchitecture of the Primate Periaqueductal Gray 400 the Peripheral Nervous System Connectivity of the Primate Periaqueductal THOMAS CARLSTEDT, STAFFAN CULLHEIM Gray 405 AND MÅRTEN RISLING Functional Aspects 413 The Spinal Cord-Spinal Nerve Root Junction 251 Conclusion 417 Developmental Aspects 254 References 418 Experimental Studies of the Transitional Region 255 Brachial and Lumbosacral Plexuses 259 13. Raphe Nuclei References 262 JEAN-PIERRE HORNUNG 10. Organization of Human Brain Divisions of the Raphe Nuclei 425 Stem Nuclei Connectivity 430 Functional Considerations 436 YURI KOUTCHEROV, XU-FENG HUANG, GLENDA HALLIDAY AND GEORGE PAXINOS Acknowledgments 440 References 440 Autonomic Regulatory Centers 273 Reticular Formation 301 14. Substantia Nigra and Locus Coeruleus Tegmental Nuclei 305 GLENDA HALLIDAY Locus Coeruleus 306 Raphe Nuclei 307 Substantia Nigra 451 Ventral Mesencephalic Tegmentum and Locus Coeruleus and Subcoeruleus 458 Substantia Nigra 307 References 461 FrontMatter.qxd 30/9/03 4:08 PM Page ix

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15. Lower Brain Stem Regulation of 19. Circumventricular Organs Visceral, Cardiovascular, and MICHAEL J. MCKINLEY, IAIN J. CLARKE Respiratory Function AND BRIAN J. OLDFIELD WILLIAM W. BLESSING Subfornical Organ 563 Vascular Organ of the Lamina Terminalis 569 Principles of Functional Neuroanatomical Median Eminence and Neurohypophysis 573 Organization in the Brain Stem 465 Pineal Gland 577 Cadiovascular Function 466 Subcommissural Organ 580 Respiratory Function 470 Area Postrema 581 Salivation, Swallowing, and Gastrointestinal Choroid Plexus 585 Function, Nausea, and Vomiting 473 References 586 Lower Brain Stem Regulation of Vomiting 475 Lower Brain Stem Regulation of Hypothalamohypophyseal Secretion 475 Lower Brain Stem Regulation of Pelvic 20. Thalamus Viscera 476 GERARD PERCHERON References 477 General Considerations 592 Diencephalon 595 16. Reticular Formation: Thalamus 599 Eye Movements, Gaze, and Blinks Isothalamus. Constitution, Architecture, JEAN A. BÜTTNER-ENNEVER and Function 600 AND ANJA K.E. HORN Regio Superior 604 Regio Medialis 608 Eye and Head Movements 480 Regio Posterior 611 Eyelid and Blink 497 Regio Basalis 614 References 503 Regio Geniculata 619 Regio Lateralis 620 Subregio Lateralis Arcuata. Nucleus Ventralis Arcuatus. VArc 623 Subregio Caudalis. Lemniscal Territory 624 IV Subregio Lateralis Intermedia. Cerebellar Territory 626 DIENCEPHALON, BASAL Subregio Lateralis Oralis. Pallidal GANGLIA AND AMYGDALA Territory 630 Subregio Lateralis Rostralis. 17. Hypothalamus Nigral Territory 635 CLIFFORD B. SAPER Allothalamus. Involucrum 647 Regio Centralis 651 Cytoarchitecture of the Human Thalamus 514 Thalamic Stereotaxy 657 Fiber Connections of the Hypothalamus 524 References 660 Functional Organization of the Hypothalamus 530 References 542 21. The Basal Ganglia 18. Hypophysis SUZANNE N. HABER AND LUCIA STEFANEANU, GEORGE KONTOGEORGOS, MARTHA JOHNSON GDOWSKI KALMAN KOVACS, AND EVA HORVATH Topography, Cytoarchitecture, and Basic Anatomy of the Hypophysis 551 Circuitry 677 Imaging of the Hypophysis 553 Functional Basal Ganglia Connections 706 Histology 554 Functional Considerations 715 Ultrastructure 556 Acknowledgments 717 References 561 References 719 FrontMatter.qxd 30/9/03 4:08 PM Page x

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22. Amygdala 26. Motor Cortex JOSE S. DE OLMOS MASSIMO MATELLI, GIUSEPPE LUPPINO, STEFAN GEYER AND KARL ZILLES Terminology 739 Description 741 Monkey Motor Cortex 975 Acknowledgments 857 Human Motor Cortex 985 References 860 Concluding Remarks 992 Acknowledgments 992 References 992

V 27. Architecture of the Human CORTEX Cerebral Cortex KARL ZILLES 23. Hippocampal Formation RICARDO INSAUSTI AND DAVID G. AMARAL Principal Subdivisions of the Cerebral Cortex 997 Quantitative Aspects of the Cerebral Cortex 998 Gross Anatomical Features 872 Paleocortex 1000 Cytoarchitectonic Organization of the Archicortex 1003 Hippocampal Formation 880 Isocortex 1007 Hippocampal Connectivity 891 Cortical Maps of the Human Brain: Past, Clinical Anatomy 901 Present, Future 1038 Functional Considerations—The Emergence Acknowledgments 1042 Of Neuroimaging 903 References 1042 Acknowledgments 906 References 906 VI 24. Cingulate Gyrus BRENT A. VOGT, PATRICK R. HOF SYSTEMS AND LESLIE J. VOGT 28. Somatosensory System Surface Morphology 916 JON H. KAAS Regional Morphology: Four Fundamental Cingulate Subdivisions 919 Receptor Types and Afferent Pathways 1061 Functional Correlations of the Four Cingulate Relay Nuclei to Medulla and Upper Regions 920 Spinal Cord 1069 Maps of Cingulate Areas 923 Somatosensory Regions of the Midbrain 1071 Cytology of Cingulate Areas 924 Somatosensory Thalamus 1071 Comparison of the Brodmann Areas with Recent Anterior Parietal Cortex 1074 Modifications Thereof 943 Posterior Parietal Cortex 1080 Cortical Differentiation in Posterior Somatosensory Cortex of the Medial Wall: Cingulate Gyrus 943 The Supplementary Sensory Area and The Future for Cingulocentric Hypotheses and Cingulate Cortex 1083 Research 946 Somatosensory Cortex of the Lateral Dedication and Acknowledgments 947 (Sylvian) Sulcus 1084 References 947 Summary 1085 References 1086 25. The Frontal Cortex MICHAEL PETRIDES AND DEEPAK N. PANDYA 29. Trigeminal Sensory System PHIL M. E. WAITE AND KEN W. S. ASHWELL Sulcal and Gyral Morphology of the Frontal Cortex 951 Receptors and Their Innervation 1094 Architechtonic Organization 955 Trigeminal Nerves, Ganglion, and Root 1098 Corticocortical Connection Patterns 963 Brainstem Trigeminal Sensory Nuclei 1101 Acknowledgments 970 Thalamic Sites for Trigeminal Somatic References 971 Sensations 1109 FrontMatter.qxd 30/9/03 4:08 PM Page xi

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Cranial Somatosensory Cortex 1113 Conclusion 1233 References 1116 Acknowledgments 1233 References 1233 30. Pain System WILLIAM D. WILLIS, JR. AND KARIN N. WESTLUND 34. Auditory System JEAN K. MOORE AND FRED H. LINTHICUM, JR. Nociceptors 1125 Pain Transmission Neurons and Pathways 1137 The Cochlea and Cochlear Nerve 1242 Descending Pain Modulatory Systems 1147 The Brain Stem Auditory System 1251 Brain Structures Involved in Pain Perception The Forebrain Auditory System 1264 and Integration 1150 The Descending Auditory System 1271 Summary and Conclusions 1157 References 1274 References 1158 35. Visual System 31. Gustatory System RAINER GOEBEL, LARS MUCKLI, AND DAE-SHIK KIM THOMAS C. PRITCHARD AND RALPH NORGREN Central Visual Pathway 1280 Gustatory Apparatus and peripheral Primary Visual Cortex 1286 Innervation 1171 Extrastriate Cortex 1293 The Central Nervous System 1173 Acknowledgments 1301 Further Gustatory Processing 1189 References 1301 Summary 1191 Acknowledgments 1191 36. Emotional Motor System References 1191 GERT HOLSTEGE, LEONORA J. MOUTON, AND NICOLAAS M. GERRITS 32. Olfaction Basic Motor System 1306 JOSEPH L. PRICE Somatic Motor System 1309 Olfactory Mucosa 1198 Emotional Motor System 1312 Olfactory Bulb 1200 Concluding Remarks 1323 Primary Olfactory Cortex 1201 References 1324 Olfactory Projections Beyond the Primary Olfactory Cortex 1206 37. Cerebral Vascular System References 1209 OSCAR U. SCREMIN

33. Vestibular System Anatomy of Cerebral Blood Vessels 1326 Anatomy of Spinal Cord Blood Vessels 1339 JEAN A. BÜTTNER-ENNEVER Vascular Innervation 1340 AND NICOLAAS M. GERRITS Mapping Cerebral Function with Blood Flow 1341 Topography and Cytoarchitecture 1213 Global Responses of the Cerebral Circulation 1344 Connections 1221 References 1345 FrontMatter.qxd 30/9/03 4:08 PM Page xiii

Contributors

Numbers in parentheses indicate the pages on which the authors’ contributions begin.

David G. Amaral, (871), Center for Neuroscience, Martha Johnson Gdowski, (676), Department of Neuro- University of California, Davis, California, USA biology and Anatomy, University of Rochester School Ken W. S. Ashwell,(49, 95, 1093), Department of Anatomy, of Medicine, Rochester, New York, USA School of Medical Sciences, The University of New Nicolaas M. Gerrits,(1212, 1306), Department of Anatomy, South Wales, Sydney, Australia Erasmus University, Rotterdam, The Netherlands William W. Blessing, (464), Departments of Physiology Stefan Geyer, (973), C. and O. Vogt-Brain Research and Medicine, Centre for Neuroscience, Flinders Institute, Heinrich Heine University of Düsseldorf, University, Adelaide, Australia Düsseldorf, Germany Jean A. Büttner-Ennever, (479, 1212), Institute of Anatomy, Ludwig-Maximilian University Munich, Munich, Ian Gibbins, (134), Department of Anatomy and Germany Histology, Flinders University, Adelaide, Australia David Burke, (113), College of Health Sciences, The Rainer Goebel, (1280), Department of Neurocognition, University of Sydney, Sydney, Australia Faculty of Psychology, Universiteit Maastricht, Maastricht, The Netherlands Thomas Carlstedt, (250), PNI-Unit, The Royal National Orthopaedic Hospital, Stanmore, United Kingdom, Gunnar Grant, (233), Department of Neuroscience, and Karolinska Institutet, Stockholm, Sweden Karolinska Institutet, Stockholm, Sweden Pascal Carrive, (393), Department of Anatomy, School Suzanne N. Haber, (676), Department of Pharmacol- of Medical Sciences, The University of New South ogy and Physiology, University of Rochester School Wales, Sydney, Australia of Medicine, Rochester, New York, USA Iain J. Clarke, (562), Prince Henry’s Institute of Medical Research, Melbourne, Australia Glenda Halliday, (267, 449), Prince of Wales Medical Research Institute, The University of New South Staffan Cullheim, (250), Department of Neuroscience, Wales, Sydney, Australia Karolinska Institutet, Stockholm, Sweden Patrick R. Hof, (915), Fishberg Research Center for Jose DeOlmos, (739), Instituo de Investigacion Medica Neurobiology, Department of Geriatrics and Adult “Mercedes y Martin Ferreyra”, Cordoba, Argentina Development, Mount Sinai School of Medicine, Richard L. M. Faull, (190), Department of Anatomy New York, USA with Radiology, Faculty of Medical and Health Sciences, The University of Auckland, Auckland, Gert G. Holstege, (1306), Department of Anatomy and New Zealand Embryology, Faculty of Medical Sciences, University of Groningen, Groningen, The Netherlands Simon C. Gandevia, (113), Prince of Wales Medical Research Institute, The University of New South Anja K. E. Horn, (479), Institute of Anatomy, Ludwig- Wales, Sydney, Australia Maximilian University Munich, Munich, Germany

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xiv CONTRIBUTORS

Jean-Pierre Hornung, (424), Institut de Biologie Fabiola Müller, (22), University of California School Cellulaire et de Morphologie, University of Lausanne, of Medicine, Davis, California, USA Lausanne, Switzerland Ralph E. Norgren, (1171), Department of Neural and Eva Horvath, (551), Department of Laboratory Medicine Behavioral Sciences, Hershey Medical Center, and Pathobiology, St. Michael’s Hospital, University Pennsylvania State University College of Medicine, of Toronto, Toronto, Ontario, Canada Hershey, Pennsylvania, USA Xu-Feng Huang, (267), Department of Biomedical Brian J. Oldfield, (562), Howard Florey Institute of Sciences, University of Wollongong, Wollongong, Experimental Physiology and Medicine, University Australia of Melbourne, Victoria, Australia Ricardo Insausti, (871), Department of Health Sciences, Ronan O’Rahilly, (22), University of California School School of Medicine, University of Castilla-La Mancha, of Medicine, Davis, California, USA Albacete, Spain Deepak Pandya, (950), Departments of Anatomy Jon H. Kaas, (1059), Department of Psychology, and Neurobiology, Boston University School of Vanderbilt University, Nashville, Tennessee, USA Medicine, Boston, Massachusetts, USA, and Havard Dae-Shik Kim, (1280), Center for Magnetic Resonance Neurological Unit, Beth Israel Hospital, Boston, Research, University of Minnesota, Minneapolis, Massachusetts, USA MN, USA George Paxinos, (267), Prince of Wales Medical Research George Kontogeorgos, (551), Department of Pathology, Institute, The University of New South Wales, Sydney, General Hospital of Athens, Athens, Greece Australia Yuri Koutcherov, (267), Prince of Wales Medical Research Gerard Percheron, (592), Institut National de la Santé Institute, The University of New South Wales, Sydney, et de la Recherche Medicale, Paris, France Australia Michael Petrides, (950), Montreal Neurological Institute, Kalman Kovacs, (551), Department of Laboratory and Department of Psychology, McGill University, Medicine and Pathobiology, St. Michael’s Hospital, Montreal, Quebec, Canada University of Toronto, Toronto, Ontario, Canada Joseph L. Price, (1197) Department of Anatomy and Fred H. Linthicum, Jr., (1241), Department of Histo- Neurobiology, Washington University School of pathology, House Ear Institute, Los Angeles, Medicine, St. Louis, Missouri, USA California, USA Thomas C. Pritchard, (1171), Department of Neural Giuseppe Luppino,(973), Dipartimento di Neuroscienze, and Behavioral Sciences, Hershey Medical Center, Sezione di Fisiologia, Università Di Parma, Parma, Pennsylvania State University College of Medicine, Italy Hershey, Pennsylvania, USA Jürgen K. Mai, (49), Institute of Neuroanatomy, Heinrich- Mårten Risling, (250) Department of Neuroscience, Heine University of Düsseldorf, Düsseldorf, Germany Karolinska Institutet, Stockholm, Sweden, and Massimo Matelli, (973), Dipartimento di Neuroscienze, Department of Defence Medicine, Swedish Defence Sezione di Fisiologia, Università Di Parma, Parma, Research Agency (FOI), Stockholm, Sweden Italy Clifford B. Saper, (513), Harvard Medical School, Michael J. McKinley, (562), Howard Florey Institute of Department of Neurology, Beth Israel Deaconess Experimental Physiology and Medicine, University Medical Center, Boston, Massachusetts, USA of Melbourne, Victoria, Australia Jean Schoenen, (190, 233), Department of Neuro- Jean K. Moore, (1241), Department of Neuroanatomy, anatomy and Neurology, University of Liège, Liège, House Ear Institute, Los Angeles, California, USA Belgium Michael M. Morgan, (393), Department of Psychology, Oscar U. Scremin, (1325), Department of Veterans Affairs, Washington State University, Vancouver, Washington, Greater Los Angeles Healthcare System, Los Angeles, USA California, USA Leonora J. Mouton, (1306), Department of Anatomy and Lucia Stefaneanu, (551), Department of Laboratory Embryology, Faculty of Medical Sciences, University Medicine and Pathobiology, St. Michael’s Hospital, of Groningen, Groningen, The Netherlands University of Toronto, Toronto, Ontario, Canada Lars Muckli, (1280), Department of Neurophysiology, Georg F. Striedter, (3), Department of Neurobiology Max-Planck Institute of Brain Research, Frankfurt, and Behavior, University of California at Irvine, Germany Irvine, California, USA FrontMatter.qxd 30/9/03 4:08 PM Page xv

CONTRIBUTORS xv

Brent A. Vogt, (915), Cingulum NeuroSciences Insti- Phil M. E. Waite, (95, 1093), Department of Anatomy, tute, Manlius, New York, USA, and Department of School of Medical Science, The University of New Neuroscience and Physiology, State University of South Wales, Sydney, Australia New York Upstate Medical University, Syracuse, Karin N. Westlund, (1125), Department of Anatomy New York, USA and Neurosciences, University of Texas Medical Lesley J. Vogt, (915), Cingulum NeuroSciences Insti- Branch, Galveston, Texas, USA tute, Manlius, New York, USA, and Department of William D. Willis, Jr., (1125), Department of Anatomy Neuroscience and Physiology, State University of and Neurosciences, The University of Texas New York Upstate Medical University, Syracuse, Medical Branch, Galveston, Texas, USA New York, USA Karl Zilles, (973, 997), Institute of Medicine, Research Jan Voogd, (321), Department of Neuroscience, Erasmus Center Jülich, and C. & O. Vogt-Institute of Brain University Rotterdam, Rotterdam, The Netherlands Research, University of Düsseldorf, Düsseldorf, Germany FrontMatter.qxd 30/9/03 4:08 PM Page xvii

Preface

Neuroscience comprises increasingly diverse fields The present book gives an authoritative account of ranging from molecular genetics to neurophilosophy. the structure of the human brain tempered by func- The common thread between all these fields is the tional considerations. The task of describing all parts structure of the human nervous system. Knowledge of the nervous system in the context of modern on the structure, connections and function of the brain hypotheses of structural and functional organization of experimental animals is readily available. On the would be overwhelming for a single individual. We other hand the structure of the human brain was studied have, therefore, asked scientists with knowledge and by the classical anatomists and their work is difficult affection for their research areas to contribute to this to retrieve. With the current intense interest in the edited volume. We trust that the combined effort of structure of the human brain engendered particularly contributors to The Human Nervous System 2e will do by imaging studies, groups of scientists familiar with justice to the data and concepts available in our field the classical works, but who are also versed in modern while stimulating the readers’ brains, arousing curiosity neuroscience technologies, have commenced human and providing a framework for thinking. brain studies. George Paxinos and Jürgen K Mai Sydney and Düsseldorf

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