The Central Nervous System of Vertebrates Volume 1

The Central Nervous System of Vertebrates Volume 1 «Le systeme nerveux est au fond tout l'animal; les autres systemes ne sont la que pour le servir ou pour l'entretenir... » GEORGES CUYlER (1812)

»Hirnanatomie allein getrieben ware eine sterile Wissenschaft. Erst in dem Momente, wo man die Frage nach dem Verhaltnis der anatomischen Struktur zu der Funktion aufwirft, gewinnt sie Leben.« LUDWIG EDINGER (1908)

"Our primary interest is in the behavior of the living body, and we study brains because these organs are the chief instruments which regulate behavior." CHARLES }UDSON HERRICK (1948)

Springer-Verlag Berlin Heidelberg GmbH R. NIEUWENHUYS H. J. TEN DoNKELAAR C. NICHOLSON

The Central Nervous System of Vertebrates Volume 1

With Chapters in Cooperation with:

W. J. A. J. SMEETS H. WICHT

With 474 Figures and 16 Tables

~Springer Additional material to this book can be downloaded from http://extras.springer.com

ISBN 978-3-642-62127-7 ISBN 978-3-642-18262-4 (eBook) DOI 10.1007/978-3-642-18262-4

Libary of Congress Cataloging-in-Publication-Data Nieuwenhuys, R., 1927- The central nervous system of vertebrates 1 R. Nieuwenhuys, H.J. ten Donkelaar, C. Nicholson : with contributions by J.L. Dubbeldam ... [et al.]. p. cm. Includes bibliographical references.

1. Central nervous system - Anatomy. 2. Vertebrates - Anatomy. 3. Anatomy, Comparative. 4. Neuroanatomy. 1. Donkelaar, H.J. ten (Hendrik Jan), 1946-, II. Nicholson, Charles. III. Title. [DNLM: 1. Central Nervous System - anatomy & histology. 2. Anatomy, Comparative. 3. Vertebrates - anatomy & histology. WL 300 NB82ca 1997) QM451.N498 1997 573.8'616- dc21 DNLM/DLC for Library of Congress

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© Springer-Verlag Berlin Heidelberg 1998 Originally published by Springer-Verlag Berlin Heidelberg New York in 1998 The use of general descriptive names, registered names, trademarks, etc., in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the rele• vant protective laws and regulations and therefore free for general use. Product liability: The publishers cannot guarantee the accuracy of any information about dosage and application contained in this book. In every individual case the user must check such informa• tion by consulting the relevant literature. Production: PRO EDIT GmbH, Heidelberg Typesetting: Mitterweger Werksatz GmbH, Plankstadt Cover Design: Erich Kirchner, Heidelberg SPIN: 10087711 27/3136- 4 3 2 1 O- Printed on acid-free paper Preface

The plans for this book began to form more than 30 years ago when the first author was head of the section of comparative neuroanatomy at the Central Institute for Brain Research (now called the Institute for Brain Research) in Amsterdam, The Netherlands. Working there implied that one was part of a tradition since research at the "Brain Institute" - as it was usually known - had focussed exclusively on comparative neuroanatomy for 50 years. The first director of the institute, Cornelius Ubbo Ariens Kappers (1877-1946) held this position from the opening of the institute in 1909 until his death and was a disciple and associate of Ludwig Edinger (1855-1918), one of the founders of comparative neuroanatomy. Ariens Kappers had become, during his long director• ship, a neuroanatomist of international fame. His books included the monumental Vergleichende Anatomie des Nervensystems (1920-1921) and, in collaboration with G. Carl Huber and Elizabeth C. Crosby, The Comparative Anatomy of the Nervous System of Vertebrates (1936). His collected reprints, encompassing seven large volumes, his library and his enormous collection of preserved and sectioned brains, were all emphatically present in the institute. The research of Ariens Kappers and his numerous associates was almost exclu• sively based on non-experimental material which, after fixation, was embedded in celloidin, sectioned at 20 mm, stained with the Weigert-Pal method to reveal my• elinated fibres, and counterstained with paracarmine for cell bodies. Such material has obvious limitations for analysis of the microstructure and, looking back, one can only marvel that so much could be achieved with material of this kind. As an aside, it is astonishing how much aesthetic appeal this type of material provides, with its blue-black fibre tracts contrasting with the pink masses of the cells. By the 1960s "Kappers, Huber and Crosby" still remained the only available work on comparative neuroanaomy, and, indeed, it was reprinted in 1967 by the Hafner Publishing Company to try to satisfy the continuing need for such a com• prehensive study. But the original work was obviously outdated by then and, fur• thermore, it had always been limited somewhat as a systematic treatise of compar• ative neuroanatomy, since it neither attempted to describe the principles of the sub• ject nor did it set the chosen species in any wider zoological context. Finally, the limitations of Ariens Kappers' histological archive mandated that any new compre• hensive survey of vertebrate comparative neuroanatomy would have to be based on new histological material. These factors led the first author to plan the present work. In the early 1970s Charles Nicholson was invited to join the project. Some years earlier he and Rudolf Nieuwenhuys had collaborated on a study of the structure of the mormyrid cerebellum. When this research was published, it was accompanied by a comprehensive review of what was then known about the function of the elec• trosensory system in fishes (which was thought to be related to the hypertrophy of the mormyrid brain). It was originally planned that the present work would follow a somewhat similar format, combining a description of structure with a functional commentary, at an introductory level. Just as with other living material, the book VI Preface grew vigorously during its prolonged period of gestation. The book gradually developed into a reference work with the emphasis on structure and a more limited coverage of function. There were several reasons for this. First, neurophysiological research is even more biased towards mammals than neuroanatomy so that any comparative survey would be extremely fragmentary in its coverage. Second, a true comparative neurophysiology has never been attemped; rather, neurophysiologists have selected preparations which provide unusual opportunities for studying a par• ticular cell or system. In fact there are several groups, including the Myxinoids, the Brachiopterygians and the Dipnoans, which have been completely neglected by neurophysiologists so far. For all of these reasons the original "design" of the book could not be realized. However, the principle that structure and function are merely facets of a single real• ity is retained. For instance, the recent combined structural and functional research on the central nervous system of the lamprey, focussing on the control of locomo• tion, has been treated in detail and accounts in part for the length of Chap. 10. As the extent of the work and its dominant structural content became more clear, it was evident that the first author could not hope to complete the anatomical surveys in a reasonable timeframe without the assistance of a second comparative anatomist. Consequently, during the initial phase of the preparation of the text (i.e. in the early 1980s) Glenn Northcutt (Scripps Institute of Oceanography, San Diego, Calif., USA) was invited to join the project. During that phase he read early ver• sions of Chaps. 9-17 and provided valuable comments. Although keenly interested, he felt that the format of the work had been determined already so that it would be difficult for him to make a real and creative contribution and, so far as the book was concerned, our paths diverged. Mary Sue Northcutt, however, was kind enough to edit initial versions of several chapters, and we expect that even the final ver• sions will bear traces of her unequalled editorial skill. We are sure that the present work would have benefited from Glenn Northcutt's vast knowledge of comparative neuroanatomy. Some consolation was offered by the fact that in the final phase of the production of this book, his associate, Helmut Wicht, from the Department of Anatomy of the J.W. Goethe University in Frankfurt am Main, Germany, accepted our invitation to update the chapter on Myxinoids. We felt justified in appealing to Helmut Wicht for this task, because it was mainly as a result of his research that the said chapter had become outdated! Fortunately, another accomplished comparative neuroanatomist, in the person of Hans ten Donkelaar, was willing to join the project and provide the essential help to see this project through. Since completing his thesis research under the direction of Rudolf Nieuwenhuys, Hans ten Donkelaar had focussed his attention on amphi• bians and reptiles and was ideally suited to cover these topics in the present work. He has also been invaluable in working with the first author on the day-to-day mechanics of the production of material for the book, since both authors worked at the same institution for many years, while the third author, located in the United States, has interacted by means of trans-Atlantic visits which have become too numerous to count anymore. Finally, as the scope of the book continued to expand, and more to the point, the scientific literature was generated at an ever-increasing pace, it became necessary to find assistance with specific chapters which will be further detailed below. In 1968 the first author moved to the Department of Anatomy at the University ofNijmegen, The Netherlands, where he then had at his disposal the requisite facil• ities for the realization of a new book on comparative vertebrate anatomy. Some of the most important supplementary elements were: 1. A number of highly competent technicians, among them Marion Cremers• Cornelisz, Carla de Vocht-Poort and Nelly Driessen-Verijdt, were available to prepare serial sections through the brains and selected parts of the spinal cord of representative species of all vertebrate classes, with Nissl and Kluver-Barrera stains and the silver-impregnation of Bodian, as the standard techniques. Preface VII

2. The same technicians and their colleagues Roelie de Boer-van Huizen, Henk Joosten and Theo Hafmans also kept pace with the stream of new anatomical techniques, including the various anterograde and retrograde tracer methods, histofluorescence and immunohistochemistry. Electronmicroscopy also found wide application. Theo Hafmans deserves special mention, since he was respon• sible for much of the photography at the light microscopical level. 3. The presence of an illustration department (founded by Prof. H.J. Lammers) with by no less than ten competent illustrators led by Christiaan van Huijzen and later by Joep de Bekker. Almost all of the half-tone drawings, illustrating the gross anatomy of the brains of 17 species, and the India-ink drawings showing the microscopical structure at representative levels of the brains and spinal cords of 18 species, which form the central core of the present work, were fortu• nately prepared before stringent budget cuts essentially brought the illustration department to an end. The fact that one of the artists, Mr. J. P. M. Maas, long after his retirement and until the conclusion of the project, continued preparing high quality illustrations for the work, deserves a special mention. Our grateful thanks are also due to Christiaan van Huijzen, who prepared the accompanying posters 1-3. Roel Seidell prepared three sets of drawings for the gross anatomy series. Most of the drawings for Chaps. 18-20 were done by Marlu de Leeuw, who also prepared posters 4 and 5. The final phase of this project would not have been possible without the gener• ous support of Mr. A. Dousma (Audiovisual Group, University of Nijmegen) and of the Department of Anatomy and Embryology (University of Nijmegen). During the period 1992-1997, Professor D.F. Swaab, the present director of the Netherlands Institute for Brain Research, Amsterdam, kindly put the facilities of this Institute (where it all began!) at the disposal of the first author. The crucial help of Mr. G. van der Meulen, photographer at that Institute is especially acknowledged. 4. Without adequate secretarial assistance a comprehensive project of this kind could not be accomplished. Four successive, competent and highly devoted se• cretaries, Trudy van Son-Verstraeten, Margaret Shak Shie, Marion van de Coeve• ring and Inge Eijkhout, have lent their support to the project. An essential element leading to the present work was the comprehensive pro• gramme of comparative neuroanatomical research which was planned and realized in Nijmegen. This encompassed all major groups of vertebrates, except for birds and mammals, and within the framework of this programme, numerous doctoral theses were prepared. As mentioned above, the second author of the present work was one of the first "promovendi" in this programme of research at Nijmegen. Two other fundamental and important chapters also originated with work begun as Ph.D. projects. These are the chapter on "Cartilaginous Fishes" by Wil Smeets, Department of Anatomy, Free University, Amsterdam, and the chapter on "Holo• steans and Teleosts" by Hans Meek and Rudolf Nieuwenhuys, Department of Anatomy, University of Nijmegen. Thus, the research material for most of the required animal groups were covered in the course of the highly productive investigations and using the excellent facil• ities at the University of Nijmegen. Two groups, the birds and the mammals, offered problems, however. Work on the central nervous system of birds had never been included in the Nijmegen research programme. We were fortunate, however, to find Jaap Dubbeldam (Professor of Neurobehavioral Morphology, State Univer• sity Leiden, The Netherlands), an expert in this field, willing to prepare the chapter on the brain and spinal cord of this group. The problems with the mammals were primarily quantitative in nature. The body of knowledge on the central nervous system of this group of animals has grown to such enormous proportions that comprehensive surveys of current knowledge of the structure of brain and spinal cord of a single species can be pro• vided only by a large team of experts. To take three recent examples: The Rat Ner- VIII Preface vous System, 2nd edn, (1995), edited by G. Paxinos includes 22 contributions by at least 60 authors and covers 1136 pages. The Cerebral Cortex (1984-1995) edited by A. Peters and E.G. Jones spans 12 volumes with an average of 500 pages per volume and the contributors are too numerous to count. Finally, Comparative Neurobi• ology in Chiroptera, (1996) by G. Baron, H. Stephan and H. Frahm, is devoted solely to bats, yet comprises three volumes and 1596 pages! It was tempting to leave out the mammals from the present work, because of the difficulties they presented, but we felt that a book on comparative vertebrate neu• roanatomy would be incomplete without this group. It was evident, however, that within the limits set and repeatedly revised upwards over the years, for the present work only a concise and eclectic survey of the structure of the mammalian brain and spinal cord, with emphasis on comparative aspects, could be included. Very fortunately Jan Voogd, head of the Department of Anatomy, Erasmus University Rotterdam, The Netherlands, and Paul van Dongen, a former collaborator at the bepartment of Anatomy Nijmegen, now scientific editor, Department of Clinical Research at Janssen-Cilag, Tilburg, the Netherlands, were kind enough to cooperate with us on this part of the project and provide the essential, but succinct, coverage that we desired. Paul van Dongen also provided a concise, yet comprehensive, chapter on brain size in vertebrates. As noted above, and emphasised wherever possible in this work, structure and function belong together and should be studied jointly wherever possible; but addi• tionallevels of conceptual integration are required too. From the perspective of the theory of evolution, the functioning brain forms only the intermediate level in a continuum extending between two ultimate frontiers, the abiotic and biotic envi• ronment, on one hand, and the genetic reservoir of interbreeding populations, on the other. This means that genetic and comparative developmental neurobiology, neuroethology and neuroecology ultimately should be included in comparative neuroscience. Genetics, ethology and ecology are all flourishing fields of science. The comparative approach has rarely been very central in these field of research; however, it is hoped that this book will pave the way to some extent for these new and highly promising provinces of the neurosciences. In concluding this preamble the invaluable editing assistance of Ms. S. Bakker, M.Sc., is especially acknowledged, and, finally, we extend our most sincere thanks to the publishing house of Springer-Verlag and their staff- especially Dr. R. Lange, Mr. R.-P. Fischer, Mr. E. Kirchner, Ms. A. Clauss, Ms. S. Sundell and Ms. G. Wiegel, PRO EDIT GmbH, for their kind help during the preparation of this book.

Abcoude/Nijmegen/New York, August 1997 RUDOLF NIEUWENHUYS HANS J. TEN DoNKELAAR CHARLES NICHOLSON Purpose and Plan

The purpose of this book is threefold: (1) to set forth the general foundations, con• cepts and principles of comparative neuroanatomy, (2) to present a comprehensive survey of our current knowledge of the structural organisation of the brain and spinal cord of the various groups of vertebrates, and ( 3) to provide some ideas for future research. The plan of the book reflects these goals. The chapters forming the general part attempt to define the context in which the more detailed later chapters were for• mulated. Today, neuroscience is a burgeoning field in which ideas are changing rapidly. While we hope that the main body of this work will remain useful for many years, we recognise that as time passes it will be difficult for those referring to it to envisage the frame of reference of the authors. One objective of these general chapters is to indicate this frame. A second goal is to provide some definitions so that when the reader later encounters terms or concepts that are unfamiliar, the general section may be referred to for clarification. The special character of Chap. 6 should be emphasised. Although numerous contributions to the methodology of comparative neuroanatomy have been made during the last century, the synthesis presented in the second part of that chapter is new. The reader should not expect, however, that all of the structural interpreta• tions discussed in the second, specialised part are realised in the light of the methodology outlined in Chap. 6. Rather, the methodology presented is offered as a framework for future research. The same holds true for the final section of Chap. 6. The programme of comparative neuroanatomy outlined there is not an introduc• tion to the voluminous specialised part, in the sense that this part represents the realisation of such a programme. Most of the book, i.e. the presentation of a com• prehensive survey of our current knowledge of the vertebrates, is realised in the large, specialised part of the work. Our intention here was to achieve a balanced survey of our current knowledge on the brain and spinal cord of the various groups and not to profile the results of our own research. Nevertheless, all of these chapters have been written by authors with a first-hand knowledge of the central nervous system of the pertinent group of animals. In the preparation of the specialised parts many choices had to be made. The first choice was between arranging the data according to the groups of animals or according to the divisions of the central nervous system, i.e. the spinal cord, the rhombencephalon and so on. We decided to follow the first approach because it would enable us to begin each chapter with some introductory notes on the ani• mals and their lifestyle, before moving on to the central nervous system. Moreover, readers who want to study the central nervous system region by region will find our format easy to use, because each chapter is organized in a similar way and begins with a table of contents, making it simple to extract the relevant compara• tive information on any chosen brain structure. Other important choices included the species to be dealt with and the selection of the illustrations. For a discussion of these aspects the reader is referred to Chap. 8. We only note here that the pictorial central theme of all chapters of the special- X Purpose and Plan ised part is formed by (1) drawings of entire animals, (2) simple illustrations show• ing the brain in position, (3) four standard views of the brains, showing their ma• crostructure, and (4) drawings of sequences of transversely oriented microscopical sections through the spinal cord and brain of a number of species. The third and final purpose of the book, i.e. to provide a basis for and to indicate some of the prospects for future comparative neuroanatomical research, is evident in all parts of the work. As already mentioned, a conceptual basis and programme of future research is described in Chap. 6. The separate chapters of the specialised section, by recording what is known of the structural organisation of the central nervous system of the various groups of vertebrates, also serve to highlight the many gaps in our knowledge. Finally, the concluding chapter briefly surveys the major fields and "levels" of current comparative neurobiology and indicates many of the goals that lie in the future. Acknowledgements for the Use of Illustrations

Thanks for the use of illustrations are due to the following sources. Acknowledg• ments to the authors who were so kind to give their permission to use figures, are made in the figure legends. Academic Press, London Gans C (ed) Biology of the Reptilia, Vols 9 and 10 (1979} Academic Press, San Diego Paxinos G (ed) The Rat Nervous System, 2nd Ed (1995} Akademie Verlag, Berlin journal fur Hirnforschung American Association for the Advancement of Science, Washington DC Science The American Physiological Society, Bethesda journal of Neurophysiology American Society of Zoologists, Lawrence, Kansas American Zoologist ANKHO International Inc, Fayetteville, NY Brain Research Bulletin Johann Ambrosius Barth, Leipzig Nova Acta Leopoldina Brill, Leiden Netherlands journal of Zoology Cambridge University Press, Cambridge, UK The Behavioral and Brain Science; The Journal of Physiology Cell Press, Cambridge, MA Neuron Clarendon Press, Oxford Benton MJ (ed) The Phylogeny and Classification of the Tetrapods, Voll (1988) Current Biology Ltd, London Current Opinions in Neurobiology Elsevier Science, Amsterdam Brain Research; Brain Research Reviews; Progress in Brain Research Elsevier Science Ireland, Shannon Neuroscience Letters Elsevier Science Inc, New York Journal of Chemical Neuroanatomy XII Acknowledgements for the Use of Illustrations

Elsevier Science Ltd, Kidlington, UK Neuroscience; Progress in Neurobiology; Trends in Neurosciences Gustav Fischer Verlag, Jena - Stuttgart Fortschritte der Zoologie; Zoologisches Jahrbuch (Physiologie) WH Freeman and Co, New York Carroll RL, Vertebrate Paleontology and Evolution (1988) S Karger AG, Basel Acta Anatomica; Brain, Behavior and Evolution Macmillan Magazines Ltd, London Nature The University of Michigan Press, Ann Arbor Fish Neurobiology (Vol1, Northcutt RG, Davis RE, eds; Vol 2, Davis RE, Northcutt RG, eds, 1983) National Institute of Mental Health, Rockville, Maryland Greenberg N, MacLean PD (eds) Behavior and Neurobiology of Lizards (1978) The New York Academy of Sciences, New York Annals of the New York Academy of Sciences Oxford University Press, New York Shepherd GM (ed) The Synaptic Organization of the Brain, 3rd ed (1990) Oxford University Press, Oxford European Journal of Neuroscience Plenum Press, New York Ebbesson SOE (ed) Comparative Neurology of the Telencephalon (1980); Jones EG, Peters A (eds) Cerebral Cortex, Vol8A (1990) The Royal Society, London Philosophical Transactions of the Royal Society (London), Section B Science Reviews Ltd, Northwood, Middlesex Scientific Progress, Oxford Sinauer Associates Inc, Sunderland, MA Hille B (ed) Ionic Channels of Excitable Membranes, 2nd ed (1992) Society for Neuroscience, Washington DC The Journal of Neuroscience Springer Verlag, Berlin-Heidelberg-New York Advances in Anatomy, Embryology and Cell Biology; Anatomy and Embryology; Cell and Tissue Research; Experimental Brain Research; Journal of Comparative Physiol• ogy A: Studies in Brain Function Swets Publishing Service, Lisse, the Netherlands Acta Morphologica Neerlando-Scandinavica Georg Thieme Verlag, Stuttgart Hassler R, Stephan H (eds) Evolution of the Forebrain (1966) John Wiley & Sons, New York Ulinski PS, Dorsal Ventricular Ridge (1983); Kettenmann H, Grantyn R (eds) Prac• tical Electrophysiological Methods (1992) The American Journal of Anatomy; The Journal of Comparative Neurology; Journal of Morphology; Journal of Neurobiology List of Contributors

DUBBELDAM, J. 1. Van der Klaauw Laboratory, University of Leiden, P. 0. Box 9516, 2300 RA Leiden, The Netherlands

MEEK, J. Department of Anatomy & Embryology, University of Nijmegen, P. 0. Box 9101, 6500 HB Nijmegen, The Netherlands

NICHOLSON, C. Department of Physiology & Biophysics, New York University Medical Center, 550 First Avenue, New York, 10016 NY, USA

NIEUWENHUYS, R. Papehof 25, 1391 BD Abcoude, The Netherlands

SMEETS, W. J, A. J. Department of Anatomy & Embryology, Free University, Vander Boechorststraat 7, 1081 BT Amsterdam, The Netherlands

TEN DONKELAAR, H. J, Department of Anatomy & Embryology, University of Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands

VAN DONGEN, P. A. M. Linge 9, 5032 EV Tilburg, The Netherlands

VOOGD, J. Department of Anatomy, Erasmus University Rotterdam, P. 0. Box 1738, 3000 DR Rotterdam, The Netherlands

WICHT, H. Klinikum der J.- W.-Goethe-Universitat, Zentrum der Morphologie, University of Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt am Main, Germany Contents

VOLUME 1

Preface ...... v Purpo e and Plan ...... IX Acknowledgements for Figures . XI

I. GENERAL INTRODUCTORY PART

Chapter I Structure and Function of the Cellular Elements in the Central Nervous Sy tern C. NICHOL ON ...... Chapter 2 Structure and Organisation of Centres R. Nt EUWENHUYS ...... 25 Chapter 3 Structure and Organisation of Fibre Systems R. NtBUWENHUYS ...... 113 Chapter 4 Morphogenesis and General Structure R. Nt EUWE HUYS ...... 158 Chapter 5 Histogenesis R. NtEUWENHUYS 229 Chapter 6 Comparative Neuroanatomy Place, Principle and Programme R. NIEUWE HUYS ...... 273 Chapter 7 Note on Techniques H. J. TEN OONKELAAR and C. NICHOLSO 327

II. SPECIALISED PART

Chapter 8 Introduction R. NIEUWE HUYS 357 Chapter 9 Amphioxus R. NIEUWENHUYS 365 Chapter 10 Lampreys, Petromyzontoidea R. Nrsuws HUYS and C. NtCHOLSO 397 Chapter 11 Hagfishes, Myxinoidea H. WICHT and R. NIEUWENHUYS 497 Chapter 12 Cartilaginous Fishes W. J. A. J. SMEETS . .. . 551 Chapter 13 Brachlopterygian Fishes R. NtEUW£ HUYS .. 655 Chapter 14 Chondrostean Fishes R. NIEUWE HUYS .. 701 XVI Contents

VOLUME 2

II. SPECIALISED PART (Contd.)

Chapter 15 Holosteans and Teleosts J. MEEK and R. NIEUWENHUYS ...... 759 Chapter 16 Lungfishes R. NIEUWENHUYS ... , , ...... , ...... , , , . 939 Chapter 17 The Coelacanth, Latimeria chalumnae R. NIEUWENHUYS ...... 1007 Chapter 18 Urodeles H. J, TEN DONKELAAR ...... 1045 Chapter 19 Anurans H. J, TEN DONKELAAR ... , , ..... , ...... 1151 Chapter 20 Reptiles H. J, TEN DONKELAAR ...... , ...... 1315

VOLUME 3

II. SPECIALISED PART (Contd.) Chapter 21 Birds J, L. DUBBELDAM . . . 1525 Chapter 22 Mammals J. VOOGD, R. NIEUWENHUYS, P. A. M. VAN DONGEN and H. J, TEN DONKELAAR ...... 1637

III. GENERAL CONCLUDING PART Chapter 23 Brain Size in Vertebrates P. A. M. VAN DONGEN ...... 2099 Chapter 24 The Meaning of It All R. NIEUWENHUYS, H. J, TEN DONKELAAR and C. NICHOLSON . . 2135

Subject Index ...... 2197 I. GENERAL INTRODUCTORY PART

1 Structure and Function of the Cellular Elements in the Central Nervous System . . . . . 1

2 Structure and Organisation of Centres 25

3 Structure and Organisation of Fibre Systems 113

4 Morphogenesis and General Structure 158

5 Histogenesis ...... 229

6 Comparative Neuroanatomy: Place, Principles andProgrnmme ...... 273

7 Notes on Techniques 327 The Central Nervous System of Vertebrates Volume 2 R. NIEUWENHUYS H. J. TEN DONKELAAR C. NICHOLSON

The Central Nervous System of Vertebrates Volume 2

With a Chapter in Cooperation with:

J. MEEK

With 439 Figures and 10 Tables

Springer Contents

VOLUME 1

Preface ...... V Purpose and Plan ...... IX Acknowledgements for Figures XI

I. GENERAL INTRODUCTORY PART

Chapter 1 Structure and Function of the Cellular Elements in the Central Nervous System C. NICHOLSON ...... Chapter 2 Structure and Organisation of Centres R. NIEUWENHUYS ...... 25 Chapter 3 Structure and Organisation of Fibre Systems R. NIEUWENHUYS ...... 113 Chapter 4 Morphogenesis and General Structure R. NIEUWENHUYS ...... 158 Chapter 5 Histogenesis R. NIEUWENHUYS 229 Chapter 6 Comparative Neuroanatomy Place, Principles and Programme R. NIEUWENHUYS ...... 273 Chapter 7 Notes on Techniques H. J. TEN DONKELAAR and C. NICHOLSON . 327

II. SPECIALISED PART

Chapter 8 Introduction R. NIEUWENHUYS 357 Chapter 9 Amphioxus R. NIEUWENHUYS 365 Chapter 10 Lampreys, Petromyzontoidea R. NIEUWENHUYS and C. NICHOLSON 397 Chapter 11 Hagfishes, Myxinoidea H. WICHT and R. NIEUWENHUYS 497 Chapter 12 Cartilaginous Fishes W. J. A. J. SMEETS .... 551 Chapter 13 Brachiopterygian Fishes R. NIEUWENHUYS .. 655 Chapter 14 Chondrostean Fishes R. NIEUWENHUYS .. 701 VIII Contents

VOLUME 2

II. SPECIALISED PART (Contd.)

Chapter 15 Holosteans and Teleo ts J. MEEK and R. NIEUWENHUYS . 759 Chapter 16 Lungfishes R. NIEUWE HUYS •. .. ..•. 939 Chapter 17 The Coelacanth, Latimeria chalumnae R. NIEUWENHUYS ...... 1007 Chapter 18 Urodeles H. J. TEN Do KELAAR. 1045 Chapter 19 Anurans H. J. TE DONKELAAR. 1151 Chapter 20 Reptiles H. J. TEN DONKELAAR . 1315

VOLUME 3

II. SPECIALISED PART (Contd.) Chapter 21 Birds J. L. DUBBELDAM ...... 1525 Chapter 22 Mammals J. VOOGD, R. NIEUWENHUYS, P. A. M. VAN DONGEN and H. J. TEN DONKELAAR...... 1637

III. GENERAL CONCLUDING PART Chapter 23 Brain Size in Vertebrates P. A. M. VAN DONGEN ...... 2099 Chapter 24 The Meaning of It All R. NIEUWENHUYS, H. J. TEN DONKELAAR and C. NICHOLSON 2135

Subject Index ...... 2197 II. SPECIALISED PART (Contd.)

15 Holosteans and Teleosts 759

16 Lungfishes ...... 939

17 The Coelacanth, Latimeria chalumnae 1007

18 Urodeles 1045

19 Anurans 1151

20 Reptiles .. 1315 The Central Nervous System of Vertebrates Volume 3 R. NIEUWENHUYS H. J. TEN DONKELAAR C. NICHOLSON

The Central Nervous System of Vertebrates Volume 3

With Chapters in Cooperation with:

J.L. DUBBELDAM P.A.M. VAN DONGEN AND J. VOOGD

With 405 Figures and 23 Tables

Springer Contents

VOLUME 1

Preface ...... v Purpose and Plan ...... IX Acknowledgements for Figures XI

I. GENERAL INTRODUCTORY PART

II. SPECIALISED PART

Chapter 8 Introduction R. NIEUWENHUYS 357 Chapter 9 Amphioxus R. NIEUWENHUYS 365 Chapter 10 Lampreys, Petromyzontoidea R. NIEUWENHUYS and C. NICHOLSON 397 Chapter 11 Hagfishes, Myxinoidea H. WICHT and R. NIEUWENHUYS 497 Chapter 12 Cartilaginous Fishes w. J. A. J. SMEETS . . . . 551 Chapter 13 Brachiopterygian Fishes R. NIEUWENHUYS .. 655 Chapter 14 Chondrostean Fishes R. NIEUWENHUYS . . 701 VIII Contents

VOLUME 2

II. SPECIALISED PART (Contd.)

Chapter IS Holosteans and Teleosts J. MEEK and R. NrEUWENHUYS 759 Chapter 16 Lungfishes R. NIEUWENHUYS ...... 939 Chapter 17 The Coelacanth, Latimeria chalumnae R. NIEUWENHUYS ...... 1007 Chapter 18 Urodeles H. J. TEN DONKELAAR 1045 Chapter 19 Anurans H. J. TEN DONKELAAR 1151 Chapter 20 Reptiles H. J. TEN DONKELAAR 1315

VOLUME 3

II. SPECIALISED PART (Contd.) Chapter 21 Bird j. L. DUBBELDAM 1525 Chapter 22 Mammals J. VooGo, R. NIEUWE Huvs, P. A. M. VAN DoNGEN and H. J. TEN Do KELAAR ...... 1637

III. GENERAL CONCLUDING PART Chapter 23 Brain Size in Vertebrates P. A. M. VAN Do GEN ...... 2099 . Chapter 24 The Meaning of It All R. IEUWENHUYS, H.}. TE Do KELAAR and C. NICHOLSO 2135

Subject Index 2197 II. SPECIALISED PART (Contd.)

21 Birds ...... 1525

22 Mammals ...... 163 7