The Central Nervous System of Cartilaginous Fishes
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2 WIA.J. Smeets B.L. Roberts R. Nieuwenhuys The Central Nervous System of Cartilaginous Fishes Structure and Functional Correlations With 51 Figures in the Text and 139 Figures in the Atlas Springer-Verlag Berlin Heidelberg New York 1983
3 WILHELMUS J.A.J. SMEETS Former Assistant of Department of Anatomy, University of Nijmegen, The Netherlands Prof. Dr. RUDOLF NIEUWENHUYS Professor ofneuroanatomy, Department of Anatomy, University of Nijmegen, The Netherlands Dr. BARRY L. ROBERTS Member of the Staff of the Laboratory of The Marine Biological Association, Plymouth, England ISBN-13: e-isbn-13: DOI: / Library of Congress Cataloging in Publication Data. Smeets, W.J.A.J. (Wilhelmus J.A.J.), The central nervous system of cartilaginous fishes. Bibliography: p. - Inc1udes index. 1. Nervous system-fishes. 2. Chondrichthyes. 3. Central nervous system. I. Nieuwenhuys, R., Roberts, B.L. (Barry L.), III. Title. [DNLM: 1. Fishes-Anatomy and histology. 2. Fishes-Physiology. 3. Central nervous system-anatomy and histology. 4. Central nervous system-physiology. QL S637c]. QL638.6.S ' This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying machine or similar means, and storage in data banks. Under 54 of the German Copyright Law where copies are made for other than private use, a fee is payable to "Verwertungsgesellschaft Wort" Munich. by Springer-Verlag Berlin Heidelberg 1983 Softcover reprint of the hardcover I st edition 1983 The use of 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 relevant protective laws and regulations and therefore free for general use. Reproduction of the illustrations: G. Dreher GmbH, Stuttgart Typesetting, printing and bookbinding: Universitätsdruckerei H. Stürtz AG, Würzburg. 2131/
4 Preface Although a large body of data about the structure of the central nervous system of cartilaginous fishes has now been accumulated, a systematic survey of the neuromorphology of this, in so many respects, highly interesting group of animals is lacking. The present book is an effort to fill this gap. The information provided is derived partly from the literature and partly from original observations based on our own material. We have attempted to present a complete review of the relevant literature of the last 25 years, but the earlier literature has also been thoroughly scrutinized. Wherever possible we have commented on the functional significance of the various structures. The information available in the literature has been incorporated with our own findings from a detailed study of four species, the sharks Squalus acanthias and Scyliorhinus canicula, the ray Raja clavata and the holocepha Ii an Hydrolagus collei. Although these species do not reflect the total range of cartilaginous fishes they do exemplify the main features of the major groups. The book is divided into two parts: text and atlas. In the first part some brief general introductory chapters are followed by chapters dealing with the major divisions of the central nervous system: spinal cord, brain stem, cerebellum, tectum mesencephali, diencephalon and telencephalon. The text illustrations include photomicrographs and drawings of characteristic structures, some of which have been derived from the literature. A pictorial survey of what is known of the fibre connections in the chondrichthyan brain is provided by a series of diagrams projected onto the brain of Scyliorhinus. In the final chapter of the first part we have attempted to foster further research by indicating the numerous gaps in our knowledge of the structural organization of the central nervous system of cartilaginous fishes. In the second part of the book we present sets of standard illustrations of the four species studied. For each species these include (a) a diagrammatic median section through the brain, (b) a topological chart showing the disposition of the ventricular sulci and the cell masses in the brain stem, (c) topographical reconstructions of the cell masses in brain stem, diencephalon and telencephalon, and (d) sequences of photomicrographs of transversely oriented sections of the brain. It may be expected that these sets of figures will provide initial guidance in experimental studies on the brain of cartilaginous fishes. Our work has been generously supported by the Medical Faculty of the University of Nijmegen and the Laboratory of the Marine Biological Association, Plymouth, and we are grateful to many of our colleagues in these
5 VI Preface institutes for their assistance. In particular we have been helped by the excellent histological expertise given by Mrs. Nellie Driessen-Verijdt, Mrs. Carla de Vocht-Poort and Mrs. Tonny Smeulders-van Wezel, who prepared the various series on which the atlas is based. The elasmobranch brains were obtained by us at Plymouth, but the Hydrolagus material from North America was collected for us by Dr. Christine Jaeger. The drawings were provided by Mr. Chr. van Huijzen, Mr. W. Maas, Mr. J. Konings and, especially by Mr. J. Russon, whereas the text photomicrographs were prepared by Mr. A.T.A. Reynen. Our special thanks should be given to Mr. Shimon Paniry of the Free University of Amsterdam for all the excellent photomicrographs included in the atlas. We are also very appreciative of the sustained secretarial assistance given by Miss Margaret Sjak Shie throughout the preparation of the book. Furthermore, we wish to thank the following publishers for permission to reproduce illustrations from their journals: Academic Press, Alan R. Liss, Elsevier/North-Holland Biomedical Press, Karger, Springer-Verlag and The Royal Society, London. Finally, the authors thank Dr. K. F. Springer, Mrs. Th. Deigmoller, Dr. D. Czeschlik and Mr. E. Kirchner of the publishing house of Springer for their help during the publication of this book. Nijmegen/Plymouth, Spring 1983 WJ.A.J. SMEETS R. N IEUWENHUYS B.L. ROBERTS
6 Contents 1 Introduction Materials and Methods 7 3 Gross Morphology 11 4 The Overall Histological Pattern 16 5 The Spinal Cord Introductory Notes Peripheral Spinal Nerves General Organization of the Spinal Cord Fibres Ascending to the Brain in the Funiculus Dorsalis Fibres Ascending to the Brain in the Funiculus Lateralis Fibres Descending from the Brain to the Spinal Cord Regeneration of the Spinal Cord Organization of the Spinal Cord in the Embryo Functional Correlations 29 6 The Brain Stem Introductory Notes Nerve Components and Longitudinal Zones Centres and Fibre Tracts The Afferent Components of the Nervus Trigeminus and Their Centres of Termination Visceral Afferent Centres and Tracts The Octavolateral Area and Its Connections Projections to the Brain Stem from Higher Levels Formatio Reticularis Fasciculus Longitudinalis Medialis Visceromotor Nuclei Branchiomotor Nuclei Somatomotor Nuclei Certain Centres in the Isthmus Region and in the Tegmentum Mesencephali Functional Correlations 65 7 Cerebellum 7.1 Introductory Notes 7.2 Structure
7 VIn Contents 7.3 Cerebellar Afferents and Their Centres of Origin The Efferent Projections from the Cerebellar Corpus and Auriculae Functional Correlations The Tectum Mesencephali Introductory Notes Structure Connections Afferent Projections to the Tectum Tectal Efferents Comparative Considerations Functional Correlations 87 The Diencephalon Introductory Notes Morphological Pattern Ventricular Sulci Cell Masses Epithalamus Thalamus Dorsalis Thalamus Ventralis The Hypothalamus Synencephalic Region Fibre Tracts Connections Between Diencephalon and Brain Stem Connections Between Diencephalon and Telencephalon Intrinsic Diencephalic Connections Diencephalic Commissures The Tractus Opticus The Diencephalon and the Problem of Homology Ventricular Sulci Cell Masses Fibre Tracts Conclusions The Hypophysis Introductory Notes The Adenohypophysis The Neurohypophysis The Hypothalamohypophyseal Control System Functional Correlations Telencephalon Morphogenesis and Overall Structure Survey of Literature on the Histological Structure and Fibre Connections
8 Contents IX 10.3 Subdivision of the Telencephalon 10.4 Sulcal Pattern Main Fibre Systems 10.6 Cell Masses Cell Masses in the Telencephalon Impar and Subpallium Cell Masses in the Pallium Fibre Tracts Secondary Olfactory Tracts Intrinsic Telencephalic Connections Telencephalic Connections with More Caudally Situated Brain Regions Remaining Fibre Systems The Telencephalon and the Problem of Homology 10.9 Functional Correlations Concluding Remarks 11.1 Gross Morphology Subdivision of Grey Matter 11.3 Macrocircuitry Structure of Nerve Roots and Fibre Systems Microcircuitry Atlas Squalus acanthias Scyliorhinus canicula Raja clavata.. Hydrolagus collei References.. Abbreviations Subject Index
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