WIA.J. Smeets R. Nieuwenhuys B.L. Roberts 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 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: 978-3-642-68925-3 e-ISBN-13: 978-3-642-68923-9 DOI: 10.1007/978-3-642-68923-9 Library of Congress Cataloging in Publication Data. Smeets, W.J.A.J. (Wilhelmus J.A.J.), 1949- . The central nervous system of cartilaginous fishes. Bibliography: p. - Inc1udes index. 1. Nervous system-Fishes. 2. Chondrichthyes. 3. Central nervous system. I. Nieuwenhuys, R., 1927- .11. Roberts, B.L. (Barry L.), 1942- III. Title. [DNLM: 1. Fishes-Anatomy and histology. 2. Fishes-Physiology. 3. Central nervous system-Anatomy and histology. 4. Central nervous system-Physiology. QL 638.6.S637c] . QL638.6.S63 1983 597'.304188 83-336 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, broad casting, 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. 2131/3130-543210 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 struc tures, 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 Scylior hinus. 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 dis position 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 cartilagi nous fishes. Our work has been generously supported by the Medical Faculty of the University of Nijmegen and the Laboratory of the Marine Biological Associ ation, Plymouth, and we are grateful to many of our colleagues in these 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 pre pared 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 Biomed ical 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 Contents 1 Introduction . . . . . 1 2 Materials and Methods 7 3 Gross Morphology 11 4 The Overall Histological Pattern 16 5 The Spinal Cord . . . . . . 22 5.1 Introductory Notes 22 5.2 Peripheral Spinal Nerves 22 5.3 General Organization of the Spinal Cord 23 5.4 Fibres Ascending to the Brain in the Funiculus Dorsalis 27 5.5 Fibres Ascending to the Brain in the Funiculus Lateralis 27 5.6 Fibres Descending from the Brain to the Spinal Cord 28 5.7 Regeneration of the Spinal Cord . . . . . . 29 5.8 Organization of the Spinal Cord in the Embryo 29 5.9 Functional Correlations 29 6 The Brain Stem 31 6.1 Introductory Notes 31 6.2 Nerve Components and Longitudinal Zones 31 6.3 Centres and Fibre Tracts . . . . . . . . 34 6.3.1 The Afferent Components of the Nervus Trigeminus and Their Centres of Termination ...... 34 6.3.2 Visceral Afferent Centres and Tracts ..... 37 6.3.3 The Octavolateral Area and Its Connections 38 6.3.4 Projections to the Brain Stem from Higher Levels 51 6.3.5 Formatio Reticularis ...... 52 6.3.6 Fasciculus Longitudinalis Medialis 57 6.3.7 Visceromotor Nuclei 58 6.3.8 Branchiomotor Nuclei ..... 59 6.3.9 Somatomotor Nuclei ..... 61 6.3.10 Certain Centres in the Isthmus Region and in the Tegmen- tum Mesencephali 62 6.4 Functional Correlations 65 7 Cerebellum 68 7.1 Introductory Notes 68 7.2 Structure . . . . 68 VIn Contents 7.3 Cerebellar Afferents and Their Centres of Origin . . . . . . 73 7.4 The Efferent Projections from the Cerebellar Corpus and Auri- culae . . . . . . . . 75 7.5 Functional Correlations 76 8 The Tectum Mesencephali 78 8.1 Introductory Notes 78 8.2 Structure 78 8.3 Connections 81 8.3.1 Afferent Projections to the Tectum 81 8.3.2 Tectal Efferents 84 8.4 Comparative Considerations 85 8.5 Functional Correlations 87 9 The Diencephalon 89 9.1 Introductory Notes 89 9.2 Morphological Pattern 89 9.3 Ventricular Sulci 91 9.4 Cell Masses 92 9.4.1 Epithalamus 92 9.4.2 Thalamus Dorsalis 94 9.4.3 Thalamus Ventralis 94 9.4.4 The Hypothalamus 96 9.4.5 Synencephalic Region 99 9.5 Fibre Tracts · 101 9.5.1 Connections Between Diencephalon and Brain Stem · 101 9.5.2 Connections Between Diencephalon and Telencephalon 105 9.5.3 Intrinsic Diencephalic Connections · 107 9.5.4 Diencephalic Commissures · 108 9.5.5 The Tractus Opticus · 109 9.6 The Diencephalon and the Problem of Homology · 111 9.6.1 Ventricular Sulci · 111 9.6.2 Cell Masses · 112 9.6.3 Fibre Tracts · 113 9.6.4 Conclusions · 115 9.7 The Hypophysis . . 115 9.7.1 Introductory Notes . 115 9.7.2 The Adenohypophysis . 116 9.7.3 The Neurohypophysis . 119 9.7.4 The Hypothalamohypophyseal Control System . 119 9.8 Functional Correlations · 121 10 Telencephalon . . . . . . · 122 10.1 Morphogenesis and Overall Structure . 122 10.2 Survey of Literature on the Histological Structure and Fibre Connections ..................... 123 Contents IX 10.3 Subdivision of the Telencephalon 123 10.4 Sulcal Pattern . . . 125 10.5 Main Fibre Systems 126 10.6 Cell Masses . . . . · 127 10.6.1 Cell Masses in the Telencephalon Impar and Subpallium 127 10.6.2 Cell Masses in the Pallium . . 134 10.7 Fibre Tracts ......... . 137 10.7.1 Secondary Olfactory Tracts . 137 10.7.2 Intrinsic Telencephalic Connections . 141 10.7.3 Telencephalic Connections with More Caudally Situated Brain Regions . . . . . . . . . . . . . . 142 10.7.4 Remaining Fibre Systems . . . . . . . . . 145 10.8 The Telencephalon and the Problem of Homology · 146 10.9 Functional Correlations · 147 11 Concluding Remarks · 149 11.1 Gross Morphology . . · 149 11.2 Subdivision of Grey Matter · 150 11.3 Macrocircuitry ..... · 151 11.4 Structure of Nerve Roots and Fibre Systems · 153 11. 5 Microcircuitry · 153 Atlas . . . . . . . . · 155 Squalus acanthias · 155 Scyliorhinus canicula · 177 Raja clavata . . · 197 Hydrolagus collei · 217 References . . .241 Abbreviations .257 Subject Index · 261 1 Introduction The fishes are the largest class of vertebrates. jawed fishes diverged from the agnathans and They live in a wide range of aquatic habitats developed jaws from the skeleton of the bran and present a great diversity of structure, chial arches. The earliest to appear, the Acan physiology and behaviour. More than 90% thodi, arose in the Upper Silurian and were are bony fishes, and the living forms that fall followed closely by osteichthyans and placo within the scope of this book form a rather derms. The Chondrichthyes or cartilaginous small group that includes only about 800 fishes appeared later, in the lower Devonian. species. Several features obviously separate them from the bony fishes but the most dis Early in this century, the cartilaginous tinctive is their cartilaginous endoskeleton. fishes were considered to be generalized, Fossil remains are consequently rare and the primitive vertebrates and so were important evolution of cartilaginous fishes is presently to morphologists for typological compari understood only in broad terms. sons with other vertebrates. As our under The first fishes to appear in the fossil standing of these fishes has progressed, we record, dating from the Ordovician, were have come to realize that they are less simple small-mouthed jawless forms which declined in organization than had been supposed and markedly as a group by the Carboniferous that they possess elegant sensory systems, rel and which today are represented only by atively large brains, sophisticated reproduc hagfishes and lampreys. The major line of tive mechanisms, specialized osmoregulatory Table 1-1. Classification of the cartilaginous fishes (largely based on Compagno, 1977) Class Chondrichthyes I I Subclass Holocephali Elasmobranchii Superorder Squalomorphii Galeomorphii Squatinomorphii Batoidea /~ ~/~ I /I~ Order Hexanchi· Squali· Heterodonti- Orectolobi- Lamni- Carcharini- Squatini- Raji- Torpedini- Myliobati- formes formes formes formes formes formes formes formes formes formes Genus Chimaera Chlamydose· Squalus Helero- Ginglymo- Carc'ha- Scylio- Squatina Raja Torpedo Dasyalis Hydrolagus lachus Deania dontus stoma radon rhinus Platy- Narke Mohula Hexanchus Centro- Celo- Galeocerdo rhino- Hepfran- scymnus rhinus Mustelus idis chias Centro- Carcha- Rhino- phorus rhinus balos Negaprion Sphyrna Caleus Pristiurus 2 Introduction adaptations and even, in some species, ther The elasmobranch groups are represented moregulation. in this book by Squalus acanthias, a squalo Early in their history, the cartilaginous morph; Scyliorhinus canicula, a galeomorph, fishes separated into two major divisions, the and Raja clavata, a batoid, the general body Elasmobranchii and the Holocephali. The forms of which are illustrated in Fig. 1-1. living elasmobranchs (sharks and rays) com Although these species do not represent the prise four major superorders (Table 1-1): total range of cartilaginous fishes they do ex Squalomorphii, Galeomorphii, Squatino emplify the main features of the major morphii and Batoidea (Compagno 1977). groups. Moreover, they have provided the The sharks included in the Squalomorphii bulk of the data on the central nervous sys are principally dwellers of cold deep water tem in the literature, because they are rela and include about 25% of all shark species. tively common, are harmless to handle, and The group contains the primitive and rela are easily maintained in the marine labora tively uncommon six- and seven-gilled forms tory. (Chlamydoselachus, Hexanchus, Heptran Scyliorhinus is uncommon in the Western chias) as well as several better-known spe Atlantic and its place within the North cies (Centrophorus, Deania, Centroscymnus, American laboratory inventory is taken by Squalus). Mustelus in northern waters and by Gingly The Galeomorphii, constituting 75% of mostoma, or small specimens of Negaprion the sharks, differs in many respects from the and Sphyrna, in warmer waters. Work in other groups and includes most of the well North America on Batoidea has been based known sharks and dogfishes (e.g. Carcharo mostly on Raja erinacea, Raja eglanteria, don, Carcharhinus, Negaprion, Sphyrna, Rhinobatos and Plathyrhinoidis. Ginglymostoma, Mustelus, Scyliorhinus). Squalus acanthias, the spurdog, is world The Squatinomorphii contains only the wide in distribution and lives in open water, single genus, Squatina. This genus has some feeds voraciously on a great variety of other similarities with the Batoidea but resembles fish, such as herring, cod and haddock, and the Squalomorphii more closely in cranial performs extensive migrations both in Euro and pectoral fin structure. pean and North American waters. The The Batoidea includes the rajiformes roughhound, Scyliorhinus canicula, is a non (skates), with large pectoral discs and slender migratory bottom-dwelling species, living at tails, rhinobatiformes (guitar fishes), pristi depths of around 60 m, and feeding primarily formes (saw fishes), torpediniformes (electric on molluscs and crustacea. Raja clavata, the rays) and myliobatiformes (sting-, butterfly-, thornback ray, is found on the sea bottom eagle-, cow-nosed-, and devil-rays). at depths of up to 60 m and is non-migratory. The Holocephali, abundant in the Carbon It feeds primarily on crustacea. The Holoce iferous, are represented today by only six liv phali are represented in this book by the ing genera. These fish, of somewhat bizarre ratfish, Hydrolagus collei, which lives in the appearance, differ from elasmobranchs in Pacific Ocean. Other common species are several important ways. The name Holoce Hydrolagus affinis from the Gulf of Maine, phali refers to the distinctive autostylic sus Hydrolagus alberto from the Gulf of Mexico pension of the jaws of these fishes which con and the south Atlantic and Chimaera mon trasts with the hyostylic and amphistylic jaw strosa from north European waters. These suspension of elasmobranchs. The gill slits forms are mostly bottom dwellers, living in are covered by a large operculum and a spiral deep water with a wide geographic distribu valve is absent from the gut. There are also tion. They have large eyes and a well-devel important differences in skeletal organization oped lateral line system. Most of the teeth and in the structure of the brain. are fused into large toothplates adapted for