It has long been known that many elasmobranch fishes have relatively large brains. The telencephalon, in particular, has increased in size in several groups, and as a percent of total brain weight, it is as large as in some mammals. Little is known, however, about the organization, connections, and functions of the telencephalon in elasmobranchs. Early experimental studies indicated that olfaction does not dominate the telencephalon and that other sensory modalities are represented, particularly in the pallium. We have investigated the intrinsic and extrinsic connections of the telencephalon in two elasmobranch species: the thornback guitarfish, Platyrhinoidis triseriata, and the spiny dogfish, Squalus acanthias. Tracers were injected into various parts of the forebrain and olfactory pathways were found to be extensive and were seen to involve the pallium. Injections into various parts of the pallium revealed a major input from the area basalis, which receives secondary and tertiary olfactory fibers. Nonolfactory input from the diencephalon appeared relatively minor and seemed to converge with olfactory information in the dorsal pallium and area superficialis basalis. Major descending projections were seen to originate in the dorsal pallium and terminate in the hypothalamus and – in the case of Platyrhinoidis – massively in the lateral mesencephalic nucleus. Descending pathways appeared mainly crossed in Platyrhinoidis, but not in Squalus. Our data indicate that the concept of the dorsal pallium as a nonolfactory area in elasmobranchs must be reconsidered, and we suggest that many telencephalic centers, including the dorsal pallium, are involved in olfactory orientation.

1.
Bäckström K (1924): Contributions to the forebrain morphology in selachians. Acta Zoologica 5:123–240.
2.
Bleckmann H, Bullock T, Jorgensen J (1987): The lateral line mechanoreceptive mesencephalic, diencephalic, and telencephalic regions in the thornback ray, Platyrhinoidis triseriata (Elasmobranchii). J Comp Physiol A 161:67–84.
3.
Bleckmann H, Weiss O, Bullock T (1989): Physiology of lateral line mechanoreceptive regions in the elasmobranch brain. J Comp Physiol A 164:459–474.
4.
Bodznick D, Northcutt R (1984): An electrosensory area in the telencephalon of the little skate, Raja erinacea. Brain Res 298:117–124.
5.
Cohen D, Duff T, Ebbesson SOE (1973): Electrophysiological identification of a visual area in shark telencephalon. Science 182:492–494.
6.
Compagno LJV (1999): Systematics and body form; in Hamlett WC (ed): Sharks, Skates and Rays. Baltimore, Johns Hopkins University Press, pp 1–42.
7.
Dryer L, Graziadei PP (1994): Projections of the olfactory bulb in an elasmobranch fish, Sphyrna tiburo: segregation of inputs in the telencephalon. Anat Embryol (Berl) 190:563–572.
8.
Ebbesson SOE (1972): New insights into the organization of the shark brain. Comp Biochem Physiol A 42:121–129.
9.
Ebbesson SOE, Heimer L (1970): Projections of the olfactory tract fibers in the nurse shark (Ginglymostoma cirratum). Brain Res 17:47–55.
10.
Ebbesson SOE, Hodde K (1981): Ascending spinal systems in the nurse shark, Ginglymostoma cirratum. Cell Tissue Res 216:313–331.
11.
Ebbesson SOE, Schroeder D (1971): Connections of the nurse shark’s telencephalon. Science 173:254–256.
12.
Fiebig E, Bleckmann H (1989): Cell groups afferent to the telencephalon in a cartilaginous fish (Platyrhinoidis triseriata). A WGA-HRP study. Neurosci Lett 105:57–62.
13.
Gardiner JM, Atema J (2010): The function of bilateral odor arrival time differences in olfactory orientation of sharks. Curr Biol 20:1187–1191.
14.
Giuliani A, Minelli D, Quaglia A, Villani L (2002): Telencephalo-habenulo-interpeduncular connections in the brain of the shark Chiloscyllium arabicum. Brain Res 926:186–190.
15.
Hansen A, Zielinski BS (2005): Diversity in the olfactory epithelium of bony fishes: development, lamellar arrangement, sensory neuron cell types, and transduction components. J Neurocytol 34:183–208.
16.
Hara T (1994): The diversity of chemical stimulation in fish olfaction and gustation. Rev Fish Biol Fisher 4:1–35.
17.
Heimer L (1969): The secondary olfactory connections in mammals, reptiles and sharks. Ann NY Acad Sci 167:129–146.
18.
Herrick CJ (1922): Functional factors in the morphology of the forebrain of fishes. Tirada aparte del tomo I del Libro en honor de D. Santiago Ramon y Cajal. Madrid.
19.
Hodgson ES, Mathewson RF (1971): Chemosensory orientation in sharks. Ann NY Acad Sci 188:175–182.
20.
Hofmann MH, Northcutt RG (2008): Organization of major telencephalic pathways in an elasmobranch, the thornback ray Platyrhinoidis triseriata. Brain Behav Evol 72:307–325.
21.
Holmgren N (1922): Points of view concerning the forebrain morphology in lower vertebrates. J Comp Neurol. 34:391–459
22.
Johnston C (1911): The telencephalon of selachians. J Comp Neurol 21:1–113.
23.
Lisney T, Bennett M, Collin S (2007): Volumetric analysis of sensory brain areas indicates ontogenetic shifts in the relative importance of sensory systems in elasmobranchs. Raffles Bull Zool suppl 14:7–15.
24.
Lisney T, Collin S (2006): Brain morphology in large pelagic fishes: A comparison between sharks and teleosts. J Fish Biol 68:532–554.
25.
Luiten P (1981a): Two visual pathways to the telencephalon in the nurse shark (Ginglymostoma cirratum). II. Ascending thalamo-telencephalic connections. J Comp Neurol 196:539–548.
26.
Luiten P (1981b): Two visual pathways to the telencephalon in the nurse shark (Ginglymostoma cirratum). I. Retinal projections. J Comp Neurol 196:531–538.
27.
Meredith G, Smeets W (1987): Immunocytochemical analysis of the dopamine system in the forebrain and midbrain of Raja radiata: evidence for a substantia nigra and ventral tegmental area in cartilaginous fish. J Comp Neurol 265:530–548.
28.
Meredith TL, Kajiura SM (2010): Olfactory morphology and physiology of elasmobranchs. J Exp Biol 213:3449–3456.
29.
Northcutt RG [ed.] (1977): Recent advances in the biology of sharks. Proceedings of a Symposium. Am Zool 17:289–515.
30.
Northcutt RG (1978): Brain organization in the cartilaginous fishes; in Hodgson ES, Maathewson RF (eds): Sensory Biology of Sharks, Skates, and Rays. Arlington, Office of Naval Research, Department of the Navy, pp 117–193.
31.
Northcutt RG (1989): Brain variation and phylogenetic trends in elasmobranch fishes. Evolutionary and contemporary biology of elasmobranchs. J Exp Zool (suppl 2):83–100.
32.
Quintana-Urzainqui I, Sueiro C, Carrera I, Ferreiro-Galve S, Santos-Durán G, Pose-Méndez S, Mazan S, Candal E, Rodríguez-Moldes I (2012) Contributions of developmental studies in the dogfish Scyliorhinuscanicula to the brain anatomy of elasmobranchs: insights on the basal ganglia. Brain Behav Evol 80:127–141.
33.
Schluessel V, Bennett MB, Bleckmann H, Blomberg S, Collin SP (2008): Morphometric and ultrastructural comparison of the olfactory system in elasmobranchs: the significance of structure-function relationships based on phylogeny and ecology. J Morph 269:1365–1386.
34.
Schroeder D, Ebbesson SOE (1974): Nonolfactory telencephalic afferents in the nurse shark (Ginglymostoma cirratum). Brain Behav Evol 9:121–155.
35.
Schweitzer J (1986): Functional organization of the electroreceptive midbrain in an elasmobranch (Platyrhinoidis triseriata). J Comp Physiol A 158:43–58.
36.
Schweitzer J, Lowe D (1984): Mesencephalic and diencephalic cobalt-lysine injections in an elasmobranch: evidence for two parallel electrosensory pathways. Neurosci Lett 44:317–322.
37.
Smeets W (1983): The secondary olfactory connections in two chondrichthians, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 218:334–344.
38.
Smeets WJAJ (1998): Cartilaginous fishes; in Nieuwenhuys R, ten Donkelaar HJ, Nicholson C (eds): The Central Nervous System of Vertebrates. Berlin, Springer, vol 1, pp 551–654.
39.
Smeets W, Boord R (1985): Connections of the lobus inferior hypothalami of the clearnose skate Raja eglanteria (Chondrichthyes). J Comp Neurol 234:380–392.
40.
Smeets WJ, Northcutt RG (1987): At least one thalamotelencephalic pathway in cartilaginous fishes projects to the medial pallium. Neurosci Lett 78:277–282.
41.
Stuesse S, Cruce W (1991): Immunohistochemical localization of serotoninergic, enkephalinergic, and catecholaminergic cells in the brainstem and diencephalon of a cartilaginous fish, Hydrolagus colliei. J Comp Neurol 309:535–548.
42.
Stuesse S, Cruce W (1992): Distribution of tyrosine hydroxylase, serotonin, and leu-enkephalin immunoreactive cells in the brainstem of a shark, Squalus acanthias. Brain Behav Evol 39:77–92.
43.
Tester A (1963): Olfaction, gustation, and the common chemical sense in sharks; in Gilbert PW (ed): Sharks and Survival. Lexington, DC Heath & Co., pp 255–282.
44.
Theisen B, Zeiske E, Breucker H (1986): Functional morphology of the olfactory organs in the spiny dogfish (Squalus acanthias L.) and the small-spotted catshark (Scyliorhinus canicula L.). Acta Zool 67:73–86.
45.
Veselkin NP, Kovacevic N (1973): Non-olfactory telencephalic afferent projections in elasmobranch fishes. Zh Evol Biokhim Fiziol 9:585–592.
46.
Yamamoto M (1982): Comparative morphology of the peripheral olfactory organ in teleosts; in Hara TJ (ed): Chemoreception in Fishes. New York, Elsevier, pp 39–59.
47.
Yopak KE, Lisney TJ, Collin SP, Montgomery JC (2007): Variation in brain organization and cerebellar foliation in chondrichthyans: sharks and holocephalans. Brain Behav Evol 69:280–300.
48.
Yopak, KE, Lisney TJ, Darlington RB, Collin SP, Montgomery JC, Finlay BL (2010): A conserved pattern of brain scaling from sharks to primates. Proc Natl Acad Sci USA 107:12946–12951.
49.
Zeiske E, Theisen B, Gruber S (1987): Functional morphology of the olfactory organ of two carcharhinid shark species. Can J Zool 65:2406–2412.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.