Abstract
The organization of the vertebrate cerebellum has been thoroughly studied over the past century, but the function of this structure remains poorly understood. In elasmobranch fishes, the cerebellum displays tremendous variation in size and development although the basic and conservative nature of cerebellar circuitry as seen in other vertebrate taxa is largely retained. Large and morphologically complex cerebelli have evolved independently in both sharks and batoids, and the relative development of this structure in both taxa parallels those of birds and mammals. There are relatively few studies of the physiological role of the cerebellum in generating or shaping behaviors, however, and a convincing explanation of cerebellar hypertrophy in elasmobranchs is lacking. The purpose of this article is to review the current understanding of the structure of the cerebellum in elasmobranch fishes, the physiological responses of cerebellar neurons and the possible role of the cerebellum in behavior. I will also provide a number of hypotheses for future research directions, based upon models that have been suggested by different investigators. These hypotheses include models of cerebellar function as a sensory coincidence detector, a dynamic state estimator and/or a direct modulator of motor programs. Hypotheses concerning the possible organization of cerebellar microcomplexes, the evolution of afferent and efferent cerebellar connections paralleling those observed in mammals and the role of the cerebellum in learning are also suggested.
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Alvarez, R. & R. Anadon. 1987. The cerebellum of the dogfish, Scyliorhinus canicula: a quantitative study. J. Hirnforsch. 28: 133–137.
Alvarez-Otero, R. & R. Anadon. 1992. Golgi cells of the cerebellum of the dogfish, Scyliorhinus canicula (elasmobranchs): a Golgi and ultrastructural study. J. Hirnforsch. 33: 321–327.
Alvarez-Otero, R., S.D. Regueira & R. Anadon. 1993. New structural aspects of the synaptic contacts on Purkinje cells in an elasmobranch cerebellum. J. Anat. (Lond.) 182: 13–21.
Alvarez-Otero, R., S.E. Perez, M.A. Rodriguez, F. Adrio & R. Anadon. 1995. GABAergic neuronal circuits in the cerebellum of the dogfish Scyliorhinus canicula (elasmobranchs): an immunocytochemical study. Neurosci. Lett. 187: 87–90.
Alvarez-Otero, R., S.E. Perez, M.A. Rodriguez & R. Anadon. 1996. Organization of the cerebellar nucleus of the dogfish, Scyliorhinus canicula L.: a light microscopic, immunocytochemical, and ultrastructural study. J. Comp. Neurol. 368: 487–502.
Barry, M.A. 1987. Afferent and efferent connections of the primary octaval nuclei in the clearnose skate, Raja eglanteria. J. Comp. Neurol. 266: 457–477.
Brogden, W.J. & W.H. Gantt. 1937. Cerebellar coniditioned reflexes. Amer. J. Physiol. 119: 277–278.
Brogden, W.J. & W.H. Gantt. 1942. Intraneural conditioning: cerebellar conditioned reflexes. Archiv. Neurol. Psychiatry 48: 437–455.
Boord, R.L. & R.G. Northcutt. 1982. Ascending lateral line pathways to the midbrain of the clearnose skate, Raja eglanteria. J. Comp. Neurol. 207: 274–282.
Bucy, R.S. & P.D. Joseph. 1968. Filtering for stochastic processes with applications to guidance. Wiley, New York. 195 pp.
Catois, E.M. 1901. Recherches sur l'histologie et l'anatomie microscopique de l'encephale chez les poisons. Bull. Scient. France Belgique 36: 1.
Fiebig, E. 1988. Connections of the corpus cerebelli in the thornback guitarfish, Platyrhinoidis triseriata (elasmobranchii): a study with WGA-HRP and extracellular granule cell recording. J. Comp. Neurol. 286: 567–583.
Hawkes, R., S. Blyth, V. Chockkan, D. Tano, Z. Ji & C. Mascher. 1993. Structural and molecular compartmentation in the cerebellum. Can. J. Neurol. Sci. 20,Suppl. 3: S29–35.
Hawkes, R., G. Brochu, L. Dore, C. Gravel & N. Leclerc. 1992. Zebrins: molecular markers of compartmentation in the cerebellum. pp. 22–55. In: R. Llinas & C. Sotelo (ed.) The Cerebellum Revisited, Springer-Verlag, New York.
Hoggatt, A.M. & M.J. Lannoo. 1994. Monoclonal antibody antitype I and anti-zebrin II labelling in siluriform fishes: the role of shared lineage versus shared function in polypeptide co-distributions. Brain Res. 665: 181–191.
Houser, G.L. 1901. The neurons and supporting elements of the brain of a selachian. J. Comp. Neurol. 11: 65–175.
Ito, M. 1993. Movement and thought: identical control mechanisms by the cerebellum. Trends Neurosci. 16: 448–450.
Ito, M. 1997. Cerebellar microcomplexes. pp. 475–489. In: J.D. Schmahmann (ed.) International Review of Neurobiology, Academic Press, San Diego.
Kalman, R.E. 1960. A new approach to linear prediction and filtering problems. J. Basic Eng. A.S.M.E. 82: 35–45.
Kappers, C.U.A., G.C. Huber & E. Crosby. 1936. The comparative anatomy of the nervous system of vertebrates, including man. Macmillan, New York. 1845 pp.
Karamyan, A.I. 1962. Evolution of the function of the cerebellum and cerebral hemispheres. Published for the National Science Foundation by the Israel Program for Scientific Translations, Jerusalem. 109 pp.
Koester, D.M. 1983. Central projections of the octavolateralis nerves of the clearnose skate, Raja eglanteria. J. Comp. Neurol. 221: 199–215.
Konnerth, A., A.L. Obaid & B.M. Salzberg. 1987. Optical recording of electrical activity from parallel fibers and other cell types in skate cerebellar slices in vitro. J. Physiol. 393: 681–702.
Lannoo, M.J. & R. Hawkes. 1997. A search for primitive Purkinje cells: zebrin II expression in sea lampreys (Petromyzon marinus). Neurosci. Lett. 237: 53–55.
Lannoo, M.J., L. Ross, L. Maler & R. Hawkes. 1991. Development of the cerebellum and its extracerebellar Purkinje cell projection in teleost fishes as determined by zebrin II immunohistochemistry. Prog. Neurobio. 37: 329–363.
Larsell, O. 1967. The comparative anatomy and histology of the cerebellum from myxinoids through birds. The University of Minnesota Press, Minneapolis. 291 pp.
Lee, L.T. & T.H. Bullock. 1990a. Cerebellar units show several types of early responses to telencephalic stimulation in catfish. Brain Behav. Evol. 35: 278–290.
Lee, L.T. & T.H. Bullock. 1990b. Cerebellar units show several types of long-lasting posttetanic responses to telencephalic stimulation in catfish. Brain Behav. Evol. 35: 291–301.
Meek, J. 1992. Why run parallel fibers parallel? Teleostean Purkinje cells as possible coincidence detectors, in a timing device subserving spatial coding of temporal differences. Neurosci. 48: 249–283.
Meek, J., T.G. Hafmans, L. Maler & R. Hawkes. 1992. Distribution of zebrin II in the gigantocerebellum of the mormyrid fish, Gnathonemus petersii, compared with other teleosts. J. Comp. Neurol. 316: 17–31.
Myagkov, N.A. 1990. The brain sizes of living Elasmobranchii as their organization level indicator. I. General analysis. J. Hirnforsch. 32: 553–561.
New, J.G. & T.H. Bullock. 1989. Electrosensory responses in the granule cell layer of the cerebellum of an elasmobranch. Soc. Neurosci. Abstr. 15: 1138.
Nicholson, C., R. Llinas & W. Precht. 1969. Neural elements of the cerebellum in elasmobranch fishes: structural and functional characteristics. pp. 215–244. In: R. Llinas & R.F. Mathewson (ed.) Neurobiology of Cerebellar Evolution and Development, Institute for Biomedical Research, American Medical Association, Chicago.
Nicholson, L.F.B., J.C. Montgomery & R.L.M. Faull. 1994. GABA, muscarinic cholinergic, excitatory amino acid, neurotensin and opiate binding sites in the octavolateralis column and cerebellum of the skate Raja nasuta (Pisces: Rajidae). Brain Res. 652: 40–48.
Nieuwenhuys, R. 1967. Comparative anatomy of the cerebellum. pp. 1–93. In: C.A. Fox & R.S. Snider (ed.) Progress in Brain Research, Vol. 25, Elsevier, Amsterdam.
Northcutt, R.G. 1977. Elasmobranch central nervous system organization and its possible evolutionary significance. Amer. Zool. 17: 411–429.
Northcutt, R.G. 1978. Brain organization in the cartilaginous fishes. pp. 117–194. In: E.S. Hodgson & R.F. Mathewson (ed.) Sensory Biology of Sharks, Skates and Rays, Office of Naval Research, Arlington.
Northcutt, R.G. 1989. Brain variation and phylogenetic trends in elasmobranch fishes. J. Exp. Zool. 2: 83–100.
Northcutt, R.G. & W.J. Brunken. 1984. Cerebellar afferents in the little skate (Batoidea). Soc. Neurosci. Abstr. 10: 853.
Paul, D.H. 1969. Electrophysiological studies on parallel fibers of the corpus cerebelli of the dogfish Scyliorhinus canicula. pp. 245–250. In: R. Llinas & C. Sotelo (ed.) Neurobiology of Cerebellar Evolution and Development, Institute for Biomedical Research/American Medical Association, Chicago.
Paul, D.H. & B.L. Roberts. 1975. Connections between the cerebellum and the reticular formation in the dogfish Scyliorhinus canicula. J. Physiol. 249: 62–63.
Paul, D.H. & B.L. Roberts. 1979. The significance of cerebellar function for a reflexmovement of the dogfish. J. Comp. Physiol. 134: 69–74.
Paul, D.H. & B.L. Roberts. 1981. The activity of cerebellar neurones of an elasmobranch fish (Scyliorhinus canicula) during a reflex movement of a fin. J. Physiol. 321: 369–383.
Paul, D.H. & B.L. Roberts. 1983. The activity of cerebellar nuclear neurones in relation to stimuli which evoke a pectoral fin reflex in dogfish. J. Physiol. 342: 465–481.
Paul, D.H. & B.L. Roberts. 1984a. Projections of cerebellar Purkinje cells in the dogfish, Scyliorhinus. Neurosci. Lett. 44: 43–46.
Paul, D.H. & B.L. Roberts. 1984b. The activity of cerebellar neurones of the decerebrate dogfish Scyliorhinus during spontaneous swimming movements. J. Physiol. 352: 1–16.
Paulin, M.G. 1993. The role of the cerebellum in motor control and perception. Brain Behav. Evol. 41: 39–50.
Paulin, M.G. 1997. Neural representations of moving systems. pp. 516–535. In: J.D. Schmahmann (ed.) International Review of Neurobiology, Academic Press, San Diego.
Puzdrowski, R.L. 1997. Anti-zebrin II immunopositivity in the cerebellum and octavolateral nuclei in two species of stingrays. Brain Behav. Evol. 50: 358–368.
Rudeberg, S.-I. 1961. Morphogenetic studies on the cerebellar nuclei and their homologization in different vertebrates including man. Ph.D. Dissertation, University of Lund, Lund. 148 pp.
Sauerbeck, E. 1896. Beitrage zur Kenntis vom feineren Bau des Selachierhirns. Anat. Anz. B. 12: 41.
Schaper, A. 1898. The finer structure of the selachian cerebellum (Mustelis vulgaris) as shown by chrome silver preparations. J. Comp. Neurol. 8: 1–20.
Schmidt, A.W. & D. Bodznick. 1987. Afferent and efferent connections of the vestibulolateral cerebellum of the little skate, Raja erinacea. Brain Behav. Evol. 30: 282–302.
Smeets, W.J.A.J. 1982. The afferent connections of the tectum mesencephali in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J. Comp. Neurol. 205: 139–152.
Smeets, W.J.A.J., R. Nieuwenhuys & B.L. Roberts. 1983. The central nervous system of cartilaginous fishes. Springer-Verlag, New York. 266 pp.
Sterzi, G. 1905. Sulla regio parietalis dei ciclosotomi, dei selachii e degli olocefali. Anat. Anz. 27: 346–416.
ten Cate, J. 1930. Contribution a la physiologie comparée du cervelet. III. Le cervelet des plagiostomes. Archiv. need. physiol. de l'homme et des animaux 15: 479–528.
Thompson, R.F., J.K. Thompson, J.J. Kim, D.J. Krupa & P.G. Shinkman. 1998. The nature of reinforcement in cerebellar learning. Neurobiol. Learn. Mem. 70: 150–176.
Voorhoeve. 1917. Over den Bouw van de kleine hersenen der Plagiostomen (here in English). Inaugural Dissertation, University of Amsterdam, Amsterdam. 88 pp.
Wassef, M., P. Angaut, L. Arsenio-Nunes, F. Bourrat & C. Sotelo. 1992. Purkinje cell heterogeneity: its role in organizing the topography of cerebellar cortex connections. pp. 5–21. In: R. Llinas & C. Sotelo (ed.) The Cerebellum Revisited, Springer-Verlag, New York.
Welker, W. 1987. Spatial organization of somatosensory projections to granule cell cerebellar cortex: functional and connectional implications of fractured somatotopy. pp. 239–280. In: J.S. King (ed.) New Concepts in Cerebellar Neurobiology, A.R. Liss, New York.
Young, W. 1980. Field potential analysis in elasmobranch cerebellum. Brain Res. 199: 101–112.
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New, J.G. Comparative Neurobiology of the Elasmobranch Cerebellum: Theme and Variations on a Sensorimotor Interface. Environmental Biology of Fishes 60, 93–108 (2001). https://doi.org/10.1023/A:1007631405904
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DOI: https://doi.org/10.1023/A:1007631405904