Abstract
Among vertebrates, telencephalo-pontine systems exist only in birds and mammals. However, three nuclei in the diencephalon and mesencephalon of teleost fishes have been indicated — analogous to the pons — to represent relay stations between telencephalon and cerebellum. Since two of these nuclei (dorsal preglomerular nucleus, dorsal tegmental nucleus) have only been described in the highly derived, electrosensory mormyrids, we investigated telencephalic connections in two nonelectrosensory teleosts, the goldfish Carassius auratus and the freshwater butterflyfish Pantodon buchholzi, and cerebellar connections only in the latter species, since for C. auratus these connections are already established. Horseradish peroxidase tracing reveals that C. auratus has a dorsal tegmental nucleus and a paracommissural nucleus both of which are telencephalo-recipient and project to the cerebellum, and that P. buchholzi has a dorsal preglomerular nucleus with such connections. These results extend our knowlegde of the distribution and, therefore, the phylogeny of telencephalo-cerebellar systems in teleosts. Similar to tetrapods, teleosts appear to have developed telencephalo-cerebellar systems several times independently.
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References
Braford MR Jr, Northcutt RG (1983) Organization of the diencephalon and pretectum of the ray-finned fishes. In: Davis R, Northcutt RG (eds) Fish neurobiology, vol 2. University of Michigan Press, Ann Arbor, pp 117–163
Bullock TH, Bodznick DA, Northcutt RG (1983) The phylogenetic distribution of electroreception: evidence for convergent evolution of a primitive vertebrate sensory modality. Brain Res 6:25–46
Ebbesson SOE (1980) On the organization of the telencephalon inelasmobranchs. In: Ebbesson SOE (ed) Comparative neurology of the Telencephalon. Plenum Press, New York, pp 1–16
Ebbesson SOE, Hansel M, Scheich H (1981) An ‘on the slide’ modification of the DeOlmos-Heimer-HRP method. Neurosci Lett 22:1–14
Echteler SM, Saidel WM (1981) Forebrain connections in the goldfish support telencephalic homologies with land vertebrates. Science 212:683–685
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 268:567–583
Finger TE, Bell CC, Russell CJ (1981) Electrosensory pathways to the valvula cerebelli in mormyrid fish. Exp Brain Res 42:23–33
Hanker JS, Yates PE, Metz CB, Rustioni A (1977) A new specific, sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochem J 9:789–792
Ito H, Yoshimoto M (1990) Cytoarchitecture and fiber connections of the nucleus lateralis valvulae in the carp (Cyprinus carpio). J Comp Neurol 298:385–399
Ito H, Murakami T, Morita Y (1982) An indirect telencephalo-cerebellar pathway and its relay nucleus in teleosts. Brain Res 249:1–13
Karten HJ, Finger TE (1976) A direct thalamo-cerebellar pathway in pigeon and catfish. Brain Res 102:335–338
Lauder GV, Liem KF (1983) The evolution and interrelationships of the actinopterygian fishes. Bull Mus Comp Zool 150:95–197
Meek J, Nieuwenhuys R, Elsevier D (1986) Afferent and efferent connections of cerebellar lobe C3 of the mormyrid fish Gnathonemus petersi: an HRP study. J Comp Neurol 245:342–358
Murakami T, Morita Y, Ito H (1983) Extrinsic and intrinsic fiber connections of the telencephalon in a teleost, Sebastiscus marmoratus. J Comp Neurol 216:115–131
Nieuwenhuys R, Meek J (1990) The telencephalon of actinopterygian fishes. In: Jones EG, Peters A (eds) Cerebral cortex, vol 8a: Comparative structure and evolution of cerebral cortex, part 1. Plenum Press, New York London, pp 31–73
Roth G, Wullimann MF (1993) Die Evolution der Nervensysteme und der Sinnesorgane. In: Dudel J, Menzel R, Schmidt RF (eds) Lehrbuch der Neurowissenschaft. VCH, Weinheim (in press)
Striedter GF (1990) The diencephalon of the channel catfish, Ictalurus punctatus. II. Retinal, tectal, cerebellar and telencephalic connections. Brain Behav Evol 36:355–377
Vanegas H, Ebbesson SOE (1976) Telencephalic projections in two teleost species. J Comp Neurol 165:181–196
Wullimann MF, Meyer DL (1990) Phylogeny of putative cholinergic visual pathways through the pretectum to the hypothalamus in teleost fish. Brain Behav Evol 36:14–29
Wullimann MF, Northcutt RG (1987) Telencephalic and retinal projections allow reinterpretation of the diencephalon in mormyrids. Soc Neurosci Abstr 13:130
Wullimann MF, Northcutt RG (1988) Connections of the corpus cerebelli in the green sunfish and the common goldfish: A comparison of perciform and cypriniform teleosts. Brain Behav Evol 32:293–316
Wullimann MF, Northcutt RG (1989) Afferent connections of the valvula cerebelli in two teleosts, the common goldifish and the green sunfish. J Comp Neurol 289:554–567
Wullimann MF, Northcutt RG (1990) Visual and electrosensory circuits of the diencephalon in mormyrids: an evolutionary perspective. J Comp Neurol 297:537–552
Wullimann MF, Roth G (1992) Similar telencephalo-cerebellar circuitry in electrosensory and other osteoglossomorph teleost fishes. Eur J Neurosci 5 [Suppl]:290
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Wullimann, M.F., Meyer, D.L. Possible multiple evolution of indirect telencephalo-cerebellar pathways in teleosts: studies in Carassius auratus and Pantodon buchholzi . Cell Tissue Res 274, 447–455 (1993). https://doi.org/10.1007/BF00314541
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DOI: https://doi.org/10.1007/BF00314541