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Nucleus isthmi in goldfish: In vitro recordings and fiber connections revealed by HRP injections

Published online by Cambridge University Press:  02 June 2009

W. Michael King  and
John T. Schmidt
W. Michael King
Affiliation:
Department of Biological Sciences and Neurobiology Research Center, State University of New York at Albany
John T. Schmidt
Affiliation:
Department of Biological Sciences and Neurobiology Research Center, State University of New York at Albany
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Abstract

Recordings of field potentials in nucleus isthmi (NI) were obtained in an in vitro preparation of goldfish brain using a lateral approach. Horseradish peroxidase (HRP) was injected from recording electrodes to verify recordings within the nucleus and to label axonal pathways and cell bodies. Activity in NI was repetitive and could be elicited by stimulation of the optic nerve, tectum, pretectum, or tectobulbar tract. Spontaneous activity was present in some preparations and consisted of bursts with intervening silent periods. Anatomical and electrophysiological evidence indicated that the primary isthmotectal pathway is composed of fine fibers that exit NI rostrally and pass through pretectum to enter tectum rostrally. An afferent pathway consisting of both fine- and large-diameter fibers entered NI ventromedially; the large diameter axons have been previously reported in percomorph fishes, but were not thought to be present in cyprinids such as goldfish. The large diameter axons arise from labeled cell bodies in the region of the lateral thalamic nucleus. No labeled cell bodies were seen in ipsilateral nucleus pretectalis superficialis, pars magnocellularis, where they are seen in percomorphs. The fine axons, which have not been reported in percomorph fishes, were shown to arise from tectal bipolar (type VI) neurons. As in percomorphs, tectal type XIV neurons were also labeled. This and corroborating recordings from nucleus isthmi constitute the first demonstration of a tectoisthmic projection in a cyprinid fish.

Keywords

Nucleus isthmiGoldfishOptic tectumHorseradish peroxidase
Type
Articles
Information
Visual Neuroscience , Volume 10 , Issue 3 , May 1993 , pp. 419 - 437
Copyright
Copyright © Cambridge University Press 1993

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References

Kappers, C.U.Ariëns, Huber, G.C. & Crosby, E.C. (1936). The Comparative Anatomy of the Nervous System of Vertebrates, Including Man. New York: Macmillan.CrossRefGoogle Scholar
Boss, V.C. & Schmidt, J.T. (1984). Activity and the formation of ocular dominance patches in dually innervated tectum of goldfish. Journal of Neuroscience 4, 2891–2905.CrossRefGoogle ScholarPubMed
Braford, M.R. & Northcutt, R.G. (1983). Organization of the di-encephalon and pretectum of the ray-finned fishes. In Fish Neuro-biology, ed. Davis, R.E. & Northcutt, R.G., pp. 117–163. Ann Arbor, Michigan: University of Michigan Press.Google Scholar
Brantley, R.K. & Bass, A.H. (1988). Cholinergic neurons in the brain of a teleost fish (Porichthys notatus) located with a monoclonal antibody to choline acetyltransferase. Journal of Comparative Neurology 275, 87–105.CrossRefGoogle ScholarPubMed
Brauth, S.E., Kitt, C.A., Price, D.L. & Wainer, B.H. (1985). Cholinergic neurons in the telencephalon of the reptile Caiman crocodi-lus. Neuroscience Letters 58, 235–240.CrossRefGoogle Scholar
Desan, P.H., Gruberg, E.R. & Eckenstein, F. (1984). A cholinergic projection from the nucleus isthmi to the optic tectum in turtle and frog. Society for Neuroscience Abstracts 10, 575.Google Scholar
Desan, P.H., Gruberg, E.R., Greweli, K.M. & Eckenstein, F. (1987). Cholinergic innervation of the optic tectum in the frog Rana pipiens. Brain Research 413, 344–349.CrossRefGoogle ScholarPubMed
Dunn-Meynell, A.A. & Sharma, S.C. (1984). Changes in the topographically organized connections between the nucleus isthmi and the optic tectum after partial tectal ablation in adult goldfish. Journal of Comparative Neurology 227, 497–510.CrossRefGoogle ScholarPubMed
Easter, S.S., Schmidt, J.T. & Leber, S.M. (1978). The paths and destinations of the induced ipsilateral retinal projection in goldfish. Journal of Embryology and Experimental Morphology 45, 145–159.Google ScholarPubMed
Ebbesson, S.O.E. & Vanegas, H. (1976). Projections of the optic tectum in two teleost species. Journal of Comparative Neurology 165, 161–180.CrossRefGoogle ScholarPubMed
Ekström, P. (1987). Distribution of choline acetyltransferase-immuno-reactive neurons in the brain of a cyprinid teleost (Phoxinusphoxi-nus L.). Journal of Comparative Neurology 256, 494–515.CrossRefGoogle ScholarPubMed
Felix, D., Wang, S., Yan, K. & Wang, Y. (1985). The effect of acetylcholine on neurones of the amphibian nucleus isthmi. Brain Research 326, 313–316.CrossRefGoogle ScholarPubMed
Finger, T.E. (1983 a). Organization of the teleost cerebellum. In Fish Neurobiology, Vol. 1, ed. Northcutt, R.G. & Davis, R.E., pp. 261–284. Ann Arbor, Michigan: University of Michigan Press.Google Scholar
Finger, T.E. (1983 b). The gustatory system in teleost fish. In Fish Neurobiology, Vol. 1, ed. Northcutt, R.G. & Davis, R.E., pp. 285–309. Ann Arbor, Michigan: University of Michigan Press.Google Scholar
Freeman, J.A. (1979). Dendritic localization and density of acetylcholine receptors in single cells in slices of goldfish tectum. Society for Neuroscience Abstracts 5, 740.Google Scholar
Freeman, J.A. & Norden, J.J. (1984). Neurotransmitters in the optic tectum of nonmammalians. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 469–546. New York: Plenum.CrossRefGoogle Scholar
Graybiel, A.M. (1978). A satellite system of the superior colliculus: The parabigeminal nucleus and its projections to the superficial colliculus layers. Brain Research 145, 365–374.CrossRefGoogle Scholar
Grover, B.G. & Sharma, S.C. (1979). Tectal projections in the goldfish (Carassius auratus): A degeneration study. Journal of Comparative Neurology 184, 435–454.CrossRefGoogle ScholarPubMed
Grover, B.G. & Sharma, S.C. (1981). Organization of extrinsic tectal connections in goldfish (Carassius auratus). Journal of Comparative Neurology 196, 471–488.CrossRefGoogle Scholar
Gruberg, E.R. & Lettvtn, J.Y. (1980). Anatomy and physiology of a binocular system in the frog Rana pipiens. Brain Research 192, 313–322.CrossRefGoogle ScholarPubMed
Gruberg, E.R. & Udm, S.B. (1978). Topographic projections between the nucleus isthmi and the tectum of the frog Rana pipiens. Journal of Comparative Neurology 179, 487–500.CrossRefGoogle ScholarPubMed
Guthrie, D.M. (1990). The physiology of the teleostean optic tectum. In The Visual System of Fish, ed. Douglas, R. & Djamgoz, M., pp. 279–343. London: Chapman and Hall.CrossRefGoogle Scholar
Guthrie, D.M. & Banks, J.R. (1974). Input characteristics of the intrinsic cells of the optic tectum of teleost fish. Comparative Biochemistry and Physiology 47, 83–92.CrossRefGoogle ScholarPubMed
Guthrie, D.M. & Sharma, S.C. (1991). Visual responses of morphologically identified tectal cells in the goldfish. Vision Research 31, 507–524.CrossRefGoogle ScholarPubMed
Hall, W.C., Fitzpatrick, D., Klatt, L.L. & Raczkowski, D. (1989). Cholinergic innervation of the superior colliculus in the cat. Journal of Comparative Neurology 287, 495–514.CrossRefGoogle ScholarPubMed
Heiligenberg, W. & Rose, G.J. (1987). The optic tectum of the gymnotiform electric fish, Eigenmannia: Labeling of physiologically identified cells. Neuroscience 22, 331–340.CrossRefGoogle ScholarPubMed
Ito, H., Tanaka, H., Sakamoto, N. & Morita, Y. (1981). Isthmic afferent neurons identified by the retrograde HRP method in a teleost, Navodon modestus. Brain Research 207, 163–169.CrossRefGoogle Scholar
Ito, H., Sakamoto, N. & Takatsuji, K. (1982). Cytoarchitecture, fiber connections, and ultrastructure of nucleus isthmi in a teleost (Navodon modestus) with a special reference to degenerating isthmic afferents from optic tectum and nucleus pretectalis. Journal of Comparative Neurology 205, 299–311.CrossRefGoogle Scholar
Ito, H. & Yoshimoto, M. (1990). Cytoarchitecture and fiber connections of the nucleus lateralis valvulae in the carp (Cyprinus carpio). Journal of Comparative Neurology 298, 385–399.CrossRefGoogle ScholarPubMed
Jen, L.S., Dai, Z.-G. & So, K.-F. (1984). The connections between the parabigeminal nucleus and the superior colliculus in the golden hamster. Neuroscience Letters 51, 189–194.CrossRefGoogle ScholarPubMed
King, W.M. (1990). Nicotinic depolarization of optic nerve terminals augments synaptic transmission. Brain Research 527, 150–154.CrossRefGoogle ScholarPubMed
King, W.M. & Schmidt, J.T. (1991). The long latency component of retinotectal transmission: Enhancement by stimulation of nucleus isthmi or tectobulbar tract and block by nicotinic cholinergic antagonists. Neuroscience 40, 701–712.CrossRefGoogle ScholarPubMed
Kudo, K. (1923). Contributions to the knowledge of the brain of bony fishes. Proceedings of the Section of Sciences Koninklijke Akademie van Wetenschappen te Amsterdam 26, 65–78.Google Scholar
Langdon, R.B. & Freeman, J.A. (1986). Antagonists of glutaminergic neurotransmission block retinotectal transmission in goldfish. Brain Research 398, 169–174.CrossRefGoogle ScholarPubMed
Langdon, R.B. & Freeman, J.A. (1987). Pharmacology of retinotectal transmission in the goldfish: Effects of nicotinic ligands, strychnine, and kynurenic acid. Journal of Neuroscience 7, 760–773.CrossRefGoogle ScholarPubMed
Langdon, R.B., Manis, P.B. & Freeman, J.A. (1988). Goldfish retinotectal transmission in vitro: Component current sink-source pairs isolated by varying calcium and magnesium levels. Brain Research 441, 299–308.CrossRefGoogle ScholarPubMed
Lauder, G.V. & Liem, K.F. (1983). Patterns of diversity and evolution in ray-finned fishes. In Fish Neurobiology, Vol. 1, ed. Northcutt, R.G. & Davis, R.E., pp. 1–24. Ann Arbor, Michigan: University of Michigan Press.Google Scholar
Luiten, P.G.M. (1975). The horseradish peroxidase technique applied to the teleostean nervous system. Brain Research 89, 181–186.CrossRefGoogle Scholar
Luiten, P.G.M. (1981). Afferent and efferent connections of the optic tectum in the carp (Cyprinus carpio L.). Brain Research 220, 51–65.CrossRefGoogle ScholarPubMed
Manis, P.B. & Freeman, J.A. (1988). Fluorescence recordings of electrical activity in goldfish optic tectum in vitro. Journal of Neuroscience 8, 383–394.CrossRefGoogle ScholarPubMed
Matsumoto, N., Kiyama, H. & Bando, T. (1983). An intracellular study of the optic tectum of the carp in vitro. Neuroscience Letters 38, 17–22.CrossRefGoogle ScholarPubMed
Matsumoto, N. & Bando, T. (1981). Long-lasting evoked potential and repetitive firing recorded from the carp optic tectum in Cl-deficient medium in vitro. Brain Research 225, 437–441.CrossRefGoogle ScholarPubMed
Meek, J. (1981 a). The tectum mesencephali of the goldfish. Doctoral Thesis, Nijmegan.Google Scholar
Meek, J. (1981 b). Golgi-electron microscopic study of goldfish optic tectum. I. Description of afferents, cell types, and synapses. Journal of Comparative Neurology 199, 149–173.CrossRefGoogle ScholarPubMed
Meek, J. (1983). Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum. Brain Research Reviews 6, 247–297.CrossRefGoogle Scholar
Meek, J. & Schellart, N.A.M. (1978). A Golgi study of goldfish optic tectum. Journal of Comparative Neurology 182, 89–122.CrossRefGoogle ScholarPubMed
Metz, C.B., Schneider, S.P. & Fyffe, R.E.W. (1988). Selective suppression of endogenous peroxidase activity: Application for enhancing appearance of HRP-labeled neurons in vitro. Society for Neuroscience Abstracts 14, 548.Google Scholar
Mufson, E.J., Martin, T.L., Mash, D.C., Wainer, B.H. & Mesulam, M.M. (1986). Cholinergic projection from the parabigeminal nucleus (Ch8) to the superior colliculus in the mouse: A combined analysis of horseradish peroxidase transport and choline acetyltransferase immunohistochemistry. Brain Research 370, 144–148.CrossRefGoogle Scholar
Niida, A., Ohono, T. & Iwata, K.S. (1989). Efferent tectal cells of crucian carp: Physiology and morphology. Brain Research Bulletin 22, 389–398.CrossRefGoogle Scholar
Northcutt, R.G. & Braford, M.R. Jr, (1984). Some efferent connections of the superficial pretectum in the goldfish. Brain Research 296, 181–184.CrossRefGoogle ScholarPubMed
Northcutt, R.G. & Wullimann, M.F. (1988). The visual system in teleost fishes: Morphological patterns and trends. In Sensory Biology of Aquatic Animals, ed. Atema, J., Fay, R.R., Popper, A.N. & Tavolga, W.N., pp. 515–552. New York: Springer-Verlag.CrossRefGoogle Scholar
Northmore, D.P.M. (1991). Visual responses of nucleus isthmi in a teleost fish (Lepomis macrochirus). Vision Research 31, 525–535.CrossRefGoogle Scholar
Rhodes, K.J., Zottoli, S.J. & Mufson, E.J. (1986). Choline acetyltransferase immunohistochemical staining in the goldfish (Carassius auratus) brain: Evidence that the Mauthner cell does not contain choline acetyltransferase. Brain Research 381, 215–224.CrossRefGoogle Scholar
Sakamoto, N., Ito, H. & Ueda, S. (1981). Topographic projections between the nucleus isthmi and the optic tectum in a teleost, Navo-don modestus. Brain Research 224, 225–234.CrossRefGoogle Scholar
Schmidt, J.T. (1979). The laminar organization of optic fibers in the tectum of goldfish. Proceedings of the Royal Society B (London) 205, 287–306.Google ScholarPubMed
Schmidt, J.T. (1982). The formation of retinotectal projections. Trends in Neuroscience 5, 111–116.CrossRefGoogle Scholar
Schmidt, J.T. (1991). Long-term potentiation during the activity-dependent sharpening of the retinotectal map in goldfish. Annals of the New York Academy of Sciences 627, 10–25.CrossRefGoogle Scholar
Schmidt, J.T. (1992). The roles of activity, competition, and continued growth in the formation and stabilization of retinotectal connections in fish and frog. In Advances in Neural and Behavioral Development, ed. Casagrande, V., Norwood, New Jersey: Ablex Publishing Corporation (in press).Google Scholar
Schroeder, D.M. (1974). Some afferent and efferent connections of the optic tectum of a teleost, Ictalurus. Anatomical Record 178, 458.Google Scholar
Schroeder, D.M., Vanegas, H. & Ebbesson, S.O.E. (1980). Cytoarchitecture of the optic tectum of the squirrelfish, Holocentrus. Journal of Comparative Neurology 191, 337–351.CrossRefGoogle ScholarPubMed
Sherk, H. (1978). Visual response properties and visual field topography in the cat’s parabigeminal nucleus. Brain Research 145, 375–379.CrossRefGoogle ScholarPubMed
Sherk, H. (1979). A comparison of visual-response properties in cat’s parabigeminal nucleus and superior colliculus. Journal of Neuro-physiology 42, 1640–1655.CrossRefGoogle ScholarPubMed
Sligar, C.M. & Voneida, T.J. (1976). Tectal efferents in the blind cave fish Astyanax hubbsi. Journal of Comparative Neurology 165, 107–124.CrossRefGoogle ScholarPubMed
Striedter, G.F. & Northcutt, R.G. (1989). Two distinct visual pathways through the superficial pretectum in a percomorph teleost. Journal of Comparative Neurology 283, 342–354.CrossRefGoogle Scholar
Tan, M.M.L. & Harvey, A.R. (1989). The cholinergic innervation of normal and transplanted superior colliculus in the rat: An immunohistochemical study. Neuroscience 32, 511–520.CrossRefGoogle ScholarPubMed
Teyler, T.J., Lewis, D. & Shashoua, V.E. (1981). Neurophysiologi-cal and biochemical properties of the goldfish optic tectum maintained in vitro. Brain Research Bulletin 7, 45–56.CrossRefGoogle ScholarPubMed
Van Deusen, E.B. & Meyer, R.L. (1990). Pharmacologic evidence for NMDA, APB and kainate/quisqualate retinotectal transmission in the isolated whole tectum of goldfish. Brain Research 536, 86–96.CrossRefGoogle ScholarPubMed
Vanegas, H., Laufer, M. & Amat, J. (1974). The optic tectum of a Perciform Teleost, I. General configuration and cytoarchitecture. Journal of Comparative Neurology 154, 43–60.CrossRefGoogle ScholarPubMed
Vinogradova, V.M. & Manteifel, T.B. (1977). Neuronal responses in the nucleus isthmi area of the frog to optic nerve stimulation. Neirofiziologiia 9, 33–40.Google ScholarPubMed
Wang, S., Yan, K., Wang, Y., Jiang, S. & Wang, X. (1983). Neuroanatomy and electrophysiology of the lacertilian nucleus isthmi. Brain Research 275, 355–360.CrossRefGoogle ScholarPubMed
Wang, S.-J., Yan, K. & Wang, Y.-T. (1981). Visual field topography in the frog’s nucleus isthmi. Neuroscience Letters 23, 37–41.Google ScholarPubMed
Wang, S.-R. (1988). The nucleus isthmi is a visual center: Neuroanat-omy and electrophysiology. In Vision: Structure and Function, ed. Yew, D.T., So, K.F. & Tsang, D.S.C., pp. 301–364. Singapore: World Scientific.CrossRefGoogle Scholar
Waxman, S.G. & Bennett, M.V.L. (1972). Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system. Nature New Biology 238, 217–219.CrossRefGoogle ScholarPubMed
Williams, B., HernÁndez, N. & Vanegas, H. (1983). Electrophysiological analysis of the teleostean nucleus isthmi and its relationships with the optic tectum. Journal of Comparative Physiology A 152, 545–554.CrossRefGoogle Scholar
Williams, B. & Vanegas, H. (1982). Tectal projections in teleosts: Responses of some target nuclei to direct tectal stimulation. Brain Research 242, 3–9.CrossRefGoogle ScholarPubMed
Wullimann, M.F. & Meyer, D.L. (1990). Phylogeny of putative cho-linergic visual pathways through the pretectum to hypothalamus in teleost fish. Brain, Behavior, and Evolution 36, 14–29.CrossRefGoogle Scholar
Yan, K. & Wang, S.-R. (1986). Visual responses of neurons in the avian nucleus isthmi. Neuroscience Letters 64, 340–344.CrossRefGoogle ScholarPubMed
Zottoli, S.J., Rhodes, K.J., Corrodi, J.G. & Mufson, E.J. (1988). Putative cholinergic projections from the nucleus isthmi and the nucleus reticularis mesencephali to the optic tectum in the goldfish (Carassius auratus). Journal of Comparative Neurology 273, 385–398.CrossRefGoogle Scholar