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Multiple subtypes of glycine-immunoreactive neurons in the goldfish retina: Single- and double-label studies

Published online by Cambridge University Press:  02 June 2009

Stephen Yazulla
Affiliation:
Department of Neurobiology and Behavior, State University of New York, Stony Brook
Keith M. Studholme
Affiliation:
Department of Neurobiology and Behavior, State University of New York, Stony Brook

Abstract

The glycinergic system in goldfish retina was studied by immunocytochemical localization of glycine antiserum at the light-microscopical level. Numerous amacrine cells, a type of interplexiform cell, interstitial cell, and displaced amacrine cell were glycine-immunoreactive (IR). Amacrine cells, accounting for 97% of the glycine-IR neurons, were of four types based solely on their level of dendritic stratification: stratified amacrine cells of the first, third, and fifth sublayers and bistratified amacrine cells of the first and fifth sublayers. Double-labeling experiments were carried out to determine possible co-localization of glycine-IR with GABA-IR, serotonin-IR, substance P-IR and somatostatin-IR. No evidence for co-localization of glycine-IR with these other transmitter substances was found, despite reports of co-localization of these substances in retinas of other species. Glycinergic neurons in goldfish retina appear to consist of a heterogeneous population of at least seven morphologically distinct subtypes that are also neurochemically distinct in regard to GABA, serotonin, substance P, and somatostatin. Since dendritic stratification in the inner plexiform layer is correlated with ON-, OFF-response types, we suggest that the subtypes of glycine-IR amacrine cells play different roles in the encoding of visual information.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1990

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References

AmmermÜller, J. & Weiler, R. (1981). The ramification pattern of amacrine cells within the inner plexiform layer of the carp retina. Cell and Tissue Research 220, 699723.CrossRefGoogle ScholarPubMed
Ball, A.K. (1987). Immunocytochemical and autoradiographic localization of GABAergic neurons in the goldfish retina. Journal of Comparative Neurology 255, 317325.CrossRefGoogle ScholarPubMed
Ball, A.K. & Brandon, C. (1986). Localization of [3H]-GABA, [3H]-muscimol, and [3H]-glycine in goldfish retinas stained for glutamate decarboxylase. Journal of Neuroscience 6, 16211627.CrossRefGoogle ScholarPubMed
Brecha, N., Karten, H.J. & Schenker, C. (1981). Neurotensin-like and somatostatin-like immunoreactivity within amacrine cells of the retina. Neuroscience 6, 13291340.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system, I: Synapses of the dopaminergic neurons of the goldfish retina. Proceedings of the Royal Society B (London) 201, 726.Google Scholar
Eldred, W.D. & Cheung, K. (1989). Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Visual Neuroscience 2, 331338.CrossRefGoogle ScholarPubMed
Eldred, W.D., Zucker, C., Karten, H.J., and Yazulla, S. (1983). Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. Journal of Histochemistry and Cytochemistry 31, 285292.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr, Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198, 12671269.CrossRefGoogle Scholar
Kalloniatis, M. & Marc, R.E. (1989). Golgi-impregnated interplexiform cells in the goldfish retina. Investigative Ophthalmology and Visual Science (Suppl.) 30, 320.Google Scholar
Li, H.-B., Marshak, D.W., Dowling, J.E. & Lam, D.M.K. (1986). Colocalization of immunoreactive substance P and neurotensin in amacrine cells of the goldfish retina. Brain Research 366, 307313.Google ScholarPubMed
Maguire, G., Lukasiewicz, P. & Werblin, F. (1989). Amacrine cell interactions underlying the response to change in the tiger salamander retina. Journal of Neuroscience 9, 726735.CrossRefGoogle ScholarPubMed
Marc, R.E. (1982). Spatial organization of neurochemically classified interneurons of the goldfish retina, I: Local patterns. Vision Research 22, 589602.CrossRefGoogle ScholarPubMed
Marc, R.E. (1985). The role of glycine in retinal circuitry. In Retinal Transmitters and Modulators: Models for the Brain. Vol. 1, ed. Morgan, W.W., pp. 119158. Boca Raton, Florida: CRC Press.Google Scholar
Marc, R.E. (1988). The role of glycine in the mammalian retina. Progress in Retinal Research 8, 67108.CrossRefGoogle Scholar
Marc, R.E. & Lam, D.M.K. (1981). Glycinergic pathways in goldfish retina. Journal of Neuroscience 1, 152165.CrossRefGoogle ScholarPubMed
Marc, R.E., Liu, W.-L.S., Scholz, K. & Muller, J.F. (1988). Sero tonergic and serotonin-accumulating neruons in the goldfish retina. Journal of Neuroscience 8, 34273450.CrossRefGoogle Scholar
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221246.CrossRefGoogle ScholarPubMed
Murakami, M. & Shimoda, Y. (1977). Identification of amacrine and ganglion cells in the carp retina. Journal of Physiology (London) 264, 801818.CrossRefGoogle ScholarPubMed
Negishi, K. & Teranishi, T. (1989). Dendritic morphology of a class of interstitial amacrine cells in carp retina. In Neurobiology of the Inner Retina. NATO ASI Series. Vol. H31, ed. Weiler, R. & Osborne, N.N., pp. 133143. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Owczarzak, M.T. & Pourcho, R.G. (1989). Glycine immunoreactivity in the cat retina: comparison and co-localizaton with GABA. Investigative Ophthalmology and Visual Science (Suppl.) 30, 121.Google Scholar
Pourcho, R.G. & Goebel, D.J. (1985 a). A combined Golgi and auto-radiographic study of [3H]-glycine accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 219, 2535.CrossRefGoogle Scholar
Pourcho, R.G. & Goebel, D.J. (1985 b). Immunocytochemical demonstration of glycine in retina. Brain Research 348, 339342.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: an immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 11891197.CrossRefGoogle ScholarPubMed
Ramon, Y Cajal S. (1933). The Structure of the Retina. (Compiled and translated Thorpe, S.A. & Glickstein, M.), Springfield, Illinois: Charles C. Thomas, Co. 1972.Google Scholar
Sakai, H. & Hashimoto, Y. (1983). Rod input to amacrine cells in dace retina. Brain Research 270, 141160.CrossRefGoogle ScholarPubMed
Smiley, J.F. & Basinger, S.F. (1988). Somatostatin-like immunoreactivity and glycine high-affinity uptake co-localize to an interplexiform cell of the Xenopus laevis retina. Journal of Comparative Neurology 274, 608618.CrossRefGoogle Scholar
Smiley, J.F. & Basinger, S.F. (1989). Glycine high-affinity uptake labels a subpopulation of somatostatin-like immunoreactive cells in the Rana pipiens retina. Brain Research 495, 3144.CrossRefGoogle ScholarPubMed
Somogyi, P., Hodgson, A.J., Smith, A.D., Nunzi, M.G., Gorio, A. & Wu, J.-Y. (1984). Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatinor cholecystokinin-immunoreactive material. Journal of Neuroscience 4, 25902603.CrossRefGoogle ScholarPubMed
Stell, W.K., Ishida, A.T. & Lightfoot, D.O. (1977). Structural basis for ON- and OFF-center responses in retinal bipolar cells. Science 198, 12691271.CrossRefGoogle ScholarPubMed
Sternberger, L.A. (1979). Immunocytochemistry (2nd Edition). New York: John Wiley & Sons.Google ScholarPubMed
Studholme, K.M. & Yazulla, S. (1988). Localization of GABA and glycine in goldfish retina by postembed immunocytochemistry: improved visualization of synaptic structures with LR White resin. Journal of Neurocytology 17, 859870.CrossRefGoogle Scholar
Teranishi, T., Negishi, K. & Kato, S. (1985). Correlations between photoresponse and morphology of amacrine cells in the carp retina. Neuroscience Research (Suppl.) 2, S211–S226.Google ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1987). Functional and morphological correlates of amacrine cells in carp retina. Neuroscience 20, 935950.CrossRefGoogle ScholarPubMed
Thomson, A.M. (1989). Glycine modulation of the NMDA receptor/channel complex. Trends in Neurosciences 12, 349353.CrossRefGoogle ScholarPubMed
Wagner, H.-J. & Wagner, E. (1988). Amacrine cells of a teleost fish, the roach (Rutilus rutilis): a Golgi study on differentiation and layering. Philosophical Transactions of the Royal Society B (London) 321, 263324.Google Scholar
Wagner, H.-J. & Zeutzius, I. (1987). Amacrine cells with neurotensin- and somatostatin-like immunoreactivity in three species of teleosts with different colour vision. Cell and Tissue Research 248, 663673.CrossRefGoogle Scholar
Watt, C.B., Li, H.-B. & Lam, D.M.K. (1985). The presence of three neuroactive peptides in putative glycinergic amacrine cells of an avian retina. Brain Research 348, 187191.CrossRefGoogle ScholarPubMed
Weiler, R. & Ball, A.K. (1984). Co-localization of neurotensin-like immunoreactivity and [3H]-glycine uptake system in sustained amacrine cells of turtle retina. Nature 311, 759761.CrossRefGoogle ScholarPubMed
Wenthold, R. (1987). Evidence for a glycinergic pathway connecting the two cochlear nuclei: an immunocytochemical and retrograde transport study. Brain Research 415, 183187.CrossRefGoogle ScholarPubMed
Wenthold, R., Zemple, J., Parakkal, M.A. & Altschuler, R. (1986). Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Research 380, 718.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Stone, S. (1987). GABA and glycine modify the balance of rod and cone inputs to horizontal cells in the Xenopus retina. Experimental Biology 47, 1322.Google ScholarPubMed
Yamada, T., Marshak, D., Basinger, S., Walsh, J., Morley, J. & Stell, W. (1980). Somatostatin-like immunoreactivity in the retina. Proceedings of the National Academy of Sciences of the U.S.A. 3, 16911695.CrossRefGoogle Scholar
Yang, C.Y. & Yazulla, S. (1988 a). Light-microscopical localization of putative glycinergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 272, 343357.CrossRefGoogle Scholar
Yang, C.Y. & Yazulla, S. (1988 b). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 277, 96108.CrossRefGoogle Scholar
Yazulla, S. (1989). Transmitter-specific synaptic contacts involving mixed rod-cone bipolar cell terminals in goldfish retina. In Neurobiology of the Inner Retina. NATO ASI Series. Vol. H31, ed. Weiler, R. & Osborne, N.N., pp. 91102. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Yazulla, S., Studholme, K.M. & Wu, J.-Y. (1986). Comparative distribtuion of [3H]-GABA uptake and GAD immunoreactivity in goldfish retinal amacrine cells: a double-label analysis. Journal of Comparative Neurology 244, 149162.CrossRefGoogle Scholar
Yazulla, S., Studholme, K. & Wu, J.-Y. (1987). GABAergic input to the synaptic terminals of mbl bipolar cells in the goldfish retina. Brain Research 411, 400405.CrossRefGoogle Scholar
Yazulla, S. & Yang, C.-Y. (1988). Co-localization of GABA- and glycine-immunoreactivities in a subset of retinal neurons in tiger salamander. Neuroscience Letters 95, 3741.CrossRefGoogle Scholar