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Effects of light stimuli on the release of dopamine from interplexiform cells in the white perch retina

Published online by Cambridge University Press:  02 June 2009

Osamu Umino
Affiliation:
Department of Cellular and Developmental Biology, Harvard University, Cambridge
Yunhee Lee
Affiliation:
Department of Cellular and Developmental Biology, Harvard University, Cambridge
John E. Dowling
Affiliation:
Department of Cellular and Developmental Biology, Harvard University, Cambridge

Abstract

Interplexiform cells are centrifugal neurons in the retina carrying information from the inner to the outer plexiform layers. In teleost fish, interplexiform cells appear to release dopamine in the outer plexiform layer after prolonged darkness that modulates the receptive-field size and light responsiveness of horizontal cells (Mangel & Dowling, 1985; Yang et al., 1988a, b). It has been proposed that interplexiform cells may also release dopamine upon steady illumination because horizontal cells' receptive fields shrink in the light (Shigematsu & Yamada, 1988). Here, we report the shrinkage of the receptive fields of horizontal cells seen in the presence of background illumination is not blocked by dopamine antagonists, indicating that dopamine does not underlie the receptive-field size changes observed during steady illumination. Flickering light, however, does appear to stimulate the release of dopamine from the interplexiform cells, resulting in a marked reduction of horizontal cell receptive-field size. Taken together, experiments on horizontal cells indicate that dopamine is released from interplexiform cells in the teleost retina after prolonged darkness and during flickering light, but that dopamine release from interplexiform cells during steady retinal illumination is minimal.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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References

Baldridge, W.H. & Ball, A.K. (1991). Background illumination reduces horizontal cell receptive-field size in both normal and 6-hydroxydopamine-lesioned goldfish retinas. Visual Neuroscience 7, 441450.CrossRefGoogle ScholarPubMed
Baldridge, W.H., Ball, A.K. & Miller, R.G. (1987). Dopaminergic regulation of horizontal cell gap-junction particle density in goldfish retina. Journal of Comparative Neurology 265, 428436.CrossRefGoogle ScholarPubMed
Byzov, A.L. & Trifonov, Y.A. (1968). The response to electric stimulation of horizontal cells in the carp retina. Vision Research 8, 817822.CrossRefGoogle ScholarPubMed
Byzov, A.L., Trifonov, Y.A. & Chailahian, L.M. (1971). Effect of polarization of horizontal cells of the pike retina on spread of their electrical potentials. Neurofiziologiya 4, 9096.Google Scholar
Byzov, A.L., Trifonov, Y.A., Chailahian, L.M. & Golubtzov, K.W. (1977). Amplification of graded potentials in horizontal cells of the retina. Vision Research 17, 265273.CrossRefGoogle ScholarPubMed
Chino, Y.M. & Hashimoto, Y. (1986). Dopaminergic amacrine cells in the retina of Japanese dace. Brain Research 372, 323337.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1989). Light-induced dopamine release from teleost retinas acts as a light-adaptive signal to the retinal pigment epithelium. Journal of Neurochemistry 53, 870878.CrossRefGoogle Scholar
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. Journal of Physiology 414, 351375.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
Dowling, J.E. & Watling, K.J. (1981). Dopaminergic mechanisms in the teleost retina, II: Factors affecting the accumulation of cyclic AMP in pieces of intact carp retina. Journal of Neurochemistry 36, 569579.CrossRefGoogle ScholarPubMed
Dowling, J.E., Pak, M.W. & Lasater, E.M. (1985). White perch horizontal cells in culture: methods, morphology, and process growth. Brain Research 360, 331338.CrossRefGoogle ScholarPubMed
Hamasaki, D.I., Trattler, W.B. & Hajek, A.S. (1986). Light ON depresses and light OFF enhances the release of dopamine from the cat's retina. Neuroscience Letters 68, 112116.CrossRefGoogle ScholarPubMed
Hedden, W.L. & Dowling, J.E. (1978). The interplexiform cells system, II: Effects of dopamine on goldfish retinal neurons. Proceedings of the Royal Society B (London) 201, 2755.Google Scholar
Iuvone, P.M., Galli, C.L., Garrison-Gund, C.K. & Neff, N.H. (1978). Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine neurons. Science 202, 901902.CrossRefGoogle ScholarPubMed
Kamermans, M., van Kijk, B.W. & Spekreijse, J.H. (1989). Lateral feedback from monophasic horizontal cells to cones in the carp retina, II: A quantitative model. Journal of General Physiology 93, 695714.CrossRefGoogle ScholarPubMed
Kaneko, A. (1971). Electrical connexions between horizontal cells in the dogfish retina. Journal of Physiology 213, 95105.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1986). Effects of γ-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology 373, 443461.CrossRefGoogle ScholarPubMed
Kirsch, M. & Wagner, H. (1989). Release pattern of endogenous dopamine in teleost retinae during light adaptation and pharmacological stimulation. Vision Research 29, 147154.CrossRefGoogle ScholarPubMed
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437439.CrossRefGoogle ScholarPubMed
Knapp, A.G., Schmidt, K.F. & Dowling, J.E. (1990). Dopamine modulates the kinetics of ion channels gated by excitatory amino acids in retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 87, 767771.CrossRefGoogle ScholarPubMed
Kramer, S.G. (1971). Dopamine: a retinal neurotransmitter, I: Retinal uptake, storage, and light-stimulated release of [3H]-dopamine in vivo. Investigative Ophthalmology 10, 438452.Google ScholarPubMed
Kurz-Isler, G. & Wolfburg, H. (1986). Gap junctions between horizontal cells in the cyprinid fish alter rapidly their structure during light and dark adaptation. Neuroscience Letters 67, 712.CrossRefGoogle ScholarPubMed
Lamb, T.D. (1976). Spatial properties of horizontal cell responses in the turtle retina. Journal of Physiology 263, 239255.CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. (1985). Electrical coupling between pairs of isolated fish horizontal cells is modulated by dopamine and cAMP. In Gap Junctions, ed. Bennett, M.V.L. & Spray, D.C., pp. 393404. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.Google Scholar
Mangel, S.C. & Dowling, J.E. (1985). Responsiveness and receptive-field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science 229, 11071109.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Dowling, J.E. (1987). The interplexiform-horizontal cell system of the fish retina: effects of dopamine, light stimulation, and time in the dark. Proceedings of the Royal Society B (London) 231, 91121.Google Scholar
Naka, K.-I. & Rushton, W.A.H. (1967). The generation and spread of S-potentials in fish (Cyprinidae). Journal of Physiology 192, 437461.CrossRefGoogle ScholarPubMed
Negishi, K. & Drujan, B. (1979). Reciprocal changes in center and surround S-potentials of fish retina in response to dopamine. Neurochemical Research 4, 313318.CrossRefGoogle ScholarPubMed
Negishi, K.T., Teranishi, T. & Kato, S. (1983). GABA antagonist bicuculline exerts its uncoupling action on external horizontal cells through dopamine cells in carp retina. Neuroscience Letters 37, 261266.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap-junction permeability induced by dopamine and cyclic adenosine 3′:5′-monophosphate in horizontal cells of turtle retina. Journal of Neuroscience 4, 24772488.CrossRefGoogle ScholarPubMed
Shigematsu, Y. & Yamada, M. (1988). Effects of dopamine on spatial properties of horizontal cell responses in the carp retina. Neuroscience Research (Suppl.) 8, s69–s80.Google ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye coupling between external horizontal cells in carp retina. Nature 301, 243246.CrossRefGoogle ScholarPubMed
Teranishi, T. & Negishi, K. (1986). Dendritic morphology of dopaminergic cells revealed by intracellular injection of Lucifer yellow in fixed carp retina. Brain Research 370, 196199.CrossRefGoogle ScholarPubMed
Tornqvist, K., Yang, X.-L. & Dowling, J.E. (1988). Modulation of cone horizontal cell activity in the teleost fish retina, III: Effects of prolonged darkness and dopamine on electrical coupling between horizontal cells. Journal of Neuroscience 8(7), 22792288.CrossRefGoogle ScholarPubMed
Trifonov, Y.A. (1968). Study of synaptic transmission between photoreceptors and horizontal cells by means of electrical stimulation of the retina. Biofizika 13, 809817.Google Scholar
Umino, O., Watanabe, K. & Hashimoto, Y. (1989). Neural mechanisms of chromatic adaptation in L-type cone horizontal cells of the carp retina. The Japanese Journal of Physiology 39, 725742.CrossRefGoogle ScholarPubMed
Umino, O. & Dowling, J.E. (1991). Dopamine release from interplexiform cells in the retina. Effects of GnRH, FMRFamide, bicuculline, and enkephalin on horizontal cell activity. Journal of Neuroscience (in press).CrossRefGoogle ScholarPubMed
Weiler, R., Kolbinger, W. & Kohler, K. (1989). Reduced light responsiveness of the cone pathway during prolonged darkness does not result from an increase of dopaminergic activity in the fish retina. Neuroscience Letters 99, 214218.CrossRefGoogle Scholar
Yang, X.-L., Tornqvist, K. & Dowling, J.E. (1988a). Modulation of cone horizontal cell activity in the teleost fish retina, I: Effects of prolonged darkness and background illumination on light responsiveness. Journal of Neuroscience 8(7), 22592268.CrossRefGoogle ScholarPubMed
Yang, X.-L., Tornqvist, K. & Dowling, J.E. (1988b). Modulation of cone horizontal cell activity in the teleost fish retina, II: Role of interplexiform cells and dopamine in regulating light responsiveness. Journal of Neuroscience 8(7), 22692278.CrossRefGoogle ScholarPubMed
Zucker, C. & Dowling, J.E. (1987). Centrifugal fibers synapse on interplexiform cells in teleost retina. Nature 330, 166168.CrossRefGoogle ScholarPubMed