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Neuropharmacological analysis of the role of indoleamine-accumulating amacrine cells in the rabbit retina

Published online by Cambridge University Press:  02 June 2009

William J. Brunken
Affiliation:
Department of Cell Biology and Physiology, Washington University, St. Louis Department of Biology, Boston College, Chestnut Hill
Nigel W. Daw
Affiliation:
Department of Cell Biology and Physiology, Washington University, St. Louis

Abstract

In order to elucidate the role of putative indoleaminergic amacrine cells in visual processing, we have employed pharmacological agents specific for the two classes of serotonin receptor, 5-HT2 and 5-HT1, which have been identified in both the retina and brain. Perfusion of the rabbit retina with 5-HT2 selective antagonists decreases the ON-excitation of all classes of ganglion cell as well as the spontaneous activity of these cells. The effect on OFF-responses depends on the cell type: OFF-excitation of center-surround brisk and sluggish cells is increased or not affected by these drugs, but OFF excitation of ON/OFF direction selective cells is reduced. No disruption of the trigger features of direction selective or orientation selective cells was discovered, suggesting that indoleaminergic amacrine cells do not play a role in the generation of the complex properties of these cells.

5-HT1 receptors are heterogeneous and classified as a, b, or c subtypes. Since no selective antagonists are available for these sites, we have employed specific agonists. The most specific of these are for the 5-HT1A receptor. Perfusion with these agonists had physiological effects similar to those with perfusion of 5-HT2 antagonists. Thus, we have suggested that these two classes of serotonin receptors mediate opponent processes in the neural pathway. Since indoleaminergic cells make reciprocal synaptic connections with rod bipolar cell terminals, which are depolarizing in the rabbit retina, we hypothesize that 5-HT2 receptors facilitate the synaptic transmission from the depolarizing rod bipolar cell thus facilitating ON-excitation in the retinal network while 5-HT1A receptors mediate an inhibitory process. Similar self-opponent processing appears to take place in the hypothalamic and hippocampal serotonergic systems as well as in the dopaminergic retinal system. Thus, it is likely that this organization is a general feature of monoamine signal transmission in the central nervous system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1988

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References

Aghajanian, G.K. (1981). The modulating role of serotonin at multiple receptors in brain. In Serotonin Neurotransmission and Behavior, ed. Jacobs, B.L. & Gelparin, A., pp. 150185. Cambridge, MA: MIT Press.Google Scholar
Ames, A. & Pollen, D.A. (1969). Neurotransmission in central nervous tissue: a study of isolated rabbit retina. Journal of Neurophysiology 32, 424442.CrossRefGoogle ScholarPubMed
Andrade, R. & Nicoll, R.A. (1987 a). Pharmacologically distinct actions of serotonin on single pyramidal neurons of the rat hippocampus recorded in vitro. Journal of Physiology (London) 394, 99124.CrossRefGoogle ScholarPubMed
Andrade, R. & Nicoll, R.A. (1987 b). Novel anxiolytics discriminate between postsynaptic serotonin receptors mediating different physiological responses on single neurons of the rat hippocampus. Naunyn-Schiedeberg's Archives of Pharmacology 336, 510.CrossRefGoogle ScholarPubMed
Barlow, H.B., Hill, R.M. & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. Journal of Physiology (London) 173, 377407.CrossRefGoogle ScholarPubMed
Blazynski, C, Ferrendelli, J.A. & Cohen, A.I. (1985). Indoleamine-sensitive adenylate-cyclase in rabbit retina: characterization and distribution. Journal of Neurochemistry 45, 440447.CrossRefGoogle ScholarPubMed
Brunken, W.J. & Daw, N.W. (1986). 5-HT2 antagonists reduce ON-responses in the rabbit retina. Brain Research 384, 161165.CrossRefGoogle ScholarPubMed
Brunken, W.J. & Daw, N.W. (1987). The actions of serotonergic agonists and antagonists on the activity of brisk ganglion cells in the rabbit retina. Journal of Neuroscience 7, 40544065.CrossRefGoogle ScholarPubMed
Brunken, W.J. & Daw, N.W. (1988). The effects of serotonergic agonists and antagonists on the response properties of complex ganglion cells in the rabbit's retina. Visual Neuroscience 1, 181188.CrossRefGoogle ScholarPubMed
Brunken, W.J., Witkovsky, P. & Karten, H.J. (1986). Retinal neurochemistry of three elasmobranch species: an immunohistochemical approach. Journal of Comparative Neurology 243, 112.CrossRefGoogle ScholarPubMed
Brunn, A., Ehinger, B. & Sytsma, V.M. (1984). Neurotransmitter localization in the skate retina. Brain Research 295, 233248.CrossRefGoogle Scholar
Caldwell, J.H. & Daw, N.W. (1978 a). New properties of rabbit retinal ganglion cells. Journal of Physiology (London) 276, 257276.CrossRefGoogle ScholarPubMed
Caldwell, J.H. & Daw, N.W. (1978 b). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: changes in centre surround receptive field properties. Journal of Physiology (London) 276, 299310.CrossRefGoogle Scholar
Caldwell, J.H., Daw, N.W. & Wyatt, H.J. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. Journal of Physiology (London) 276, 277298.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Levick, W.R. (1974). Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. Journal of Physiology (London) 240, 457492.CrossRefGoogle Scholar
Cohen, M.L., Kruz, K.D., Mason, N.R., Fuller, R.W., Maizoni, G.P. & Grecht, W.L. (1985). Pharmacological activity of the isomers of LY 53857, potent and selective 5-HT2 receptor antagonists. Journal of Pharmacology and Experimental Therapeutics 235, 319323.Google ScholarPubMed
Colino, A. & Halliwell, J.V. (1987). Differential modulation of three separate K+ conductances in hippocampal CA1 neurons by serotonin. Nature 328, 7377.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331345.CrossRefGoogle ScholarPubMed
Daw, N.W., Ariel, M. & Caldwell, J.H. (1982). Function of neurotransmitters in the retina. Retina 2, 322331.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. & Weiner, N. (1985). Pharmacological differences between the D2 autoreceptors and D] dopamine receptor in the rabbit retina. Journal of Pharmacology and Experimental Therapeutics 233, 747754.Google Scholar
Ehinger, B. & Floren, I. (1976). Indoleamine-accumulating neurons in the retina of the rabbit, cat, and goldfish. Cell Tissue Research 175, 3748.CrossRefGoogle Scholar
Ehinger, B. & Holmgren, I. (1979). Electron Microscopy of the indoleamine-accumulating neurons in the retina of the rabbit. Cell Tissue Research 197, 175194.CrossRefGoogle ScholarPubMed
Engel, G., Gothert, M., Hoyer, D., Schlecher, E. & Hillenbrand, K. (1986). Identity of inhibitory presynaptic 5-hydroxytryptamine (5-HT) autoreceptors in rat brain cortex with 5-HT1B binding sites. Naunyn-Schmiedebergs Archives of Pharmacology 317, 277285.CrossRefGoogle Scholar
Fukuda, Y. & Stone, J. (1974). Retinal distribution and cortical projections of X-, Y-, and W-cells of the cat's retina. Journal of Neurophysiology 37, 749772.CrossRefGoogle Scholar
Gozlan, H., El Mestikawy, S., Pichat, L., Glowinski, J. & Hammon, M. (1983). Identification of presynaptic serotonin autoreceptors using a new ligand: 3H-PAT. Nature 305, 140142.CrossRefGoogle ScholarPubMed
Gudelsky, G.A., Koenig, J.I. & Meltzer, H.Y. (1986). Ther-moregulatory responses to serotonin (5-HT) receptor stimulation in the rat. Evidence for opposing roles of 5-HT2 and 5-HT1a receptors. Neuropharmacology 25, 13071313.CrossRefGoogle Scholar
Holmgren-Taylor, I. (1982). Electron microscopical observations on the indoleamine-accumulating neurons and their synaptic connections in the retina of the cat. Journal of Comparative Neurology 208, 144156.CrossRefGoogle ScholarPubMed
Jensen, R.J. & Daw, N.W. (1986). Effects of dopamine and its agonists and antagonists of the receptive field properties of ganglion cells in the rabbit retina. Neuroscience 17, 837855.CrossRefGoogle ScholarPubMed
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.CrossRefGoogle ScholarPubMed
Leysen, J.E., Awouters, F., Kennis, L., Laduron, P.M., Vandenberk, J. & Janssen, P.A.J. (1981). Receptor binding profile of R41 468, a novel antagonist at 5-HT2 receptors. Life Science 28, 10151022.CrossRefGoogle ScholarPubMed
Leysen, J.E., Niemegeers, C.J.E., Van Nueten, J.M. & Laduron, P.M. (1982). [3H] Ketanserin (R41 468), a selective 3-H-ligand for serotonin 2 receptor binding sites. Binding properties, brain distribution, and functional role. Molecular Pharmacology 21, 301314.Google ScholarPubMed
Mangel, S.C., Brunken, W.J. & Miller, R.F. (1987). Serotonin antagonists reduce the efficacy of horizontal to ganglion cell transmission in the inner retina. Society for Neuroscience Abstracts 13, 1055.Google Scholar
Middlemiss, D.N. & Fozard, J.R. (1983). 8-hydroxy-2-(di-n-propylamino) tetralin discrimination between subtypes of the 5-HT, recognition sites. European Journal of Pharmacology 90, 151153.CrossRefGoogle Scholar
Mitchell, C.K. & Redburn, D.A. (1985). Analysis of pre- and post-synaptic factors of the serotonin system in rabbit retina. Journal of Cell Biology 100, 6473.CrossRefGoogle Scholar
Osborne, N.N. (1980). In vitro experiments on the metabolism, uptake, and release of 5-hydroxytryptamine in bovine retina. Brain Research 184, 283297.CrossRefGoogle Scholar
Osborne, N.N. (1981). Binding of [3H] serotonin to membranes of the bovine retina. Experimental Eye Research 33, 371380.CrossRefGoogle ScholarPubMed
Osborne, N.N. (1982). Evidence for serotonin being a neurotransmitter in the retina. In Biology of Serotoninergic Transmission, ed. Osborne, N.N., pp 401430. New York: Wiley and Sons.Google Scholar
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. Journal of Neuroscience 6, 33313347.CrossRefGoogle ScholarPubMed
Smith, R.G., Freed, M.A. & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: functional architecture of rod-cone network. Journal of Neuroscience 6, 35053517.CrossRefGoogle ScholarPubMed
Stanford, L.R. (1987). W-cells in the cat retina: correlated morphological and physiological evidence for two distinct classes. Journal of Neurophysiology 57, 218244.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M.A. & Smith, R.G. (1986). Microcircuitry and functional architecture of the cat retina. Trends in Neuroscience 9, 186192.CrossRefGoogle Scholar
Thier, P. & Wassle, H. (1984). Indoleamine-mediated reciprocal modulation of ON-centre and OFF-centre ganglion cell activity in the retina of the cat. Journal of Physiology (London) 351, 613630.CrossRefGoogle ScholarPubMed
Tornqvist, K.S., Hansson, C. & Ehinger, B. (1983). Immunohistochemical and quantitative analysis of 5-hydroxytryptamine in the retina of some vertebrates. Neurochemistry International 5, 299308.CrossRefGoogle ScholarPubMed
Tricklebank, M.D., Farber, C., Middlemiss, D.N. & Fozard, J.R. (1985). Subtypes of the 5-HT receptor mediating the behavioral responses to 5-methoxy-N, N-dimethyltryptamine in the rat. European Journal of Pharmacology 117, 1524.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1986). Morphological identification of serotonin-accumulating neurons in the living retina. Science 233, 444446.CrossRefGoogle ScholarPubMed
Verge, D., Doval, G., Patey, A., Gozlan, H., El Mestikawy, S. & Hamon, M. (1985). Presynaptic 5-HT autoreceptors on serotoninergic cell bodies and/or dendrites but not terminals are of the 5-HT1A subtype. European Journal of Pharmacology 113, 463464.CrossRefGoogle Scholar
Wassle, H., Voigt, T. & Patel, B. (1987). Morphological and immunocytochemical identification of indoleamine-accumulating neurons in the cat retina. Journal of Neuroscience 7, 15741585.CrossRefGoogle ScholarPubMed
Witkovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholeamine and indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217225.CrossRefGoogle Scholar