Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-29T20:17:16.765Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of serotonergic agonists and antagonists on ganglion cells in the goldfish retina

Published online by Cambridge University Press:  02 June 2009

Steven H. Hensley  and
Joel L. Cohen
Steven H. Hensley
Affiliation:
Biomedical Sciences Ph.D. Program and Department of Anatomy and School of Medicine and School of Science and Mathematics, Wright State University, Dayton, Ohio
Joel L. Cohen
Affiliation:
Biomedical Sciences Ph.D. Program and Department of Anatomy and School of Medicine and School of Science and Mathematics, Wright State University, Dayton, Ohio
Get access Rights & Permissions [Opens in a new window]

Abstract

Extracellular recordings were made from the isolated goldfish retina during superfusion with various serotonergic agonists and antagonists to determine the effects of these drugs on the maintained activity and response properties of the ganglion cells. Superfusion of the retina with serotonin (25–500 μM) increased the maintained activity of OFF-center ganglion cells and decreased the maintained activity of ON-center ganglion cells. In addition, serotonin also attenuated the excitatory responses to annular stimuli, suggesting a decrease in the strength of surround input to the ganglion cells. The effects of serotonin on OFF-center ganglion cells were mimicked by the nonselective 5-HT1, agonist 5-MeOT and the 5-HT1 receptor agonist 8-OH-DPAT, while only 5-MeOT mimicked the action of serotonin on ON-center ganglion cells. The effects of exogenously applied serotonin on the ganglion cells could be blocked by the mixed 5-HT1/5-HT2 receptor antagonist methysergide but not by the 5-HT2 receptor antagonist mianserin or the dopamine receptor antagonist haloperidol.

These results support previous anatomical and biochemical evidence that serotonin functions in a neurotransmitter or neuromodulatory role in the teleost retina and suggest that serotonin may be involved in modulating the maintained activity and surround input to the ganglion cells. The results also indicate that two different types of receptors may mediate the actions of serotonin in the ON and OFF pathways, respectively.

Keywords

Ganglion cellGoldfishMaintained activityReceptive fieldSerotoninTeleost
Type
Research Articles
Information
Visual Neuroscience , Volume 9 , Issue 3-4 , October 1992 , pp. 353 - 364
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adolph, A.R. (1989). Pharmacological actions of peptides and indoleamines on turtle retinal ganglion cells. Visual Neuroscience 3, 411–423.CrossRefGoogle ScholarPubMed
Arvidsson, L.-E., Hacksell, V., Nilsson, J.L.G., Hjorth, S., Carlsson, A., Lindberg, P., Sanchez, D. & Wilkstrom, H. (1981). 8-Hydroxy-2-(di-n-propylamino)tetralin, a new centrally acting 5-hydroxytryptamine receptor agonist. Journal of Medicinal Chemistry 24, 921–923.CrossRefGoogle ScholarPubMed
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957). Change of organization in the receptive fields of the cat's retina during dark adaptation. Journal of Physiology 137, 338–354.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1982). Sustained synaptic input to ganglion cells of mudpuppy retina. Journal of Physiology 326, 91–108.CrossRefGoogle ScholarPubMed
Bradley, P.B., Encel, G., Feniuk, W., Fozard, J.R., Humphrey, P.P.A., Middlemiss, D.N., Mylecharane, E.J., Richardson, B.P. & Saxena, P.R. (1986). Proposals for the classification and nomenclature of functional receptors for 5-hydroxytryptamine. Neuropharmacology 25, 563–576.CrossRefGoogle ScholarPubMed
Brunken, W.J. & Daw, N.W. (1988). Neuropharmacological analysis of the role of indoleamine-accumulating amacrine cells in the rabbit retina. Visual Neuroscience 1, 275–285.CrossRefGoogle ScholarPubMed
Daw, N.W. (1968). Colour-coded ganglion cells in the goldfish retina: Extension of their receptive fields by means of new stimuli. Journal of Physiology 197, 567–592.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: II. Modulation by gamma-aminobutyric acid and serotonin. Journal of Neurochemistry 46, 1022–1031.CrossRefGoogle ScholarPubMed
Devivo, M. & Maayani, S. (1986). Characterization of the 5-hydroxy-tryptamine1A receptor-mediated inhibition of forskolin-stimulated adenylate cyclase activity of guinea pig and rat hippocampal membranes. Journal of Pharmacology and Experimental Therapeutics 238, 248–253.Google Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Dowling, J.E. & Watling, K.J. (1981). Dopaminergic mechanisms in the teleost retina. 11. Factors affecting the accumulation of cyclic AMP in pieces of intact carp retina. Journal of Neurochemistry 36, 569–579.CrossRefGoogle Scholar
Dumuis, A., Bouhelal, R., Sebben, M., Cory, R. & Bockaert, J. (1989). A nonclassical 5-hydroxytryptamine receptor positively coupled with adenylate cyclase in the central nervous system. Molecular Pharmacology 34, 880–887.Google Scholar
Ehinger, B. & Floren, I. (1976). Indoleamine-accumulating neurons in the retina of rabbit, cat and goldfish. Cell and Tissue Research 175, 37–48.CrossRefGoogle Scholar
Famiglietti, E.V. Jr, Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of on and off pathways to ganglion cells in carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Clennon, R.A. (1987). Central serotonin receptors as targets for drug research. Journal of Medicinal Chemistry 30, 1–12.CrossRefGoogle Scholar
Gurevich, N., Wu, P.H. & Carlen, P.L. (1990). Serotonin agonist and antagonist actions in hippocampal CAI neurons. Canadian Journal of Physiology and Pharmacology 68, 586–595.CrossRefGoogle Scholar
Hedden, W.L. Jr & Dowling, J.E. (1978). The interplexiform cell system. II. Effects of dopamine on goldfish retinal neurones. Proceedings of the Royal Society B (London) 201, 27–55.Google ScholarPubMed
Herrick-Davis, K. & Titeler, M. (1988). Detection and characterization of the serotonin 5-HT1D receptor in rat and human brain. Journal of Neurochemistry 50, 1624–1631.CrossRefGoogle Scholar
Holmgren-Taylor, I. (1983). Synaptic organization of the indoleamine-accumulating neurons in the cyprinid retina. Cell and Tissue Research 229, 317–335.Google ScholarPubMed
Hoyer, D. (1988). Functional correlates of serotonin 5-HT1, recognition sites. Journal of Receptor Research 8, 59–81.CrossRefGoogle ScholarPubMed
Hoyer, D., Engel, G. & Kalkman, H.O. (1985). Molecular pharmacology of 5-HT1 and 5-HT2 recognition sites in rat and pig brain membranes: Radioligand binding studies with, [3H’5-HT, [3H]8-OH-DPAT, (-)[125I]iodocyanopindolol, [3H]mesulergine and [3H]ketanserin. European Journal of Pharmacology 118, 13–23.CrossRefGoogle Scholar
Jensen, R.J. (1991). Involvement of glycinergic neurons in the diminished surround activity of ganglion cells in the dark-adapted rabbit retina. Visual Neuroscience 6, 43–53.CrossRefGoogle ScholarPubMed
Kaneko, A. (1973). Receptive field organization of bipolar and amacrine cells in the goldfish retina. Journal of Physiology 235, 133–153.CrossRefGoogle ScholarPubMed
Kaneko, A., Nishimura, Y., Tachibana, M., Tauchi, M. & Shimai, K. (1981). Physiological and morphological studies of signal pathways in the carp retina. Vision Research 21, 1519–1526.CrossRefGoogle ScholarPubMed
Kato, S., Sugawara, K. & Negishi, K. (1983). Light-evoked and antidromic activation of ganglion cells of the carp retina in a chloride free medium. Vision Research 23, 1745–1747.CrossRefGoogle Scholar
Kato, S., Teranishi, T., Kuo, C.H. & Negishi, K. (1982). 5-Hydroxy-tryptamine stimulates [3H]dopamine release from the fish retina. Journal of Neurochemistry 39, 493–498.CrossRefGoogle ScholarPubMed
Levine, M.W., Saleh, E.J. & Yarnold, P.R. (1988). Statistical properties of the maintained discharge of chemically isolated ganglion cells in goldfish retina. Visual Neuroscience 1, 31–46.CrossRefGoogle ScholarPubMed
Levine, M.W. & Shefner, J.M. (1977). Variability in ganglion cell firing patterns; implications for separate “on” and “off” processes. Vision Research 17, 765–776.CrossRefGoogle Scholar
Marc, R.E., Liu, W-L.S., Scholz, K. & Muller, J.F. (1988). Serotonergic and serotonin-accumulating neurons in the goldfish retina. Journal of Neuroscience 8, 3427–3450.CrossRefGoogle ScholarPubMed
Marshak, D., Ariel, M. & Brown, E. (1988). Distribution of synaptic inputs onto goldfish retinal ganglion cell dendrites. Experimental Eye Research 46, 965–978.CrossRefGoogle ScholarPubMed
Masland, R.H. & Ames, A. (1976). Responses to acetylcholine of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.CrossRefGoogle Scholar
Miller, R.F. & Dacheux, R.F. (1976a). Synaptic organization and ionic basis of on and off channels in mudpuppy retina. II. Chloride-dependent ganglion cell mechanisms. Journal of General Physiology 67, 661–678.CrossRefGoogle Scholar
Miller, R.F. & Dacheux, R.F. (1976b). Synaptic organization and ionic basis of on and off channels in mudpuppy retina. III. A model of ganglion cell receptive field organization based on chloride-free experiments. Journal of General Physiology 67, 679–690.CrossRefGoogle Scholar
Negishi, K. & Drujan, B. (1979). Effects of catecholamines and related compounds on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 311–334.CrossRefGoogle ScholarPubMed
O'connor, P., Dorison, S.J., Watling, K.J. & Dowling, J.E. (1986). Factors affecting release of 3H-dopamine from perfused carp retina. Journal of Neuroscience 6, 1857–1865.CrossRefGoogle ScholarPubMed
Osborne, N.N. (1984). Indoleamines in the eye with special reference to the serotonergic neurones of the retina. In Progress in Retinal Research, ed. Osborne, N.N. & Chader, G.J., pp. 61–103. Oxford: Pergamon Press.Google Scholar
Osborne, N.N. (1990). Effects Of Gtp, Forskolin, Sodium Fluoride, Serotonin, Dopamine, And Carbachol On Adenylate Cyclase In Teleost Retina. Neurochemical Research 15, 523–528.CrossRefGoogle ScholarPubMed
Osborne, N.N., Nesselhut, T., Nicholas, D.A., Patel, S. & Cuello, A.C. (1982). Serotonin-containing neurons in vertebrate retinas. Journal of Neurochemistry 39, 1519–1528.CrossRefGoogle ScholarPubMed
Redburn, D.A. (1985). Serotonin neurotransmitter systems in vertebrate retina. In Retinal Neurotransmitters and Modulators: Models for the Brain, ed. Morgan, W.W., pp. 107–122. Boca Raton, Florida: CRC Press, Inc.Google Scholar
Richardson, B.P. & Hoyer, D. (1990). Selective agonists and antagonists at 5-hydroxytryptamine receptor subtypes. In Serotonin — From Cell Biology to Pharmacology and Therapeutics, ed. Paoletti, R., Vanhoutte, P.M., Brunelle, N. & Maggi, F.M., pp. 265–276. Boston, Massachusetts: Kluwer Academic Publishers.Google Scholar
Sakai, H.M. & Naka, K-I. (1988). Dissection of the neuron network in the catfish inner retina. I. Transmission to ganglion cells. Journal of Neurophysiology 60, 1549–1567.CrossRefGoogle ScholarPubMed
Schmidt, A.W. & Peroutka, S.J. (1989). 5-Hydroxytryptamine receptor “families”. FASEB Journal 3, 2242–2249.CrossRefGoogle ScholarPubMed
Schoeffter, P. & Hoyer, D. (1988). Centrally acting hypotensive agents with affinity for 5-HT1A binding sites inhibit forskolin-stimulated adenylate cyclase activity in calf hippocampus. British Journal of Pharmacology 95, 975–985.CrossRefGoogle ScholarPubMed
Sharp, T., Bramwell, S.R., Hjorth, S. & Grahame-Smith, D.G. (1989). Pharmacological characterization of 8-OH-DPAT-induced inhibition of rat hippocampal 5-HT release in vivo as measured by microdialysis. British Journal of Pharmacology 98, 989–997.CrossRefGoogle ScholarPubMed
Shefner, J.M. & Levine, M.W. (1979). A comparison of properties of goldfish retinal ganglion cells as a function of lighting conditions during dissection. Vision Research 19, 83–89.CrossRefGoogle ScholarPubMed
Shenker, A., Maayani, S., Weinstein, H. & Green, J.P. (1987). Pharmacological characterization of two 5-hydroxytryptamine receptors coupled to adenylate cyclase in guinea pig hippocampal membranes. Molecular Pharmacology 31, 357–367.Google ScholarPubMed
Snodderly, D.M. Jr (1973). Extracellular single unit recording. In Bioelectric Recording Techniques, Part A. Cellular Processes and Brain Potentials, ed. Thompson, R. & Patterson, M., pp. 137–163. New York: Academic Press.Google Scholar
Spekreijse, H., Wagner, H.G. & Wolbarsht, M.L. (1972). Spectral and spatial coding of ganglion cell responses in goldfish retina. Journal of Neurophysiology 35, 73–86.CrossRefGoogle ScholarPubMed
Starke, K., Gothert, M. & Kilbinoer, H. (1989). Modulation of neurotransmitter release by presynaptic autoreceptors. Physiological Reviews 69, 864–989.CrossRefGoogle ScholarPubMed
Thibos, L.N. & Werblin, F.S. (1978a). The response properties of the steady antagonistic surround in the mudpuppy retina. Journal of Physiology 278, 79–99.CrossRefGoogle ScholarPubMed
Thibos, L.N. & Werblin, F.S. (1978b). The properties of surround antagonism elicited by spinning windmill patterns in the mudpuppy retina. Journal of Physiology 278, 101–116.CrossRefGoogle ScholarPubMed
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 351, 613–630.CrossRefGoogle ScholarPubMed
Tornqvist, K., Hansson, C.H. & Ehinger, B. (1983). Immunohisto-chemical and quantitative analysis of 5-hydroxytryptamine in the retina of some vertebrates. Neurochemistry International 5, 299–308.CrossRefGoogle Scholar
Van Buskirk, R. & Dowling, J.E. (1981). Isolated horizontal cells from carp retina demonstrate dopamine-dependent accumulation of cyclic AMP. Proceedings of the National Academy of Sciences of the U.S.A. 78, 7825–7829.CrossRefGoogle ScholarPubMed
Waeber, C., Schoeffter, P., Pazos, A., Palacios, J.M. & Hoyer, D. (1988). Molecular pharmacology of 5-HT1D recognition sites: Radioligand binding studies in human, pig and calf brain membranes. Naunyn-Schmiedeberg's Archives of Pharmacology 337, 595–601.CrossRefGoogle ScholarPubMed
Watling, K.J. & Dowling, J.E. (1981). Dopamine mechanisms in the teleost retina. I. Dopamine-sensitive adenylate cyclase in homogenates of carp retina: Effects of agonists, antagonists and ergots. Journal of Neurochemistry 36, 559–568.CrossRefGoogle ScholarPubMed
Wunk, D.F. & Werblin, F.S. (1979). Synaptic inputs to the ganglion cells in the tiger salamander retina. Journal of General Physiology 73, 265–286.CrossRefGoogle Scholar