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Modulation of endogenous dopamine release in the turtle retina: Effects of light, calcium, and neurotransmitters

Published online by Cambridge University Press:  02 June 2009

Walter Kolbinger
Affiliation:
Department of Anatomy and Cell Biology, University of Ulm, 89081 Ulm, Germany
Reto Weiler
Affiliation:
Department of Neurobiology, University of Oldenburg, 26129 Oldenburg, Germany

Abstract

In the turtle retina, dopamine has been observed in a small population of amacrine cells. Whereas the effect of dopamine has been intensively studied, knowledge about the release of this transmitter and the neuronal control of its release are still poorly understood. We therefore decided to study the release of endogenous dopamine. Isolated retinas were superfused with Ringer’s solutions and stimulated with increased potassium, light, or drugs which interfere with neurotransmitter systems. Dopamine was analyzed by using aluminum-oxide extraction and high-pressure liquid chromatography (HPLC) with electrochemical detection. Increased potassium (25 mM) caused a five-fold increase in the basal release. When calcium was replaced by cobalt, no increase was induced by 25 mM potassium. Flickering light increased the basal release of endogenous dopamine by a factor of three. The effect of flickering light was greater in the presence of additional steady background illumination. Kainate (10 μM), an agonist for excitatory amino acids, doubled the basal dopamine release. Bicuculline (10 μM), a γ-amino butyric acid (GABA) antagonist, increased the release to about six times the basal level. Naloxone (10 μM), an opiate antagonist, increased the release to eight times the basal level. These findings suggest that dopamine is released from amacrine cells in the turtle retina in a calcium-dependent manner, which is most likely a vesicular release. Dopamine release is induced by flickering light vs. darkness and vs. steady background illumination. A moderate background illumination alone does not significantly increase basal dopamine release. Drug treatment during the release experiments suggests that dopaminergic neurons receive an excitatory input either directly or indirectly from glutamatergic bipolar and/or amacrine cells and inhibitory inputs either directly or indirectly from GABAergic amacrine cells and from enkephalinergic amacrine cells or efferent fibers.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1993

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References

Ball, A.K., Kolbinger, W. & Weiler, R. (1988). Contacts between GABAergic and dopaminergic amacrine cells in the turtle retina. Investigative Ophthalmology and Visual Science 29, 272.Google Scholar
Bauer, B., Ehinger, B. & Aberg, L. (1980). [3H]-Dopamine release from the rabbit retina. Albrecht von Graefes Archiv für klinische und experimentelle Ophthalmologie 215, 7986.Google Scholar
Boatright, J.H., Hoel, M.J. & Iuvone, P.M. (1989). Stimulation of endogenous dopamine release and metabolism in amphibian retina by light- and K+-evoked depolarization. Brain Research 482, 164168.Google Scholar
Brainard, G.C. & Morgan, W.W. (1987). Light-induced stimulation of retinal dopamine: A dose-response relationship. Brain Research 424, 199203.Google Scholar
Cajal, S.R.Y (1893). La rétine des vertébrés. La Cellule 9, 119257.Google Scholar
Dong, C.-J. & McReynolds, J.S. (1991). The relationship between light, dopamine release, and horizontal cell coupling in the mudpuppy retina. Journal of Physiology 440, 291309.Google Scholar
Dong, C.-J. & McReynolds, J.S. (1992). Comparison of the effects of flickering and steady light on dopamine release and horizontal cell coupling in the mudpuppy retina. Journal of Neurophysiology 67, 364372.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. & Weiner, N. (1982). Enkephalins modulate [3H]-dopamine release from rabbit retina in vitro. Journal of Pharmacology and Experimental Therapeutics 244, 634639.Google Scholar
Ehinger, B. (1976). Biogenic monoamines as transmitters in the retina. In Transmitters in the Visual Process, ed. Bonting, S.L., pp. 364375. Oxford, England: Pergamon Press.Google Scholar
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. & Dowling, J.E. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 83218325.CrossRefGoogle ScholarPubMed
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. & Karten, H.J. (1983). Characterization and quantification of peptidergic amacrine cells in the turtle retina: Enkephalin, neurotensin, and glucagon. Journal of Comparative Neurology 221, 371381.CrossRefGoogle ScholarPubMed
Frederick, J.M., Rayborn, M.E., Laties, A.M., Lam, D.M.-K. & Hollyfield, J.G. (1982). Dopaminergic neurons in the human retina. Journal of Comparative Neurology 210, 6579.CrossRefGoogle ScholarPubMed
Godley, B.F. & Wurtman, R.J. (1988). Release of endogenous dopamine from the superfused rabbit retina in vitro: Effect of light stimulation. Brain Research 452, 393395.Google Scholar
Herdon, H. & Nahorski, S.R. (1987). Comparison between radiola-belled and endogenous dopamine release from striatal slices: Effects of electrical-field stimulation and regulation by D2-autoreceptors. Naunyn-Schmiedeberg’s Archives of Pharmacology 335, 238242.Google Scholar
Herdon, H., Strupish, J. & Nahorski, S.R. (1985). Differences between the release of radiolabelled and endogenous dopamine from superfused rat brain slices: Effects of depolarizing stimuli, amphetamine, and synthesis inhibition. Brain Research 348, 309320.Google Scholar
Ishita, S., Negishi, K., Teranishi, T., Shimada, Y. & Kato, S. (1988). GABAergic inhibition on dopaminergic cells of the fish retina: A [3H]-dopamine release study with isolated cell fractions. Journal of Neurochemistry 50, 16.Google Scholar
Kirsch, M. & Wagner, H.-J. (1989). Release pattern of endogenous dopamine during light adaptation and pharmacological stimulation. Vision Research 29, 147154.Google Scholar
Kolb, H., Cline, C, Wang, H.H. & Brecha, N. (1987). Distribution and morphology of dopaminergic amacrine cells in the retina of the turtle (Pseudemys scripta elegans). Journal of Neurocytology 16, 577588.Google Scholar
Kolbinger, W., Kohler, K., Oetting, H. & Weiler, R. (1990). Endogenous dopamine and cyclic events in the fish retina. I. HPLC assay of total content, release, and metabolic turnover during different light/dark cycles. Visual Neuroscience 5, 143149.Google Scholar
Kramer, S.G. (1971). Dopamine: A retinal neurotransmitter. I. Retinal uptake, storage, and light-stimulated release of [H3]-dopamine in vivo. Investigative Ophthalmology 10, 438452.Google Scholar
Liang, N.Y. & Rutledge, C.O. (1982). Evidence for carrier-mediated efflux of dopamine from corpus striatum. Biochemical Pharmacology 31, 24792484.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 5596.CrossRefGoogle ScholarPubMed
Nguyen-Legros, J., Versaux-Botteri, C, Vigny, A. & Raoux, N. (1985). Tyrosine hydroxylase immunohistochemistry fails to demonstrate dopaminergic interplexiform cells in the turtle retina. Brain Research 339, 323328.Google Scholar
O'Connor, P., Dorison, S.J., Waiting, K.J. & Dowling, J.E. (1986). Factors affecting release of [3H]-dopamine from perfused carp retina. Journal of Neuroscience 6, 18571865.Google Scholar
O'Connor, P.M., Zucker, C.L. & Dowling, J.E. (1987). Regulation of dopamine release from interplexiform cell processes in the outer plexiform layer of the carp retina. Journal of Neurochemistry 49, 916920.CrossRefGoogle ScholarPubMed
Perlman, I., Normann, R.A. & Anderton, P.J. (1987). The effects of prolonged superfusions with acidic amino acids and their agonists on field potentials and horizontal cell photoresponses in the turtle retina. Journal of Neurophysiology 57, 10221032.Google Scholar
Piccolino, M., Neyton, J. & Gerschenfeld, H.M. (1984). Decrease of gap-junction permeability induced by dopamine and cyclic aden-osine 3′,5′-monophosphate in horizontal cells of turtle retina. Journal of Neuroscience 4, 24772488.Google Scholar
Piccolino, M., Witkovsky, P. & Trimarchi, C. (1987). Dopaminergic mechanisms underlying the reduction of electrical coupling between horizontal cells of the turtle retina induced by d-amphet-amine, bicuculline, and veratridine. Journal of Neuroscience 7, 22732284.Google Scholar
Pollard, J. & Eldred, W.D. (1990). Synaptic analysis of amacrine cells in the turtle retina which contain tyrosine hydroxylase-like immunoreactivity. Journal of Neurocytology 19, 5366.Google Scholar
Sarthy, P.V. & Lam, D.M.-K. (1979). The uptake and release of [3H]-dopamine in the goldfish retina. Journal of Neurochemistry 32, 12691277.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 Scholar
Teranishi, T., Negism, K. & Kato, S. (1984). Regulatory effect of dopamine on spatial properties of horizontal cells in carp retina. Journal of Neuroscience 4, 12711280.Google Scholar
Weiler, R. (1985). Mesencephalic pathway to the retina exhibits enkephalin-like immunoreactivity. Neuroscience Letters 55, 1116.Google Scholar
Weiler, R. & Akopian, A. (1992). Effects of background illuminations. on the receptive-field size of horizontal cells in the turtle retina are mediated by dopamine. Neuroscience Letters 140, 121124.Google Scholar
Weiler, R. & Ball, A.K. (1984). Co-localization of neurotensin-like immunoreactivity and [3H]-glycine uptake system in sustained amacrine cells of the turtle retina. Nature 311, 759761.Google Scholar
Weiler, R., Kohler, K., Wagner, H.-J. & Wolburg, H. (1988). Neuromodulation in the retinas of lower vertebrates. Neuroscience Research (Suppl.) 8, S183S196.Google Scholar
Weiler, R. & Ball, A.K. (1989). Enkephalinergic modulation of the dopamine system in the turtle retina. Visual Neuroscience 3, 455461.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
Weiler, R. & Schütte, M. (1985). Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of a turtle Pseudemys scripta elegans. Cell and Tissue Research 241, 373382.Google Scholar
Witkovsky, P., Eldred, W. & Karten, H.J. (1984). Catecholamine-and indoleamine-containing neurons in the turtle retina. Journal of Comparative Neurology 228, 217225.Google Scholar