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Similar effects of carbachol and dopamine on neurons in the distal retina of the tiger salamander

Published online by Cambridge University Press:  02 June 2009

William A. Hare
Affiliation:
Division of Neurobiology, Department of Molecular and Cell Biology, University of California, Berkeley
W. Geoffrey Owen
Affiliation:
Division of Neurobiology, Department of Molecular and Cell Biology, University of California, Berkeley

Abstract

Though there is considerable evidence that dopamine is an important retinal neuromodulator that mediates many of the changes in the properties of retinal neurons that are normally seen during light adaptation, the mechanism by which dopamine release is controlled remains poorly understood. In this paper, we present evidence which indicates that dopamine release in the retina of the tiger salamander, Ambystoma tigrinum, is driven excitatorily by a cholinergic input. We compared the effects of applying carbachol to those of dopamine application on the responses of rods, horizontal cells, and bipolar cells recorded intracellularly from the isolated, perfused retina of the tiger salamander. Micromolar concentrations of dopamine reduced the amplitudes of rod responses throughout the rods' operating range. The ratio of amplitudes of the cone-driven to rod-driven components of the responses of both horizontal and bipolar cells was increased by activation of both D1 and D2 dopamine receptors. Dopamine acted to uncouple horizontal cells and also off-center bipolar cells, the mechanism in the case of horizontal cells depending only upon activation of D1 receptors. Carbachol, a specific cholinomimetic, applied in five- to ten-fold higher concentrations, produced effects that were essentially identical to those of dopamine. These effects of carbachol were blocked by application of specific dopamine blockers, however, indicating that they are mediated secondarily by dopamine. We propose that the dopamine-releasing amacrine cells in the salamander are under the control of cells, probably amacrine cells, which secrete acetylcholine as their transmitter.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Attwell, D., Werblin, F.S. & Wilson, M. (1982). The properties of single cones isolated from the tiger salamander retina. Journal of Physiology 328, 259283.CrossRefGoogle ScholarPubMed
Besharse, J.C., Iuvone, P.M. & Pierce, M.E. (1988). Regulation of rhythmic photoreceptor metabolism: A role for post-receptoral mechanisms. In Progress in Retinal Research 7, 2161.CrossRefGoogle Scholar
Bigel, V., Wenk, H., Meyer, U. & Luth, H.-J. (1979). Cholinergic mechanisms in the visual system of the rat. Progress in Brain Research 49, 472.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Borges, S. & Wilson, M. (1987). Structure of the receptive fields of bipolar cells in the salamander retina. Journal of Neurophysiology 58, 12751291.CrossRefGoogle ScholarPubMed
Brainard, G.C. & Morgan, W.W. (1987). Light-induced stimulation of retinal dopamine: A dose-response relationship. Brain Research 424, 199203.CrossRefGoogle ScholarPubMed
Capovilla, M., Hare, W.A. & Owen, W.G. (1987). Voltage gain of signal transfer from retinal rods to bipolar cells in the tiger salamander. Journal of Physiology 391, 125140.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986 a). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: I. Induction of cone contraction is mediated by D2 receptors. Journal of Neurochemistry 46, 10061021.CrossRefGoogle ScholarPubMed
Dearry, A. & Burnside, B. (1986 b). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: II. Modulation by γ-aminobutyric acid and serotonin. Journal of Neurochemistry 46, 10221031.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
Dearry, A., Edelman, J., Miller, S. & Burnside, B. (1990). Dopamine induces light-adaptive retinomotor movements in bullfrog cones via D2 receptors, in retinal pigment epithelium via D1 receptors. Journal of Neurochemistry 54, 13671378.CrossRefGoogle ScholarPubMed
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
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.CrossRefGoogle ScholarPubMed
Drujan, B.D., Negishi, K. & Laufer, M. (1980). Studies on putative neurotransmitters in the distal retina. Neurochemistry 1, 143150.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Graham, L.T. (1974). Comparative aspects of neurotransmitters in the retina. In The Eye, Vol. 6, Comparative Physiology, ed. Davson, H. & Graham, L.T., pp. 283342. New York: Academic Press.Google Scholar
Hanani, M. (1993). Receptive field properties of horizontal cells in the tiger salamander retina: Contributions of rods and cones. Vision Research 10, 11151119.Google Scholar
Hare, W.A. & Owen, W.G. (1990 a). Effects of dopamine on rods and horizontal cells in the tiger salamander retina. Investigative Ophthalmology and Visual Science (Suppl.) 31, 334.Google Scholar
Hare, W.A. & Owen, W.G. (1990 b). Spatial organization of the bipolar cell's receptive field in the retina of the tiger salamander. Journal of Physiology 421, 223245.Google ScholarPubMed
Hare, W.A. & Owen, W.G. (1992 a). Effects of 2-amino-4-phosphonobutyric acid on cells in the distal layers of the tiger salamander's retina. Journal of Physiology 445, 741757.CrossRefGoogle ScholarPubMed
Hare, W.A. & Owen, W.G. (1992 b). Dopamine release in the tiger salamander retina: Is it stimulated by a cholinergic synapse? Investigative Ophthalmology and Visual Science (Suppl.) 33, 1405.Google Scholar
Hedden, W.L. & Dowling, J.E. (1978). The interplexiform cell system. II. Effects of dopamine on goldfish retinal neurones. Proceedings of the Royal Society B 201, 2751.Google ScholarPubMed
Kaneko, A. & Shtmazaki, H. (1976). Synaptic transmission from photoreceptors to the second-order neurons in the carp retina. In Neural Principles in Vision, ed. Zettler, F. & Weiler, R., pp. 143157. Berlin-Heidelberg: Springer-Verlag.CrossRefGoogle Scholar
Kirsch, M. & Wagner, H.-J. (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 and Visual Science 5, 143149.Google Scholar
Lamb, T.D. & Simon, E.J. (1976). The relation between intercellular coupling and electrical noise in turtle photoreceptors. Journal of Physiology 263, 257286.CrossRefGoogle ScholarPubMed
Lasater, E.M. (1987). Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase. Proceedings of the National Academy of Sciences of the U.S.A. 84, 73197323.CrossRefGoogle ScholarPubMed
Lasater, E.M. & Dowling, J.E. (1985). Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proceedings of the National Academy of Sciences of the U.S.A. 82, 30253029.CrossRefGoogle ScholarPubMed
Lewis, P.R. & Shute, C.C.D. (1965). Fine localization of acetylcholinesterase in the optic nerve and retina of the cat. Journal of Physiology 180, 8P10P.Google Scholar
Li, T., Wu, S.M., Lam, D.M.K. & Watt, C.B. (1990). Localization of classical neurotransmitters in interneurons of the larval tiger salamander retina. Investigative Ophthalmology and Visual Science 31, 262271.Google ScholarPubMed
Marshall, L.M. & Werblin, F.S. (1978). Synaptic transmission to the horizontal cells in the retina of the larval tiger salamander. Journal of Physiology 279, 321346.CrossRefGoogle Scholar
Naka, K.-I. & Rushton, W.A.H. (1967). The generation and spread of S-potentials in fish (cyprinidae). Journal of Physiology 192, 437471.CrossRefGoogle ScholarPubMed
Neal, M.J. (1983). Cholinergic mechanisms in the vertebrate retina. Progress in Retinal Research 2, 191212.CrossRefGoogle Scholar
Neal, M.J., Cunningham, T.A., Joseph, J.M. & Collins, J.F. (1981). The effect of 2-amino-4-phosphonobutyrate (APB) on acetylcholine release from the rabbit retina: Evidence for on-channel input to cholinergic amacrine cells. Neuroscience Letters 26, 301.CrossRefGoogle ScholarPubMed
Negishi, K. & Drujan, B.D. (1979). Similarities in effects of acetylcholine and dopamine on horizontal cells in the fish retina. Journal of Neuroscience Research 4, 335349.CrossRefGoogle ScholarPubMed
Negishi, K., Teranishi, T. & Kato, S. (1983). A GABA antagonist, bicucculine, exerts its uncoupling action on external horizontal cells through dopamine cells in the carp retina. Neuroscience Letters 37, 261266.CrossRefGoogle 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
Piccolino, M., Neyton, J., Witkovsky, P. & Gerschenfeld, H.M. (1982). γ-Aminobutyric acid antagonists decrease junctional communication between L-type horizontal cells of the retina. Proceedings of the National Academy of Sciences of the U.S.A. 79, 36713675.CrossRefGoogle Scholar
Piccolino, M., Witkovsky, P., Neyton, J., Gerschenfeld, H.M. & Trimarchi, C. (1985). Modulation of gap junction permeability by dopamine and GABA in the network of horizontal cells of the turtle retina. In Microcircuitry of the Retina, a Cajal Memorial, ed. Gallego, A. & Gouras, P., pp. 6676. Amsterdam: Elsevier.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-amphetamine, bicucculine and veratridine. Journal of Neuroscience 7, 22732284.Google Scholar
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movements I. Interaction of melatonin and dopamine in the control of cone length. Journal of General Physiology 86, 671689.CrossRefGoogle ScholarPubMed
Puro, D.G. (1985). Cholinergic systems. In Retinal Transmitters and Modulators: Models for the Brain, Vol. 1, ed. Morgan, W.W., pp. 6391. Chicago, Illinois: CRC Press.Google Scholar
Reading, H.W. (1983). Dopaminergic receptors in bovine retina and their interaction with thyrotropin-releasing hormone. Journal of Neurochemistry 41, 15871595.CrossRefGoogle ScholarPubMed
Ross, C.D. & McDougal, D.B. (1976). The distribution of choline acetyltransferase activity in the vertebrate retina. Journal of Neurochemistry 26, 521526.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1983). Dopamine modulates S-potential amplitude and dye-coupling between horizontal cells in the carp. Nature 301, 243246.CrossRefGoogle Scholar
Watt, C.B., Yang, S.Z., Lam, D.M.K. & Wu, S.M. (1988). Localization of tyrosine-hydroxylase-like immunoreactive amacrine cells in the larval tiger salamander retina. Journal of Comparative Neurology 272, 114126.CrossRefGoogle ScholarPubMed
Weiler, R., Kohler, K., Kolbinger, W., Wolburg, H., Kurz-Isler, G. & Wagner, H.J. (1988). Dopaminergic modulation in the retinas of lower vertebrates. Neuroscience Research (Suppl.) 8, S183–S196.Google Scholar
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
Witkovsky, P. & Dearry, A. (1992). Functional roles of dopamine in the vertebrate retina. Progress in Retinal Research 11, 247290.CrossRefGoogle Scholar
Witkovsky, P., Nicholson, C., Rice, M.E., Bohmaker, K. & Meller, E. (1993). Extracellular dopamine concentration in the retina of the clawed frog, Xenopus laevis. Proceedings of the National Academy of Sciences of the U.S.A. 90, 56675671.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Schutte, M. (1991). The organization of dopaminergic neurons in vertebrate retinas. Visual Neuroscience 7, 113124.CrossRefGoogle ScholarPubMed
Witkovsky, P. & Shi, S.-P. (1990). Slow light and dark adaptation of horizontal cells in the Xenopus retina: A role for endogenous dopamine. Visual Neuroscience 5, 405413.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
Witkovsky, P., Stone, S. & Besharse, J. (1988 a). Dopamine modifies the balance of rod and cone inputs to horizontal cells of the Xenopus retina. Brain Research 449, 332336.CrossRefGoogle ScholarPubMed
Witkovsky, P., Stone, S. & Besharse, J. (1988 b). The effects of dopamine and related ligands on photoreceptor to horizontal cell transfer in the Xenopus retina. Biomedical Research (Suppl. 2) 9, 93107.Google Scholar
Witkovsky, P., Stone, S. & Tranchina, D. (1989). Photoreceptor to horizontal cell synaptic transfer in the Xenopus retina: Modulation by dopamine ligands and a circuit model for interactions of rod and cone inputs. Journal of Neurophysiology 62, 864881.CrossRefGoogle Scholar
Wu, S.M. & Dowling, J.E. (1978). L-Aspartate: Evidence for a role in cone photoreceptor synaptic transmission in the carp retina. Proceedings of the National Academy of Sciences of the U.S.A. 75, 52055209.CrossRefGoogle ScholarPubMed
Yamada, M. & Saito, T. (1988). Effects of dopamine on bipolar cells in the carp retina. Biomedical Research (Suppl. 2) 9, 125130.Google Scholar
Yang, C.-Y., Lukasiewicz, P., Macuire, G., Werblin, F.S. & Yazulla, S. (1991). Amacrine cells in the tiger salamander retina: Morphology, physiology, and neurotransmitter identification. Journal of Comparative Neurology 312, 1932.CrossRefGoogle ScholarPubMed
Zucker, C. & Yazulla, S. (1982). Localization of synaptic and non-synaptic nicotinic-acetylcholine receptors in the goldfish retina. Journal of Comparative Neurology 204, 188195.CrossRefGoogle Scholar