Hostname: page-component-848d4c4894-mwx4w Total loading time: 0 Render date: 2024-06-21T16:30:16.645Z Has data issue: false hasContentIssue false
  • English
  • Français

Slow light and dark adaptation of horizontal cells in the Xenopus retina: A role for endogenous dopamine

Published online by Cambridge University Press:  02 June 2009

Paul Witkovsky  and
Xiao-Ping Shi
Paul Witkovsky
Affiliation:
Daniel B. Kirby Eye Institute, Department of Ophthalmology, New York University Medical Center, New York Department of Physiology and Biophysics, New York University Medical Center
Xiao-Ping Shi
Affiliation:
Daniel B. Kirby Eye Institute, Department of Ophthalmology, New York University Medical Center, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

A role for endogenous dopamine in the control of rod and contributions to a second-order retinal neuron, the horizontal cell (HC) was studied in the Xenopus retina. Relative rod and cone contributions were estimated from HC responses to scotopically balanced 491- and 650-nm flashes. In eyecups prepared in light then placed in darkness, cone input to the HC slowed and diminished on a time scale of hours. The decline in cone input was balanced by a slow growth of rod input to the HC. Administration of D-amphetamine, a dopamine releasing agent, restored the light-adapted waveform.

The kinetics of slow light adaptation were examined by recording HC responses from eyecups that had been dark-adapted previously for 11–14 h. When test flashes fell on a dark field, cone input to the HC grew for 2–4 h, reached a plateau, and later declined. If, however, flashes were superimposed on a weak background field, cone input to the HC continued to increase monotonically at about 10%/h. This increase was abolished by superfusion with a nonspecific dopamine receptor blocker, cis-flupenthixol (50 μM), resulting in the complete suppression of cone-to-horizontal cell synaptic transfer and the enhancement of rod-to-horizontal cell communication. Subcutaneous injection of reserpine, a drug that depletes dopamine stores (2 mg/kg on 1–4 successive days), or intraocular injection of the dopamine neurotoxin, 6-hydroxydopamine (10–30 μg) slowed and reduced the amplitude of cone input to the HC, even in completely light-adapted eyes. Subsequent treatment with D-amphetamine (5–50 μM) or dopamine (10 μM) partially restored the normal response.

Our experimental findings are consistent with the following hypothesis. Weak light is sufficient to stimulate dopamine release; dopamine augments cone-to-horizontal cell synaptic transfer and reduces rod-to-horizontal cell communication. The rapid kinetics of the fully light-adapted response depend on the presence of dopamine. Thus, dopamine appears to be an intraretinal signal for slow light adaptation.

Keywords

Light adaptationDark aptationDopamineHorizontal cellXenopus
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 4 , October 1990 , pp. 405 - 413
Copyright
Copyright © Cambridge University Press 1990

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

Bassic, C.J. & Powers, M.K. (1986). Daily fluctuations in the detectability of dim lights by humans. Physiological Behavior 38, 871–877.Google Scholar
Bassic, C.J. & Powers, M.K. (1987). Circadian rhythm in goldfish visual sensitivity. Investigative Ophthalmology and Visual Science 28,1811–;1815.Google Scholar
Bauer, B., Ehinger, B. & Aberg, L. (1980). [3H]-dopamine release from the rabbit retina. Albrecht Von Graefe's Archiv fr Klinische und Experimentelle Ophthalmologie 215, 71–78.CrossRefGoogle Scholar
Besharese, J.C. & Iuvone, P.M. (1983). Circadian clock in Xenopus eye controlling retinal serotonin N-acetyltransferase. Nature 305,133–135.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, 164–168.Google Scholar
Brainard, G.C. & Morgan, W.W. (1987). Light-induced stimulation of retinal dopamine: a dose-response relationship. Brain Research 424, 199–203.CrossRefGoogle ScholarPubMed
Da, Prada M. (1977). Dopamine content and synthesis in retina and n. accumbens septi: pharmacological and light-induced modifications. In Advances in Biochemistry and Psychopharmacology, ed. Costa, E. & Gessa, G.L., pp. 311–319. New York: Raven Press.Google Scholar
Dearry, A. & Burnside, B. (1986). Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas, I: Induction of cone contraction is mediated by D2 receptors Journal of Neurochemistry 46, 1006–1021.Google Scholar
Djamgoz, M.B.A., Downing, J.E.G., Kirsch, M., Prince, D.J. & Wagner, H.J. (1988). Plasticity of cone horizontal cell functioning in cyprinid fish retina: effects of background illumination of moderate intensity. Journal of Neurocytology 17, 701–710.Google Scholar
Dowling, J.E. & Ripps, H. (1970). Visual adaptation in the retina of the skate. Journal of General Physiology 56, 491–520.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. (1983). Melatonin is a potent modulation of dopamine release in the retina Nature 306, 782–784.Google Scholar
Ehinger, B. (1982). Neurotransmitter systems in the retina. Retina 2, 305–321.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Shapley, R.M. ( 1973). Adaptation and dynamics of cat retinal ganglion cells. Journal of Physiology 233, 271–309.Google Scholar
Fowlkes, D.H., Karwoski, C.J. & Proenza, L.M. (1984). Endogenous circadian rhythm in electroretinogram of free-moving lizards. Investigative Ophthalmology and Visual Science 25, 121–124.Google ScholarPubMed
Gerschenfeld, H.M., Neyton, J., Piccolino, M. & Witkovsky, P. (1982). L-horizontal cells of the turtle: network organization and coupling modulation. In Biomedical Research (suppl.) ed. Kaneko, A., Tsukahara, N. & Uchizono, K., pp. 21–32. Tokyo: Biomedical Research Foundation.Google 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, 27–51.Google ScholarPubMed
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. Sceince 202, 901–912.CrossRefGoogle ScholarPubMed
Jaffe, E.H., Urbina, M., Ayala, C., Drujan, Y. & Drujan, B.D. (1987). Dopamine and noradrenaline content in fish retina: modulation by serotonin. Journal of Neuroscience Research 18, 345–351.CrossRefGoogle ScholarPubMed
Jonsson, G. (1980). Chemical neurotoxins as denervation tools in neurobiology.Annual Review of Neuroscience 3, 169–187.Google Scholar
Kebabian, J.W. & Calne, D.B. (1979). Multiple receptors for dopamine. Nature 277, 93–96.CrossRefGoogle ScholarPubMed
Kirsch, M. & Wagner, H.J. (1989). Release pattern of endogenous dopamine in teleost retinae during light adaptation and pharmacological stimulation. Vision Research 29, 147–154.CrossRefGoogle ScholarPubMed
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino-acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437–439.Google Scholar
Kramer, S.G. (1971). Dopamine: a retinal neurotransmitter, I: Retinal uptake, storage, and light-stimulated release of [3H]-dopamine in vivo. Investigative Ophthalmology 10, 438–452.Google ScholarPubMed
Lamb, T.D., McNaughton, P.A. & Yau, K.-W. (1981). Spatial spread of activation and background desensitization in toad rod outer segments. Journal of Physiology 319, 463–496.Google Scholar
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. 393–404. Cold Spring Harbor: 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, 1107–1109.Google Scholar
Moore, K.E. (1978). The action of amphetamine on neurotransmitters: a brief review. Biological Psychiatry 12, 451–462.Google Scholar
Morgan, W.W. & Kamp, C.W.A. (1980). GABAergic influence on the light-induced increase dopamine turnover in the dark-adapted rat retina. Journal of Neurochemistry 34, 1082–1086.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, 916–920.Google Scholar
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, 2477–2488.Google Scholar
Piccolino, M., Neyton, J., Witkovsky, P. & Gerschenfeld, H.M. (1982). γ-aminobutyric acid antagonists decrease junctional communication between L-horizontal cells of the retina. Proceedings of the National Academy of Sciences of the U.S.A. 79, 3671–3675.Google Scholar
Piccolino, M., Witkovsky, P. & Trimarchi, D. (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 718, 2273–2284.Google Scholar
Pierce, M.E. & Besharse, J.C. (1986). Melatonin and dopamine interactions in the regulation of rhythmic photoreceptor metabolism. In Pineal and Retinal Relationships, ed. O'Brien, P.J. & Kein, D.C., pp. 219–237. New York: Academic Press.Google Scholar
Purkinje, J.E. (1825). Beobachtungen und Versuche zur Physiologie der Sinne, Vol. 2. Berlin: G. Reiner.Google Scholar
Raynauld, J.-P., Laviolette, J.R. & Wagner, H.-J. (1979). Goldfish retina: a correlate between cone activity and morphology of the horizontal cell in cone pedicules. Science 204, 1436–1438.Google Scholar
Schütte, M. & Witkovsky, P. (1990). Dopaminergic interplexiform cells and fibers in the Xenopus retina. Journal of Neurocytology (accepted for publication).Google Scholar
Seeman, P. & Grigoriadis, D. (1987). Dopamine receptors in brain and periphery. Neurochemistry International 10, 1–25.Google Scholar
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. In Progress in Retinal Research. Vol. 3, ed. Osborne, N.N. & Chader, G.J., pp. 263–346. Oxford: Pergamon Press.Google Scholar
Slotkin, T.A. (1974). Reserpine. In Neuropoisons: Their Pathophysiological Actions, Vol. 2, ed. Simpson, L.L. & Curtis, D.R., pp. 1–60. New York: Plenum Press.Google Scholar
Stockton, R.A. & Slaughter, M.M. (1989). B-wave of the electroretinogram. A reflection of ON biopolar cell activity. Journal of General Physiology 93, 101–122.Google Scholar
Stone, S. & Witkovsky, P. (1984). The actions of γ-aminobutyric acid, glycine, and their antagonists upon horizontal cells of the Xenopus retina. Journal of Physiology 353, 249–264.CrossRefGoogle 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, 243–246.Google Scholar
Witkovsky, P., (1980). Excitation and adaptation in the vertebrate retina. In Current Topics in Eye Research, ed. Davson, J. & Zadunaisky, J., pp. 1–66. New York: Academic Press.Google Scholar
Witkovsky, P., Levine, J., Engbretson, G.A., Hassin, G. & Macnichol, E.F. Jr, (1981). A microspectrophotometric study of normal and artificial visual pigments in the photoreceptors of Xenopus laevis. Vision Research 21, 867–873.CrossRefGoogle ScholarPubMed
Witkovsky, P., Stone, S. & Besharse, J. (1988 a). The effects of dopamine and related ligands on photoreceptor to horizontal cell signal transfer in the Xenopus retina. Biomedical Research (Suppl.) 9,(2) 93–107.Google Scholar
Witkovsky, P., Stone, S. & Besharse, J.C. (1988 b). Dopamine modifies the balance of rod and cone inputs to horizontal cells of the Xenopus retina. Brain Research 449, 332–336.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, 864–881.Google Scholar
Wu, S.M. (1988). Synaptic transmission from rods to horizontal cells in dark-adapted tiger salamander retina. Vision Research 28, 1–8.Google Scholar
Yamada, M. & Saito, T. (1988). Effects of dopamine on bipolar cells in the carp retina. Biomedical Research (suppl.) 9, 125–130.Google Scholar
Yang, X.L., Tornqvist, K. & Dowling, J.E. (1988). 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, 2259–2268.Google Scholar