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Involvement of glycinergic neurons in the diminished surround activity of ganglion cells in the dark-adapted rabbit retina

Published online by Cambridge University Press:  02 June 2009

Ralph J. Jensen
Ralph J. Jensen
Affiliation:
Department of Biomedical Sciences, Southern College of Optometry, Memphis
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Abstract

Previous studies have reported that the surround responses of retinal ganglion cells weaken or disappear upon dark adaptation. The mechanism(s) by which this occurs is largely unknown, although changes in activity of retinal dopaminergic neurons have been implicated. In the light-adapted rabbit retina, the surround ON responses of OFF-center ganglion cells have been shown to be markedly reduced or abolished by a dopamine antagonist. This effect of a dopamine antagonist was recently shown to be reversed by the glycine antagonist strychnine and by compounds that elevate intracellular cAMP levels. The present study was conducted to determine whether strychnine and cAMP-elevating compounds could bring out the surround ON responses in OFF-center ganglion cells that are diminished upon dark adaptation. Extracellular recordings of OFF-center brisk ganglion cells were made from isolated, superfused retinal preparations. During the course of dark adaptation, the surround On responses of many cells decreased markedly.Application in both brisk-transient and brisk-sustained OFF-center ganglion cells. The center OFF responses of these cells, on the other hand, were not enhanced by strychnine. Of the cAMP-elevating compounds tested, 8-(4-chlorophenylthio) cyclic AMP was the most effective in bringing out the surround ON responses in dark-adapted OFF-center ganglion cells. The findings from this study suggest that under dark-adapted conditions glycinergic neurons inhibit the surround component of OFF-center ganglion cells. The release of glycine from these neurons is suggested to be regulated by a cAMP-dependent mechanism.

Keywords

Rabbit retinaGanglion cellsDark adaptationStrychnineCyclic AMP
Type
Research Article
Information
Visual Neuroscience , Volume 6 , Issue 1 , January 1991 , pp. 43 - 53
Copyright
Copyright © Cambridge University Press 1991

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References

Arkin, M.S. & Miller, R.F. (1987). Subtle actions of 2-amino-4- phosphonobutyrate (APB) on the OFF pathway in the mudpuppy retina. Brain Research 426, 142–148.CrossRefGoogle ScholarPubMed
Arkin, M.S. & Miller, R.F. (1988). Bipolar origin of synaptic inputs to sustained OFF-ganglion cells in the mudpuppy retina. Journal of Neurophysiology 60, 1122–1142.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
Barlow, H.B. & Levick, W.R. (1976). Threshold setting by the surround of cat retinal ganglion cells. Journal of Physiology 259, 737–757.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. & Dowling, J.E. (1985). Roles of aspartate and glutamate in synaptic transmission in rabbit retina, I: Outer plexiform layer. Journal of Neurophysiology 53, 699–713.CrossRefGoogle ScholarPubMed
Bolz, J., Wässle, H. & Thier, P. (1984). Pharmacological modulation of ON and OFF ganglion cells in the cat retina. Neuroscience 12, 875–885.CrossRefGoogle Scholar
Bowling, D.B. (1980). Light responses of ganglion cells in the retina of the turtle. Journal of Physiology 299, 173–196.CrossRefGoogle ScholarPubMed
Brainard, G.C. & Morgan, W.W. (1987). Light-induced stimulation of retinal dopamine: a dose-response relationship. Brain Research 424, 199–203.CrossRefGoogle ScholarPubMed
Chen, E. P.-C. & Linsenmeier, R.A. (1989). Effects of 2-amino-4-phosphonobutyric acid on responsitivity and spatial summation of X cells in the cat retina. Journal of Physiology 419, 59–75.CrossRefGoogle Scholar
Dacheux, R.F. & Miller, R.F. (1981). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina, I: Receptors, horizontal, and bipolar cells. Journal of Comparative Neurology 198, 307–326.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, 331–345.CrossRefGoogle ScholarPubMed
Daw, N.W., Brunken, W.J. & Jensen, R.J. (1989). The function of monoamines in the rabbit retina, In The Neurobiology of the Inner Retina. ed. Osborne, N. & Weiler, R., pp. 363–374. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Dolan, R.P. & Schiller, P.H. (1989). Evidence for only depolarizing rod bipolar cells in the primate retina. Visual Neuroscience 2, 421–424.CrossRefGoogle ScholarPubMed
Dong, C.-J. & McReynolds, J.S. (1989). APB increases apparent coupling between horizontal cells in mudpuppy retina. Vision Research 29, 541–544.Google ScholarPubMed
Donner, K. (1981). Receptive fields of frog retinal ganglion cells: Response formation and light-dark adaptation. Journal of Physiology 319, 131–142.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, 393–395.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1989). Mechanism and site of action of a dopamine D1 antagonist in the rabbit retina. Visual Neuroscience 3, 573–585.CrossRefGoogle ScholarPubMed
Jensen, R.J. & Daw, N.W. (1984). Effects of dopamine antagonists on receptive fields of brisk cells and directionally selective cells in the rabbit retina. Journal of Neuroscience 4, 2972–2985.CrossRefGoogle ScholarPubMed
Jensen, R.J. & Daw, N.W. (1986). Effects of dopamine and its agonists and antagonists on the receptive-field properties of ganglion cells in the rabbit retina. Neuroscience 17, 837–855.CrossRefGoogle ScholarPubMed
Kolb, H., Cuenca, N. & DeKorver, L. (1990). Postembed staining reveals the synaptic relationships of the dopaminergic amacrine cell of the cat retina. Investigative Ophthalmology and Visual Science 31, 209.Google Scholar
Kolb, H. & Nelson, R. (1984). Neural architecture of the cat retina. In Progress in Retinal Research. Vol. 3, ed. Osborne, N. & Chader, J., pp. 21–60. New York: Pergamon Press.Google Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37–68.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Dowling, J.E. (1987). The interplexiform-horizontal cell system of the fish retina: Effects of dopamine, light stimulation, and time in the dark. Proceedings of the Royal Society B (London) 231, 91–121.Google ScholarPubMed
Marc, R.E. & Lru, W.-L.S. (1985). (3H) Glycine-accumulating neurons of the human retina. Journal of Comparative Neurology 232, 241–260.CrossRefGoogle ScholarPubMed
Masland, R. & Ames, A. (1976). Response to acetycholine of ganglion cells in isolated mammalian retina. Journal of Neurophysiology 39, 1220–1235.CrossRefGoogle Scholar
Massey, S.C., Redburn, D.A. & Crawford, M.L.J. (1983). The effects of 2-amino-4-phosphonobutyric acid (APB) on the ERG and ganglion cell discharge of rabbit retina. Vision Research 23, 1607–1613.CrossRefGoogle ScholarPubMed
Mitchell, C.K. & Redburn, D.A. (1988). AP4 inhibits chloride-dependent binding and uptake of [3H]-glutamate in rabbit retina. Brain Research 459, 298–311.CrossRefGoogle ScholarPubMed
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
Nawy, S., Sie, A. & Copenhagen, D.R. (1989). The glutamate analog 2-amino-4-phosphonobutyrate antagonizes synaptic transmission from cones to horizontal cells in the goldfish retina. Proceedings of the National Academy of Sciences of the U.S.A. 86, 1726–1730.CrossRefGoogle ScholarPubMed
Neal, M.J., Cunningham, J.R., James, T.A., Joseph, M. & Collings, J.F. (1981). The effect of 2-amino-4-phosphonobutyrate (APB) on acetylcholine release from the rabbit retina: Evidence for on-channel input o cholinergic amacrine cells. Neuroscience Letters 26, 301–305.CrossRefGoogle Scholar
Nelson, R. (1977). Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Neurology 172, 109–136.CrossRefGoogle ScholarPubMed
Nelson, R. (1982). All amacrine cells quicken time course of rod signals in the cat retinal. Journal of Neurophysiology 47, 928–947.CrossRefGoogle Scholar
Nelson, R. & Kolb, H. (1985). A17: A broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592–614.CrossRefGoogle ScholarPubMed
Parkinson, D. & Rando, R.R. (1983). Effect of light on dopamine turnover and metabolism in rabbit retina. Investigative Ophthalmology and Visual Science 24, 384–388.Google ScholarPubMed
Pourcho, R.G. (1982). Dopaminergic amacrine cells in the cat retina. Brain Research 252, 101–109.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1985). A combined Golgi and auto- radiographic study of [3H]-glycine-accumulating amacrine cells in the cat retina. Journal of Comparative Neurology 233, 473–480.CrossRefGoogle Scholar
Pourcho, R.G. & Goebel, D.J. (1987). Visualization of endogenous glycine in cat retina: An immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
Raviola, E. & Dacheux, R.F. (1987). Excitatory dyad synapse in rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 84, 7324–7328.CrossRefGoogle ScholarPubMed
Sandell, J.H., Masland, R.H., Raviola, E. & Dacheux, R.F. (1989). Connection of indoleamine-accumulating cells in the rabbit retina. Journal of Comparative Neurology 283, 303–313.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1981). 2-Amino-4-phosphonobutyric acid: A new pharmacological tool for retinal research. Science 211, 182–185.CrossRefGoogle Scholar
Smith, R.G., Freed, M.A. & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: Functional architecture of the rod-cone network. Journal of Neuroscience 6, 3505–3517.CrossRefGoogle ScholarPubMed
Stell, W.K., Detwiler, P.B., Wagner, H.G. & Wolbarsht, M.L. (1975). Giant retinal ganglion cells in dogfish (Mustelus): Electrophysiology of single ON-center units. In Vision in Fishes, ed. Ali, M.-A. pp. 99–112. New York: Plenum Press.CrossRefGoogle Scholar
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M. & Smith, R.G. (1986). Microcircuitry and functional architecture of the cat retina. Trends in Neurosciences 9, 186–192.CrossRefGoogle Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of All amacrine cells in mammalian retina. Journal of Neuroscience 7, 4115–4128.CrossRefGoogle ScholarPubMed