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Potassium-evoked directionally selective responses from rabbit retinal ganglion cells

Published online by Cambridge University Press:  02 June 2009

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

Abstract

Previous studies have shown that directionally selective (DS) retinal ganglion cells cannot only discriminate the direction of a moving object but they can also discriminate the sequence of two flashes of light at neighboring locations in the visual field: that is, the cells elicit a DS response to both real and apparent motion. This study examines whether a DS response can be elicited in DS ganglion cells by simply stimulating two neighboring areas of the retina with high external K+. Extracellular recordings were made from ON-OFF DS ganglion cells in superfused rabbit retinas, and the responses of these cells to focal applications of 100 mM KCl to the vitreal surface of the retina were measured. All cells produced a burst of spikes (typically lasting 50–200 ms) when a short pulse (10–50 ms duration) of KCl was ejected from the tip of a micropipette that was placed within the cell's receptive field. When KCl was ejected successively from the tips of two micropipettes that were aligned along the preferred-null axis of a cell, sequence-dependent responses were observed. The response to the second micropipette was suppressed when mimicking motion in the cell's null direction, whereas an enhancement during apparent motion in the opposite direction frequently occurred. Sequence discrimination in these cells was eliminated by the GABA antagonist picrotoxin and by the Ca2+-channel blocker ω-conotoxin MVIIC, two drugs that are known to abolish directional selectivity in these ganglion cells. The spatiotemporal properties of the K+-evoked sequence-dependent responses are described and compared with previous findings on apparent motion responses of ON-OFF DS ganglion cells.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

Amthor, F.R. & Grzywacz, N.M. (1993). Inhibition in ON-OFF directionally selective ganglion cells of the rabbit retina. Journal of Neurophysiology 69, 21742187.Google Scholar
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161185.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in rabbit's retina. Journal of Physiology 178, 477504.CrossRefGoogle ScholarPubMed
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: Dendritic branching and ultrastructural connectivity. Brain Research 426, 119130.Google Scholar
Brandon, C. & Criswell, M.H. (1995). Displaced starburst amacrine cells of the rabbit retina contain the 67-kDa isoform, but not the 65-kDa isoform, of glutamate decarboxylase. Visual Neuroscience 12, 10531061.Google Scholar
Brecha, N., John, D., Peichl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate-decarboxylase and gamma-aminobutyrate immunoreactivity. Proceedings of the National Academy of Sciences of the U.S.A. 85, 61876191.CrossRefGoogle ScholarPubMed
Caldwell, J.H., Daw, N.W. & Wyatt, H.J. (1978). Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: Lateral interactions for cells with more complex receptive fields. Journal of Physiology 276, 277298.Google Scholar
Chao, T.I., Henke, A., Reichelt, W., Eberhardt, W., Reinhardt-Maelicke, S. & Reichenbach, A. (1994). Three distinct types of voltage-dependent K+ channels are expressed by Müller (glial) cells of the rabbit retina. Pflügers Archiv 426, 5160.Google Scholar
Cohen, E.D. & Miller, R.F. (1995). Quinoxalines block the mechanism of directional selectivity in ganglion cells of the rabbit retina. Proceedings of the National Academy of Sciences of the U.S.A. 92, 11271131.CrossRefGoogle ScholarPubMed
Famiglietti, E. V.(1983). “Starburst” amacrine cells and cholinergic neurons: Mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138144.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1987). Starburst amacrine cells in cat retina are associated with bistratified, presumed directionally selective, ganglion cells. Brain Research 413, 404408.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. (1992). Dendritic co-stratification of ON and ON-OFF directionally selective ganglion cells with starburst amacrine cells in rabbit retina. Journal of Comparative Neurology 324, 322335.CrossRefGoogle Scholar
Famiglietti, E.V. & Tumosa, N. (1987). Immunocytochemical staining of cholinergic amacrine cells in rabbit retina. Brain Research 413, 398403.Google Scholar
Grzywacz, N.M. & Amthor, F.R. (1993). Facilitation in ON-OFF directionally selective ganglion cells of the rabbit retina. Journal of Neurophysiology 69, 21882199.CrossRefGoogle ScholarPubMed
Hayden, S.A., Mills, J.W. & Masland, R.M. (1980). Acetylcholine synthesis by displaced amacrine cells. Science 210, 435437.CrossRefGoogle ScholarPubMed
Holden, A.L. (1977). Responses of directional ganglion cells in the pigeon retina. Journal of Physiology 270, 253269.CrossRefGoogle ScholarPubMed
Hughes, A. & Vaney, D.I. (1981). Contact lenses change the projection of visual field onto rabbit peripheral retina. Vision Research 21, 955956.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1989). Mechanism and site of action of a dopamine D1 antagonist in the rabbit retina. Visual Neuroscience 3, 573585.CrossRefGoogle ScholarPubMed
Jensen, R.J. (1995). Effects of Ca2+ channel blockers on directional selectivity of rabbit retinal ganglion cells. Journal of Neurophysiology 74, 1223.CrossRefGoogle ScholarPubMed
Karwoski, C.J., Lu, H.-K. & Newman, E.A. (1989). Spatial buffering of light-evoked potassium increases by retinal Müller (glial) cells, Science 244, 578580.Google Scholar
Kittila, C.A. & Massey, S.C. (1995). Directionally selective retinal ganglion cells show sensitivity to glutamate under cholinergic blockade. Investigative Ophthalmology and Visual Science 36, S865.Google Scholar
Masland, R.H. & Ames, A. III, (1976). Responses to ACh of ganglion cells in an isolated mammalian retina. Journal of Neurophysiology 39, 12201235.CrossRefGoogle Scholar
Masland, R.H. & Livingstone, C.J. (1976). Effects of stimulation with light on synthesis and release of acetylcholine by an isolated mammalian retina. Journal of Neurophysiology 39, 12101219.Google Scholar
Masland, R.H. & Mills, J.W. (1979). Autoradiographic identification of acetylcholine in the rabbit retina. Journal of Cell Biology 83, 159178.CrossRefGoogle ScholarPubMed
Masland, R.H., Mills, J.W. & Cassidy, C. (1984 a). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society B (London) 223, 121139.Google Scholar
Masland, R.H., Mills, J.W. & Hayden, S.A. (1984 b). Acetylcholine-synthesizing amacrine cells: Identification and selective staining by using radioautography and fluorescent markers. Proceedings of the Royal Society B (London) 223, 79100.Google ScholarPubMed
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. In Progress in Retinal Research (Vol 9), ed. Osborne, N. & Chader, J., pp. 399425. Oxford, England: Pergamon Press.Google Scholar
Massey, S.C. & Neal, M.J. (1979). The light-evoked release of acetylcholine from the rabbit retina in vivo and its inhibition by gammaaminobutyric acid. Journal of Neurochemistry 32, 13271329.Google Scholar
Michael, C.R. (1966). Receptive fields of directionally selective units in the optic nerve of the ground squirrel. Science 152, 10921095.CrossRefGoogle ScholarPubMed
Neal, M.J. & Massey, S.C. (1980). The release of acetylcholine and amino acids from the rabbit retina in vivo. Neurochemistry 1, 191208.Google Scholar
Newman, E.A. (1987). Distribution of potassium conductance in mammalian Müller (glial) cells: A comparative study. Journal of Neuroscience 7, 24232432.Google ScholarPubMed
Newman, E.A. (1989). Potassium conductance block by barium in amphibian Müller cells. Brain Research 498, 308314.CrossRefGoogle ScholarPubMed
Newman, E.A. (1993). Inward-rectifying potassium channels in retinal glial (Müller) cells. Journal of Neuroscience 13, 33333345.CrossRefGoogle ScholarPubMed
Newman, E.A., Frambach, D.A. & Odette, L.L. (1984). Control of extracellular potassium levels by retinal glial cell K+ siphoning. Science 225, 11741175.Google Scholar
O'Malley, D.M. & Masland, R.H. (1989). Co-release of acetylcholine and γ-aminobutyric acid by a retinal neuron. Proceedings of the National Academy of Sciences of the U.S.A. 86, 34143418.Google Scholar
O'Malley, D.M., Sandell, J.H. & Masland, R.H. (1992). Co-release of acetylcholine and GABA by the starburst amacrine cells. Journal of Neuroscience 12, 13941408.Google Scholar
Puro, D.G. & Stuenkel, E.L. (1995). Thrombin-induced inhibition of potassium currents in human retinal glial (Müller) cells. Journal of Physiology 485, 337348.Google Scholar
Reichelt, W., Müller, T., Pastor, A., Pannicke, T., Orkand, P.M., Kettenmann, H. & Schnitzer, J. (1993). Patch-clamp recordings from Müller (glial) cell endfeet in the intact isolated retina and acutely isolated Müller cells of mouse and guinea-pig. Neuroscience 57, 599613.CrossRefGoogle ScholarPubMed
Reichelt, W. & Pannicke, T. (1993). Voltage-dependent K+ channels in guinea pig Müller (glial) cells show different sensitivities to blockade by Ba2+. Neuroscience Letters 155, 1518.CrossRefGoogle Scholar
Vaney, D.I. (1984). “Coronate” amacrine cells in the rabbit retina have the “starburst” dendritic morphology. Proceedings of the Royal Society B (London) 220, 501508.Google ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research (Vol. 9), ed. Osborne, N. & Chader, J., pp. 49100. Oxford, England: Pergamon Press.Google Scholar
Vaney, D.I., Peichl, L. & Boycott, B.B. (1981). Matching populations of amacrine cells in the inner nuclear and ganglion cell layers of the rabbit retina. Journal of Comparative Neurology 199, 373391.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369373.CrossRefGoogle ScholarPubMed
Wyatt, H.J. & Daw, N.W. (1975). Directionally sensitive ganglion cells in the rabbit retina: Specificity for stimulus direction, size, and speed. Journal of Neurophysiology 38, 613626.Google Scholar
Wyatt, H.J. & Daw, N.W. (1976). Specific effects of neurotransmitter antagonists on ganglion cells in rabbit retina. Science 191, 204205.Google Scholar
Yang, G. & Masland, R.H. (1994). Receptive fields and dendritic structure of directionally selective retinal ganglion cells. Journal of Neuroscience 14, 52675280.CrossRefGoogle ScholarPubMed