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Physiological and morphological properties of OFF- and ON-center bipolar cells in the Xenopus retina: Effects of glycine and GABA

Published online by Cambridge University Press:  02 June 2009

Susan Stone  and
Michael Schutte
Susan Stone
Affiliation:
Department of Ophthalmology, New York University Medical Center, New York
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Abstract

We studied the morphology and center-surround organization of Lucifer Yellow injected OFF- and ON-center bipolar cells in the light-adapted Xenopus retina and the effects of glycine and GABA on their cone-mediated light responses. In both classes of cell, prominent antagonistic surround responses up to 20 mV in amplitude could be evoked without first suppressing the center responses with steady illumination. An additional feature of the light-evoked bipolar cell response was a pronounced (up to –24 mV) delayed hyperpolarizing after potential (DHAP) which followed the depolarizing responses of both classes of bipolar cell.

The morphological features of dye-injected bipolar cells conformed to the general idea of segregation of ON and OFF pathways in the inner and outer interplexiform layer, however, the morphology of axonal arborizations was different for both classes. OFF-center cells ramified symmetrically around the primary branchpoint, whereas ON-center cells had a strongly asymmetrical arrangement of their axonal tree.

The center and surround responses were differentially sensitive to glycine and GABA. Glycine eliminated the antagonistic surround responses in both OFF and ON cells; the center responses were reduced to some extent but were not eliminated. In contrast, GABA affected the hyperpolarizing responses much more strongly than the depolarizing response components. That is, the amplitude of the center response in the OFF cell and the surround response in the ON cell was reduced 80–90% during exposure to GABA, whereas the surround and center depolarizations of OFF and ON cells, respectively, were reduced only 0–10%.

Our findings implicate a role for GABAergic and glycinergic pathways in the center-surround organization of bipolar cells in Xenopus retina. In addition, the results suggest that the pathways mediating center-surround antagonism may be different in OFF-bipolar cells vs. ON-bipolar cells.

Keywords

RetinaBipolar cellGlycineGABACenter-surround organization
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 4 , October 1991 , pp. 363 - 376
Copyright
Copyright © Cambridge University Press 1991

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References

Apell, H.-J. (1989). Electrogenic properties of the Na, K pump. Journal of Membrane Biology 110, 103–114.CrossRefGoogle ScholarPubMed
Attwell, D., Werblin, F.S., Wilson, M. & Wu, S.M. (1983). A signreversing pathway from rods to double and single cones in the retina of the tiger salamander. Journal of Physiology 336, 313–333.CrossRefGoogle ScholarPubMed
Attwell, D., Mobbs, P., Tessier-Lavigne, M. & Wilson, M. (1987). Neurotransmitter-induced currents in retinal bipolar cells of the axolotl. Ambystoma Mexicanum. Journal of Physiology 387, 125–161.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O-Bryan, P.M. (1971). Receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265–294.CrossRefGoogle ScholarPubMed
Borges, S. & Wilson, M. (1990). The lateral spread of signal between bipolar cells of the tiger salamander retina. Biological Cybernetics 63, 45–50.CrossRefGoogle ScholarPubMed
Cajal, S.R.Y. (1892). La retine des vertebres. La Cellule 9, 121–246.Google Scholar
Dacheux, R.F. & Miller, R.Famiglietti. (1976). Photoreceptor-bipolar cell transmission in the perfused retina eyecup of the mudpuppy. Science 191, 963–964.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Werblin, F. (1969). Organization of retina of the mudpuppy. Necturus maculosus: I. Synaptic structure. Journal of Neurophysiology 32, 315–338.CrossRefGoogle ScholarPubMed
Famiglietti, E.V., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Graydon, M.L. & Giorgi, P.P. (1984). Topography of the retinal ganglion cell layer of Xenopus. Journal of Anatomy 139, 145–157.Google ScholarPubMed
Hare, W.A. & Owen, D.G. (1990). Spatial organization of the bipolar cell's receptive field in the retina of the tiger salamander. Journal of Physiology 421, 223–245.CrossRefGoogle ScholarPubMed
Hollyfield, J.G., Rayborn, M.E., Sarthy, P.V. & Lam, D.M.K. (1979). The emergence, localization, and maturation of neurotransmitter systems during development of the retina I. Xenopus laevis, I:γ-aminobutyric acid. Journal of Comparative Neurology 188, 597–598.Google ScholarPubMed
Ishida, A.T., Stell, W.K. & Lightfoot, D.O. (1980). Rod and cone inputs to bipolar cells in goldfish retina. Journal of Comparative Neurology 191, 623–633.Google ScholarPubMed
Kaneko, A. & Tachibana, M. (1986). Effects of γ-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology 373, 443–461.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1987). GABA mediates the negative feedback from amacrine to bipolar cells. Neuroscience Research 6, S239–S252.Google ScholarPubMed
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860–876.CrossRefGoogle ScholarPubMed
Kondo, H. & Toyoda, J. (1983). GABA and glycine effects on the bipolar cells of the carp retina. Vision Research 23, 1259–1264.CrossRefGoogle ScholarPubMed
Koontz, M.A. & Hendrickson, A.E. (1990). Distribution of GABA-immunoreactive amacrine cell synapses in the inner plexiform layer of macaque monkey retina. Visual Neuroscience 5, 17–28.CrossRefGoogle ScholarPubMed
Lasansky, A. (1978). Contacts between receptors and electrophysiologically identified neurons in the retina of the larval tiger salamander. Journal of Physiology 285, 531–542.CrossRefGoogle ScholarPubMed
Lauger, P. (1987). Dynamics of ion-transport systems in membranes. Pharmacological Reviews 67, 1296–1331.Google ScholarPubMed
Maguire, G., Maple, B., Lukasiewicz, P. & Werblin, F. (1989a). Gamma-aminobutyrate type B receptor modulation of L-type calcium channel current at bipolar cell terminals in the retina of the tiger salamander. Proceedings of the National Academy of Sciences of the U.S.A. 86, 10144–10147.CrossRefGoogle ScholarPubMed
Maguire, G., Lukasiewicz, P. & Werblin, F. (1989b). Amacrine cell interactions underlying the response to change in the tiger salamander retina. Journal of Neuroscience 9, 726–735.CrossRefGoogle ScholarPubMed
Marc, R.E., Stell, W.K., Bok, D. & Lam, D.M.K. (1978). GABAergic pathways in the goldfish retina. Journal of Comparative Neurology 182, 221–246.CrossRefGoogle ScholarPubMed
Marc, R.E. (1985). The role of glycine in retinal circuitry. In Retinal Transmitters and Modulators: Models for the Brain, ed. Morgan, W.W., pp. 119–158. Boca Raton, Florida: CRC Press, Inc.,Google Scholar
Marchiafava, P.L. (1978). Horizontal cells influence membrane potential of bipolar cells in the retina of the turtle. Nature 275, 141–142.CrossRefGoogle ScholarPubMed
Marchiafava, P.L. & Weiler, R. (1980). Intracellular analysis and structural correlates of the organization of inputs to ganglion cells in the retina of the turtle. Proceedings of the Royal Society B (London) 208, 103–113.Google Scholar
Matsumoto, N. & Naka, K.-I. (1972). Identification of intracellular responses in the frog retina. Brain Research 42, 59–71.CrossRefGoogle ScholarPubMed
Miller, R.F. & Dacheux, R.F. (1983). Intracellular chloride in retina neurons: measurement and meaning. Vision Research 23, 399–411.CrossRefGoogle ScholarPubMed
Miller, R.F., Frumkes, T.E., Slaughter, M. & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina I. Receptors, horizontal cells, bipolars, and G-cells. Journal of Neurophysiology 45, 743–763.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Owen, W.G. & Hare, W.A. (1989). Signal transfer from photoreceptors to bipolar cells in the retina of the tiger salamander. Neuroscience Research (7 Suppl.) 10, S77–S88.Google ScholarPubMed
Rayborn, M.E., Sarthy, P.V., Lam, D.M.K. & Hollyfield, J.G. (1981). The emergence, localization and maturation of neurotransmitter systems during development of the retina in Xenopus laevis, II: Glycine. Journal of Comparative Neurology 195, 585–593.CrossRefGoogle ScholarPubMed
Richter, A. & Simon, E.J. (1975). Properties of centre-hyperpolarizing, red-sensitive bipolar cells in the turtle retina. Journal of Physiology 248, 317–334.CrossRefGoogle ScholarPubMed
Saito, T., Kondo, H. & Toyoda, J.I. (1978). Rod and cone signals in the on-center bipolar cell: their different ionic mechanisms. Vision Research 18, 591–595.CrossRefGoogle ScholarPubMed
Saito, T., Kujiraoka, T. & Toyoda, J.-I. (1984). Electrical and morphological properties of off-center bipolar cells in the carp retina. Journal of Comparative Neurology 222, 200–208.CrossRefGoogle ScholarPubMed
Sakuranaga, M. & Naka, K.-I. (1985). Signal transmission in the catfish retina I. Transmission in the outer retina. Journal of Neurophysiology 53, 373–389.CrossRefGoogle ScholarPubMed
Schütte, M. (1991). [125I]SCH 23982: a new tool for rapid visualization of dopaminergic neurons in lower vertebrate retinas. Neuroscience Letters 121, 29–33.CrossRefGoogle Scholar
Schütte, M. & Weiler, R. (1987). Morphometric analysis of serotonergic bipolar cells in the retina and its implications for retinal image processing. Journal of Comparative Neurology 260, 619–626.CrossRefGoogle Scholar
Schütte, M. & Witkovsky, P. (1990). Serotonin-like immunoreactivity in the retina of the clawed frog (Xenopus laevis). Journal of Neurocytology 19, 504–518.CrossRefGoogle ScholarPubMed
Schütte, M. & Witkovsky, P. (1991). Dopaminergic interplexiform cells and centrifugal fibres in the Xenopus retina. Journal of Neurocytology 20, 195–207.CrossRefGoogle ScholarPubMed
Skrzypek, J. & Werblin, F. (1983). Lateral interactions in absence of feedback to cones. Journal of Neurophysiology 49, 1007–1016.CrossRefGoogle ScholarPubMed
Smiley, J.F. & Basinger, S.F. (1988). Somatostatin-like immunoreactivity and glycine high-affinity uptake colocalize to an interplexiform cell of the Xenopus laevis retina. Journal of Comparative Neurology 274, 608–618.CrossRefGoogle Scholar
Smiley, J.F. & Yazulla, S. (1990). Characterization of glycinergic contacts in the outer plexiform layer of the Xenopus laevis retina using antibodies to glycine, GABA, and glycine receptors. Journal of Comparative Neurology 299, 375–388.CrossRefGoogle ScholarPubMed
Smith, T.G., Stell, W.K., Brown, J.E., Freeman, J.A. & Murray, G.C. (1968). A role for the sodium pump in photoreception in Limulus. Science 162, 456–457.CrossRefGoogle ScholarPubMed
Stone, S.L. (1991). Bipolar cell responses in the Xenopus retina exhibit a delayed hyperpolarizing after-potential (DHAP). Investigative Ophthalmology and Visual Science (Suppl) 32, 1089 (Abstract).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
Stone, S. & Witkovsky, P. (1987). Center-surround organization of Xenopus horizontal cells and its modification by γ-aminobutyric acid and strontium. Experimental Biology 47, 1–12.Google ScholarPubMed
Stone, S., Witkovsky, P. & Schütte, M. (1990). A chromatic horizontal cell in the Xenopus retina: intracellular staining and synaptic pharmacology. Journal of Neurophysiology 64, 1683–1694.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1984). γ-Aminobutyric acid acts at axon terminals of turtle photoreceptors: Difference in sensitivity among cell types. Proceedings of the National Academy of Sciences of the USA 81, 7961–7964.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1987). γ-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells. Proceedings of the National Academy of Sciences of the U.S.A. 84, 3501–3505.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells. Visual Neuroscience 1, 297–305.CrossRefGoogle ScholarPubMed
Tessier-Lavigne, M., Attwell, D., Mobbs, P. & Wilson, M. (1988). Membrane currents in retinal bipolar cells of the axolotl. Journal of General Physiology 91, 49–72.CrossRefGoogle ScholarPubMed
Toyoda, J.-I. & Kujiraoka, T. (1982). Analyses of bipolar cell responses elicited by polarization of horizontal cells. Journal of General Physiology 79, 131–145.CrossRefGoogle ScholarPubMed
Weiler, R. (1981). The distribution of center-depolarizing and center-hyperpolarizing bipolar cell ramifications within the inner plexiform layer of turtle retina. Journal of Comparative Physiology 144, 459–464.CrossRefGoogle Scholar
Weiler, R. & Schütte, M. (1985a). 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, 373–382.CrossRefGoogle ScholarPubMed
Weiler, R. & Schütte, M. (1985b). Kainic acid-induced release of serotonin from OFF-bipolar cells in the turtle retina. Brain Research 360, 379–383.CrossRefGoogle ScholarPubMed
Werblin, F. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy. Necturus maculosus II Intracellular recording. Journal of Neurophysiology 32, 339–355.CrossRefGoogle ScholarPubMed
Werblin, F., Maguire, G., Lukasiewicz, P., Eliasof, S. & Wu, S.M. (1988). Neural interactions mediating the detection of motion in the retina of the tiger salamander. Visual Neuroscience 1, 317–329.CrossRefGoogle ScholarPubMed
Werblin, F.S. (1977). Synaptic interactions mediating bipolar response in the retina of the tiger salamander. In Vertebrate Photoreception, ed. Barlow, H.B. & Fatt, P., pp. 205–230. London: Academic Press.Google Scholar
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, 13–22.Google ScholarPubMed
Witkovsky, P., Stone, S. & Macdonald, E.D. (1988). Morphology and synaptic connections of HRP-filled, axon-bearing horizontal cells in the Xenopus retina. Journal of Comparative Neurology 275, 29–38.CrossRefGoogle ScholarPubMed
Wu, S.M. (1986). Effects of gamma-aminobutyric acid on cones and bipolar cells of the tiger salamander retina. Brain Research 365, 70–77.CrossRefGoogle ScholarPubMed
Yazulla, S. (1986). GABAergic mechanisms in the retina. In Progress in Retinal Research, ed. Osborne, N. & Chader, J., pp. 1–52. New York: Pergamon Press.Google Scholar
Yeh, H.H., Lee, M.B. & Cheun, J.E. (1990). Properties of GABA-activated whole-cell currents in bipolar cells of the rat retina. Visual Neuroscience 4, 349–357.CrossRefGoogle ScholarPubMed