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Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination

Published online by Cambridge University Press:  02 June 2009

Wallace B. Thoreson  and
Dwight A. Burkhardt
Wallace B. Thoreson
Affiliation:
Vision Laboratory, Departments of Psychology and Physiology and Graduate Program in Neuroscience, University of Minnesota, Minneapolis
Dwight A. Burkhardt
Affiliation:
Vision Laboratory, Departments of Psychology and Physiology and Graduate Program in Neuroscience, University of Minnesota, Minneapolis
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Abstract

The effects of synaptic blocking agents on the antagonistic surround of the receptive field of cone photoreceptors were studied intracellular recording in the retina of hte turtle (Pseudemys scripta elegans) Illumination of a cone's receptive-field surround typically evoked a hybriid depolarizing response composed of two componests: (1) the graded synaptic feedback depolarization and (2) the prolonged depolarization a distinctive, intrinsic response of the cone. The locus of action of synaptic blocking agents was analyzed by comparing their effects on the light-evoked response of horizontal cells, the hybrid cone depolarization evoked by surround illumination, and the pure prolonged depolarization evoked by intracellular current injection.

The excitatory amino-acid antagonists, d-O-phosphoserine (DOS) and kynurenic acid (KynA), suppressed the light responses of horizontal cells and eliminated the surround-evoked, hybrid cone depolarization without affecting the prolonged depolarization evoked by current injection. Cobalt at 5–10 mM suppressed horizontal cell responses and thereby eliminated surround-evoked cone depolarizations. Cobalt (5–10 mM) also blocked the current-evoked prolonged depolarization, suggesting that the intrinsic cone mechanisms responsible for the prolonged depolarization are likely to be calcium-dependent.

Various GABA agonists and antagonists were found to have no effect on the surround-evoked depolarizations of cones. In contrast, a very low concentration of cobalt (0.5 mM) selectively suppressed the light-evoked feedback depolarization of cones without affecting horizontal cell responses or the current-evoked prolonged depolarization. Cobalt at 0.5 mM thus blocks the light-evoked action of the cone feedback synapse while sparing feedforward synaptic transmission from cones to horizontal cells. The implications of the present work for the possible neurotransmitters used at these synapses is discussed.

Keywords

Cone feedbackProlonged depolarizationGlutamateGABACobalt
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 6 , December 1990 , pp. 571 - 583
Copyright
Copyright © Cambridge University Press 1990

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References

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 (London) 214, 265–294.CrossRefGoogle ScholarPubMed
Betz, H. (1987). Biology and structure of the mammalian glycine receptor. Trends in Neuroscience 10, 113–117.CrossRefGoogle Scholar
Braestrup, C. & Anderson, P.H. (1987), Effects of heavy metal cations and other sulfhydryl reagants on brain dopamine D1 receptors: evidence for involvement of a thiol group in the conformation of the active site. Journal of Neurochemistry 48, 1667–1672.CrossRefGoogle Scholar
Burkhardt, D.A. (1972). Effects of picrotoxin and strychnine upon electrical activity of the proximal retina. Brain Research 43, 246–249.Google Scholar
Burkhardt, D.A. (1977), Responses and receptive-field organization of cones in perch retinas. Journal of Neurophysiology 40, 53–62.CrossRefGoogle ScholarPubMed
Burkhardt, D.A. & Gottesman, J. (1987). Light adaptation and responses to contrast flashes in cones of the walleye retina. Vision Research 27, 1409–1420.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J. & Thoreson, W.B. (1988). Prolonged depolarization in turtle cones evoked by current injection and stimulation of the receptive field surround. Journal of Physiology (London) 407, 329–348.CrossRefGoogle ScholarPubMed
Burkhardt, D.A., Gottesman, J. & Thoreson, W.B. (1989). An eyecup slice preparation for intracellular recording in vertbrate retinas. Journal of Neuroscience Methods 28, 179–187.Google Scholar
Byzov, A.L. (1977). Model feedback mechanism between horizontal cells and photoreceptors of the vertebrate retina. Neirofiziologiya 9, 89–94.Google Scholar
Byzov, A.L. & Shura-Bura, T.M. (1986). Electrical feedback mechanism in the processing of signals in the outer plexiform layer. Vision Research 26, 33–34.CrossRefGoogle ScholarPubMed
Cerverro, L. & MacNichol, E.F. Jr. (1972). Inactivation of horizontal cells in turtle retina by glutamate and aspartate. Science 178, 767–768.Google Scholar
Chappell, R.L., Sakuranaga, M. & Naka, K.-I. (1985). Dynamics of turtle horizontal cell response. Journal of General Physiology 86, 423–453.Google Scholar
Coleman, P.A., Massey, S.C. & Miller, R.F. (1986). Kynurenic aciddistinguishes kainate and quisqualate receptors in the vertebrate retina. Brain Research 381, 172–175.CrossRefGoogle ScholarPubMed
Collingridge, G.L. & Lester, R.A.J. (1989). Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacological Reviews 40, 143–210.Google Scholar
Copenhagen, D.R. & Jahr, C. (1989). Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341, 536–539.Google Scholar
Dani, J.A. & Eisenman, G. (1989). Monovalent and divalent cation permeation in acetylcholine receptor channels. Ion transport related to structure. Journal of General Physiology 89, 959–983.CrossRefGoogle Scholar
DeVries, G. & Friedman, A.H. (1978). GABA, picrotoxin, and retinal sensitivity. Brain Research 148, 530–535.Google Scholar
Djamgoz, M.B.A. & Ruddock, K.H. (1979). Effects of picrotoxin, and strychnine on fish retinal S potentials: evidence for inhibitory control of depolarizing responses. Neurosciecne Letters 12, 329–334.Google Scholar
Drujan, B.D. (1982). Biochemical correlates of the S potential. In The S Potential, ed. Drujan, B.D. & Laufer, M., pp. 281–305. New York: Alan R. Liss.Google ScholarPubMed
Eliasof, S. & Weeblin, F. (1989). GABAA-and GABAB-mediated synaptic transmission ro conses in the tiger salamander retina. Incestigative Ophthalmology and Visual Science (Suppl.) 30, 163.Google Scholar
Fuortes, M.G.F., Schwartz, E.A. & Simon, E.J. (1973). Colour-de-pendence of cone responses in the turtle retina. Journal of Physiology (London) 303, 515–533.Google Scholar
Fuortes, M.G.F. & Simon, E.J. (1974). Interactions leading to horizontal cell responses in the turtle retina. Journal of Physiology (London) 240, 177–198.Google Scholar
Gerschenfeld, H.M. & Piccolind, M. (1977). Muscarinic antagonists block cone to horizontal cell transmission in turtle retina. Nature 268, 257–259.Google Scholar
Gerschenfed, H.M. & Piccolino, M. (1980). Sustained effects of L-horizontal cells on trutle cones. Proceedings of the Royal Society B (London) 206, 465–480.Google Scholar
Gottlob, I., Wündsch, F.K. (1988). The rabbit electroretinogram: effects of GABA and its antagonists. Vision Research 28, 203–210.CrossRefGoogle ScholarPubMed
Gouras, P. S-potentials, (1972). In Handbook of Sensory Physiology Vol. VII'F;2, Physiology of Photoreceptor Organs, ed. Fuortes, M.G.F., pp. 513–529. New York: Springer-Verlag.CrossRefGoogle Scholar
Hurd, L.B., 11 & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 9–20.CrossRefGoogle ScholarPubMed
Kamermans, M., van Dijk, B.W. & Spekerdijse, H. (1989). Lateral feedback from monophasic horizontal cells to cones in carp retina, II: A quantitative model. Journal of General Physiology 93, 695–714.Google Scholar
Kaneko, A. & Tachibana, M. (1986 a). Effects of γ-aminobutyric acid on i'Fated cone photoreceptors of the turtle retina. Journal of Physiology (London) 373, 443–461.Google Scholar
Kaneko, A. & Tachibana, M. (1986 b). Blocking effects of cobalt and related ions on the γ-aminobutryic acid-induced current in turtle retinal cones. Journal of Physiology (London) 373, 463–479.CrossRefGoogle Scholar
Krogsgaard-Larsen, P. (1981). γ-Aminobutyric acid agonists, antagonists, and uptake inhibitors. Design and therapeutic aspects. Journal of Medicinal Chemistry 24, 1377–1383.CrossRefGoogle ScholarPubMed
Lam, D.M.K. & Ayoub, G.S. (1983). Biochemical and biophysical studies of i'Fated horisontal cells from the teleost retina. Vision Research 23, 433–444.CrossRefGoogle Scholar
Lasansky, A. (1971). Synaptic organization of cone cells in the turtle retina. Philosophical Transactions of the Royal society B (London) 262, 365–381.Google Scholar
Lasansky, A. (1981). Synaptic action mediating cone responses to annulat illumination in the retina of hte larval tiger salamander. Journal of Physiology (London) 310, 205–214.Google Scholar
Lasansky, A. (1984). synaptic responses of retinal photoreceptors. In Photoreceptors ed. Borsellino, A. & Cervetto, L., pp. 221–231. New York: Plenum Publishing Corp.Google Scholar
Lasater, E.M. (1982). A white-noise analysis of responses and receptive fields of catfish cones. Journal of Neurophysiology 47, 1057–1068.Google Scholar
Lasater, E.M. & Lam, D.M. (1984). The identification and some functions of GABaergic neurons in the distal catifish retina. Vision Research 24, 497–506.Google Scholar
Mackerer, C.R. & Kochman, R.L. (1978). Effects of cations and anions on the binding of [3H/-diazepam to rat brain. Proceedinngs of the Society for Experimental Biology and Medicine 158, 393–397.CrossRefGoogle ScholarPubMed
Massey, S.C. & Miller, R.F. (1987). Excitatory amino acid receptors of rod- and cone-driven horisontal cells in the rabbit retina Journal of Neurophysiology 57, 645–659.Google Scholar
Mielak, D. & Farb, H.H. (1988). Divalent cations modulate GABAa-receptor affinity and desensitization. Society for Neuroscience Abstracts 14, 344.Google Scholar
Miller, A.M. & Schwartz, E.A. (1983). Evidence for the identification of synaptic transmitters released by photoreceptors of the toad retina. Journal of Physiology (London) 334, 325–349.Google Scholar
Miller, R.F. & Slaughter, M.M. (1985). Excitatory amino acid receptors in the vertebrate retina. In Retinal Transmitters and Modulators: Models for the Brain, Vol. II, ed., Morgan, W.W., pp. 123–160. Boca Raton, Florida: CRC Press.Google Scholar
Miller, R.F. & Slaughter, M.M. (1986). Excitatory amino acid receptors of the retina: diversity of subtypes and conductance mechanisms. Trends in Neuroscience 9, 211–218.CrossRefGoogle Scholar
Miller, R.J. (1987), Calcium channels in neurons. In Structure and Physiology of the Slow Inward Calcium Channel. Receptor Biochemistry and Methodology, Vol. 9, ed. Venter, J.C. & Triggle, D., pp. 161–246. New York: Alan R. Liss.Google Scholar
Mizuno, S., Ogawa, N. & Mori, A. (1983). Differential effects of some transition metal cations on the binding of bgr;-carboline-3-carboxyl-ate and diazepam. Neurochemical Research 8, 873–880.Google Scholar
Murakami, M., Shimoda, Y., Nakatani, K., Miyachi, E.-I, & Watanabe, S.-I. (1982 a). GABA-mediated negative feedback from horisontal cells to cones in carp retina. Japanese Journal of Physiology 32, 911–926.Google Scholar
Murakami, M., Shimoda, Y., Nakatani, K., Miyachi, E.-I, & Watanabe, S.-I. (1982 b). GABA-mediated negative feedback and color opponenct in carp retina. Japanese Journal of Physiology 32, 927–935.Google Scholar
Normann, R.A., Lipetz, L.E. & Muller, J.F. (1988). Does GABAergic feedback mediate the depolarizing photoresponses of “C-type” horizontal cells in the turtle retina? Investigative Ophthalmology and Visual Science (Suppl.) 29, 224.Google Scholar
O'Bryan, P.M. (1973). Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. Journal of physiology (London) 235, 207–223.CrossRefGoogle ScholarPubMed
O'Dell, T. & Christensen, B. (1989 a). A voltage-cl'6 study of i'Fated stingray horizontal cell non-NMDA excitatory amino acid receptors. Journal of Neurophysiology 61, 162–172.Google Scholar
O'Dell, T. & Christensen, B. (1989 b). Horizontal cells i'Fated from catfish retina contain two types of excitatory amino acid receptors. Journal of Neurophysiology 61, 1097–1109.CrossRefGoogle ScholarPubMed
Penchev, A., Vitanova, L., Kupenova, P. & Belcheva, S. (1987). Participation of GABA in the sensitivity control of the OFF response in the trutle ERG. Acta Physiologica et Pharmacologica Bulgarica 13, 10–16.Google Scholar
Piccolino, M. (1986). Horizontal cells: historical controversies and new interest. Progress in Retinal Research 5, 147–163.Google Scholar
Piccolino, M. & Gerschenfeld, H.M. (1977). Lateral interactions in the outer plexiform layer of turtle retinas after atropine block of horizontal cell. Nature 268, 259–261.Google Scholar
Piccolino, M. & Gerschenfeld, H.M. (1980). Characteristics and ionic processes involved in feedback spikes of turtle cones. Proceedings of the Royal Society B (London) 206, 465–480.Google ScholarPubMed
Piccolino, M., Neyton, J., Witkovsky, P. & Gerschenfeld, H.M. (1982). γ-aminobutyric acid antagonists decrease junctional communication between horizontal cells of the retina. Proceedings of the National Academy of Sciences of the U.S.A. 79, 3671–3675.Google Scholar
Pinto, L.H. & Pak, W.L. (1974) Light-induced changes in photoreceptor membrane resistance and potential in gecko retinas, II: Preparations with active lateral interactions. Journal of General Physiology 64, 49–69.Google Scholar
Schaeffer, S.F., Raviola, E. & Heuser, J.E. (1982). Membrane specializations in the outer plexiform layer of the turtle retina. Journal of Comparative Neurology 204, 253–267.CrossRefGoogle ScholarPubMed
Scheuhammer, A.M. & Cherian, M.G. (1985). Effects of heavy metal cations, sulfhydryl reagents, and other chemical agents on striatal D2 dopamine receptors. Biochemical Pharmacology 39, 3405–3413.Google Scholar
Schwartz, E.A. (1982). Calcium-independent release of GABA from i'Fated horizontal cells of the toad retina. Journal of Physiology (London) 323, 211–227.Google Scholar
Schwartz, E.A. (1989). Depolarization without calcium can release γ-aminobutyric acid from a retinal neuron. Science 238, 350–355.CrossRefGoogle Scholar
Skrzypek, J. & Werblin, F. (1983). Lateral interactions in absence of feedback to cones. Journal of Neurophysiology 49, 1007–1016.Google Scholar
Slaughter, M.M. & Miller, R.F. (1985 a). Identification of a distinct synaptic glutamate receptor on horizontal cells in mudpuppy retina. Nature 314, 96–97.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1985 b). Characterization of an extended glutamate receptor of the ON bipolar neuron in the vertebrate retina. Journal of Neuroscience 5, 224–233.Google Scholar
Stell, W.K., Lightfoot, D.O., Wheeller, T.G., Leeper, H.F. (1975). Goldfish retina: functional polarization of horizontal cell dendrites and synapses. Science 190, 989–990.Google Scholar
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
Tachibana, M. & Kaneko, M. (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 U.S.A. 81, 7961–7964.Google Scholar
Thoreson, W.B. & Burkhardt, D.A. (1988). Cellular mechanisms of surround antagonism in turtle cones. Society for Neuroscience Abstracts 14, 161.Google Scholar
Thoreson, W.B. & Burkhardt, D.A. (1991).Ionic influences on the prolonged depolarization of turtle cones in situ. Journal of Neurophysiology 65, in press.Google Scholar
Wu., S.M. (1986). Effects of gamma-aminobutyric acid on cones and bipolar cells of the tiger salamander retina. Brain Research 365, 70–77CrossRefGoogle ScholarPubMed
Wu, S.M. & Dowling, J.E. (1980). Effects of GABA and glycine on the distal cells of the cyprinid retina. Brain Research 199, 401–414.Google Scholar
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 1–52.Google Scholar
Yazulla, S. & Kleinschmidt, J. (1983). Carrier-mediated release of GABA from retinal horizontal cells. Brain Research 263, 63–75.Google Scholar
Yazulla, S., Studholme, K.M., Vitorica, J. & DeBlas, A.L. (1989). Immunocytochemical localization of GABAA receptors in goldfish and chicken retinas. Journal of Comparative Neurology 280, 15–26.Google Scholar