Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T16:56:39.733Z Has data issue: false hasContentIssue false
  • English
  • Français

Synaptic connections involving immunoreactive glycine receptors in the turtle retina

Published online by Cambridge University Press:  02 June 2009

Charles L. Zucker  and
Berndt Ehinger
Charles L. Zucker
Affiliation:
Schepens Eye Research Institute and Harvard Medical School, Department of Ophthalmology, Boston
Berndt Ehinger
Affiliation:
Department of Ophthalmology, University of Lund, Lund, Sweden
Get access Rights & Permissions [Opens in a new window]

Abstract

The distribution of glycine receptors in the turtle retina was studied with the aid of a monoclonal antibody that detects the 93-kD protein associated with the strychnine-sensitive glycine receptor. Light microscopically, receptors were found in the inner plexiform layer and, more sparsely, in the innermost parts of the inner nuclear layer. No receptors were seen to be associated with photoreceptor cells, horizontal cells, or any other structures in the distal inner nuclear layer or outer plexiform layer. Ultrastructurally, glycine receptors were found on the inner face of postsynaptic membranes of processes from amacrine and presumed ganglion cells and always involved amacrine cell processes as the presynaptic element. Such glycine receptor immunoreactive synapses onto amacrine cell processes were distributed throughout the inner plexiform layer with a peak density near the middle. On the other hand, output synapses onto ganglion cell processes displaying immunoreactive glycine receptor sites showed a bimodal distribution in the inner plexiform layer. Glycine receptor immunoreactivity was not detected on bipolar cells, but presumed glycine-utilizing processes (i.e. those presynaptic to immunoreactive glycine receptors) were occasionally found to be postsynaptic in bipolar cell dyads. The majority of the synaptic input to the presumed glycine-utilizing amacrine cell processes was from other amacrine processes, some of which were themselves glycine utilizing. The observations suggest that glycinergic synapses in the turtle retina are, to a large extent, engaged in processing interamacrine signals.

Keywords

Strychnine-sensitive glycine receptorsAmacrine cellsImmunohistochemistryElectron microscopyTurtle retina
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 5 , September 1993 , pp. 907 - 914
Copyright
Copyright © Cambridge University Press 1993

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

Altschuler, R.A., Betz, H., Parakkal, M.H., Reeks, K.A. & Wenthold, R.J. (1986). Identification of glycinergic synapses in the cochlear nucleus through immunocytochemical localization of the postsynaptic receptor. Brain Research 369, 316–320.CrossRefGoogle ScholarPubMed
Ammermüller, J. & Weiler, R. (1988). Physiological and morphological characterization of OFF-center amacrine cells in the turtle retina. Journal of Comparative Neurology 273, 137–148.CrossRefGoogle ScholarPubMed
Anderton, P.J. & Millar, T.J. (1989). MK801-induced antagonism of NMDA–preferring excitatory amino acid receptors in horizontal cells of the turtle retina. Neuroscience Letters 101, 331–336.CrossRefGoogle ScholarPubMed
Aprison, M.H. & Werman, R. (1965). The distribution of glycine in cat spinal cord. Life Sciences 4, 2075–2083.CrossRefGoogle ScholarPubMed
Araki, T., Yamano, M., Murakami, T., Wanaka, A., Betz, H. & Tohyama, M. (1988). Localization of glycine receptors in the rat central nervous system: An immunocytochemical analysis using monoclonal antibody. Neuroscience 25, 613–624.CrossRefGoogle ScholarPubMed
Ariel, M. & Adolph, A.R. (1985). Neurotransmitter inputs to direc-tionally sensitive turtle retinal ganglion cells. Journal of Neurophys-iology 54, 1123–1143.CrossRefGoogle ScholarPubMed
Becker, C.M., Hoch, W. & Betz, H. (1989). Sensitive immunoassay shows selective association of peripheral and integral membrane proteins of the inhibitory glycine receptor complex. Journal of Neurochemistry 53, 124–131.CrossRefGoogle ScholarPubMed
Becker, C.-M., Seitanidou, T. & Triller, A. (1991). Conservation of antigenic epitopes of the inhibitory glycine receptor in rodent and goldfish CNS. Molecular Brain Research 11, 327–333.CrossRefGoogle ScholarPubMed
Bolz, J., Thier, P., Voigt, T. & Wässle, H. (1985). Action and localization of glycine and taurine in the cat retina. Journal of Physiology (London) 362, 395–413.CrossRefGoogle ScholarPubMed
Bonaventure, N., Wioland, N. & Roussel, G. (1980). Effects of some amino acids (GABA, glycine, taurine) and of their antagonists (picro-toxin, strychnine) on spatial and temporal features of frog retinal ganglion cell responses. Pflüger's Archives 385, 51–64.CrossRefGoogle ScholarPubMed
Cohen, B.N., Fain, G.L. & Fain, M.J. (1989). GABA and glycine channels in isolated ganglion cells from the goldfish retina. Journal of Physiology (London) 418, 53–82.CrossRefGoogle ScholarPubMed
Cohen, E. & Sterling, P. (1986). Accumulation of [3H]-glycine by cone bipolar neurons in the cat retina. Journal of Comparative Neurology 250, 1–7.CrossRefGoogle ScholarPubMed
Cooper, E.J., Millar, T.J. & Anderton, P.J. (1990). Distribution of [3H]MK-801 binding in the turtle retina: An autoradiographical study. Neuroscience Letters 112, 127–132.CrossRefGoogle ScholarPubMed
Cunningham, R. & Miller, R.F. (1980). Electrophysiological analysis of taurine and glycine action on neurons of the mudpuppy retina. I. Intracellular recording. Brain Research 197, 123–138.CrossRefGoogle ScholarPubMed
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1991). Glutamate, GABA, and glycine in the human retina – an immunocyto-chemical investigation. Journal of Comparative Neurology 311, 483–494.CrossRefGoogle Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society B (London) 166, 80–111.Google ScholarPubMed
Dubin, M.W. (1970). The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron-microscopic analysis. Journal of Comparative Neurology 140, 479–506.CrossRefGoogle ScholarPubMed
Ehinger, B. & Falck, B. (1971). Autoradiography of some suspected neurotransmitter substances: GABA, glycine, aspartic acid, glutamic acid, histamine, dopamine, and L-dopa. Brain Research 33, 157–172.CrossRefGoogle ScholarPubMed
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. & Dowling, J.E. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 8321–8325.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Cheung, K. (1989). Immunocytochemical localization of glycine in the retina of the turtle (Pseudemys scripta). Visual Neuroscience 2, 331–338.CrossRefGoogle ScholarPubMed
Eldred, W.D., Zucker, C, Karten, H.J. & Yazulla, S. (1983). Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. Journal of Histochemistry and Cytochemistry 31, 285–292.CrossRefGoogle ScholarPubMed
Frumkes, T.E., Miller, R.F., Slaughter, M. & Dacheux, R.F. (1981). Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina: III. Amacrine-mediated inhibitory influences on ganglion cell receptive-field organization: A model. Journal of Neurophysiology 45, 783–804.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Koontz, M.A., Pourcho, R.G., Sarthy, P.V. & Goebel, D. J. (1988). Localization of glycine-containing neurons in the Macaca monkey retina. Journal of Comparative Neurology 273, 473–487.CrossRefGoogle ScholarPubMed
Ikeda, H. & Sheardown, M.J. (1983). Functional transmitters at retinal ganglion cells in the cat. Vision Research 23, 1161–1174.CrossRefGoogle ScholarPubMed
Jäger, J. & Wässle, H. (1987). Localization of glycine uptake and receptors in the cat retina. Neuroscience Letters 75, 147–151.CrossRefGoogle ScholarPubMed
Johnson, J.W. & Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529–531.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1984). Neural architecture of the cat retina. Progress in Retinal Research 3, 21–60.CrossRefGoogle Scholar
Marc, R.E. (1985). The role of glycine in retinal circuitry. In Retinal Transmitters and Modulators: Models for the Brain, Vol. I, ed. Morgan, W.H., pp. 119–158. Boca Raton, Florida: CRC Press.Google Scholar
Marc, R.E. (1989). The role of glycine in the mammalian retina. Progress in Retinal Research 8, 67–108.CrossRefGoogle Scholar
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. 1. Receptors, horizontal cells, bipolars, and G-cells. Journal of Neurophysiology 45, 743–763.CrossRefGoogle Scholar
Muller, J.F. & Marc, R.E. (1990). GABAergic and glycinergic pathways in the inner plexiform layer of the goldfish retina. Journal of Comparative Neurology 291, 281–304.CrossRefGoogle ScholarPubMed
Murakami, T., Araki, T., Yamano, M., Wanaka, A., Betz, H. & Tohyama, M. (1988). Localization of the glycine receptors in the rat central nervous system: An immunocytochemical analysis. Advances in Experimental and Medical Biology 236, 71–80.CrossRefGoogle ScholarPubMed
Pfeiffer, F., Simler, R., Grenningloh, G. & Betz, H. (1984). Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proceedings of the National Academy of Sciences of the U.S.A. 81, 7224–7227.CrossRefGoogle ScholarPubMed
Pourcho, R.G. (1980). Uptake of [3H]-glycine and [3H]-GABA by amacrine cells in the cat retina. Brain Research 198, 333–346.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1987 a). A combined Golgi and auto-radiographic study of 3H-glycine-accumulating cone bipolar cells in the cat retina. Journal of Neuroscience 7, 1178–1188.CrossRefGoogle Scholar
Pourcho, R.G. & Goebel, D.J. (1987 b). Visualization of endogenous glycine in cat retina: An immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1990). Autoradiographic and immunocytochemical studies on glycine-containing neurons in the retina. In Glycine Neurotransmission, ed. Ottersen, O.P. & Storm-Mathisen, J., pp. 355–389. Chichester, New York, Brisbane, Toronto, Singapore: John Wiley & Sons.Google Scholar
Pourcho, R.G. & Owczarzak, M.T. (1991 a). Connectivity of glycine-immunoreactive amacrine cells in the cat retina. Journal of Comparative Neurology 307, 549–561.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Owczarzak, M.T. (1991 b). Glycine receptor immunoreactivity is localized at amacrine cell synapses in cat retina. Visual Neuroscience 7, 611–618.CrossRefGoogle ScholarPubMed
Rayborn, M.E., Sarthy, P.V., Lam, D.M. & 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
Seitanidou, T., Nicola, M.A., Triller, A. & Korn, H. (1991). Immunohistochemical localization of glycine receptors and a linked polypeptide in the goldfish brain. Journal of Receptor Research 11, 359–370.CrossRefGoogle Scholar
Seitanidou, T., Triller, A. & Korn, H. (1988). Distribution of glycine receptors on the membrane of a central neuron: An immunoelectron microscopy study. Journal of Neuroscience 8, 4319–4333.CrossRefGoogle ScholarPubMed
Smiley, J.F. & Basinger, S.F. (1988). Somatostatin-like immunoreactivity and glycine high-affinity uptake colocalize to an interplexi-form cell of the Xenopus laevis retina. Journal of Comparative Neurology 274, 608–618.CrossRefGoogle Scholar
Smiley, F.J. & Yazulla, S. (1990). Glycinergic contacts in the outer plexiform layer of the Xenopus laevis retina characterized by antibodies to glycine, GABA and glycine receptors. Journal of Comparative Neurology 299, 375–388.CrossRefGoogle ScholarPubMed
Triller, A., Cluzeaud, F. & Korn, H. (1987). Gamma-aminobutyric acid-containing terminals can be apposed to glycine receptors at central synapses. Journal of Cell Biology 104, 947–956.CrossRefGoogle ScholarPubMed
Triller, A., Cluzeaud, F., Pfeiffer, F., Betz, H. & Korn, H. (1985). Distribution of glycine receptors at central synapses: An immunoelectron microscopy study. Journal of Cell Biology 101, 683–688.CrossRefGoogle ScholarPubMed
Triller, A., Seitanidou, T., Franksson, O. & Korn, H. (1990). Size and shape of glycine receptor clusters in a central neuron exhibiting a somato-dendritic gradient. New Biology 2, 637–641.Google Scholar
Triller, A., Seitanidou, T., Franksson, O. & Korn, H. (1991). Use of confocal microscope for the cellular analysis of the glycine syn-aptic receptor. Journal of Receptor Research 11, 347–357.CrossRefGoogle Scholar
Van Den Pol, A.N. & Gorcs, T. (1988). Glycine and glycine receptor immunoreactivity in brain and spinal cord. Journal of Neuroscience 8, 472–492.CrossRefGoogle ScholarPubMed
Vaney, D.E., Young, H.M. & Gynther, I.C. (1991). The rod circuit in the rabbit retina. Visual Neuroscience 7, 141–154.CrossRefGoogle ScholarPubMed
Wässle, H., Yamashita, M., Greferath, U., Grunert, U. & Muller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99–112.CrossRefGoogle ScholarPubMed
Weiler, R. & Ball, A.K. (1984). Co-localization of neurotensin-like immunoreactivity and [3H]-glycine uptake system in sustained amacrine cells of turtle retina. Nature 311, 759–761.CrossRefGoogle ScholarPubMed
Weiler, R., Ball, A.K. & Ammermüller, J. (1991). Neurotransmitter systems in the turtle retina. Progress in Retinal Research 10, 1–26.CrossRefGoogle Scholar
Yang, C.-Y., Yazulla, S. (1988). Light-microscopic localization of putative glycinergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 272, 343–357.CrossRefGoogle ScholarPubMed
Yazulla, S. & Studholme, K.M. (1991 a). Glycinergic interplexiform cells make synaptic contact with amacrine cell bodies in goldfish retina. Journal of Comparative Neurology 310, 1–10.CrossRefGoogle ScholarPubMed
Yazulla, S. & Studholme, K.M. (1991 b). Glycine-receptor immunoreactivity in retinal bipolar cells is postsynaptic to glycinergic and GABAergic amacrine cell synapses. Journal of Comparative Neurology 310, 11–20.CrossRefGoogle ScholarPubMed
Yazulla, S. & Yang, C.Y. (1988). Colocalization of GABA and glycine immunoreactivities in a subset of retinal neurons in tiger salamander. Neuroscience Letters 95, 37–41.CrossRefGoogle Scholar
Zucker, C.L. & Ehinger, B. (1992). Heterogeneity of receptor immunoreactivity at synapses of glycine utilizing neurons. Proceedings of the Royal Society B (London) 249, 89–94.Google ScholarPubMed