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Functional properties of a metabotropic glutamate receptor at dendritic synapses of ON bipolar cells in the amphibian retina

Published online by Cambridge University Press:  02 June 2009

Ning Tian
Affiliation:
Departments of Biophysical Sciences, Physiology, and Ophthalmology, School of Medicine, State University of New York, Buffalo
Malcolm M. Slaughter
Affiliation:
Departments of Biophysical Sciences, Physiology, and Ophthalmology, School of Medicine, State University of New York, Buffalo

Abstract

Perforated patch-voltage and current-clamp recordings were obtained from ON bipolar cells in the amphibian retinal slice preparation. The currents produced by the photoreceptor transmitter were compared to the currents produced by selective metabotropic glutamate agonists: L-2-amino-4-phosphonobutyrate (L-AP4, APB) and 1S,3R 1-amino-1,3 cyclopentanedicarboxylic acid (1S,3R ACPD). Both agonists produced currents that were very similar to that produced by the photoreceptor transmitter in terms of conductance and reversal potential. The similarities suggest that the metabotropic glutamate receptors are functionally localized to the synaptic region of ON bipolar dendrites. The synaptic conductance rarely exceeded the non-synaptic conductance. The mean input resistance of ON bipolar neurons was 770 MΩ in the light and 1.2 GΩ in the dark. The average light-regulated synaptic conductance was 57% of the non-synaptic conductance. The L-AP4 regulated conductance averaged 77% of the non-synaptic conductance, while the 1S,3R ACPD regulated conductance averaged 95% of the non-synaptic conductance. This balance between synaptic and non-synaptic conductance indicates that the synapse will not shunt the cell and the conductance ratio serves to maximize incremental gain at the photoreceptor to ON bipolar synapse. This conductance mechanism makes the ON bipolar cell well equipped to relay rod signals.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Ashmore, J.F. & Copenhagen, D.R. (1980). Different postsynaptic events in two types of retinal bipolar cell. Nature 288, 8486.CrossRefGoogle ScholarPubMed
Ashmore, J.F. & Falk, G. (1980). Responses of rod bipolar cells in the dark-adapted retina of the dogfish, Scyliorhinus canicula. Journal of Physiology 300, 115150.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, 125161.CrossRefGoogle ScholarPubMed
Ayoub, G.S., Korenbrot, J.I. & Copenhagen, D.R. (1989). Release of endogenous glutamate from isolated cone photoreceptors of the lizard. Neuroscience Research (Suppl.) 10, S47–S56.Google ScholarPubMed
Dacheux, R.F. & Miller, R.F. (1976). Photoreceptor-bipolar cell transmission in the perfused retina eyecup of the mudpuppy. Science 191, 963964.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, 331345.CrossRefGoogle ScholarPubMed
Falk, G. (1988). Signal transmission from rods to bipolar and horizontal cells: A synthesis. Progress in Retinal Research 8, 255279.CrossRefGoogle Scholar
Frumkes, T.E. & Miller, R.F. (1979). Pathways and polarities of synaptic interactions in the inner retina of the mudpuppy: II. Insight revealed by an analysis of latency and threshold. Brain Research 161, 1324.CrossRefGoogle ScholarPubMed
Hanke, W., Cook, N.J. & Kaupp, U.B. (1988). cGMP-dependent channel protein from photoreceptor membranes: Single-channel activity of the purified and reconstituted protein. Proceedings of the National Academy of Sciences of the U.S.A. 85, 9498.CrossRefGoogle ScholarPubMed
Hirano, A.A. & MacLeish, P.R. (1991). Glutamate and 2-amino-4-phosphonobutyrate evoke an increase in potassium conductance in retinal bipolar cells. Proceedings of the National Academy of Sciences of the U.S.A. 88, 805809.CrossRefGoogle ScholarPubMed
Horn, R. & Marty, A. (1988). Muscarinic activation of ionic currents measured by a new whole-cell recording method. Journal of General Physiology 922, 145159.CrossRefGoogle Scholar
Ishida, A.T., Kaneko, A. & Tachibana, M. (1984). Responses of solitary retinal horizontal cells from Carassius auratus to glutamate and related amino acids. Journal of Physiology 348, 255270.CrossRefGoogle ScholarPubMed
Karschin, A. & Wässle, H. (1990). Voltage- and transmitter-gated currents in isolated rod bipolar cells of rat retina. Journal of Neurophysiology 63, 860876.CrossRefGoogle ScholarPubMed
Lasater, E.M. (1988). Membrane currents of retinal bipolar cells in culture. Journal of Neurophysiology 60, 14601480.CrossRefGoogle ScholarPubMed
Lindau, M. & Neher, E. (1988). Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflügers Archives 411, 137146.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D., Maple, B.R. & Werblin, F.S. (1994). A novel GABA receptor on bipolar cell terminals in the tiger salamander retina. Journal of Neuroscience 14, 12021212.CrossRefGoogle ScholarPubMed
Maguire, G., Maple, B., Lukasiewicz, P. & Werblin, F. (1989). 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, 1014410147.CrossRefGoogle ScholarPubMed
Miller, R.F. & Slaughter, M.M. (1986). Excitatory amino acids of the retina: Diversity of subtypes and conductance mechanisms. Trends in Neurosciences 9, 211218.CrossRefGoogle Scholar
Murakami, M., Ohtsuka, T. & Shimazaki, H. (1975). Effects of aspartate and glutamate on the bipolar cells in the carp retina. Vision Research 15, 456458.CrossRefGoogle ScholarPubMed
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mGLUR6 with a high selectivity for L-2-amino-4-phosphonobutyrate. Journal of Biological Chemistry 268, 1186811873.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269271.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1991). cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677683.CrossRefGoogle ScholarPubMed
Nelson, R. (1973). A comparison of electrical properties of neurons in Necturus retina. Journal of Neurophysiology 36, 519535.CrossRefGoogle ScholarPubMed
Nomura, A., Shigemoto, R., Nakamura, Y., Okamoto, N., Mizuno, N. & Nakanishi, S. (1994). Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77, 361369.CrossRefGoogle ScholarPubMed
Nygaard, R.W. & Frumkes, T.E. (1982). LEDs: Convenient, inexpensive sources for visual experimentation. Vision Research 22, 435440.CrossRefGoogle ScholarPubMed
Palmer, E., Monaghan, D.T. & Cotman, C.W. (1989). Trans-ACPD, a selective agonist of the phosphoinositide-coupled excitatory amino acid receptor. European Journal of Pharmacology 166, 585587.CrossRefGoogle ScholarPubMed
Pugh, E.N. & Lamb, T.D. (1990). Cyclic GMP and calcium: The internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Research 30, 19231948.CrossRefGoogle ScholarPubMed
Schoepp, D., Bockaert, J. & Sladeczek, F. (1990). Pharmacological and functional characteristics of metabotropic excitatory amino acid receptors. Trends in Pharmacological Sciences 11, 508515.CrossRefGoogle ScholarPubMed
Shiells, R.A., Falk, G. & Naghshineh, S. (1981). Action of glutamate and aspartate analogues on rod horizontal and bipolar cells. Nature 294, 592594.CrossRefGoogle ScholarPubMed
Shiells, R.A. & Falk, G. (1990). Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proceedings of the Royal Society B (London) 242, 9194.Google ScholarPubMed
Shiells, R.A. & Falk, G. (1992). The glutamate-receptor linked cGMP cascade of retinal on-bipolar cells is pertussis and cholera toxinsensitive. Proceedings of the Royal Society B (London) 247, 1720.Google ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1981). 2-Amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182185.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1985). Characterization of an extended glutamate receptor of the ON bipolar neuron in the vertebrate retina. Journal of Neuroscience 5, 224233.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1987). Gamma-aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: Evidence for a negative feedback from amacrine cells. Proceedings of the National Academy of Sciences of the U.S.A. 84, 35013505.CrossRefGoogle ScholarPubMed
Tachibana, M., Okada, T., Arimura, T., Kobayashi, K. & Piccolino, M. (1993). Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina. Journal of Neuroscience 13, 28982909.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, 4972.CrossRefGoogle ScholarPubMed
Thoreson, W.B. & Miller, R.F. (1993). Membrane currents evoked by excitatory amino acid agonists in ON bipolar cells of the mudpuppy retina. Journal of Neurophysiology 70, 13261338.CrossRefGoogle Scholar
Tian, N. & Slaughter, M.M. (1994). Pharmacological similarity between the retinal APB receptor and the family of metabotropic glutamate receptors. Journal of Neurophysiology 71, 22582268.CrossRefGoogle ScholarPubMed
Toyoda, J. (1973). Membrane resistance changes underlying bipolar cell response in the carp retina. Vision Research 13, 283294.CrossRefGoogle ScholarPubMed
Wässle, H., Grünert, U., Cook, N.J. & Molday, R.S. (1992). The cGMP-gated channel of rod outer segments is not localized in bipolar cells of the mammalian retina. Neuroscience Letters 134, 199202.CrossRefGoogle Scholar
Wässle, H., Yamashita, M., Greferath, U., Grünert, U. & Muller, F. (1991). The rod bipolar cell of the mammalian retina. Visual Neuroscience 7, 99112.CrossRefGoogle ScholarPubMed
Werblin, F.S. (1978). Transmission along and between rods in the tiger salamander retina. Journal of Physiology 280, 449470.CrossRefGoogle ScholarPubMed
Wu, S.-M. (1987). Synaptic connections between neurons in living slices of the larval salamander retina. Journal of Neuroscience Methods 20, 139149.CrossRefGoogle ScholarPubMed
Yamashita, M. & Wässle, H. (1991). Responses of rod bipolar cells isolated from the rat retina to the glutamate agonist 2-amino-4-phosphonobutyric acid (APB). Journal of Neuroscience 11, 23722382.CrossRefGoogle Scholar