Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-25T05:26:11.835Z Has data issue: false hasContentIssue false
  • English
  • Français

Responses of rod bipolar cells isolated from dogfish retinal slices to concentration-jumps of glutamate

Published online by Cambridge University Press:  02 June 2009

R.A. Shiells  and
G. Falk
R.A. Shiells
Affiliation:
Department of Physiology, University College London, Gower St., London WC1E 6BT, UK
G. Falk
Affiliation:
Department of Physiology, University College London, Gower St., London WC1E 6BT, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Rod on-bipolar cell light responses are mediated by a class of metabotropic glutamate receptor which is coupled via a G-protein to the control of a cGMP cascade, with cGMP acting to open cation channels, whilst off-bipolar cells possess ionotropic glutamate receptors. Whole-cell voltage-clamp recordings were obtained from on- and off-bipolar cells of dark-adapted dogfish retinal slices, identified by their light responses. Isolated cells were exposed to concentration-jumps of glutamate. At negative voltage-clamp potentials, on-bipolar cells responded to glutamate with outward currents with a mean delay of 10.8 ms, whilst off-bipolar cells responded with inward currents without any delay. Neither cell type showed desensitization to applied steps of glutamate. The dose-response relation for on-bipolar cells showed no gradual saturation, but increased linearly with a sharp cutoff above 200 μM glutamate. This dose-response relation could be fitted with a theoretical expression assuming Michaelis-Menten kinetics for the action of glutamate on receptors and a linear relation between the concentration of receptors bound to glutamate and the fall in cGMP this induces. The dose-response relation of off-bipolar cells showed saturation with a limiting slope of 2 at low glutamate concentrations, suggesting that two molecules of glutamate are required to open each channel by a cooperative mechanism. The glutamate receptor coupled cGMP cascade of rod on-bipolar cells can account for high synaptic voltage gain.

Keywords

Bipolar cellRetinaGlutamate receptorCyclic GMPConcentration-jump
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 6 , November 1994 , pp. 1175 - 1183
Copyright
Copyright © Cambridge University Press 1994

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

Ames, A. III, Walseth, T.F., Heyman, R.A., Barad, M., Graeff, R.M. & Goldberg, N.D. (1986). Light-induced changes in cGMP metabolic flux correspond with electrical responses of photoreceptors. Journal of Biological Chemistry 261, 13034–13042.CrossRefGoogle ScholarPubMed
Arshavsky, V.Y. & Bownds, M.D. (1992). Regulation of deactivation of photoreceptor G protein by its target enzyme and cGMP. Nature 357, 416–417.CrossRefGoogle Scholar
Ashmore, J.F. & Falk, G. (1979). Transmission of visual signals to bipolar cells near absolute threshold. Vision Research 19, 419–423.CrossRefGoogle ScholarPubMed
Ashmore, J.F. & Falk, G. (1980 a). Responses of rod bipolar cells in the dark-adapted retina of the dogfish, Scyliorhinus canicula. Journal of Physiology 300, 115–150.CrossRefGoogle ScholarPubMed
Ashmore, J.F. & Falk, G. (1980 b). The single-photon signal in rod bipolar cells of the dogfish retina. Journal of Physiology 300, 151–166.CrossRefGoogle ScholarPubMed
Attwell, D., Mobbs, P., Tessier-Lavigne, M. & Wilson, M. (1987). Neurotransmitter-induced currents in retinal bipolar cells of the axolptl, Ambystoma mexicanum. Journal of Physiology 387, 125–161.CrossRefGoogle ScholarPubMed
Belgum, J.H. & Copenhagen, D.R. (1988). Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus). Journal of Physiology 396, 225–246.CrossRefGoogle ScholarPubMed
Cobbs, W.H. & Pugh, E.N. Jr. (1987). Kinetics and components of the flash photocurrent of isolated retinal rods of the larval salamander, Ambystoma tigrinum. Journal of Physiology 394, 529–572.CrossRefGoogle ScholarPubMed
Colquhoun, D., Jonas, P. & Sackmann, B. (1992). Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices. Journal of Physiology 458, 261–289.CrossRefGoogle ScholarPubMed
Cone, R.A. (1963). Quantum relations of the rat electroretinogram. Journal of General Physiology 46, 1267–1286.CrossRefGoogle ScholarPubMed
Dizhoor, A.M., Ray, S., Kumar, S., Niemi, G., Spencer, M., Brolley, D., Walsh, K.A., Philipov, P.P., Hurley, J.B. & Stryer, L. (1991). Recoverin: A calcium sensitive activator of retinal rod guanylate cyclase. Science 251, 915–918.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Shapley, R.M. (1973). Flux, not retinal illumination, is what cat retinal ganglion cells really care about. Journal of Physiology 233, 311–326.CrossRefGoogle Scholar
Falk, G. (1989). Signal transmission from rods to bipolar and horizontal cells: A synthesis. Progress in Retinal Research 8, 255–279.CrossRefGoogle Scholar
Falk, G. & Fatt, P. (1972). Physical changes induced by light in the rod outer segments of vertebrates. In Handbook of Sensory Physiology, Vol. VII/I, Photochemistry of Vision, ed. Dartnall, H.J.A., pp. 235–244. Berlin: Springer.Google Scholar
Falk, G. & Fatt, P. (1974 a) Limitations to single-photon sensitivity in vision. In Lecture Notes in Biomathematics, Vol. 4: Physics and Mathematics of the Nervous System, ed. Conrad, M., Guttinger, W., & Dal Cin, M., pp. 171–204. Berlin: Springer.Google Scholar
Falk, G. & Fatt, P. (1974 b). The dynamic voltage-transfer function for rod-bipolar cell transmission. Vision Research 14, 739–741.CrossRefGoogle ScholarPubMed
Falk, G. & Shiells, R.A. (1986). Do horizontal cell responses contribute to the electroretinogram (ERG) in dogfish? Journal of Physiology 381, 113P.Google Scholar
Fulton, A.B. & Rushton, W.A.H. (1978). The human rod ERG: Correlation with psychophysical responses in light and dark adaptation. Vision Research 18, 785–792.CrossRefGoogle ScholarPubMed
Gilbertson, T.A., Scobey, R. & Wilsom, M. (1991). Permeation of calcium ions through non-NMDA glutamate channels in retinal bipolar cells. Science 251, 1613–1615.CrossRefGoogle ScholarPubMed
Hirano, A.A. & MacLeish, P.R. (1991). Glutamate and 2-amino-4-phos-phonobutyrate evoke an increase in potassium conductance in retinal bipolar cells. Proceedings of the National Academy of Sciences of the USA 88, 805–809.CrossRefGoogle ScholarPubMed
Hsu, Y.-T. & Molday, R.S. (1993). Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 361, 76–79.CrossRefGoogle ScholarPubMed
Kaneko, A., De La Villa, P. & Sasaki, T. (1993). Glutamate-induced responses in identified cat bipolar cells. XXXII Congress of the International Union of Physiological Sciences. Sunday Abstracts pp. 4.Google Scholar
Kawamura, S. & Murakami, M. (1991). Calcium-dependent regulation of cyclic GMP phosphodiesterase by a protein from frog retinal rods. Nature 349, 420–423.CrossRefGoogle ScholarPubMed
Kim, H.G. & Miller, R.F. (1993). Properties of synaptic transmission from photoreceptors to bipolar cells in the mudpuppy retina. Journal of Neurophysiology 69, 352–360.CrossRefGoogle ScholarPubMed
Lagnado, L. & Baylor, D.A. (1994). Calcium controls light-triggered formation of catalytically active rhodopsin. Nature 367, 273–277.CrossRefGoogle ScholarPubMed
Lamb, T.D. & Matthews, H.R. (1988). External and internal actions in the response of salamander retinal rods to altered external calcium concentration. Journal of Physiology 403, 473–494.CrossRefGoogle ScholarPubMed
Levttzkj, A. (1984). Receptors. A Quantitative Approach. Menlo Park: Benjamin/Cummings. Chap. 5, pp. 91–101.Google Scholar
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shioemoto, R., Mizuno, N. & Nakanishi, S. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. Journal of Biological Chemistry 268, 11868–11873.CrossRefGoogle ScholarPubMed
Nakanishi, S. (1992). Molecular diversity of glutamate receptors and implications for brain function. Science 258, 597–603.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346, 269–271.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1991). cGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter. Neuron 7, 677–683.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, 361–369.CrossRefGoogle ScholarPubMed
Pugh, E.N. Jr. & Lamb, T.D. (1993). Amplification and kinetics of the activation steps in phototransduction. Biochimica et Biophysica Acta 1141, 111–149.CrossRefGoogle ScholarPubMed
Sasaki, T. & Kaneko, A. (1993). Glutamate-induced responses in off-type bipolar cells of the cat retina. Investigative Ophthalmology and Visual Science 34, 1381.Google Scholar
Shiells, R.A., Falk, G. & Naghshineh, S. (1981). Action of glutamate and aspartate analogues on rod horizontal and bipolar cells. Nature 294, 592–594.CrossRefGoogle ScholarPubMed
Shiells, R.A., Falk, G. & Naghshineh, S. (1986). Ionophoretic study of the action of excitatory amino acids on rod horizontal cells of the dogfish retina. Proceedings of the Royal Society B (London) 227, 121–135.Google Scholar
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, 91–94.Google ScholarPubMed
Shiells, R.A. & Falk, G. (1992 a). The glutamate receptor linked cGMP cascade of retinal on-bipolar cells is pertussis and cholera toxinsensitive. Proceedings of the Royal Society B (London) 247, 17–20.Google ScholarPubMed
Shiells, R.A. & Falk, G. (1992 b). Properties of the cGMP-activated channel of retinal on-bipolar cells. Proceedings of the Royal Society B (London) 247, 21–25.Google ScholarPubMed
Shiells, R.A. & Falk, G. (1992 c). Retinal on-bipolar cells contain a nitric oxide-sensitive guanylate cyclase. Neuroreport 3, 845–848.CrossRefGoogle ScholarPubMed
Shiells, R.A. & Falk, G. (1993). Responses of bipolar cells isolated from retinal slices of dogfish to concentration jumps of glutamate. Journal of Physiology 473, 9P.Google Scholar
Stockton, M. & Slaughter, M.M. (1989). B-wave of the electroretinogram. A reflection of ON bipolar cell activity. Journal of General Physiology 93, 101–122.CrossRefGoogle ScholarPubMed