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Involvement of ON and OFF retinal channels in the eye and head horizontal optokinetic nystagmus of the frog

Published online by Cambridge University Press:  02 June 2009

Y. H. Yücel
Affiliation:
Département de Neurophysiologie et de Biologie des Comportements, Centre de Neurochimie du CNRS, Strasbourg, France
B. Jardon
Affiliation:
Département de Neurophysiologie et de Biologie des Comportements, Centre de Neurochimie du CNRS, Strasbourg, France
N. Bonaventure
Affiliation:
Département de Neurophysiologie et de Biologie des Comportements, Centre de Neurochimie du CNRS, Strasbourg, France

Abstract

The specific role of ON and OFF retinal information channels in the generation of the horizontal optokinetic nystagmus (OKN) of the frog was studied. Coil recordings of monocular eye and head OKN were obtained before and after intravitreal injection of two drugs that block either ON or OFF channels. The intravitreal injection of 2-amino-4-phosphonobutyrate (APB), a glutamate analog that selectively blocks the ON retinal channel, strongly reduced or even cancelled the monocular OKN of the head and of the eye. The intravitreal injection of another glutamate analog, the cis-2, 3-piperidine dicarboxylic acid (PDA) that especially blocks the OFF retinal channel, did not affect the gain velocity of the slow phase of both the horizontal monocular head and eye OKN, for low stimulus velocities. Our results suggest that the retinal ON information channel, but not the OFF channel, is involved in the generation of the slow phase of the OKN of the frog, at least at low drum velocities.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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References

Ariel, M. (1987). Synaptic drugs injected into the vitreous affect the retinal control of turtle eye movements. 17th Annual Meeting Society of Neuroscience Abstracts 13, Part 3, 1053.Google Scholar
Bäckström, A.-C., Hemilä, S. & Reuter, T. (1978). Directional selectivity and color coding in the frog retina. Medical Biology 56, 7283.Google ScholarPubMed
Barlow, H.B., Fitzhug, R. & Kuffler, S.W. (1957). Change of organization in the receptive fields of the cat's retina during dark adaptation. Journal of Physiology 137, 338354.CrossRefGoogle ScholarPubMed
Birukow, G. (1937). Untersuchungen über den optischen Drehnystagmus über die Sehscharfe des Grasfrosches (Rana temporaria). Zeitschrift für Vergleichende Physiologie 25, 92142.CrossRefGoogle Scholar
Bolz, J., Wässle, H. & Thier, P. (1984). Pharmacological modulation of ON and OFF ganglion cells in the cat retina. Neuroscience 12, 875885.CrossRefGoogle Scholar
Bonaventure, N., Wioland, N. & Bigenwald, J. (1983). Involvement of GABAergic mechanisms in the optokinetic nystagmus of the frog. Experimental Brain Research 50, 433441.Google ScholarPubMed
Bonaventure, N., Yücel, Y.H. & Jardon, B. (1987). Effects of the glutamate antagonists, 2–4 amino-phosphonobutyric acid (APB) and cis-2, 3,-piperidine dicarboxylic acid (PDA), on ERG, retinal ON-OFF ganglion cell responses and optokinetic nystagmus (OKN) in the frog. The Second World Congress of Neuroscience (IBRO), p. 731.Google Scholar
Buhl, E.H. & Peichl, L. (1986). Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of AOS. Journal of Comparative Neurology 253, 163174.CrossRefGoogle Scholar
Chen, E.P. & Linsenmeier, R.A. (1987). The effects of APB on the contrast sensitivity of cat retinal X cells. 17th Annual Meeting Society of Neuroscience Abstracts 13, Part 2, 381.Google Scholar
Cochran, S.L., Dieringer, N. & Precht, W. (1984). Basic optokinetic ocular reflex pathways in the frog. Journal of Neuroscience 4, 4357.CrossRefGoogle ScholarPubMed
Collewun, H. (1975). Direction-selective units in the rabbit's nucleus of the optic tract. Brain Research 100, 489508.CrossRefGoogle Scholar
Conover, W.J. (1971). The use of ranks. In Practical Nonparametric Statistics, pp. 203216. New York, London, Sydney, Toronto: Wiley.Google Scholar
Cunningham, J.R. & Neal, M.J. (1985). Effect of excitatory amino acid on gamma-aminobutyric acid release from frog horizontal cells. Journal of Physiology 362, 5167.CrossRefGoogle ScholarPubMed
Davies, J., Evans, R.H., Jones, A.W., Smith, D.A.S. & Watkins, J.C. (1982). Differential activation and blockade of excitatory amino-acid receptors in the mammalian and amphibian central nervous systems. Comparative Biochemistry and Physiology 27, 211224.Google Scholar
DeMarco, P.J., Nussdorf, J.D., Brockman, D.A. & Powers, M.K. (1987). The ON channel is necessary for optokinetic nystagmus at high spatio-temporal frequency in goldfish. 17th Annual Meeting Society of Neuroscience Abstracts 13, Part 3, 1053.Google Scholar
Dieringer, N. & Precht, W. (1982). Compensatory head and eye movement in the frog and their contribution to stabilization of gaze. Experimental Brain Research 47, 394406.CrossRefGoogle ScholarPubMed
Dieringer, N., Cochran, S.L. & Precht, W. (1983). Differences in the central organization of gaze stabilizing reflexes between frog and turtle. Journal of Comparative Physiology 153, 495508.CrossRefGoogle Scholar
Gioanni, H., Rey, J., Villalobos, J. & Dalbera, A. (1984). Single unit activity in the nucleus of the basal optic root (nBOR) during optokinetic, vestibular, and visuo-vestibular stimulations in the alert pigeon (Columbia livia). Experimental Brain Research 57, 4960.CrossRefGoogle ScholarPubMed
Gordon, J. & Hood, D.C. (1976). Anatomy and physiology of the frog retina. In The Amphibian Visual System. A Multidisciplinary Approach, ed. Fite, K.V., pp. 2986. New York, San Francisco, London: Academic Press.CrossRefGoogle Scholar
Gruberg, E.R. & Grasse, K.L. (1984). Basal optic complex in the frog (Rana pipiens): a physiological and HRP study. Journal of Neurophysiology 51, 9981010.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. (1983). Effects of early monocular deprivation on visual input to cat nucleus of the optic tract. Experimental Brain Research 51, 236246.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. (1986). Visual inputs relevant for OKN in mammals. In The Oculomotor and Skeletal Motor Systems: Differences and Similarities: Progress in Brain Research, Vol. 64, ed. Freund, H.-J., Buttner, U., Cohen, B. & Noth, J., pp. 7584. Amsterdam, New York, Oxford: Elsevier.CrossRefGoogle Scholar
Hoffmann, K.-P. & Schoppmann, A. (1981). A quantitative analysis of the direction-specific responses of neurons in the cat's nucleus of the optic tract. Experimental Brain Research 42, 146157.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. & Stone, J. (1985). Retinal input to the nucleus of the optic tract of the cat assessed by antidromic activation of ganglion cells. Experimental Brain Research 59, 395403.CrossRefGoogle Scholar
Jardon, B., Yücel, Y.H. & Bonaventure, N. (1989). Role of the glutamatergic system in the separation of the ON and OFF channels in the frog retina; possible modulation by the cholinergic and glycinergic systems. European Journal of Pharmacology.CrossRefGoogle Scholar
Katte, O. & Hoffmann, K.-P. (1980). Direction-specific neurons in the pretectum of the frog (Rana esculenta). Journal of Comparative Physiology 140, 5357.CrossRefGoogle Scholar
Knapp, A.G. & Ariel, M. (1984). Selective blockade of retinal ON channel eliminates horizontal optokinetic nystagmus in rabbits. The Annual Meeting of the Association of Research in Vision and in Ophthalmology 25, 229.Google Scholar
Koch, U.T. (1977). A miniature movement detector applied to recording of wing beats in Locusta. Fortschritte der Zoologie 24, 327332.Google Scholar
Kondrashev, S.L. & Orlov, O.Y. (1976). Direction-sensitive neurons in the frog visual system. Neirofiziologiya 8, 196198.Google Scholar
Lazar, G., Alkonyi, B. & Tòth, P. (1983). Re-investigation of the role of the accessory optic system and pretectum in the horizontal optokinetic head nystagmus of the frog. Lesion experiments. Ada Biologica Hungarica 34, 385393.Google ScholarPubMed
Mallach, R., Strong, N. & Van Sluyter, R.C. (1981). Analysis of monocular optokinetic nystagmus in normal and visually deprived kittens. Brain Research 210, 367372.CrossRefGoogle Scholar
Manteuffel, G. (1984). Electrophysiology and anatomy of direction specific pretectal units in the salamander (Salamandra salamandra). Experimental Brain Research 54, 415425.CrossRefGoogle Scholar
Maturana, H.R., Lettvin, J.Y., McCulloch, W.S. & Pitts, W.H. (1960). Anatomy and physiology of vision in the frog (Rana pipiens). Journal of General Physiology 43 (Suppl.), 129175.CrossRefGoogle Scholar
Miller, R.F. & Slaughter, N.M. (1986). Excitatory amino-acid receptors of the retina: diversity of subtypes and conductance mechanisms. Trends in Neuroscience 9, 211217.CrossRefGoogle Scholar
Montgomery, N., Fite, K.V. & Bengston, L. (1981). The accessory optic system of Rana pipiens: neuroanatomical connections and intrinsic organization. Journal of Comparative Neurology 203, 595612.CrossRefGoogle ScholarPubMed
Montgomery, N., Fite, K.V., Taylor, M. & Bengston, L. (1982). Neuronal correlates of optokinetic nystagmus in the mesencephalon of Rana pipiens: functional analysis. Brain Behavior Evolution 21, 137153.CrossRefGoogle Scholar
Montgomery, N., Fite, K.V. & Grigonis, A.M. (1985). The pretectal nucleus Lentiformis Mesencephali of Rana pipiens. Journal of Comparative Neurology 234, 264275.CrossRefGoogle ScholarPubMed
Neal, M.J., Cunningham, J.R., James, T.A., Joseph, M. & Collins, J.F. (1981). The effect of 2-amino-4-phosphonobutyrate (APB) on acetylcholine release from rabbit retina: evidence for ON channel input to cholinergic amacrine cells. Neuroscience Letters 26, 301305.CrossRefGoogle ScholarPubMed
Oyster, C.W. & Barlow, H.B. (1967). Direction-selective units in rabbit retina: distribution of preferred directions. Science 155, 841842.CrossRefGoogle ScholarPubMed
Oyster, C.W., Takahahi, E. & Collewun, H. (1972). Direction-selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit. Vision Research 12, 183193.CrossRefGoogle ScholarPubMed
Rademaker, G.G.J. & Braak, Ter J.W.G. (1948). On the central mechanism of some optic reactions. Brain 71, 4876.CrossRefGoogle ScholarPubMed
Schiller, P.H. (1982). Central connections of the retinal ON and OFF pathways. Nature 297, 580583.CrossRefGoogle ScholarPubMed
Schiller, P.H., Sandell, J.H. & Maunsell, J.H.R. (1986). Function of the ON and OFF channels of the visual system. Nature 322, 824825.CrossRefGoogle ScholarPubMed
Shells, R.A., Falk, G. & Naghshineh, S. (1981). Action of glutamate and aspartate analogues on rod horizontal and bipolar cells. Nature 294, 592594.CrossRefGoogle Scholar
Simpson, J.I., Soodak, R.E. & Hess, R.E. (1979). The accessory optic system and its relation to the vestibulocerebellum. In Reflex Control of Posture and Movement: Progress in Brain Research, Vol: 50, Granit R. & Pompeiano O., pp. 715724. Amsterdam, New York, Oxford, North Holland: Elsevier.CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R. (1981). 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 211, 182185.CrossRefGoogle ScholarPubMed
Smith, E.L., Duncan, G.C., Harwerth, R.S.S. & Crawford, M.L.J. (1987). Spatial contrast sensitivity deficits produced by ON channel blocked in the Rhesus Monkey. 17th Annual Meeting—Society of Neuroscience Abstracts 13, Part 2, 381.Google Scholar
Sücher, N., Przybyzewski, A. & Grusser, O.-J. (1986). The effect of amino-phosphonobutyric acid (APB) and of cis-2, 3-piperidine dicarboxylic acid (PDA) on flash responses of retinal ganglion cells. In Abstract of Annual Meeting of Neuroscience 13, 381.Google Scholar
Van Hof-Van, Duin J. (1978). Direction preference of optokinetic response in monocularly tested normal kittens and light-deprived cats. Archives Italiennes de Biologie 116, 471477.Google Scholar
Watanabe, S. & Murakami, M. (1984). Synaptic mechanisms of directional selectivity in ganglion cells of frog retina as revealed by in-tracellular recordings. Japanese Journal of Physiology 34, 497511.Google Scholar
Yücel, Y.H., Jardon, B. & Bonaventure, N. (1989) Is a retinal input involved in the generation of eye-resetting fast phase in the frog eye optokinetic nystagmus? Neuroscience Letters.CrossRefGoogle ScholarPubMed