Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-22T17:21:25.840Z Has data issue: false hasContentIssue false
  • English
  • Français

Nonlinearity of the inhibition underlying retinal directional selectivity

Published online by Cambridge University Press:  02 June 2009

Franklin R. Amthor  and
Norberto M. Grzywacz
Franklin R. Amthor
Affiliation:
Department of Psychology and Neurobiology Research Center, University of Alabama at Birmingham, Birmingham
Norberto M. Grzywacz
Affiliation:
Center for Biological Information Processing, Massachusetts Institute of Technology, Cambridge, and The Smith-Kettlewell Eye Research Institute, San Franciso
Get access Rights & Permissions [Opens in a new window]

Abstract

An important mechanism for the discrimination of direction of motion in the retina is a spatially asymmetric inhibition. This inhibition has been postulated to operate either as a subtraction, like in difference-of-Gaussians' models, or as a division, like in shunting-inhibition models of directional selectivity. The latter, but not the former, is nonlinear. This raises the question of whether the inhibitory mechanism involved in directional selectivity is nonlinear. To investigate this issue, we studied the linearity of the contrast dependence of the extracellularly recorded responses to apparent motions in ON-OFF directionally selective ganglion cells of the rabbit retina. The results show that the inhibition underlying directional selectivity is nonlinear and fits shunting-inhibition models well. Other biophysical mechanisms that might account for the type of nonlinearity observed in the data are also considered.

Keywords

RabbitRetinaGanglion cellsDirectional selectivityNonlinear inhibitionShunting inhibition
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 3 , March 1991 , pp. 197 - 206
Copyright
Copyright © Cambridge University Press 1991

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

Adelson, E.H. & Bergen, J.R. (1985). Spatio-temporal energy models for the perception of motion. Journal of the Optical Society of America A 2, 284–299.CrossRefGoogle Scholar
Albrecht, D.G. & De Valois, R.L. (1981). Striate cortex responses to periodic patterns with and without the fundamental harmonics. Journal of Physiology 319, 497–514.CrossRefGoogle ScholarPubMed
Ames, A.A., III & Hastings, A.B. (1956). Studies on water and electrolytes in nervous tissue. Journal of Neurophysiology 19, 201–212.CrossRefGoogle ScholarPubMed
Amthor, F.R. & Grzywacz, N.M. (1988). The time course of inhibition and the velocity independence of direction selectivity in the rabbit retina. Investigative Ophthalmology and Visual Science 29, 225.Google Scholar
Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1984). Morphology of ON-OFF direction-selective ganglion cells in the rabbit retina. Brain Research 298, 187–190.CrossRefGoogle ScholarPubMed
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97–121.CrossRefGoogle ScholarPubMed
Ariel, M. & Adolph, A.R. (1985). Neurotransmitter inputs to directionally sensitive turtle retinal ganglion cells. Journal of Neurophysiology 54, 1123–1143.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982). Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. Journal of Physiology 324, 161–185.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in rabbit's retina. Journal of Physiology 178, 477–504.CrossRefGoogle ScholarPubMed
Caldwell, J.H., Daw, N.W. & Wyatt, H.J. (1978). Effects of picrotoxin and stychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. Journal of Physiology 276, 277–298.CrossRefGoogle Scholar
Coombs, J.S., Eccles, J.C. & Fatt, P. (1955). The inhibitory suppression of reflex discharges from motoneurones. Journal of Physiology 130, 396–413.CrossRefGoogle ScholarPubMed
Dacheux, R.F., Delmelle, M., Miller, R.F. & Noell, W.K. (1973). Isolated rabbit retina preparation suitable for intracellular and extracellular analysis. Federation Proceedings 32, 327.Google Scholar
DeVoe, R.D., Carras, P.L., Criswell, M.H. & Guy, R.G. (1989). Not by ganglion cells alone: Directional selectivity is widespread in identified cells of the turtle retina. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 235–246. Berlin, F.R.G.: Springer-Verlag.CrossRefGoogle Scholar
Dodge, F.A. & Rahamimoff, R. (1967). Cooperative action of calcium ions in transmitter release at the neuromuscular junction. Journal of Physiology 193, 419–432.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Dunn, O.J. & Clark, V.A. (1987). Applied Stat istics: Analysis of Variance and Regression. New York: John Wiley.Google Scholar
Grzywacz, N.M. & Amthor, F.R. (1988). What are the directionally selective subunits of rabbit retinal ganglion cells? Society for Neuroscience Abstracts 14, 603.Google Scholar
Grzywacz, N.M. & Amthor, F.R. (1989 a). Facilitation in ON-OFF directionally selective ganglion cells of the rabbit retina. Society for Neuroscience Abstracts 15, 969.Google Scholar
Grzywacz, N.M. & Amthor, F.R. (1989 b). A computationally robust anatomical model for retinal directional selectivity. In Advances in Neural Information Processing Systems Vol. 1, ed. Touretzky, D.S., pp. 477–484. Palo Alto, California: Morgan Kaufman Publishers.Google Scholar
Grzywacz, N.M., Amthor, F.R. & Mistler, L.A. (1990). Applicability of quadratic and threshold models to motion discrimination in the rabbit retina. Biological Cybernetics 64, 41–49.CrossRefGoogle ScholarPubMed
Grzywacz, N.M. & Koch, C. (1987). Functional properties of models for direction selectivity in the retina, Synapse 1, 417–434.CrossRefGoogle ScholarPubMed
Grzywacz, N.M. & Yuille, A.L. (1990). A model for the estimate of local image velocity by cells in the visual cortex. Proceedings of the Royal Society B (London) 239, 129–161.Google Scholar
Heeger, D.J. (1987). A model for the extraction of image flow. Journal of the Optical Society of America A 4, 1455–1471.CrossRefGoogle Scholar
Jack, J.J.B., Noble, D. & Tsien, R.W. (1975). Electric Current Flow in Excitable Cells. Hong Kong: Clarendon Press.Google Scholar
Kandel, E.R. & Schwartz, J.H. (1985). Principles of Neural Science. New York: Elsevier.Google Scholar
Kernell, D. (1970). Cell properties of importance for the transfer of signals in nervous pathways. In Excitatory Synaptic Mechanisms ed. Andersen, P.O. & Jansen, J., pp. 269–273. Oslo, Norway: Universitetsforlag.Google Scholar
Koch, C., Poggio, T. & Torre, V. (1982). Retinal ganglion cells: a functional interpretation of dendritic morphology. Philosophical Transactions of the Royal Society B 298, 227–264.Google ScholarPubMed
Madison, D.V. & Nicoll, R.A. (1982). Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature 299, 636–638.CrossRefGoogle ScholarPubMed
Marchiafava, P.L. (1979). The responses of retinal ganglion cells to stationary and moving visual stimuli. Vision Research 19, 1203–1211.CrossRefGoogle ScholarPubMed
Masland, R.H., Mills, W. & Cassidy, C. (1984). The functions of acetylcholine in the rabbit retina. Proceedings of the Royal Society B (London) 223, 121–139.Google ScholarPubMed
Miller, R.F. (1979). The neuronal basis of ganglion-cell receptive-field organization and the physiology of amacrine cells. In The Neurosciences Fourth Study Program, ed. Schmitt, F.O. & Worden, F.G., pp. 227–245. Cambridge, Massachusetts: MIT Press.Google Scholar
Poggio, T. & Reichardt, W.E. (1973). Considerations on models of movement detection. Kybernetik 13, 223–227.CrossRefGoogle ScholarPubMed
Rall, W. (1964). Theoretical significance of dendritic trees for neuronal input-output relations. In Neural Theory and Modelling, ed. Reiss, R.F., pp. 73–79. Stanford, California: Stanford University Press.Google Scholar
Schwindt, P.C. & Crill, W.E. (1982). Factors influencing motoneuron rhythmic firing: results from a voltage-clamp study. Journal of Neurophysiology 48, 875–890.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Victor, J.D. (1980). The effect of contrast on the nonlinear response of the Y cell. Journal of Physiology 302, 535–547.CrossRefGoogle ScholarPubMed
Smith, S.J., Augustine, G.J. & Charlton, M.P. (1985). Transmission at voltage-clamped giant synapse of the squid: evidence for cooperativity of presynaptic calcium action. Proceedings of the National Academy of Sciences of the U.S.A. 82, 622–625.CrossRefGoogle ScholarPubMed
Stephens, M.A. (1987). Regression tests of fit. In Goodness-of-Fit, Colloquia Mathematica Societatis János Bolyai, Vol. 45, ed. Révész, P., Sarkadi, K. & Sen, P.K., pp. 541–557. Amsterdam: North- Holland Publishing Company.Google Scholar
Torre, V. & Poggio, T. (1978). A synaptic mechanism possibly underlying directional selectivity to motion. Proceedings of the Royal Society B (London) 202, 409–416.Google Scholar
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.CrossRefGoogle ScholarPubMed
Victor, J.D. (1987). The dynamics of the cat retina X cell centre. Journal of Physiology (London) 386, 219–246.CrossRefGoogle ScholarPubMed
Victor, J.D. (1988). The dynamics of the cat retina Y cell subunit. Journal of Physiology (London) 405, 289–320.CrossRefGoogle ScholarPubMed
Watanabe, S.-I. & Murakami, M. (1984). Synaptic mechanisms of directional selectivity in ganglion cells of frog retina as revealed by intracellular recordings. Japanese Journal of Physiology 34, 497–511.Google ScholarPubMed
Wyatt, H.J. & Daw, N.W. (1975). Directionally sensitive ganglion cells in the rabbit retina: specificity for stimulus direction, size, and speed. Journal of Neurophysiology 38, 613–626.CrossRefGoogle ScholarPubMed