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Complicated substructure from simple circularly symmetric Gaussian processes within the centers of goldfish ganglion cell receptive fields

Published online by Cambridge University Press:  02 June 2009

Roger P. Zimmerman  and
Michael W. Levine
Roger P. Zimmerman
Affiliation:
Departments of Neurological Sciences and Physiology, Rush Medical College, Chicago, and Department of Anatomy and Cell Biology and Committee on Neuroscience, University of Illinois at Chicago, Chicago
Michael W. Levine
Affiliation:
Department of Psychology and Committee on Neuroscience, University of Illinois at Chicago, Chicago
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Abstract

The center of the receptive field of some retinal ganglion cells exhibits an interesting fine structure: the relative amplitudes of responses to onset and responses to offset of a small spot of light varies systematically as the spot is positioned at various places within the center. Although this pattern may appear complicated, a simple model can account for it in detail. The model postulates that the ganglion cell receives input from separate ON and OFF processes within the center of its receptive field. These processes have the form of Gaussian functions and are laterally displaced from each other. These central ON and OFF input processes are not associated with the additional antagonistic surround of the receptive field.

The model is examined for various parameters of the input processes. The observed systematic variation in the ratio of offset to onset responses is predicted when the two processes are of nearly equal width (standard deviation of the Gaussians). Receptive fields made of more than two Gaussians produce various patterns, depending on the relative standard deviations of the Gaussians. Oblong fields, reminiscent of those found in visual cortex, may be generated from a relatively small number of circularly symmetric Gaussian processes.

Keywords

Retinal ganglion cellsGoldfish retinaSubregionsGaussian processes
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 6 , December 1991 , pp. 547 - 559
Copyright
Copyright © Cambridge University Press 1991

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References

Arkin, M.S. & Miller, R.F. (1988). Bipolar origin of synaptic inputs to sustained OFF-ganglion cells in the mudpuppy retina. Journal of Neurophysiology 60, 1122–1142.CrossRefGoogle ScholarPubMed
Atick, J.J. & Redlich, A.N. (1990). Mathematical model of the simple cells in the visual cortex. Biological Cybernetics 63, 99–109.CrossRefGoogle Scholar
Barlow, H.B. (1953). Summation and inhibition in the frog's retina. Journal of Physiology 119, 69–88.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R. & Mcreynolds, J.S. (1982). Sustained synaptic input to ganglion cells of mudpuppy retina. Journal of Physiology 326, 91–108.CrossRefGoogle ScholarPubMed
Bolz, J., Wässle, H. & Thier, P. (1984). Pharmacological modulation of ON and OFF ganglion cells in the cat retina. Neuroscience 12, 875–885.CrossRefGoogle Scholar
Bonds, A.B. (1989). Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Visual Neuroscience 2, 41–55.CrossRefGoogle ScholarPubMed
Borges, S. & Wilson, M. (1990). The lateral spread of signal between bipolar cells of the tiger salamander retina. Biological Cybernetics 63, 45–50.CrossRefGoogle ScholarPubMed
Chen, E.P. & Freeman, A.W. (1989). A model for spatiotemporal frequency responses in the X-cell pathway of the cat's retina. Vision Research 29, 271–291.CrossRefGoogle Scholar
Cleland, B.G. & Lee, B.B. (1985). A comparison of visual responses of cat lateral geniculate nucleus neurones with those of ganglion cells afferent to them. Journal of Physiology 369, 249–268.CrossRefGoogle Scholar
Cleland, B.G., Levick, W.R. & Sanderson, K.J. (1973). Properties of sustained and transient ganglion cells in the cat retina. Journal of Physiology 228, 649–680.CrossRefGoogle ScholarPubMed
Davis, G.W. & Naka, K.-I. (1980). Spatial organizations of catfish retinal neurons, I: Single- and random-bar stimulation. Journal of Neurophysiology 43, 807–831.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C., Robson, J.G., Schweitzer-Tong, D.E. & Watson, A.B. (1983). Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation. Journal of Physiology 341, 279–307.CrossRefGoogle ScholarPubMed
Eysel, U.T., Crook, J.M. & Machemer, H.F. (1990). GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex. Experimental Brain Research 80, 626–630.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr, Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells in the carp retina. Science 198, 1267–1269.CrossRefGoogle Scholar
Ferster, D. (1987). Origin of orientation-selective EPSPs in simple cells of cat visual cortex. Journal of Neuroscience 7, 1780–1791.CrossRefGoogle ScholarPubMed
Ferster, D. & Koch, C. (1987). Neuronal connections underlying orientation selectivity in cat visual cortex. Trends in Neuroscience 10, 487–492.CrossRefGoogle Scholar
Gilbert, C.D. & Wiesel, T.N. (1985). Intrinsic connectivity and receptive-field properties in visual cortex. Vision Research 25, 365–374.CrossRefGoogle ScholarPubMed
Ginsburg, K.S., Johnsen, J.A. & Levine, M.W. (1984). Common noise in the firing of neighboring ganglion cells in goldfish retina. Journal of Physiology 351, 433–450.CrossRefGoogle ScholarPubMed
Gordon, J. & Shapley, R.M. (1978). Contrast sensitivity and spatial summation in frog and eel retinal ganglion cells. In Visual Psychophysics and Physiology, ed. Armington, J.C., Krauskopf, J. & Wooten, B.R., pp. 315–329. New York: Academic Press.CrossRefGoogle Scholar
Hare, W.A. & Owen, W.G. (1990). Spatial organization of the bipolar cell's receptive field in the retina of the tiger salamander. Journal of Physiology 421, 233–245.CrossRefGoogle ScholarPubMed
Hartline, H.K. (1938). The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. American Journal of Physiology 121, 400–415.CrossRefGoogle Scholar
Hata, Y., Tsumoto, T., Sato, H., Hagihara, K. & Tamura, H. (1988). Inhibition contributes to orientation selectivity in visual cortex of cat. Nature 336, 815–817.CrossRefGoogle Scholar
Heggelund, P. & Moors, J. (1983). Orientation selectivity and the spatial distribution of enhancement and suppression in receptive fields of cat striate cortex cells. Experimental Brain Research 52, 235–247.Google ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology 262, 265–284.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.CrossRefGoogle ScholarPubMed
Ishida, A., Stell, W.K. & Lightfoot, D.O. (1980). Rod and cone inputs to bipolar cells in the goldfish retina. Journal of Comparative Neurology 191, 315–335.CrossRefGoogle ScholarPubMed
Jones, J.P. & Palmer, L.A. (1987). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1187–1211.CrossRefGoogle ScholarPubMed
Kaneko, A. (1970). Physiological and morphological identification of horizontal, bipolar, and amacrine cells in goldfish retina. Journal of Physiology 207, 623–633.CrossRefGoogle ScholarPubMed
Kaneko, A. (1973). Receptive-field organization of bipolar and amacrine cells in the goldfish retina. Journal of Physiology 235, 133–153.CrossRefGoogle ScholarPubMed
Kujiraoka, T.&Saito, T. (1986). Electrical coupling between bipolar cells in carp retina. Proceedings of the National Academy of Sciences of the U.S.A. 83, 4063–4066.CrossRefGoogle ScholarPubMed
Lasater, E.M. (1982). Spatial receptive fields of catfish retinal ganglion cells. Journal of Neurophysiology 48, 823–835.CrossRefGoogle ScholarPubMed
Lehky, S.R.&Sejnowski, T.J. (1982). Network model of shape-fromshading: neural function arises from both receptive and projective fields. Nature 333, 452–454.CrossRefGoogle Scholar
Levick, W.R. (1972). Receptive fields of retinal ganglion cells. In Physiology of Photoreceptor Organs; Handbook of Sensory Physiology VII, Part 2, Fuortes, M.G.F., 531–566. Berlin and New York: Springer-Verlag.CrossRefGoogle Scholar
Levine, M.W.&Shefner, J.M. (1977). Variability in ganglion cell firing patterns; implications for separate "ON" and "OFF" processes. Vision Research 17, 765–776.CrossRefGoogle Scholar
Levine, M.W.&Shefner, J.M. (1977). X-like and not-X-like cells in goldfish retina. Vision Research 19, 95–97.CrossRefGoogle Scholar
Levine, M.W.&Shefner, J.M. (1981). Distance-dependent interactions between the rod and the cone systems in goldfish retina. Experimental Brain Research 44, 353–361.CrossRefGoogle ScholarPubMed
Levine, M.W.&Zimmerman, R.P. (1985). Mechanisms contributing to the receptive fields of ganglion cells in the retinae of fish. Investigative Ophthalmology and Visual Science (Suppl.) 26, 263.Google Scholar
Levine, M.W.&Zimmerman, R.P. (1987). The correspondence between subregions in overlapping receptive fields of neighboring ganglion cells. Investigative Ophthalmology and Visual Science (Suppl.) 28, 240.Google Scholar
Levine, M.W.&Zimmerman, R.P. (1988). Evidence for local circuits within the receptive fields of retinal ganglion cells in goldfish. Visual NeuroScience (Suppl.) 1, 377–385.CrossRefGoogle ScholarPubMed
Levine, M.W.&Zimmerman, R.P. (1990). Complex receptive-field structure from simple circularly symmetric Gaussian processes. Investigative Ophthalmology and Visual Science (Suppl.) 31, 116.Google Scholar
Lukasiewicz, P.D.&Werblin, F.S. (1990). The spatial distribution of excitatory and inhibitory inputs to ganglion cell dendrites in the tiger salamander retina. Journal of Neuroscience 10, 210–221.CrossRefGoogle ScholarPubMed
Mcguire, B.A., Stevens, J.K.&Sterling, P. (1990). Microcircuitry of beta ganglion cells in cat retina. Journal of Neuroscience 6, 907–918.CrossRefGoogle Scholar
Movshon, J.A., Thompson, I.D.&Tolhurst, D.J. (1978). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology 283, 53–77.CrossRefGoogle ScholarPubMed
Müller, F., Wassle, H.&Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
Murakami, M.&Shimoda, Y. (1977). Identification of amacrine and ganglion cells in the carp retina. Journal of Physiology 264, 801–818.CrossRefGoogle ScholarPubMed
Rodieck, R.W.&Stone, J. (1965). Analysis of receptive fields of cat retinal ganglion cells. Journal of Neurophysiology 28, 833–849.CrossRefGoogle ScholarPubMed
Schwartz, E.A. (1973). Organization of ON-OFF cells in the retina of the turtle. Journal of Physiology 230, 1–14.CrossRefGoogle ScholarPubMed
Shapley, R., Dawi, S.&Kaplan, E. (1985). The receptive-field surround's temporal response properties are spatially inhomogeneous. Investigative Ophthalmology and Visual Science (Suppl.) 26, 195.Google Scholar
Shapley, R.&Gordon, J. (1978). The eel retina. Ganglion cell classes and spatial mechanisms. Journal of General Physiology 71, 139–155.CrossRefGoogle ScholarPubMed
Shefner, J.M.&Levine, M.W. (1979). A comparison of properties of goldfish retinal ganglion cells as a function of lighting conditions during dissection. Vision Research 19, 83–89.CrossRefGoogle ScholarPubMed
So, Y.T.&Shapley, R. (1981). Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate interneurons. Journal of Neurophysiology 45, 107–120.CrossRefGoogle Scholar
Soodak, R.E. (1986). Two-dimensional modeling of visual receptive fields using Gaussian subunits. Proceedings of the National Academy of Sciences of the U.S.A. 83, 9259–9263.CrossRefGoogle ScholarPubMed
Soodak, R. E. (1987). The retinal ganglion cell mosaic defines orientation columns in striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 84, 3936–3940.CrossRefGoogle ScholarPubMed
Soodak, R. E., Shapley, R. M. & Kaplan, E. (1987). Functional subunits of receptive-field centers in cat X and Y cells. Investigative Ophthalmology and Visual Science (Suppl.) 28, 240.Google Scholar
Spitzer, H. & Hochstein, S. (1985). A complex-cell receptive-field model. Journal of Neurophysiology 53, 1266–1286.CrossRefGoogle ScholarPubMed
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.CrossRefGoogle ScholarPubMed
Tanaka, K. (1985). Organization of geniculate inputs to visual cortical cells in the cat. Vision Research 25, 357–364.CrossRefGoogle ScholarPubMed
Thibos, L. N. & Levick, W. R. (1983). Bimodal receptive fields of cat retinal ganglion cells. Vision Research 23, 1561–1572.CrossRefGoogle ScholarPubMed
Wässle, H., Boycott, B. B. & Illing, R. -B (1981). Morphology and mosaic of ON- and OFF-beta cells in the cat retina and some functional considerations. Proceedings of the Royal Society B (London) 212, 177–195.Google Scholar