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Cone receptive field in cat retina computed from microcircuitry

Published online by Cambridge University Press:  02 June 2009

R. G. Smith
Affiliation:
Department of Anatomy, School of Medicine, University of Pennsylvania, Philadelphia
P. Sterling
Affiliation:
Department of Anatomy, School of Medicine, University of Pennsylvania, Philadelphia

Abstract

The receptive-field profile of the cone in cat retina was computed. The computation was based on (1) the known anatomical circuit connecting cones via narrow-field bipolar cells to the on-beta ganglion cell; (2) the known physiological receptive-field profile of the on-beta (X) cell at the corresponding eccentricity; and (3) a model in which the beta receptive field arises by linear superposition of cone receptive fields. The computed cone receptive field has a center/surround organization with a center almost as broad as that of the beta cell center. The cone surround is comparably broad to that of the beta cell but somewhat lower in peak amplitude. The problems to which the center/surround receptive field are the solution, namely, signal compression and noise reduction, apparently must be solved before the first synapse of the visual pathway.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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References

Barlow, H.B. (1981). The Ferrier lecture: critical limiting factors in the design of the eye and visual cortex. Proceedings of the Royal Society B (London) 212, 134.Google Scholar
Barlow, H.B.Levick, W.R. (1976). Threshold setting by the surround of cat retinal ganglion cells. Journal of Physiology 259, 737757.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.-W. (1979). The membrane current of single rod outer segments. Journal of Physiology 288, 589611.CrossRefGoogle ScholarPubMed
Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. (1971). The receptive fields of cones in the retina of the turtle. Journal of Physiology 214, 265294.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology 240, 397419.CrossRefGoogle ScholarPubMed
Boycott, B.B., Peichl, L. & Wässle, H. (1978). Morphological types of horizontal cell in the retina of the domestic cat. Proceedings of the Royal Society B (London) 203, 229245.Google 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, 271291.CrossRefGoogle Scholar
Chun, M.H. & Wässle, H. (1989). GABA-like immunoreactivity in the cat retina: electron microscopy. Journal of Comparative Neurology 279, 5567.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Levick, W.R. (1974). Properties of rarely encountered types of ganglion cell in the cat's retina and an overall classification. Journal of Physiology 240, 457492.CrossRefGoogle Scholar
Cleland, B.G., Levick, W.R. & Wässle, H. (1975). Physiological identification of a morphological class of cat retinal ganglion cells. Journal of Physiology 248, 151171.CrossRefGoogle ScholarPubMed
Cleland, B.G., Harding, T.H. & Tulunay-Keesey, U. (1979). Visual resolution and receptive-field size: examination of two kinds of cat retinal ganglion cell. Science 205, 10151017.CrossRefGoogle ScholarPubMed
Cohen, E.D, & Sterling, P. (1990 a). Anatomical circuit for the beta ganglion cell receptive field (submitted for publication).Google Scholar
Cohen, E.D. & Sterling, P. (1990 b). Demonstration of cell types among core bipolar neurons of cat retina. Philosophical Transactions of the Royal Society (in press).Google Scholar
Cohen, E.D. & Stering, P. (1990 c). Convergence and divergence of cones onto bipolar cells in the central area of cat retina. Philosophical Transactions of the Royal Society (in press).Google Scholar
Copenhagen, D.R. & Green, D.G. (1987). Spatial spread of adaptation within the cone network of turtle retina. Journal of Physiology 393, 763776.CrossRefGoogle ScholarPubMed
Creutzfeldt, O.D., Sakmann, B., Scheich, H. & Korn, A. (1970). Sensitivity distribution and spatial summation within receptive-field center of retinal on-center ganglion cells and transfer function of the retina. Journal of Neurophysiology 33, 654671.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Lennie, P. (1982). The influence of temporal level on receptive-field organization of retinal ganglion cells in cat. Journal of Physiology 333, 343366.CrossRefGoogle ScholarPubMed
Detwiler, P.B. & Hodgkin, A.L. (1979). Electrical coupling between cones in turtle retina. Journal of Physiology 291, 75100.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C., Lennie, P. & Shapley, R.M. (1975). Surround contribution to light adaptation in cat retinal ganglion cells. Journal of Physiology 247, 579588.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C., Robson, J.G., Schweitzer-Tong, D.E. & Watson, A.B. (1983). Spatiotemporal interactions in cat retinal ganglion cells showing linear spatial summation. Journal of Physiology 341, 279307.CrossRefGoogle ScholarPubMed
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517552.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr. (1981). Functional architecture of cone bipolar cells in mammalian retina. Vision Research 21, 15591564.CrossRefGoogle ScholarPubMed
Freed, M.A. & Sterling, P. (1988). The on-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 23032320.CrossRefGoogle ScholarPubMed
Frishman, L.J., Freeman, A.W., Troy, J.B., Schwettzer-Tong, D.E. & Eeroth-Cugell, C.E. (1987). Spatiotemporal-frequency responses of cat retinal ganglion cells. Journal of General Physiology 89, 559628.Google ScholarPubMed
Hayhoe, M.M. & Smith, M.V., (1989). The role of spatial filtering in sensitivity regulation. Vision Research 29, 457469.CrossRefGoogle ScholarPubMed
Hochstein, S., & Shapley, R.M. (1976). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology 262, 265284.CrossRefGoogle ScholarPubMed
Kaneko, A. & Tachibana, M. (1986). Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology 373, 443461.CrossRefGoogle ScholarPubMed
Koch, C., Poggio, T. & Torre, V. (1982). Retinal ganglion cells: a functional interpretation of dendritic morphology Philosophical Transactions of the Royal Society B (London) 298, 227264.Google ScholarPubMed
Kolb, H. (1977). The organization of the outer plexiform layer in the retina of the cat: electron-microscopic observations. Journal of Neurocytology 6, 131153.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: electron-microscopic observations. Journal of Neurocytology 8, 295329.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1984). Neural architecture of the cat retina. Trends in Retinal Research 3, 2160.Google Scholar
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells, and ganglion cells of the cat retina: a Golgi study. Vision Research 21, 10811114.CrossRefGoogle ScholarPubMed
Kraft, T.W. & Burkhardt, D.A. (1986). Telodendrites of cone photoreceptors: structure and probable function. Journal of Comparative Neurology 249, 1327.CrossRefGoogle ScholarPubMed
Laughlin, S.B., Howard, J. & Blakeslee, B. (1987). Synaptic limitations to contrast coding in the retina of the blowfly Calliphora. Proceedings of the Royal Society B (London) 231, 437467.Google ScholarPubMed
Liebman, P.A., Parker, K.R. & Dratz, E.A. (1987). The molecular mechanism of visual excitation and its relation to the structure and composition of the rod outer segment. Annual Review of Physiology 49, 765791.CrossRefGoogle Scholar
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G. & Enroth-Cugell, C. (1982). Receptive-field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 11731183.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Miller, R.F. (1987). Horizontal cells contribute to the receptive-field surround of ganglion cells in the rabbit retina. Brain Research 414, 182186.CrossRefGoogle Scholar
McGuire, B.A., Stevens, J.K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. Journal of Neuroscience 6, 907918.CrossRefGoogle ScholarPubMed
Murakami, M., Shimoda, Y., Nakatani, K., Miyachi, E. & Watanabe, S. (1982). GABA-mediated negative feedback from horizontal cells to cones in carp retina. Japanese Journal of Physiology 32, 911926.Google ScholarPubMed
Nelson, R. (1977). Cat cones have rod input: a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Neurology 172, 109136.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 11831195.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1985). A17: a broad-field amacrine cell in the rod system of the cat retina. Journal of Neurophysiology 54, 592614.CrossRefGoogle ScholarPubMed
Normann, R.A., Perlman, I., Kolb, H., Jones, J. & Daly, S.J. (1984). Direct excitatory interactions between cones of different spectral types in the turtle retina. Science 224, 625627.CrossRefGoogle ScholarPubMed
Peichl, L. & Wässle, H. (1979). Size, scatter, and coverage of ganglion cell receptive-field centers in the cat retina. Journal of Physiology 291, 117141.CrossRefGoogle ScholarPubMed
Piccolino, M., Neyton, J. & Gershenfeld, H. (1981). Center-surround antagonistic organization in small-field luminosity horizontal cells of turtle retina. Journal of Neurophysiology 45, 363375.CrossRefGoogle ScholarPubMed
Pugh, E.N. & Altman, J. (1988). A role for calcium in adaptation. Nature 334, 1617.CrossRefGoogle ScholarPubMed
Rall, W. (1967). Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. Journal of Neurophysiology 30, 11381168.CrossRefGoogle ScholarPubMed
Raviola, E. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina: a freeze-fracture study in monkeys and rabbits. Journal of Cell Biology 65, 192222.CrossRefGoogle ScholarPubMed
Robson, J.G. & Enroth-Cugell, C.E. (1978). Light distribution in the cat's retinal image. Vision Research 18, 159173.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583601.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Stone, J. (1965). Response of retinal ganglion cells to moving visual patterns. Journal of Neurophysiology 28, 819832.CrossRefGoogle ScholarPubMed
Sakmann, B. & Creutzfeldt, O.D. (1969). Scotopic and mesopic light adaptation in the cat's retina. Pflügers Archives 313, 168185.CrossRefGoogle ScholarPubMed
Sarthy, P.V. & Fu, M. (1989). Localization of L-glutamic acid decarboxylase mRNA in cat retina horizontal cells by in situ hybridization. Journal of Comparative Neurology 288, 593600.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. Progress in Retinal Research 3, 263346.CrossRefGoogle Scholar
Smith, R.G., Freed, M.A. & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network. Journal of Neuroscience 6, 35053517.CrossRefGoogle ScholarPubMed
Sneyd, J. & Tranchina, D. (1989). Phototransduction in cones: an inverse problem in enzyme kinetics. Bulletin of Mathematical Biology 51, 749784.CrossRefGoogle ScholarPubMed
Srinivasan, M.V., Laughlin, S.B. & Dubs, A. (1982). Predictive coding: a fresh view of inhibition in the retina. Proceedings of the Royal Society B (London) 216, 427459.Google ScholarPubMed
Steinberg, R.H., Reid, M. & Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of Comparative Neurology 148, 229248.CrossRefGoogle ScholarPubMed
Sterling, P., Freed, M.A. & Smith, R.G. (1988). Architecture of rod and cone circuits to the on-beta ganglion cell. Journal of Neuroscience 8, 623642.CrossRefGoogle Scholar
Tsukamoto, Y., Smith, R.G. & Sterling, P. (1990 a). Collective coding improves signal-to-noise ratio in ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 87, 18601864.CrossRefGoogle Scholar
Tsukamoto, Y., Masarachia, P.G., Schein, S.J. & Sterling, P. (1990 b). Gap junctions between the pedicles of macaque foveal cones. Society of Neuroscience Abstracts 16, 407.Google Scholar
Wässle, H. (1971). Optical quality of the cat eye. Vision Research 11, 9951006.CrossRefGoogle ScholarPubMed
Werblin, F.S. (1974). Control of retinal sensitivity, II: Lateral interactions at the outer plexiform layer. Journal of General Physiology 63, 6287.CrossRefGoogle Scholar
Wiesel, T.N. (1960). Receptive fields of ganglion cells in the cat's retina. Journal of Physiology 153, 583594.CrossRefGoogle ScholarPubMed