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Normalization of cell responses in cat striate cortex

  • David J. Heeger (a1)

Abstract

Simple cells in the striate cortex have been depicted as half-wave-rectified linear operators. Complex cells have been depicted as energy mechanisms, constructed from the squared sum of the outputs of quadrature pairs of linear operators. However, the linear/energy model falls short of a complete explanation of striate cell responses. In this paper, a modified version of the linear/energy model is presented in which striate cells mutually inhibit one another, effectively normalizing their responses with respect to stimulus contrast. This paper reviews experimental measurements of striate cell responses, and shows that the new model explains a significantly larger body of physiological data.

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Adelson, E.H. & Bergen, J.R. (1985). Spatiotemporal energy models for the perception of motion. Journal of the Optical Society of America A 2, 284299.
Albrecht, D.G., Farrar, S.B. & Hamilton, D.B. (1984). Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. Journal of Physiology (London) 347, 713739.
Albrecht, D.G. & Geisler, W.S. (1991). Motion sensitivity and the contrast-response function of simple cells in the visual cortex. Visual Neuroscience 7, 531546.
Albrecht, D.G. & Hamilton, D.B. (1982). Striate cortex of monkey and cat: Contrast response function. Journal of Neurophysiology 48, 217237.
Bishop, P.O., Coombs, J.S. & Henry, G.H. (1973). Receptive fields of simple cells in the cat striate cortex. Journal of Physiology (London) 231, 3160.
Blakemore, C. & Tobin, E.A. (1972). Lateral inhibition between orientation detectors in the cat's visual cortex. Experimental Brain Research 15, 439440.
Bolz, J. & Gilbert, C.D. (1986). Generation of end-inhibition in the visual cortex via interlaminar connections. Nature 320, 362365.
Bonds, A.B. (1989). Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Visual Neuroscience 2, 4155.
Bonds, A.B. (1991). Temporal dynamics of contrast gain in single cells of the cat striate cortex. Visual Neuroscience 6, 239255.
Bonds, A.B., DeBusk, B.C. & Ming, S. (1990). Stimulation far beyond the receptive field of cat striate cortical cells strongly mediates responsiveness: A mechanism for global inhibition. Investigative Opthalmology and Visual Science (Suppl.) 31, 429.
Bullier, J. & Henry, G.H. (1979a). Ordinal position of neurons in cat striate cortex. Journal of Neurophysiology 42, 12511263.
Bullier, J. & Henry, G.H. (1979b). Neural path taken by afferent streams in striate cortex of the cat. Journal of Neurophysiology 42, 12641270.
Bullier, J. & Henry, G.H. (1979c). Laminar distribution of first-order neurons and afferent terminals in cat striate cortex. Journal of Neurophysiology 42, 12711281.
Campbell, F.W., Cooper, G.F. & Enroth-Cugell, C. (1968). The angular selectivity of visual cortical cells to moving gratings. Journal of Physiology (London) 198, 237250.
Campbell, F.W., Cooper, G.F. & Enroth-Cugell, C. (1969). The spatial selectivity of visual cells of the cat. Journal of Phvsiology (London) 203, 223235.
Chao-Yi, Li. & Creutzfeldt, O. (1984). The representation of contrast and other stimulus parameters by single neurons in area 17 of the cat. Pflugers Archives 401, 304314.
Dean, A.F. (1980). The contrast-dependence of direction selectivity. Journal of Physiology (London) 303, 38p-39p.
Dean, A.F. (1981). The relationship between response amplitude and contrast for cat striate cortical neurones. Journal of Physiology (London) 318, 413427.
Dean, A.F. (1983). Adaptation-induced alteration of the relation between response amplitude and contrast in cat striate cortical mechanisms. Vision Research 23, 249256.
Dean, A.F., Hess, R.F. & Tolhurst, D.J. (1980). Divisive inhibition involved in direction selectivity. Journal of Physiology (London) 308, 84p-85p.
Dean, A.F. & Tolhurst, D.J. (1983). On the distinctiveness of simple and complex cells in the visual cortex of the cat. Journal of Physiology (London) 344, 305325.
Dean, A.F. & Tolhurst, D.J. (1986). Factors influencing the temporal phase of response to bar and grating stimuli for simple cells in the cat striate cortex. Experimental Brain Research 62, 143151.
Dean, A.F., Tolhurst, D.J. & Walker, N.S. (1982). Nonlinear temporal summation by simple cells in cat striate cortex demonstrated by failure of superposition. Experimental Brain Research 45, 456458.
DeAngelis, G.C., Ohzawa, I., Freeman, R.D. & Ghose, G. (1990). Properties of length and width tuning of cells in the cat's striate cortex. Investigative Opthalmology and Visual Science (Suppl.) 32, 430.
DeAngelis, G.C., Robson, J.G., Ohzawa, I. & Freeman, R.D. (1992). The organization of suppression in receptive fields of neurons in the cat's visual cortex. Journal of Neurophysiology (in press).
DeBruvn, E.J. & Bonds, A.B. (1986). Contrast adaptation in the cat is not mediated by GABA. Brain Research 383, 339342.
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 219240.
DeValois, K. & Tootell, R. (1983). Spatial-frequency-specific inhibition in cat striate cortex cells. Journal of Physiology (London) 336, 359376.
DeValois, R.L., Thorell, L.G. & Albrecht, D.G. (1985). Periodicity of striate-cortex-cell receptive fields. Journal of the Optical Society of America A 2, 11151123.
Douglas, R.J., Martin, K.A.C. & Whitteridge, D. (1988). Selective responses of visual cortical cells do not depend on shunting inhibition. Nature 332, 642644.
Dreher, B. (1972). Hypercomplex cells in the cat's striate cortex. Investigative Opthalmology 11, 355356.
Emerson, R.C. & Citron, M.C. (1989). Linear and nonlinear mechanisms of motion selectivity in single neurons of the cat's visual cortex. In Proceedings of IEEE International Conference on Systems, Man, and Cybernetics, ed pp. 448453. Cambridge, Massachusetts: IEEE.
Ferster, D. (1981). A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex. Journal of Physiology (London) 311, 623655.
Ferster, D. & Lindstrom, S. (1983). An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. Journal of Physiology (London) 342, 181215.
Freeman, R.D., Ohzawa, I. & Robson, J.G. (1987). A comparison of monocular and binocular inhibitory processes in the visual cortex of cat. Journal of Physiology (London) 396, 69p.
Gilbert, C.D. (1977). Laminar differences in receptive properties of cells in cat primary visual cortex. Journal of Physiology (London) 268, 391421.
Gilbert, C.D. & Wiesel, T.N. (1990). The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Research 30, 16891701.
Glezer, V.D., Tscherbach, T.A., Gauselman, V.E. & Bondarko, V.E. (1980). Linear and nonlinear properties of simple and complex receptive fields in area 17 of the cat visual cortex. Biological Cybernetics 37, 195208.
Glezer, V.D., Tscherbach, T.A., Gauselman, V.E. & Bondarko, V.E. (1982). Spatio-temporal organization of receptive fields of the cat striate cortex. Biological Cybernetics 43, 3549.
Gulyas, B., Orban, G.A., Duysens, J. & Maes, H. (1987). The suppressive influence of moving textured backgrounds on responses of cat striate neurons to moving bars. Journal of Neurophysiology 57, 17671791.
Hammond, P. & Ahmed, B. (1985). Length summation of complex cells in cat striate cortex: A reappraisal of the special/standard classification. Neuroscience 15, 639649.
Hammond, P. & MacKay, D.M. (1977). Differential responsiveness of simple and complex cells in cat striate cortex to visual texture. Experimental Brain Research 30, 275296.
Hammond, P. & MacKay, D.M. (1978). Modulation of simple cell activity in cat by moving textured backgrounds. Journal of Physiology (London) 284, 117p.
Hammond, P. & MacKay, D.M. (1981). Modulatory influences of moving textured backgrounds on responsiveness of simple cells in feline striate cortex. Journal of Physiology (London) 319, 431442.
Hammond, P., Mouat, G.S. & Smith, A.T. (1985). Motion after-effects in cat striate cortex elicited by moving gratings. Experimental Brain Research 60, 411416.
Hammond, P., Mouat, G.S. & Smith, A.T. (1986). Motion after-effects in cat striate cortex elicited by moving texture. Vision Research 26, 10551060.
Hammond, P., Mouat, G.S. & Smith, A.T. (1988). Neural correlates of motion after-effects in cat striate cortical neurones: Monocular adaptation. Experimental Brain Research 72, 120.
Hammond, P., Pomfrett, C.J.D. & Ahmed, B. (1989). Neural motion after-effects in the cat's striate cortex: Orientation selectivity. Vision Research 29, 16711683.
Hata, Y., Tsumoto, T., Sato, H., Hagihara, K. & Tamura, H. (1988). Inhibition contributes to orientation selectivity in visual cortex of cat. Nature 335, 815817.
Heeger, D.J. (1990). Nonlinear model of cat striate physiology. Society for Neuroscience Abstracts 16, 229.
Heeger, D.J. (1991). Nonlinear model of neural responses in cat visual cortex. In Computational Models of Visual Processing, ed Landy, M., Movshon, J.A., pp. 119133. Cambridge, Massachusetts: MIT Press.
Heeger, D.J. (1992a). Half-squaring in responses of cat simple cells. Visual Neuroscience (in press).
Heeger, D.J. (1992b). Modeling simple cell direction selectivity with normalized, half-squared, linear operators. Investigative Ophthalmology and Visual Science (Suppl.) 33 (in press).
Heeger, D.J. & Adelson, E.H. (1989). Nonlinear model of cat striate cortex. Optics News 15, A-42.
Hess, R., Negishi, K. & Creutzfeldt, O.D. (1975). The horizontal spread of intracortical inhibition in the visual cortex. Experimental Brain Research 22, 415419.
Hoffman, K.R. & Stone, J. (1971). Conduction velocity of afferent to cat visual cortex: A correlation with cortical receptive fields of single cells in cat striate cortex. Brain Research 32, 460466.
Holub, R.A. & Morton-Gibson, M. (1981). Response of visual cortical neurons of the cat to moving sinusoidal gratings: Response-contrast functions and spatiotemporal integration. Journal of Neurophysiology 46, 12441259.
Hubel, D. & Wiesel, T. (1962). Receptive fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106154.
Hubel, D. & Wiesel, T. (1965). Receptive field and functional architecture in two nonstriate visual areas (18–19) of the cat. Journal of Neurophysiology 28, 229289.
Kaji, S. & Kawabata, N. (1985). Neural interactions of two moving patterns in the direction and orientation domain in the complex cells of cat's visual cortex. Vision Research 25, 749753.
Kato, H., Bishop, P.O. & Orban, G.A. (1978). Hypercomplex and simple/complex cell classifications in cat striate cortex. Journal of Neurophysiology 41, 10711095.
Kulikowski, J.J. & Bishop, P.O. (1982). Silent periodic cells in the cat striate cortex. Vision Research 22, 191200.
Kulikowski, J.J., Bishop, P.O. & Kato, H. (1981). Spatial arrangement of responses by cells in the cat visual cortex to light and dark bars and edges. Experimental Brain Research 44, 371385.
Maddess, T., McCourt, M.E., Blakeslee, B. & Cunningham, R.B. (1988). Factors governing the adaptation of cells in area 17 of the cat visual cortex. Biological Cybernetics 59, 229236.
Maffei, L. & Fiorentini, A. (1973). The visual cortex as a spatialfrequency analyzer. Vision Research 13, 12551267.
Maffei, L. & Fiorentini, A. (1976). The unresponsive regions of visual cortical receptive fields. Vision Research 16, 11311139.
Maffei, L., Fiorentini, A. & Bisti, S. (1973). Neural correlate of perceptual adaptation to gratings. Science 182, 10361038.
Marlin, S.G., Hasan, S.J. & Cynader, M.S. (1988). Direction-selective adaptation in simple and complex cells in cat striate cortex. Journal of Neurophysiology 59, 13141330.
Martin, K.A.C. & Whitteridge, D. (1984). Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. Journal of Physiology (London) 353, 463504.
McLean, J. & Palmer, L.A. (1989). Contribution of linear spatiotemporal receptive-field structure to velocity selectivity of simple cells in area 17 of cat. Vision Research 29, 675679.
Morrone, M.C., Burr, D.C. & Maffei, L. (1982). Functional implications of cross-orientation inhibition of cortical visual cells. Proceedings of the Royal Society B (London) 216, 335354.
Movshon, J.A. (1975). The velocity tuning of single units in cat striate cortex. Journal of Physiology (London) 249, 445468.
Movshon, J.A. & Lennie, P. (1979). Pattern-selective adaptation in visual cortical neurones. Nature 278, 850852.
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978a). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology (London) 283, 5377.
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978b). Receptive-field organization of complex cells in the cat's striate cortex. Journal of Physiology (London) 283, 7999.
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978c). Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. Journal of Physiology (London) 283, 101120.
Murphy, P.C. & Sillito, A.M. (1987). Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature 329, 727729.
Nelson, J.I., Lingner, I. & Bremmer, F. (1991). Adaptation and disadaptation in cat A17 cells stimulated only beyond their classic receptive fields. Investigative Ophthalmology and Visual Science (Suppl.) 32, 1252.
Nelson, J.J. & Frost, B.J. (1978). Orientation-selective inhibition from beyond the classic visual receptive field. Brain Research 139, 359365.
Nelson, S.B. (1991). Temporal interactions in the cat visual system. I. Orientation-selective suppression in visual cortex. Journal of Neuroscience 11, 344356.
Ohzawa, I. & Freeman, R.D. (1986). The binocular organization of simple cells in the cat's visual cortex. Journal of Neurophysiology 56, 221242.
Ohzawa, I., Sclar, G. & Freeman, R.D. (1982). Contrast gain control in the cat visual cortex. Nature 298, 266268.
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651667.
Pettigrew, J.D., Nikara, T. & Bishop, P.O. (1968). Responses to moving slits by single units in cat striate cortex. Experimental Brain Research 6, 373390.
Pollen, D. & Ronner, S. (1983). Visual cortical neurons as localized spatial-frequency filters. IEEE Transactions on Systems, Man, and Cybernetics 13, 907916.
Pollen, D.A., Andrews, B.W. & Feldon, S.E. (1978). Spatial-frequency selectivity of periodic complex cells in the visual cortex of the cat. Vision Research 18, 665682.
Pollen, D.A., Gaska, J.P. & Jacobson, L.D. (1989). Physiological constraints on models of visual cortical function. In Models of Brain Function, ed Cotterill, R.M.J., Cambridge University Press.
Reid, R.C., Soodak, R.E. & Shapley, R.M. (1987). Linear mechanisms of directional selectivity in simple cells of cat striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 84, 87408744.
Reid, R.C., Soodak, R.E. & Shapley, R.M. (1991). Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. Journal of Neurophysiology 66, 505529.
Robson, J.G. (1988). Linear and nonlinear operations in the visual system. Investigative Ophthalmology and Visual Science (Suppl.) 29, 117.
Robson, J.G., Deangelis, G.C., Ohzawa, I. & Freeman, R.D. (1991). Cross-orientation inhibition in cat cortical cells originates from within the receptive field. Investigative Ophthalmology and Visual Science (Suppl.) 32, 429.
Rose, D. (1977). Responses of single units in cat visual cortex to moving bars of light as a function of bar length. Journal of Physiology (London) 271, 123.
Saul, A.B. & Cynader, M.S. (1989a). Adaptation in single units in the visual cortex: The tuning of aftereffects in the spatial domain. Visual Neuroscience 2, 593607.
Saul, A.B. & Cynader, M.S. (1989b). Adaptation in single units in the visual cortex: The tuning of aftereffects in the temporal domain. Visual Neuroscience 2, 609620.
Sclar, G. & Freeman, R.D. (1982). Orientation selectivity of the cat's striate cortex is invariant with stimulus contrast. Experimental Brain Research 46, 457461.
Sclar, G., Maunsell, J.H.R. & Lennie, P. (1990). Coding of image contrast in central visual pathways of the macaque monkey. Vision Research 30, 110.
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain control. Progress in Retinal Research 3, 263346.
Singer, W., Tretter, F. & Cynader, M. (1975). Organization of cat striate cortex: A correlation of receptive-field properties with afferent and efferent connections. Journal of Neurophysiology 38, 10801098.
Skottun, B.C., Bradley, A., Sclar, G., Ohzawa, I. & Freeman, R.D. (1987). The effects of contrast on visual orientation and spatial-frequency discrimination: A comparison of single cells and behavior. Journal of Neurophysiology 57, 773786.
Spekreuse, H. & van den Berg, T.J.T.P. (1971). Interaction between colour and spatial coded processes converging to retinal ganglion cells in goldfish. Journal of Physiology (London) 215, 679692.
Sperling, G. & Sondhi, M.M. (1968). Model for visual luminance discrimination and flicker detection. Journal of the Optical Society of America 58, 11331145.
Stone, J. & Dreher, B. (1973). Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex. Journal of Neurophysiology 36, 551567.
Tanaka, K. (1983). Cross-correlation analysis of geniculostriate neuronal relationships in cats. Journal of Neurophysiology 49, 13031318.
Tanaka, K. (1985). Organization of geniculate inputs to visual cortical cells in the cat. Vision Research 25, 357364.
Tolhurst, D.J. & Dean, A.F. (1987). Spatial summation by simple cells in the striate cortex of the cat. Experimental Brain Research 66, 607620.
Tolhurst, D.J. & Dean, A.F. (1991). Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex. Visual Neuroscience 6, 421428.
Tolhurst, D.J., Walker, N.S., Thompson, I.D. & Dean, A.F. (1980). Nonlinearities of temporal summation in neurones in area 17 of the cat. Experimental Brain Research 38, 431435.
Toyama, K., Kimura, M. & Tanaka, T. (1981). Organization of cat visual cortex as investigated by cross-correlation technique. Journal of Neurophysiology 46, 202214.
Ullman, S. & Schechtman, G. (1982). Adaptation and gain normalization. Proceedings of the Royal Society B (London) 216, 299313.
Vautin, R.G. & Berkeley, M.A. (1977). Responses of single cells in cat visual cortex to prolonged stimulus movement: Neural correlates of visual aftereffect. Journal of Neurophysiology 40, 10511065.
Vidyasaoar, T.R. (1990). Pattern adaptation in cat visual cortex is a cooperative phenomenon. Neuroscience 36, 175179.
von der Heydt, R., Hanny, P. & Adorjani, C. (1978). Movement aftereffects in the visual system. Archives of Italian Biology 116, 248254.
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