Abstract

We review how neurons in the principal pathway connecting the retina to the visual cortex represent information about the chromatic and spatial characteristics of the retinal image. Our examination focuses particularly on individual neurons: what are their visual properties, how might these properties arise, what do these properties tell us about visual signal transformations, and how might these properties be expressed in perception? Our discussion is inclined toward studies on old-world monkeys and where possible emphasizes quantitative work that has led to or illuminates models of visual signal processing.

© 2005 Optical Society of America

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D. J. Calkins, P. Sterling, “Evidence that circuits for spatial and color vision segregate at the first retinal synapse,” Neuron 24, 313–321 (1999).
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1996 (6)

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K. Zipser, V. A.F. Lamme, P. H. Schiller, “Contextual modulation in primary visual cortex,” J. Neurosci. 16, 7376–7389 (1996).
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1995 (13)

L. J. Croner, E. Kaplan, “Receptive fields of P and M ganglion cells across the primate retina,” Vision Res. 35, 7–24 (1995).
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A. G. Leventhal, K. G. Thompson, D. Liu, Y. Zhou, S. J. Ault, “Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex,” J. Neurosci. 15, 1808–1818 (1995).
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D. P. Edwards, K. P. Purpura, E. Kaplan, “Contrast sensitivity and spatial frequency response of primate cortical neurons in and around the cytochrome oxidase blobs,” Vision Res. 35, 1501–1523 (1995).
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1994 (8)

S. Nelson, L. Toth, B. Sheth, M. Sur, “Orientation selectivity of cortical neurons during intracellular blockade of inhibition,” Science 265, 774–777 (1994).
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G. C. DeAngelis, R. D. Freeman, I. Ohzawa, “Length and width tuning of neurons in the cat’s primary visual cortex,” J. Neurophysiol. 71, 347–374 (1994).
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T. Yoshioka, J. B. Levitt, J. S. Lund, “Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: anatomy of interlaminar projections,” Visual Neurosci. 11, 467–489 (1994).
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D. M. Dacey, B. B. Lee, “The blue-on opponent pathway in the primate retina originates from a distinct bistratified ganglion cell,” Nature 367, 731–735 (1994).
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J. Rabin, E. Switkes, M. Crognale, M. E. Schneck, A. J. Adams, “Visual evoked potentials in three-dimensional color space: correlates of spatio-chromatic processing,” Vision Res. 34, 2657–2671 (1994).
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S. H.C. Hendry, T. Yoshioka, “A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus,” Science 264, 575–577 (1994).
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1993 (4)

H. Komatsu, Y. Ideura, “Relationships between color, shape, and pattern selectivities of neurons in the inferior temporal cortex of the monkey,” J. Neurophysiol. 70, 677–694 (1993).
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P. Lennie, J. Pokorny, V. C. Smith, “Luminance,” J. Opt. Soc. Am. A 10, 1283–1293 (1993).
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G. C. DeAngelis, I. Ohzawa, R. D. Freeman, “Spatiotemporal organization of simple-cell receptive fields in the cat’s striate cortex. II. Linearity of temporal and spatial summation,” J. Neurophysiol. 69, 1118–1135 (1993).
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1992 (8)

G. C. DeAngelis, J. G. Robson, I. Ohzawa, R. D. Freeman, “Organization of suppression in receptive fields of neurons in cat visual cortex,” J. Neurophysiol. 68, 144–163 (1992).
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D. J. Heeger, “Normalization of cell responses in cat striate cortex,” Visual Neurosci. 9, 181–197 (1992).
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J. J. Knierim, D. C. Van Essen, “Neuronal responses to static texture patterns in area V1 of the alert macaque monkey,” J. Neurophysiol. 67, 961–980 (1992).
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S. Hendry, R. K. Carder, “Organization and plasticity of GABA neurons and receptors in monkey visual cortex,” Prog. Brain Res. 90, 477–502 (1992).
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E. A. Lachica, V. A. Casagrande, “Direct W-like geniculate projections to the cytochrome oxidase (CO) blobs in primate visual cortex: axon morphology,” J. Comp. Neurol. 319, 141–158 (1992).
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J. R.H. Maunsell, J. R. Gibson, “Visual response latencies in striate cortex of the macaque monkey,” J. Neurophysiol. 68, 1332–1344 (1992).
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1991 (5)

R. C. Reid, R. E. Soodak, R. M. Shapley, “Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex,” J. Neurophysiol. 66, 505–529 (1991).
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B. C. Skottun, R. S. De Valois, D. H. Grosof, J. A. Movshon, D. G. Albrecht, A. B. Bonds, “Classifying simple and complex cells on the basis of response modulation,” Vision Res. 31, 1079–1086 (1991).
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1990 (5)

G. Sclar, J. H.R. Maunsell, P. Lennie, “Coding of image contrast in central visual pathways of the macaque monkey,” Vision Res. 30, 1–10 (1990).
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D. J. Tolhurst, A. F. Dean, “The effects of contrast on the linearity of spatial summation of simple cells in the cat’s striate cortex,” Exp. Brain Res. 79, 582–588 (1990).
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P. Lennie, J. Krauskopf, G. Sclar, “Chromatic mechanisms in striate cortex of macaque,” J. Neurosci. 10, 649–669 (1990).
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H. R. Rodman, C. G. Gross, T. D. Albright, “Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal,” J. Neurosci. 10, 1154–1164 (1990).
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1989 (5)

H. R. Rodman, C. G. Gross, T. D. Albright, “Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal,” J. Neurosci. 9, 2033–2050 (1989).
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G. Sclar, P. Lennie, D. D. DePriest, “Contrast adaptation in striate cortex of macaque,” Vision Res. 29, 747–755 (1989).
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M. S. Silverman, D. H. Grosof, R. L. De Valois, S. D. Elfar, “Spatial-frequency organization in primate striate cortex,” Proc. Natl. Acad. Sci. U.S.A. 86, 711–715 (1989).
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A. B. Bonds, “Role of inhibition in the specification of orientation-selectivity of cells in the cat striate cortex,” Visual Neurosci. 2, 41–55 (1989).
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1988 (10)

D. Ferster, “Spatially opponent excitation and inhibition in simple cells of the cat visual cortex,” J. Neurosci. 8, 1172–1180 (1988).
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1987 (6)

D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis ,” J. Physiol. (London) 390, 145–160 (1987).

R. E. Soodak, “The retinal ganglion cell mosaic defines orientation columns in striate cortex,” Proc. Natl. Acad. Sci. U.S.A. 84, 3936–3940 (1987).
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1986 (1)

J. Krauskopf, D. R. Williams, M. B. Mandler, A. M. Brown, “Higher order color mechanisms,” Vision Res. 26, 23–32 (1986).
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1985 (11)

R. G. Vautin, B. M. Dow, “Color cell groups in foveal striate cortex of the behaving macaque,” J. Neurophysiol. 54, 273–292 (1985).
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I. Ohzawa, G. Sclar, R. D. Freeman, “Contrast gain control in the cat’s visual system,” J. Neurophysiol. 54, 651–667 (1985).
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E. H. Adelson, J. R. Bergen, “Spatiotemporal energy models for the perception of motion,” J. Opt. Soc. Am. A 2, 284–299 (1985).
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H. Spitzer, S. Hochstein, “A complex-cell receptive field model,” J. Neurophysiol. 53, 1266–1286 (1985).
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1984 (10)

L. G. Thorell, R. L. De Valois, D. G. Albrecht, “Spatial mapping of monkey V1 cells with pure color and luminance stimuli,” Vision Res. 24, 751–769 (1984).
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M. S. Livingstone, D. H. Hubel, “Anatomy and physiology of a color system in the primate visual cortex,” J. Neurosci. 4, 309–356 (1984).
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G. G. Blasdel, D. Fitzpatrick, “Physiological organization of layer 4 in macque striate cortex,” J. Neurosci. 4, 880–895 (1984).
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A. M. Derrington, P. Lennie, “Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque,” J. Physiol. (London) 357, 219–240 (1984).

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1983 (4)

G. Buchsbaum, A. Gottschalk, “Trichromacy, opponent colours coding and optimum colour information transmission in the retina,” Proc. R. Soc. London, Ser. B 220, 89–113 (1983).
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J. Bullier, H. Kennedy, “Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey,” Exp. Brain Res. 53, 168–172 (1983).
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K. K. De Valois, R. B.H. Tootell, “Spatial-frequency-specific inhibition in cat striate cortex cells,” J. Physiol. (London) 336, 359–376 (1983).

1982 (8)

D. G. Albrecht, D. B. Hamilton, “Striate cortex of monkey and cat: contrast response function,” J. Neurophysiol. 48, 217–237 (1982).
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J. O’Kusky, M. Colonnier, “A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys,” J. Comp. Neurol. 210, 278–290 (1982).
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1981 (5)

F. M. de Monasterio, S. J. Schein, E. P. McCrane, “Staining of blue-sensitive cones of the macaque retina by a fluorescent dye,” Science 213, 1278–1281 (1981).
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W. Fries, “The projection from the lateral geniculate nucleus to the prestriate cortex of the macaque monkey,” Proc. R. Soc. London, Ser. B 213, 73–86 (1981).
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1980 (2)

N. Y. Kiang, “Processing of speech by the auditory nervous system,” J. Acoust. Soc. Am. 68, 830–835 (1980).
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1979 (5)

J. A. Movshon, P. Lennie, “Pattern-selective adaptation in visual cortical neurones,” Nature 278, 850–852 (1979).
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R. Shapley, J. D. Victor, “The contrast gain control of the cat retina,” Vision Res. 19, 431–434 (1979).
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K. S. Rockland, D. N. Pandya, “Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey,” Brain Res. 179, 3–20 (1979).
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1978 (5)

J. K. Bowmaker, H. J.A. Dartnall, J. N. Lythgoe, J. D. Mollon, “The visual pigments of rods and cones in the rhesus monkey, Macaca mulatta ,” J. Physiol. (London) 274, 329–348 (1978).

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1977 (5)

P. H. Schiller, J. G. Malpeli, “The effect of striate cortex cooling on area 18 cells in the monkey,” Brain Res. 126, 366–369 (1977).
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1976 (2)

S. Hochstein, R. M. Shapley, “Quantitative analysis of retinal ganglion cell classification,” J. Physiol. (London) 262, 237–264 (1976).

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1975 (2)

V. Smith, J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm,” Vision Res. 15, 161–171 (1975).
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1974 (2)

O. D. Creutzfeldt, U. Kuhnt, L. A. Benevento, “An intracellular analysis of visual cortical neurones to moving stimuli: response in a co-operative neuronal network,” Exp. Brain Res. 21, 251–274 (1974).
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1973 (1)

L. Maffei, A. Fiorentini, S. Bisti, “Neural correlate of perceptual adaptation to gratings,” Science 182, 1036–1038 (1973).
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1972 (3)

D. H. Hubel, T. N. Wiesel, “Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey,” J. Comp. Neurol. 146, 421–450 (1972).
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1970 (1)

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Figures (4)

Fig. 1
Fig. 1

Hypothetical receptive fields of P cells, illustrating the potential consequences of drawing indiscriminately or selectively on inputs from different classes of cones. (a) Receptive fields near the fovea, where the center input arises predominantly from a single cone. Without selection of cone inputs to the surround (left) the spatial frequency selectivity of the neuron will be band pass when measured with achromatic stimuli or stimuli that isolate the center cone type (in this case L) but low pass when measured with stimuli that isolate the other type (M). With selection of cone inputs to the surround (right), spatial frequency tuning will be low pass when measured with a cone-isolating grating of either type. (b) Receptive field in near periphery (ca. 10°), where the center receives input from a small number of cones. With or without selection of cone type (left), orientation selectivity measured with a grating of preferred spatial frequency will vary with the cone type that is isolated. With selection of cone type in the center (right), orientation selectivity will be independent of grating chromaticity. (Courtesy of S. Solomon.)

Fig. 2
Fig. 2

How the random arrangement of L and M cones in the retinal mosaic can give rise to color opponency in cortical receptive fields. (a) The mosaic of identified cones in foveal retina of the macaque (from Ref. [63]). (b) The spatial distribution of sensitivity within a notional simple cell receptive field tuned to 4 c . deg 1 . (c) A cartoon of the two principal subregions of the receptive field superimposed as a window on the mosaic. Clustering of L and M cones results in the different subregions of the receptive fields (assuming they draw on all available cones) receiving L- and M-cone inputs in different proportions.

Fig. 3
Fig. 3

How space and spatial frequency are jointly represented by cortical receptive fields. (a) Two-dimensional spatial frequency space, namely, the Fourier plane. Each point represents a grating of a particular orientation and spatial frequency, as indicated by the grating images placed on the appropriate locations of the space to the left and above the origin; the blob at the origin is a “grating” of zero spatial frequency. A tuning curve in orientation and spatial frequency forms a more or less compact zone in this space, as indicated by the contour map below and to the right of the origin. The Fourier transform of this tuning curve, as indicated by the arrows, gives (b) the receptive field profile of the matched linear neuron (shown in perspective and contour-map views), which is clearly similar to that of many simple cortical receptive fields. (c) The two-dimensional tuning curves of a population of cortical cells in macaque V1 are plotted in the Fourier plane. They are dispersed in orientation and spatial frequency to tile the space (from De Valois et al.[118]). Each tuning curve corresponds to an underlying spatial filter that can be computed by the arithmetic cartooned in (a) and (b).

Fig. 4
Fig. 4

Motion is orientation in space–time and is detected by receptive fields that are oriented in space–time. (a) A schematic diagram of a vertical bar in rightward motion (left), the volume it traces out in space–time (middle), and a view from “above” of the x t plane within which one can imagine a tilted receptive field that would be selective for direction of motion (right, from Adelson and Bergen[139]). (b) A three-dimensional space–time map of the receptive field of a simple cell from cat V1, derived with a reverse-correlation technique. At the top are four spatial receptive field maps computed by correlating each spike with a preceding random stimulus at four different indicated delays. The evolution of the receptive field with time is visualized by collapsing the resulting three-dimensional volume onto the x t plane indicated in perspective at the bottom right and brought upright at the bottom left. The receptive field is oriented in space–time, and the orientation predicts the neuron’s direction preference (courtesy of G. C. DeAngelis after Ref. [277]).

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