Abstract
Perceptually, color is used to discriminate objects by hue and to identify color boundaries. The primate retina and the lateral geniculate nucleus (LGN) have cell populations sensitive to color modulation, but the role of the primary visual cortex (V1) in color signal processing is uncertain. We re-evaluated color processing in V1 by studying single-neuron responses to luminance and to equiluminant color patterns equated for cone contrast. Many neurons respond robustly to both equiluminant color and luminance modulation (color-luminance cells). Also, there are neurons that prefer luminance (luminance cells), and a few neurons that prefer color (color cells). Surprisingly, most color-luminance cells are spatial-frequency tuned, with approximately equal selectivity for chromatic and achromatic patterns. Therefore, V1 retains the color sensitivity provided by the LGN, and adds spatial selectivity for color boundaries.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Zeki, S. A Vision of the Brain (Blackwell Science, Oxford, 1993).
Wallach, H. Ueber visuell wahrgenommene Bewegungsrichtung. Psych. Forsch. 20, 325–380 (1935). Translated into English in Wüerger, S., Shapley, R. & Rubin, N. On the visually perceived direction of motion. Perception 25, 1317–1368 (1996).
Lennie, P. in Color Vision: From Genes to Perception (eds. Gegenfurtner, K. R. & Sharpe, L. T.) 235–247 (Cambridge Univ. Press, Cambridge, UK, 1999).
Livingstone, M. & Hubel, D. H. Anatomy and physiology of a color system in the primate visual cortex. J. Neurosci. 4, 309–356 (1984).
Thorell, L. G., De Valois, R. L. & Albrecht, D. G. Spatial mapping of monkey V1 cells with pure color and luminance stimuli. Vision Res. 24, 751–769 (1984).
Ts'o, D. Y. & Gilbert, C. D. The organization of chromatic and spatial interactions in the primate striate cortex. J. Neurosci. 8, 1712–1727 (1988).
Lennie, P., Krauskopf, J. & Sclar, G. Chromatic mechanisms in striate cortex of macaque. J. Neurosci. 10, 649–669 (1990).
Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215–243 (1968).
Dow, B. M. Functional classes of cells and their laminar distribution in monkey visual cortex. J. Neurophysiol. 37, 927–946 (1974).
Engel, S. A., Zhang, X. & Wandell, B. A. Color tuning in human visual cortex measured using functional magnetic resonance imaging. Nature 388, 68–71 (1997).
van der Horst, G. J. C. & Bouman, M. A. Spatiotemporal chromaticity discrimination. J. Opt. Soc. Am. 59, 1482–1488 (1969).
Mullen, K. T. The contrast sensitivity of human colour vision to red-green and blue-yellow chromatic gratings. J. Physiol. (Lond.) 359, 381–400 (1985).
De Valois, R. L. & De Valois, K. K. Spatial Vision (eds. Broadbent, D. E. et al.) 218 (Oxford Univ. Press, New York, 1988).
Kaplan, E., Shapley, R. M. & Purpura, K. Color and luminance contrast as tools for probing the primate retina. Neurosci. Res. Suppl. 8, S151–S165 (1988).
Bradley, A., Switkes, E. & De Valois, K. Orientation and spatial frequency selectivity of adaptation to color and luminance gratings. Vision Res. 28, 841–856 (1988).
Krauskopf, J. Effect of retinal image stabilization on the appearance of heterochromatic targets. J. Opt. Soc. Am. 53, 741–744 (1963).
Yarbus, A. L. Eye Movements and Vision (Plenum, New York, 1967).
Callaway, E. M. Local circuits in primary visual cortex of the macaque monkey. Annu. Rev. Neurosci. 21, 47–74 (1998).
Hawken, M. J., Parker, A. J. & Lund, J. S. Laminar organization and contrast sensitivity of direction-selective cells in the striate cortex of the Old World monkey. J. Neurosci. 8, 3541–3548 (1988).
Leventhal, A. G., Thompson, K. G., Liu, D., Zhou, Y. & Ault, S. J. 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).
Cole, G. R., Stromeyer, C. F. I. & Kronauer, R. E. Visual interactions with luminance and chromatic stimuli. J. Opt. Soc. Am. A 7, 128–140 (1990).
De Valois, K. K. & Switkes, E. Simultaneous masking interactions between chromatic and luminance gratings. J. Opt. Soc. Am. 73, 11–18 (1983).
Switkes, E., Bradley, A. & De Valois, K. K. Contrast dependence and mechanisms of masking interactions among chromatic and luminance gratings. J. Opt. Soc. Am. A 5, 1149–1162 (1988).
Shevell, S. K. & Wei, J. Chromatic induction: border contrast or adaptation to surrounding light. Vision Res. 38, 1561–1566 (1998).
Krauskopf, J., Williams, D. R., Mandler, M. B. & Brown, A. Higher order color mechanisms. Vision Res. 26, 23–32 (1986).
Jameson, D. & Hurvich, L. M. Perceived color and its dependence on focal, surrounding, and preceding stimulus variables. J. Opt. Soc. Am. 49, 890–898 (1959).
Reid, R. C. & Shapley, R. M. Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus. Nature 356, 716–718 (1992).
Michael, C. R. Color vision mechanisms in monkey striate cortex: dual-opponent cells with concentric receptive fields. J. Neurophysiol. 41, 572–588 (1978).
Gouras, P. Opponent-color cells in different layers of foveal striate cortex. J. Physiol. (Lond.) 238, 583–602 (1974).
Van Essen, D. C., Newsome, W. T., Maunsell, J. H. & Bixby, J. L. The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: asymmetries, areal boundaries, and patchy connections. J. Comp. Neurol. 244, 451–480 (1986).
DeYoe, E. A. & Van Essen, D. C. Concurrent processing streams in monkey visual cortex. Trends Neurosci. 11, 219–226 (1988).
Levitt, J. B., Lund, J. S. & Yoshioka, T. Anatomical substrates for early stages in cortical processing of visual information in the macaque monkey. Behav. Brain Res. 76, 5–19 (1996).
Boyd, J. D. & Casagrande, V. A. Relationships between cytochrome oxidase (CO) blobs in primate primary visual cortex (V1) and the distribution of neurons projecting to the middle temporal area (MT). J. Comp. Neurol. 409, 573–591 (1999).
Kiper, D. C., Fenstemaker, S. B. & Gegenfurtner, K. R. Chromatic properties of neurons in macaque area V2. Vis. Neurosci. 14, 1061–1072 (1997).
Gegenfurtner, K.R., Kiper, D. C. & Levitt, J. B. Functional properties of neurons in macaque area V3. J. Neurophysiol. 77, 1906–1923 (1997).
Sceniak, M.P., Ringach, D. L., Hawken, M. J. & Shapley, R. Contrast's effect on spatial summation by macaque V1 neurons. Nat. Neurosci. 2, 733–739 (1999).
Estevez, O. & Spekreijse, H. The “silent substitution” method in visual research. Vision Res. 22, 681–691 (1982).
Stockman, A. & Sharpe, L. T. Spectral sensitivities of the middle- and long-wavelength sensitive cones derived from measurements in observers of known genotype. Vision Res. 40, 1711–1737 (2000).
Skottun, B.C. et al. Classifying simple and complex cells on the basis of response modulation. Vision Res. 31, 1079–1086 (1991).
Shapley, R.M. & Hawken, M. J. in Color Vision: From Genes to Perception (eds. Gegenfurtner, K. R. & Sharpe, L. T.) 221–234 (Cambridge Univ. Press, Cambridge, 1999).
Mardia, K.V. Statistics of Directional Data (Academic, London, 1972).
Batschelet, E. Circular Statistics in Biology (Academic, London, 1981).
Levick, W.R. & Thibos, L. N. Analysis of orientation bias in cat retina. J. Physiol. (Lond.) 329, 243–261 (1982).
Lund, J.S., Hendrickson, A. E., Ogren, M. P. & Tobin, E. A. Anatomical organization of primate visual cortex area V1. J. Comp. Neurol. 202, 19–45 (1981).
Acknowledgements
We thank D. Ringach, M. Sceniak, I. Mareschal, J.A. Henrie and F. Mechler for helping with the physiology experiments. L. Smith helped in the histological reconstruction and during physiology experiments. We also thank R.C. Reid for comments on the manuscript. This work was supported by National Institutes of Health grant EY01472 and EY8300, National Institute of Mental Health predoctoral grant MH12430-01 and Core Grant for Vision Research P30-EY13079.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Johnson, E., Hawken, M. & Shapley, R. The spatial transformation of color in the primary visual cortex of the macaque monkey. Nat Neurosci 4, 409–416 (2001). https://doi.org/10.1038/86061
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/86061
This article is cited by
-
The neural origin for asymmetric coding of surface color in the primate visual cortex
Nature Communications (2024)
-
Perception of Color and Its Encoding in the Cortex in Primates
Neuroscience and Behavioral Physiology (2023)
-
Automatic, Early Color-Specific Neural Responses to Object Color Knowledge
Brain Topography (2023)
-
Monkey V1 epidural field potentials provide detailed information about stimulus location, size, shape, and color
Communications Biology (2021)
-
Chromatic micromaps in primary visual cortex
Nature Communications (2021)