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Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing

Nature Neuroscience volume 15, pages 913–919 (2012)Cite this article

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Abstract

Understanding color vision requires knowing how signals from the three classes of cone photoreceptor are combined in the cortex. We recorded from individual neurons in the primary visual cortex (V1) of awake monkeys while an automated, closed-loop system identified stimuli that differed in cone contrast but evoked the same response. We found that isoresponse surfaces for half the neurons were planar, which is consistent with linear processing. The remaining isoresponse surfaces were nonplanar. Some were cup-shaped, indicating sensitivity to only a narrow region of color space. Others were ellipsoidal, indicating sensitivity to all color directions. The major and minor axes of these nonplanar surfaces were often aligned to a set of three color directions that were previously identified in perceptual experiments. These results suggest that many V1 neurons combine cone signals nonlinearly and provide a new framework in which to decipher color processing in V1.

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Figure 1: Predicted color tuning under three models of cone signal combination.
Figure 2: Data from three example neurons (two projections for each).
Figure 3: Normalized cone weights derived from the orientations of planar fits to staircase terminations.
Figure 4: Isoresponse surface fits, grating responses and predictions of grating responses for the three example neurons.
Figure 5: Scatterplot of correlation coefficients between actual and predicted responses to colored gratings.
Figure 6: Distribution of principal axes of quadratic isoresponse surfaces.
Figure 7: F1/F0 modulation ratios separated by isoresponse surface shape.

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Acknowledgements

The authors would like to thank A. Pasupathy, M. Shadlen, E.J. Chichilnisky, F. Rieke and G. Field for comments on the manuscript, J.P. Weller for modeling the adaptive sampling procedure, J. Gold for supplying UDP communication software, and E. Grover and L. Tait for technical assistance. This work was supported by a US National Institutes of Health (National Institute of General Medical Sciences) Training Grant (C.A.H.), the Achievement Rewards for College Scientists Foundation (C.A.H.), the McKnight Foundation (G.D.H.), and US National Institutes of Health grants RR000166 and EY018849 (G.D.H.).

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Authors and Affiliations

  1. Department of Physiology and Biophysics, University of Washington, Washington National Primate Research Center, Seattle, Washington, USA

    Gregory D Horwitz

  2. Program in Neurobiology and Behavior, University of Washington, Seattle, Washington, USA

    Charles A Hass

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  1. Gregory D Horwitz
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  2. Charles A Hass
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G.D.H. designed the experiments and analyzed the data. G.D.H. and C.A.H. conducted the experiments and wrote the manuscript.

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Correspondence to Gregory D Horwitz.

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Horwitz, G., Hass, C. Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing. Nat Neurosci 15, 913–919 (2012). https://doi.org/10.1038/nn.3105

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