Selective adaptation to color contrast in human primary visual cortex

Abstract

How neural activity produces our experience of color is controversial, because key behavioral results remain at odds with existing physiological data. One important, unexplained property of perception is selective adaptation to color contrast. Prolonged viewing of colored patterns reduces the perceived intensity of similarly colored patterns but leaves other patterns relatively unaffected. We measured the neural basis of this effect using functional magnetic resonance imaging. Subjects viewed low-contrast test gratings that were either red-green (equal and opposite long- and middle-wavelength cone contrast, L-M) or light-dark (equal, same-sign, long- and middle-wavelength cone contrast, L+M). The two types of test gratings generated approximately equal amounts of neural activity in primary visual cortex (V1) before adaptation. After exposure to high-contrast L-M stimuli, the L-M test grating generated less activity in V1 than the L+M grating. Similarly, after adaptation to a high-contrast L+M grating, the L+M test grating generated less activity than the L-M test grating. Behavioral measures of adaptation using the same stimuli showed a similar pattern of results. Our data suggest that primary visual cortex contains large populations of color-selective neurons that can independently adjust their responsiveness after adaptation. The activity of these neural populations showed effects of adaptation that closely matched perceptual experience.

Fig. 1.

Experimental methods. A, Blocks of low-contrast L+M and L-M test stimuli alternated with either uniform mean field presentations (no-adaptation condition; top) or high-contrast adapting stimuli (adaptation conditions;bottom). Stimuli shown are schematic; see Materials and Methods for stimulus details. B, Visual areas were identified using standard techniques for mapping retinotopic organization. Area V1 is shown here on a pseudocoronal slice.C, Sample V1 time courses for portions of a no-adaptation (top) and adaptation (bottom) scan in a single subject. The low-contrast test stimuli generate peaks in the no-adaptation time course and troughs in the adaptation time course.

Fig. 2.

fMRI results from experiment 1. A, Grand average V1 responses for the three adaptation conditions are shown, with responses to L-M tests shown as broken linesand responses to L+M tests shown as solid lines. Selective adaptation is evident as lower responses to L-M tests than to L+M tests, under conditions of L-M adaptation. B, fMRI response amplitudes were estimated by fitting sinusoids to the V1 time courses. Error bars in all figures represent one SEM, computed across subjects. After L-M adaptation, responses to L-M tests were reliably weaker than L+M responses (t₍₃₎ = 2.78; p < 0.05).

Fig. 3.

Behavioral results. A, Thebars indicate the reduction in apparent contrast that was produced by 2 Hz adapting stimuli (experiment 1) for L-M and L+M test stimuli. Subjects adjusted the color and contrast of an unadapted stimulus to match a test stimulus viewed under conditions of adaptation. Adapting to L-M reduced the apparent contrast of L-M tests more than it reduced the contrast of L+M tests (t₍₃₎ = 22.2; p < 0.01). As in the fMRI results, adapting to L+M had a nonselective effect. B, When adapting stimuli drifted at 8 Hz (experiment 2), L-M adaptation again produced selective adaptation (t₍₃₎ =8.26; p < 0.01). Adapting to L+M now also had a selective effect, reducing the apparent contrast of L+M tests more than L-M tests (t₍₃₎ = 5.32; p < 0.01).

Fig. 4.

fMRI results from experiment 2. A, Grand average V1 responses for the three adaptation conditions are shown, with responses to L-M tests shown as broken lines, responses to L+M tests shown as solid lines, and responses to zero-contrast, mean field tests shown as dotted lines. Selective adaptation is evident as lower responses to L-M tests than to L+M tests under conditions of L-M adaptation and also as lower responses to L+M tests than to L-M tests under conditions of L+M adaptation. B, fMRI response amplitudes were estimated by fitting a model hemodynamic response convolved with the stimulus time course to the V1 responses. After L-M adaptation, responses to L-M tests were reliably weaker than L+M responses (t₍₃₎ = 2.98;p < 0.05). After L+M adaptation, responses to L+M tests were reliably weaker than L-M responses (t₍₃₎ = 27.1; p < 0.01).