Spatial and Temporal Properties of Cone Signals in Alert Macaque Primary Visual Cortex

Abstract

Neurons in the lateral geniculate nucleus cannot perform the spatial color calculations necessary for color contrast and color constancy. Under neutral-adapting conditions, we mapped the cone inputs (L, M, and S) to 83 cone-opponent cells representing the central visual field of the next stage of visual processing, primary visual cortex (V1), to determine how the color signals are spatially transformed. Cone-opponent cells, constituting ∼10% of V1 cells, formed two populations, red–green (L vs M; 66 of 83) and blue–yellow (S vs L+M; 17 of 83). Many cone-opponent cells (48 of 83) were double-opponent, with circular receptive-field centers and crescent-shaped surrounds (0.63° offset) that had opposite chromatic tuning to the centers and a time-to-peak 11 ms later than the centers. The remaining cone-opponent cells were either spatially opponent in only one cone system (20 of 83) or lacked spatial opponency (15 of 83). Cells lacking spatial opponency had smaller receptive fields (0.5–0.7°) than spatial-opponent cell centers (∼1°). We found that red–green cells received S-cone input, which aligned with M input, and, unlike blue–yellow cells, red–green cells gave push–pull responses: receptive-field centers of red-ON cells were excited by both L increments (bright red) and M decrements (dark red) and were suppressed by both L decrements (dark green) and M increments (bright green). Excitatory responses to decrements were slightly larger than to increments, which may account for the lower detection and discrimination thresholds of decrements shown psychophysically. By virtue of their specialized receptive fields, the neurons described here spatially transform the cone signals and represent the first stage in the visual system at which spatially opponent color calculations are made.