Peaked Encoding of Relative Luminance in Macaque Areas V1 and V2

Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri Submitted 4 October 2004; accepted in final form 31 October 2004 It is widely presumed that throughout the primate visual pathway neurons encode the relative luminance of objects (at a given light adaptation level) using two classes of monotonic function, one positively and the other negatively sloped. Based on computational considerations, we hypothesized that early visual cortex also contains neurons preferring intermediate relative luminance values. We tested this hypothesis by recording from single neurons in areas V1 and V2 of alert, fixating macaque monkeys during presentation of a large, spatially uniform patch oscillating slowly in luminance and surrounded by a static texture background. A substantial subset of neurons responsive to such low spatial frequency luminance stimuli in both areas exhibited prominent and statistically reliable response peaks to intermediate rather than minimal or maximal luminance values. When presented with static patches of different luminance but of the same spatial configuration, most neurons tested retained a preference for intermediate relative luminance. Control experiments using luminance modulation at multiple low temporal frequencies or reduced amplitude indicate that in the slow luminance-oscillating paradigm, responses were more strongly modulated by the luminance level than the rate of luminance change. These results strongly support our hypothesis and reveal a striking cortical transformation of luminance-related information that may contribute to the perception of surface brightness and lightness. In addition, we tested many luminance-sensitive neurons with large chromatic patches oscillating slowly in luminance. Many cells, including the gray-preferring neurons, exhibited strong color preferences, suggesting a role of luminance-sensitive cells in encoding information in three-dimensional color space. Address for reprint requests and other correspondence: D. C. Van Essen, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO 63110 (E-mail: vanessen{at}brainvis.wustl.edu )