“Black” Responses Dominate Macaque Primary Visual Cortex V1

Achromatic visual information is transferred from the retina to the brain through two parallel channels: ON-center cells carry "white" information and OFF-center cells "black" information (Nelson et al., 1978; Schiller, 1982; Schiller et al., 1986). Responses of ON and OFF retinal and thalamic neurons are approximately equal in magnitude (Krüger and Fischer, 1975; Kremers et al., 1993), but psychophysical studies have shown that humans detect light decrements (black) better and faster than increments (white) (Blackwell, 1946; Short, 1966; Krauskopf, 1980; Whittle, 1986; Bowen et al., 1989; Chan and Tyler, 1992; Kontsevich and Tyler, 1999; Chubb and Nam, 2000; Dannemiller and Stephens, 2001). From recordings of single-cell activity in the macaque monkey's primary visual cortex (V1), we found that black-dominant neurons substantially outnumbered white-dominant neurons in the corticocortical output layers 2/3, but the numbers of black- and white-dominant neurons were nearly equal in the thalamocortical input layer 4c. These results strongly suggest that the black-over-white preference is generated or greatly amplified in V1. The predominance of OFF neurons in layers 2/3 of V1, which provide visual input to higher cortical areas, may explain why human subjects detect black more easily than white. Furthermore, our results agree with human EEG and fMRI findings that V1 responses to decrements are stronger than to increments, though the OFF/ON imbalance we found in layers 2/3 of macaque V1 is much larger than in the whole V1 population in the human V1 experiments (Zemon et al., 1988, 1995; Olman et al., 2008).