Abstract
Humans are more sensitive to black than to white targets (Blackwell, 1946; Bowen et al., 1989; Chubb et al., 2004; Chubb and Nam, 2000; Dannemiller and Stephens, 2001; Kontsevich and Tyler, 1999; Krauskopf, 1980; Short, 1966; Tyler and Chan, 1992; Whittle, 1986). Such a bias for negative contrast was also reported in physiological responses in the human primary visual cortex (V1) measured by VEP (Zemon et al., 1988) and by BOLD fMRI signal (Olman et al., 2008). Consistent with human neurophysiology results, we found strong black-dominant responses in layer 2/3 of the Macaque V1 for single neurons' spike activity (Yeh et al., 2009). However the neural mechanisms that cause the black-white asymmetry in perception and neurophysiology have not been investigated before now. In seeking the mechanism of this black-dominance, we recorded visually-driven responses of multi-unit activity (MUA) and the local field potential (LFP) in Macaque V1 to black and white squares at high contrast (∼0.2 deg) on a grey background and used track reconstruction to identify the laminar locations of our recording sites.
We found a clear laminar pattern of MUA preference for black stimuli: while black-dominant responses were observed in layer 2/3, the black-preference was only seen in layer 4Cb but not in layer 4Ca. Compared to strong and sustained black-dominant responses in layer 2/3, black-dominant responses were much more transient and weaker in layer 4Cb. The dynamic difference of black-dominant MUA and LFP between layer 2/3 and 4Cb implies that black-dominance in layer 2/3 was not generated by a feedforward-plus-threshold mechanism applied to layer 4Cb signals.
We conclude: 1) black-dominance originates in the parvocellular pathway for high contrast condition; 2) black-dominance is significantly amplified by a recurrent excitatory-inhibitory network in layer 2/3 producing the strong black-preference of layer 2/3 neurons and downstream visual perception.
NIH-EY001472, NSF-0745253, the Swartz Foundation and the Robert Leet and Clara Guthrie Patterson Trust Postdoctoral Fellowship.