A Contrast and Surface Code Explains Complex Responses to Black and White Stimuli in V1

Abstract

We investigated the cortical mechanisms underlying the visual perception of luminance-defined surfaces and the preference for black over white stimuli in the macaque primary visual cortex, V1. We measured V1 population responses with voltage-sensitive dye imaging in fixating monkeys that were presented with white or black squares of equal contrast around a mid-gray. Regions corresponding to the squares' edges exhibited higher activity than those corresponding to the center. Responses to black were higher than to white, surprisingly to a much greater extent in the representation of the square's center. Additionally, the square-evoked activation patterns exhibited spatial modulations along the edges and corners. A model comprised of neural mechanisms that compute local contrast, local luminance temporal modulations in the black and white directions, and cortical center-surround interactions, could explain the observed population activity patterns in detail. The model captured the weaker contribution of V1 neurons that respond to positive (white) and negative (black) luminance surfaces, and the stronger contribution of V1 neurons that respond to edge contrast. Also, the model demonstrated how the response preference for black could be explained in terms of stronger surface-related activation to negative luminance modulation. The spatial modulations along the edges were accounted for by surround suppression. Overall the results reveal the relative strength of edge contrast and surface signals in the V1 response to visual objects.

Representation of Color Surfaces in V1: Edge Enhancement and Unfilled Holes

“…Indeed, we found that early VSD responses to achromatic squares of different sizes (1°-3°) are strongest at the squares' edges (Zurawel et al, 2014). We also found that these edge-dominant responses are evident early after stimulus onset for chromatic squares, that is, square objects defined only by color difference with the background.…”

“…1,2,4,7A,8), all conditions shared equal contrast and this practice was not necessary. The latency of response onset was calculated by fitting a linear regression line to the rising phase of activation and calculating its intersection with the baseline (Zurawel et al, 2014). Similar results were obtained when we computed the latency using a different approach: finding the point where the signal crossed 2 SDs of the baseline activity.…”

“…Shortly after stimulus onset (ϳ60 ms) the maps had rectangle-like patterns in the V1 imaged area, as expected from the known retinotopic organization of V1. The early evoked response was activated mainly along the contour (edges) of the square while at the center of activation there was a hole resulting from a weaker VSD response (recently reported for 2°achromatic squares; Zurawel et al, 2014). The overall VSD response that was averaged over the entire activation patch (Fig.…”

“…The higher corner responses were also evident for achromatic squares (Wilcoxon signed rank test, p Ͻ 10 Ϫ3 , n ϭ 18; p Ͻ 10 Ϫ8 , n ϭ 46; p Ͻ 10 Ϫ3 , n ϭ 13 for 1°, 2°, and 3°squares, respectively). The ratio between corner and mid-edge responses was similar for all chromatic and achromatic stimuli (mean ratio Ϯ1 SEM over edges: 1.35 Ϯ 0.04 for achromatic 2°squares and 1.36 Ϯ 0.05 for chromatic 2°squares; Zurawel et al, 2014).…”

“…Luminance-surface-coding in V1 is better understood. V1 responses to the edges of surfaces are higher than responses to the center (Friedman et al, 2003;Dai and Wang, 2012;Zurawel et al, 2014) resulting in a lower activation, a "hole," located at center-related cortical regions. Several studies reported neuronal filling-in of the center's response in illusory and real surfaces (De Weerd et al, 1995;Lamme et al, 1999;Hung et al, 2001;Huang and Paradiso, 2008).…”