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

Abstract

The neuronal mechanism underlying the representation of color surfaces in primary visual cortex (V1) is not well understood. We tested on color surfaces the previously proposed hypothesis that visual perception of uniform surfaces is mediated by an isomorphic, filled-in representation in V1. We used voltage-sensitive-dye imaging in fixating macaque monkeys to measure V1 population responses to spatially uniform chromatic (red, green, or blue) and achromatic (black or white) squares of different sizes (0.5°-8°) presented for 300 ms. Responses to both color and luminance squares early after stimulus onset were similarly edge-enhanced: for squares 1°and larger, regions corresponding to edges were activated much more than those corresponding to the center. At later times after stimulus onset, responses to achromatic squares' centers increased, partially "filling-in" the V1 representation of the center. The rising phase of the center response was slower for larger squares. Surprisingly, the responses to color squares behaved differently. For color squares of all sizes, responses remained edge-enhanced throughout the stimulus. There was no filling-in of the center. Our results imply that uniform filled-in representations of surfaces in V1 are not required for the perception of uniform surfaces and that chromatic and achromatic squares are represented differently in V1.Key words: color; monkeys; population coding; primary visual cortex; surfaces; VSDI Introduction "… space and color are not distinct elements but, rather, are interdependent aspects of a unitary process of perceptual organization." (Kanizsa, 1979).The above quotation from Kanizsa's (1979) book guides our work on the neural basis of color perception. The brain needs to construct a color signal to recover the reflective properties of surfaces. Therefore, the neural mechanisms of color perception must make comparisons of the color signals from different locations in the visual image; they must take into account the spatial layout of the scene (Delahunt and Brainard, 2004; Shevell and Kingdom, 2008). It is not known yet in detail how the brain integrates form and color but many scientists who investigated the problem concluded that the primary visual cortex (V1) plays an important role (Johnson et al., 2001(Johnson et al., , 2008 Friedman et al., 2003;Wachtler et al., 2003; Hurlbert and Wolf, 2004).Many investigators have reported the existence of colorresponsive neurons in V1 of macaque monkeys (Thorell et al., 1984; Victor et al., 1994; Leventhal et al., 1995;Johnson et al., 2001; Friedman et al., 2003). Most of the color-sensitive neurons in V1 are double-opponent cells; they are orientation-tuned and respond best to intermediate spatial frequency gratings or to sharp edges in the visual image (ϳ30 -40% of V1 cells). Doubleopponent cells were shown to be sensitive to achromatic luminance patterns as well as to color patterns. Single-opponent cells Received March 29, 2015; revised July 18, 2015; accepted July 22, 2015. Author contributions: S.Z., R.S....

Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations

“…For achromatic surfaces, V1 response characteristics were indicative of a fill-in process, in which surface information emanates from the surface's edge. This was not the case for chromatic surfaces (Zweig et al, 2015), which suggests that the V1 representation of surface color may largely depend on single-opponent LGN inputs to V1 and responses of V1 neurons with RFs within the uniform surface (Livingstone et al, 1984;Shapley and Hawken, 2011;Zweig et al, 2015). In the present study, we observed that chromatic surfaces exhibited much stronger gamma-band synchronization yet more suppressed firing than achromatic surfaces.…”

“…Surround modulation is mediated by lateral and feedback connections, through which a given V1 neuron can be informed about a larger region of space than covered by its classical receptive field (Angelucci et al, 2017;Gilbert, 1992;Lund et al, 2003). Numerous related functions and computations have been linked to surround modulation, such as normalization (Carandini and Heeger, 2011), contour integration (Liang et al, 2017), perceptual filling-in (Land, 1959;Wachtler et al, 2003;Zweig et al, 2015), figureground separation (Lamme, 1995), computation of a saliency map (Coen-Cagli et al, 2012;Li, 2002), as well as efficient and predictive coding operations (Rao and Ballard, 1999;Vinje and Gallant, 2000). Theories of efficient coding postulate that surround suppression of neuronal firing may contribute to remove image redundancies across space from neuronal representations (Barlow, 2001;Coen-Cagli et al, 2012, 2015Rao and Ballard, 1999;Schwartz and Simoncelli, 2001;Simoncelli and Olshausen, 2001;Vinje and Gallant, 2000;Zhu and Rozell, * These authors contributed equally * * These authors contributed equally 2013).…”

“…Edge-derived representations likely rely on an inductive "fill-in" process, in which neurons with RFs at the surface's edge signal the difference between the color and luminance of the surface and the background. This may then change the firing of neurons with RFs at the surface's center (Land, 1959;Wachtler et al, 2003;Zweig et al, 2015). The relative contributions of local (center) versus edge-derived representations remain largely unknown and likely differ between chromatic and achromatic surfaces (Zurawel et al, 2014;Zweig et al, 2015).…”

“…This may then change the firing of neurons with RFs at the surface's center (Land, 1959;Wachtler et al, 2003;Zweig et al, 2015). The relative contributions of local (center) versus edge-derived representations remain largely unknown and likely differ between chromatic and achromatic surfaces (Zurawel et al, 2014;Zweig et al, 2015). Voltage-sensitive dye recordings of V1 populations, comparing the responses at the surface's center to the edge, have shown that representations of achromatic surfaces depend more strongly on a "fill-in" process than chromatic surfaces (Zweig et al, 2015).…”

“…The relative contributions of local (center) versus edge-derived representations remain largely unknown and likely differ between chromatic and achromatic surfaces (Zurawel et al, 2014;Zweig et al, 2015). Voltage-sensitive dye recordings of V1 populations, comparing the responses at the surface's center to the edge, have shown that representations of achromatic surfaces depend more strongly on a "fill-in" process than chromatic surfaces (Zweig et al, 2015). Because contextual interactions likely have a different nature for achromatic than chromatic stimuli, we asked whether there are differences in the contextual modulation of firing activity and gamma-band synchronization between these two classes of stimuli.…”