Spatial Structure of Cone Inputs to Color Cells in Alert Macaque Primary Visual Cortex (V-1)

Abstract

The spatial structure of color cell receptive fields is controversial. Here, spots of light that selectively modulate one class of cones (L, M, or S, or loosely red, green, or blue) were flashed in and around the receptive fields of V-1 color cells to map the spatial structure of the cone inputs. The maps generated using these cone-isolating stimuli and an eye-position-corrected reverse correlation technique produced four findings. First, the receptive fields were Double-Opponent, an organization of spatial and chromatic opponency critical for color constancy and color contrast. Optimally stimulating both center and surround subregions with adjacent red and green spots excited the cells more than stimulating a single subregion. Second, red-green cells responded in a luminance-invariant way. For example, red-on-center cells were excited equally by a stimulus that increased L-cone activity (appearing bright red) and by a stimulus that decreased M-cone activity (appearing dark red). This implies that the opponency between L and M is balanced and argues that these cells are encoding a single chromatic axis. Third, most color cells responded to stimuli of all orientations and had circularly symmetric receptive fields. Some cells, however, showed a coarse orientation preference. This was reflected in the receptive fields as oriented Double-Opponent subregions. Fourth, red-green cells often responded to S-cone stimuli. Responses to M-and S-cone stimuli usually aligned, suggesting that these cells might be red-cyan. In summary, red-green (or red-cyan) cells, along with blue-yellow and black-white cells, establish three chromatic axes that are sufficient to describe all of color space. Three classes of cones with peak absorptions in the long (560 nm), medium (530 nm), and short (450 nm) wavelengths of light mediate the discrimination of color; they are referred to as L-, M-, and S-cones. The cones are sometimes referred to as red, green, and blue, but each cone class does not code the perception of a single color. Instead, color is mediated by an opponent process (Hering, 1964). This is reflected in the receptive fields of two classes of cells in the lateral geniculate nucleus (LGN), Type I and Type II cells (Fig. 1 A, B) (Wiesel and Hubel, 1966). Type II cells are thought to represent the retinal and geniculate origin of the perceptual blue-yellow axis. These cells have spatially simple receptive fields consisting of one region, and stimulation with different wavelengths within this region causes the cell to respond in different ways: blue-on Type II cells would be excited by blue light and suppressed by yellow light (Fig. 1 B) (Wiesel and Hubel, 1966;Dacey and Lee, 1994). Because the evidence for red-green Type II cells is paltry (Wiesel and Hubel, 1966;De Monasterio and Gouras, 1975;Dreher et al., 1976;De Monasterio, 1978) (for review, see Rodieck, 1991), Type I cells have been invoked as the origin for the red-green axis. Type I cells are chromatically opponent (Fig. 1 A), although their receptive field centers are m...

Spatial Dependence of Color Assimilation by the Watercolor Effect

“…This result is consistent with an S-cone antagonistic center-surround (+S/−S) receptive field (Monnier and Shevell 2004). Such neurons are not found in the retina (Dacey 2000), but have been reported in the visual cortex (Conway 2001;Solomon et al 2004). The transition from assimilation to contrast suggested by Hurvich (1975, 1989) might be related to S-cone spatial antagonism.…”

Blue-Yellow Signals Are Enhanced by Spatiotemporal Luminance Contrast in Macaque V1

“…These contrasts are comparable to those used in previous studies (Conway 2001;Johnson et al 2001Johnson et al , 2004. Unlike stimuli used in these previous studies, however, our stimulus largely modulated the three cone types together.…”

“…Thus cone contrasts in cone isolating directions (e.g., L cone direction conditional on M and S cone activations constrained to be at their mean levels) were smaller: (L: 0.03, M: 0.03, S: 0.22). These L and M cone contrasts are 3-10 times smaller than those used by Johnson et al (2001Johnson et al ( , 2004 and Conway (2001), but the S-cone contrast is comparable.…”

“…This assumption has been made, either implicitly or explicitly, in studies that employ cone-isolating stimuli to estimate the weights with which cone inputs are integrated (Conway 2001;Johnson et al 2001;Landisman and Ts'o 2002). While the linearity assumption is justified for many V1 neurons, it is clearly inappropriate for others (Conway 2001;Hanazawa et al 2000;Hubel and Wiesel 1968;Lennie et al 1990;Vautin and Dow 1985). For example, a V1 neuron that responds to S cone stimulation, but only when L-and M-cone excitations are appropriately balanced, does not integrate cone inputs linearly and thus cannot be characterized with coneisolating stimuli (Hanazawa et al 2000).…”

Color-tuned neurons are spatially clustered according to color preference within alert macaque posterior inferior temporal cortex

“…Some specialized cells in the retina, lateral geniculate nucleus, and V1 show coneopponent responses of the sort that would be expected to be necessary to bring about color perception. But these cells are restricted to encoding only a limited range of colors that does not reflect the dimensions of perceptual color space (21)(22)(23)(24). Colorselective neurons also are found in subcompartments of V2 known as the thin stripes (25), which receive color signals from V1.…”