Equiluminance cells in visual cortical area v4

Abstract

We report a novel class of V4 neuron in the macaque monkey that responds selectively to equiluminant colored form. These "equiluminance" cells stand apart because they violate the well established trend throughout the visual system that responses are minimal at low luminance contrast and grow and saturate as contrast increases. Equiluminance cells, which compose ∼22% of V4, exhibit the opposite behavior: responses are greatest near zero contrast and decrease as contrast increases. While equiluminance cells respond preferentially to equiluminant colored stimuli, strong hue tuning is not their distinguishing feature-some equiluminance cells do exhibit strong unimodal hue tuning, but many show little or no tuning for hue. We find that equiluminance cells are color and shape selective to a degree comparable with other classes of V4 cells with more conventional contrast response functions. Those more conventional cells respond equally well to achromatic luminance and equiluminant color stimuli, analogous to color luminance cells described in V1. The existence of equiluminance cells, which have not been reported in V1 or V2, suggests that chromatically defined boundaries and shapes are given special status in V4 and raises the possibility that form at equiluminance and form at higher contrasts are processed in separate channels in V4.

Figure 1.

Color and shape stimuli. A, The 25 chromaticities used in the study are shown in the CIE chromaticity diagram. The colors occupied three triangles at increasing distances from the achromatic point (no. 1) and represented three levels of color contrast: colors 2–7 composed the low color contrast band; 8–13, the mid color contrast band; and 14–25, the high color contrast band. Each of the 25 chromaticities was presented at four different luminance contrasts relative to the achromatic background labeled 1. B, Shape stimuli used to characterize the shape preferences of neurons. A subset (10–29) of these shapes was presented in eight orientations at 45° intervals to study shape selectivity. Some shapes that show rotational symmetry were presented at fewer rotations. For example, shapes labeled 1 and 2 were presented at two and four rotations, respectively. Shape labeled 1 was used to characterize color and luminance preferences of example neurons whose data are shown in Figure 2, A, B, and D; shape labeled 2 was used to characterize the example neuron whose data are shown in Figure 2C.

Figure 2.

Single neuronal examples of four types of luminance contrast selectivity in V4. A–D, Raster plots show single trial responses for six repeats of 25 colors grouped by luminance contrast (rows). Rasters are ordered by color numbering in Figure 1A. Thus, within each raster plot, rows 1–6 from the bottom depict responses to color 1 in the CIE diagram, 7–12 represent responses to color 2, etc. The x-axis (for rasters and PSTHs) represents time relative to stimulus onset. Stimuli were presented for 300 ms. PSTHs were Gaussian-smoothed with σ = 5 ms; line color represents luminance contrast. The inset in A shows enlarged version of the 40 ms epoch starting 30 ms after stimulus onset to facilitate response latency comparison across luminance contrasts. Contrast response functions (bottom panel) show mean responses, normalized across colors (see Materials and Methods), versus luminance contrast. Error bars indicate SEM. Example neurons responded strongest to positive luminance contrast (bright cell) (A); negative luminance contrast (dark cell) (B); high contrast, either positive or negative (contrast cell) (C); and stimuli that were nominally equiluminant with the background (equiluminance cell) (D).

Figure 3.

Color preferences and consistency of luminance contrast preference across chromaticities. Mean responses of the example neurons in Figure 2 were linearly interpolated to construct the response surfaces shown here as a function of chromaticity and luminance contrast. Each column depicts an example neuron, and each row represents one of the tested luminance contrasts. For each panel, the CIE x- and CIE y-coordinates are plotted along the x- and y-axes, and the color scale denotes the strength of the mean response evoked by each stimulus. Mean responses were calculated from stimulus onset to stimulus offset across six presentations. Color scale runs from pale blue (weak responses), through black (intermediate responses), to bright red (strong responses). A, Bright cell. Preference for positive luminance contrasts is clearly evident, but color preference is not: most chromaticities at C_lum = 125% (bottom row) evoked strong responses (red) from this neuron. B, Dark cell. This neuron exhibited moderate color tuning with preferred responses clustered close to the red region of the CIE diagram at C_lum = −50%. Preference for negative luminance contrasts is consistent across chromaticities. C, Contrast cell. There is some clustering of preferred responses (red points) close to the achromatic point; responses at C_lum = 0 were consistently weak at all chromaticities. D, Equiluminance cell. Moderate clustering of preferred responses along the green-magenta axis at C_lum = 0; responses near the achromatic point, which represents the background color, were weak; this results in an annulus clustering of preferred responses. Responses of all chromaticities, except the background color, were strongest at C_lum = 0.

Figure 4.

Classification of cells based on contrast response functions. Cells were classified into one of six categories (bright, dark, contrast, equiluminance, flat, and peak) based on two correlation values: r_bright (x-axis of scatterplot), which measures the coefficient of correlation between C_lum and neuronal responses to the different chromaticities for C_lum ≥ 0, and r_dark (y-axis of scatterplot), which measures the correlation between C_lum and neuronal responses for C_lum ≤ 0. Only those chromaticities that evoked responses significantly greater than baseline at one or more luminance contrasts were included in the r_bright and r_dark calculations (see Materials and Methods). Mean contrast response functions grouped according to the properties of r_bright and r_dark (listed in the corresponding breakouts; for details, see Results) for bright, dark, contrast, and equiluminance cells are shown in the top right, bottom left, bottom right, and top left respectively. ∼ denotes not significantly different from 0. Number of cells in each breakout panel is indicated by n.

Figure 5.

Slopes of the contrast response functions and example cell studied at three background luminances. A, Each dot represents a cell. S_bright (x-axis of scatterplot) represents the slope given by a linear regression fit between C_lum and neuronal responses to the different chromaticities for C_lum ≥ 0, and S_dark (y-axis of scatterplot) represents the slope between C_lum and neuronal responses for C_lum ≤ 0. The dot colors and analysis details are as in Figure 4. Because the positive contrast range for C_lum was 0–125% and the negative contrast range was 0 to −50% and responses were normalized to lie between 0 and 1, the maximum slope limit along the x- and y-axes are 0.008 (1/125) and 0.02 (1/50) respectively. Across our population, slopes span this entire range. B, Normalized responses (y-axis) plotted as a function of stimulus luminance (x-axis) for an example equiluminance cell studied at three different background luminances. At each background luminance (denoted by line style), individual chromatic contrast response functions were constructed as detailed in Materials and Methods; their mean (±SEM) is plotted here as a function of stimulus luminance rather than contrast. Responses peaked at the stimulus luminance that matched the background luminance, suggesting that luminance contrast, rather than absolute luminance, dictated the response.

Figure 6.

Time course of the population response for each cell class. Population PSTHs show the average normalized response (see Materials and Methods) relative to stimulus onset for bright, dark, contrast, equiluminance, and flat cells. Number of cells contributing to each histogram is indicated by n. Because few cells were categorized as peak cells (n = 5), the corresponding PSTHs are not shown. Stimulus duration was 300 ms except for a few cells (3–6 in each category; 500 ms). The line color represents stimulus contrast as per the legend. The response to near equiluminant stimuli (red line) was always the latest response, regardless of whether it was the strongest or weakest response on average. As in the examples in Figure 2, bright, contrast, and dark cells responded strongest to high-contrast stimuli, while equiluminance cells responded best to 0% contrast.

Figure 7.

Population PSTHs as a function of color contrast. Stimuli were divided into three groups based on color contrast: chromaticities 2–7 (low color contrast band), 8–13 (mid color contrast band), and 14–25 (high color contrast band). Population PSTHs for equiluminance cells based on these three groups of stimuli are shown for stimuli at 0% luminance contrast (shades of red) and 125% luminance contrast (shades of blue). The x- and y-axes are as in Figure 6. At 0% luminance contrast, peak amplitudes are similar for the three color contrasts, suggesting that responses of equiluminance cells to high color contrast are not also suppressed. Responses emerged earlier for higher color contrasts for stimuli at 0% luminance contrast but not for stimuli at 125% luminance contrast.

Figure 8.

Finer sampling of the contrast response function. A, Each panel shows the responses of an equiluminance cell to a preferred chromaticity (red line) and the achromatic stimulus (black line) presented at C_lum = 0, ±2.5, ±5, ±25, and ±50% luminance contrasts. Mean responses (across 20 repetitions) are plotted against luminance contrast (x-axis). Error bars represent SEM. In four representative single cells, chromatic responses tended to be high near 0% contrast and gradually declined for higher contrasts (25–50%). Responses to achromatic contrasts were typically bimodal with weakest responses at zero and high contrasts. Responses to the best achromatic contrast were weaker than to chromatic stimuli near equiluminance. B, Normalized population response across all 13 cells on which the finer sampling was conducted. The responses of each cell were normalized by the response to the chromatic stimulus at 0% luminance contrast. Thus, at C_lum = 0, y for the red line equals 1 by definition. Across the population, chromatic contrast response functions were quite narrow: responses decline to 50% of the peak at ±25% contrast. For this range of contrasts, responses to achromatic contrasts were much weaker. Note that the x-axes here range from −50 to +50, unlike in Figures 2 and 4, in which they range from −50 to +125.

Figure 9.

Color sensitivity indices of V4 neurons and the goodness of fit of linear cone excitation models with or without rectification. A, Color sensitivity index, SI, is the ratio of the maximum response among equiluminant stimuli, Re, to the maximum response among achromatic stimuli, Ra. Each point shows SI for one cell. Color represents the classification from Figure 4. The dotted lines identify the range of sensitivity indices (0.5 < SI < 2.0) that were classified as color luminance cells by Johnson et al. (2001). Sensitivity indices of the vast majority of V4 neurons, except most equiluminance cells, fell in this range. Most equiluminance cells, however, had sensitivity indices >2.0. For 14 cells (3 bright, 1 dark, 9 equiluminance, and 1 flat cell), Ra was zero; these cells are shown at the right extreme (note broken x-axis). B, Histogram of goodness of fit values for bright (top left), dark (top right), contrast (bottom left), and equiluminance (bottom right) cells. For each cell, we fit the neuronal responses with linear cone excitation models with or without rectification (see Materials and Methods). Goodness of fit (x-axis) is given by the percentage of variance explained by the best fitting model. Some bright, dark, and contrast cells were well described by a rectified linear model, but for most equiluminance cells, linear cone excitation-based models provided a poor fit of the data (see Results). Mean goodness of fit for bright, dark, contrast, and equiluminance cells were 35.7, 50.1, 32.0, and 17.9, respectively.

Figure 10.

Color preferences across the V4 population. A, Mean and SD across cells for the number of colors (of 25) that elicited significant responses different from baseline for at least one of the four luminance contrasts tested; cells are grouped into categories (per Fig. 4) labeled here by the first letter of the category name: bright (n = 49), dark (n = 27), contrast (n = 51), equiluminance (n = 44), flat (n = 21), and peak cells (n = 5). B, Number of colors that elicited more than half-maximum responses at the preferred contrast. C–H, Distribution of preferred colors that elicited the maximum response for neurons grouped by category. The x- and y-axes correspond to CIE xy coordinates. Grayscale indicates the number of cells that responded best to the corresponding color. In several cases, rectangles are white and not visible because no cell had a peak response at the corresponding color.

Figure 11.

Hue tuning of six example equiluminance cells. A–F, Color images show the normalized, linearly interpolated response surface based on responses to stimuli at 0% luminance contrast. Color scale runs from blue to black to red representing low to high responses in the CIE space. Corresponding line plots show raw responses as a function of color direction in the CIE chromaticity diagram. Color direction (x-axis) was measured relative to the achromatic point, 0° is to the right, and angles increase counterclockwise. The red, green, and blue arrows mark the corresponding color directions. The pale gray, dark gray, and black lines represent responses to stimuli of low, mid, and high color contrasts, respectively. Error bars show SEM. The horizontal dashed line indicates the baseline response. Examples A–C show unimodal tuning for hue at one or more saturations. Examples D and E also show statistically significant modulation of response as a function of color direction but lack unimodal hue tuning. Example F (same cell as in Fig. 3D) did not differ significantly from uniform tuning. See Results for details.

Figure 12.

Shape preferences across the V4 population. A, Mean and SD across cells for the fraction of shapes that evoked responses significantly different from baseline. B, Mean and SD for the fraction of shapes that evoked more than half-maximum responses. The x-axis shows first letter of cell class names, as in Figure 10A.