Shape encoding consistency across colors in primate V4

Abstract

Neurons in primate cortical area V4 are sensitive to the form and color of visual stimuli. To determine whether form selectivity remains consistent across colors, we studied the responses of single V4 neurons in awake monkeys to a set of two-dimensional shapes presented in two different colors. For each neuron, we chose two colors that were visually distinct and that evoked reliable and different responses. Across neurons, the correlation coefficient between responses in the two colors ranged from -0.03 to 0.93 (median 0.54). Neurons with highly consistent shape responses, i.e., high correlation coefficients, showed greater dispersion in their responses to the different shapes, i.e., greater shape selectivity, and also tended to have less eccentric receptive field locations; among shape-selective neurons, shape consistency ranged from 0.16 to 0.93 (median 0.63). Consistency of shape responses was independent of the physical difference between the stimulus colors used and the strength of neuronal color tuning. Finally, we found that our measurement of shape response consistency was strongly influenced by the number of stimulus repeats: consistency estimates based on fewer than 10 repeats were substantially underestimated. In conclusion, our results suggest that neurons that are likely to contribute to shape perception and discrimination exhibit shape responses that are largely consistent across colors, facilitating the use of simpler algorithms for decoding shape information from V4 neuronal populations.

Fig. 1.

Shape stimuli. A subset (7 to 17) of the 34 stimuli shown was used to characterize the shape preferences of neurons. These shapes were designed to explore a range of convex and concave contour features known to drive selective V4 responses (Bushnell et al. 2011a; Pasupathy and Connor 2001). All shapes were presented in 8 orientations at 45° intervals. Stimuli were sized such that all parts of all stimuli were entirely within the receptive field (RF) of the cell. Because shapes were centered at a radial distance of 0.25 × RF radius from the center of the RF (which was the axis of rotation), the different rotations sampled different positions within the RF. This positioning strategy, which seems arbitrary here, was dictated by the requirements of a previous study (Bushnell et al. 2011a) where it is described in detail; it does not impact the present results or conclusions.

Fig. 2.

Responses of an example V4 neuron with highly consistent shape responses across colors. A and B: responses to 14 shapes (rows) presented at 8 orientations (columns) in green (A) and magenta (B). The background gray level of each icon represents the average response, per scale bar, across N = 20 repeats to the superimposed shape. Qualitatively, this neuron did not show strong color preferences, but 2-way ANOVA revealed significant (P < 0.01) main effects for color, shape, and their interaction on the responses of the cell, which were marginally stronger to shapes in green (A). Shape preferences were consistent across colors: in both colors, responses were strong to several shapes with a concavity to the right or lower right of the shape. The RF of this neuron was centered at 8.2° from the fixation point. C: scatter plot of responses shown in A (X-axis) and B (Y-axis). Points lie below the line of slope = 1 (dashed line). The correlation coefficient between responses in the 2 colors (r_C) was 0.87.

Fig. 3.

Responses of 2 example V4 neurons showing moderately consistent shape responses across colors. A and B: responses of a neuron to 14 shapes (rows) presented at 8 orientations (columns) in blue (A) and red (B). All other details are as in Fig. 2. This neuron exhibited moderate color tuning; responses were stronger to shapes in blue (A) than in red (B). Shape preferences were largely consistent: in both colors, responses were strongest to shapes with a sharp convexity pointing up. The RF of this neuron was centered at 2.6° from the fixation point. C: scatter plot of responses shown in A (X-axis) and B (Y-axis). Responses (based on N = 20 repeats) were largely below the diagonal line, reflecting stronger responses to shapes in blue. Correlation coefficient between responses in the 2 colors was 0.58. D and E: responses of a neuron that underwent detailed color characterization. D: each panel shows the neuron's chromatic responses at one of the luminance contrasts tested (−50%, 0%, 50%, and 125%). The X- and Y-axes of each panel represent CIE x- and y-coordinates respectively. Surface color indicates average response strength across 6 repeats, per scale bar. Responses at −50% contrast were uniformly weak. At 0% and positive contrasts, neurons showed a moderate level of color selectivity, responding strongest to stimuli in blue and magenta. For the highest luminance contrast panel (125%), labels 1 and 2 identify the 2 chosen stimulus colors (green and blue, respectively); responses were moderate for green and strong for blue. E: scatter plot of responses (based on N = 16 repeats) to shapes presented in green and blue (1 and 2 in D) along the X- and Y-axes, respectively. This neuron responded preferentially to a few shapes, but the responses in the 2 colors were largely consistent, yielding a correlation coefficient of 0.58.

Fig. 4.

Population results. A: histogram of shape consistency (r_C) across 60 V4 neurons. Shape consistency was quantified by the correlation coefficient between shape responses in 2 different colors. Across the population, shape consistency values varied widely, ranging from −0.03 to 0.93 (median 0.54). B: scatter plot of shape dispersion (X-axis) vs. shape consistency (Y-axis). Shape dispersion was quantified as the ratio of the variance to the mean response across all shapes. For each cell, represented by a pair of dots connected by a line, the open and filled symbols represent shape dispersion based on shapes in the preferred and nonpreferred colors, respectively. There was a significant positive correlation (r = 0.54 for preferred color and r = 0.55 for nonpreferred color; P < 0.0001) between shape dispersion and Fisher-transformed shape consistency values. The vertical dashed line denotes shape dispersion = 1.5, the cutoff between poorly and strongly selective neurons. C: scatter plot of F-test statistic (X-axis) vs. shape consistency (Y-axis). The 1-way ANOVA F-test statistic measures across-shape variability vs. within-shape variability. Note broken X-axis. There was a strong and significant positive correlation between F value and Fisher-transformed shape consistency (r = 0.74 and 0.63 for preferred and nonpreferred colors, respectively; P < 0.01) D: histogram of shape consistency values for shape-selective and unselective cells classified on the basis of whether they exhibited significant shape selectivity as based on a 1-way ANOVA (P < 0.05). Cells with significant selectivity to shape presented in both colors were classified as shape selective. Shape-selective cells (44/60) had shape consistency values that ranged from 0.16 to 0.93 (median 0.63).

Fig. 5.

Effect of stimulus repeats on shape consistency and shape dispersion. A: scatter plot of minimum number of stimulus repetitions vs. shape consistency. For a cell, if minimum number of repeats (X-axis) is N, then mean shape responses would be based on N or N + 1 repeats, because data collection was terminated during the (N + 1)th repeat. Red crosses represent the mean shape consistency at the corresponding number of repeats. Overall, there was a trend of increasing shape consistency with increasing number of stimulus repeats, and shape consistency appears to plateau somewhat for N > 10. Fisher-transformed shape consistency and minimum number of repeats were positively correlated (r = 0.56, P < 0.0001). B: scatter plot of shape consistency values based on all stimulus repeats (r_C; X-axis) vs. 4 stimulus repeats (r_C4, Y-axis). We randomly chose 4 repeats without replacement and computed the mean responses and shape consistency based on those repeats. The whole procedure was repeated 100 times; the average consistency across these 100 repetitions is reported as r_C4. In all except 1 case, shape consistency based on 4 repeats was less than that based on more stimulus repeats. Cells for which data collection was terminated on the 5th run, i.e., minimum number of repeats = 4, are shown as open symbols. These values do not lie on the diagonal, because although the Y-axis was based on mean responses derived from 4 repeats, the X-axis measure was based on mean shape responses derived from 4 or 5 repeats. C: bar graph of the mean difference in shape consistency values based on all stimulus repeats (r_C) and 4 repeats (r_C4) as a function of minimum number of repeats. X-axis is the same as in A. Y-axis is the difference between X- and Y-axes in B with cells grouped on the basis of the number of repeats. The difference r_C − r_C4 increases with increasing stimulus repeats, implying that there was a systematic underestimate in shape consistency for small number of stimulus repeats. D: shape-response dispersion (X-axis) vs. shape consistency (Y-axis) for cells studied with >10 repeats (n = 22 cells). This plot is similar to Fig. 4B, except that it includes only those cells studied with >10 repeats. As before, there was a strong relationship between shape dispersion and shape consistency. E: shape-response dispersion (X-axis) vs. shape consistency based on 4 stimulus repeats. Y-axis is the same as in B. As with r_C4 computation described in B, shape dispersion for each cell was the average across 100 repetitions of a bootstrap procedure, each producing a shape dispersion value based on 4 randomly chosen trial repeats. This confirms that the relationship between shape dispersion and shape consistency is not due to the dependence of both measures on the number of stimulus repeats.

Fig. 6.

Relationship between shape consistency, stimulus color choices, and color selectivity. A: relationship between color distance between the chosen colors and shape consistency. Color distance (X-axis) is quantified by the Euclidean distance in CIE space between the 2 colors used to study each cell. Data from 1 cell, studied with shapes presented at 2 different achromatic luminance contrasts (and no color contrast), is shown at X = 0. No systematic relationship is evident between shape consistency and the chosen colors. B: histogram of shape consistency values for color-selective and unselective cells (analogous to Fig. 4D). Cells were classified on the basis of whether or not a 2-way ANOVA revealed a significant (P < 0.05) main effect of color and/or an interaction between color and shape responses. All except 9 cells (open bars) were significantly modulated by color. Cells that were not color selective tended to exhibit weaker consistency in shape responses across colors. C: scatter plot of color-response dispersion (X-axis) vs. shape consistency. Color-response dispersion was quantified by the ratio of the variance to mean across 25 colors presented at the same luminance contrast as the colors used to study shape responses. Each filled circle corresponds to data from a cell that was studied with 2 colors that differed only in their chromaticity values. Cells studied with colors that differed in both chromaticity and luminance are indicated by open circles. Four of these cells are associated with 2 dispersion values (2 open circles connected by a line) at each of the 2 luminance contrasts tested. Three neurons represented by a single open circle were studied with maximum luminance achromatic stimulus (no other colors were studied at this luminance contrast, and thus no color dispersion can be calculated) and another color at one of the four standard luminance contrasts (see materials and methods). No systematic relationship is evident between shape consistency and color-response dispersion. D: scatter plot of shape-response dispersion vs. color-response dispersion for the 35 cells that underwent detailed color characterization. X-axis plots shape-response dispersion in the preferred color (same as open symbols along X-axis in Fig. 4B). Y-axis is the same as X-axis in C. No systematic relationship is evident between shape- and color-response dispersion; the strength of color selectivity exhibited by a cell did not predict the strength of its shape selectivity.