Organization of hue selectivity in macaque V2 thin stripes

Abstract

V2 has long been recognized to contain functionally distinguishable compartments that are correlated with the stripelike pattern of cytochrome oxidase activity. Early electrophysiological studies suggested that color, direction/disparity, and orientation selectivity were largely segregated in the thin, thick, and interstripes, respectively. Subsequent studies revealed a greater degree of homogeneity in the distribution of response properties across stripes, yet color-selective cells were still found to be most prevalent in the thin stripes. Optical recording studies have demonstrated that thin stripes contain both color-preferring and luminance-preferring modules. These thin stripe color-preferring modules contain spatially organized hue maps, whereas the luminance-preferring modules contain spatially organized luminance-change maps. In this study, the neuronal basis of these hue maps was determined by characterizing the selectivity of neurons for isoluminant hues in multiple penetrations within previously characterized V2 thin stripe hue maps. The results indicate that neurons within the superficial layers of V2 thin stripe hue maps are organized into columns whose aggregated hue selectivity is closely related to the hue selectivity of the optically defined hue maps. These data suggest that thin stripes contain hue maps not simply because of their moderate percentage of hue-selective neurons, but because of the columnar and tangential organization of hue selectivity.

Fig. 1.

Hue selectivity in a single thin stripe penetration. A: low-magnification, color-coded orientation map centered on visual area 2 (V2) just posterior to the lunate sulcus. The white outline indicates the region reproduced at higher magnification illustrated in B. B: color-coded map illustrating the representation of orientation in area V2. The vector summation of single-condition responses to 4 different orientations was calculated for each pixel. The assigned color indicates the pixel preferred orientation and the pixel brightness indicates the magnitude of orientation selectivity. Bright orientation maps are observed in V2 thick and interstripe type II that are located to the right of the dark region of low orientation selectivity corresponding to the V2 thin stripe. The crosses and letters refer to electrode penetrations directed within the V2 thin stripe. C: color-coded, statistically significant (P < 0.005) peak (>75%) hue response contours calculated from the single-condition optical responses to each tested isoluminant hue. D: higher-magnification view of the peak hue map from the black outlined box in C, indicating the locations of electrode penetration H. E: polar representation of stimulus color angles and an example of single-hue responses (black) and resultant summed vector (red), indicating preferred hue (4.28°; red) and vector magnitude (hue selectivity, 0.46). F: bubble plot of L-M cone vs. S-cone contrast values of the 7 hue stimuli used in these experiments. G: conventional tuning curves of net firing rate response means and SEs as a function of hue for 3 single units recorded within 720 μm of the cortical surface. H: polar plots of single-hue responses (black vectors) and summed vectors (red) for 3 single-unit recording sites in this penetration. These cells were highly selective for hue (vector magnitudes of 0.572, 0.656, and 0.466) and shared very similar preferred color angles (38.14, 49.08, and 41.82°). I: normalized hue responses represented as a function of L-M vs. S-cone contrasts. The area of each circle represents the relative response compared with the hue generating the maximum response. J: average cell color vector magnitude and preferred color angle calculated across the 3 cells in this penetration. K: penetration average responses represented as conventional tuning curve (left), polar representation of hue response vectors and summed vector (middle), and relative response as a function of cone contrasts (right). The penetration average response was highly selective for hue (bias = 0.553) and preferred a color angle of 43.68° (orange). L: optical response calculated within a 210 × 210 μm region of interest (ROI) centered on the point of electrode penetration. Only 6 hues were tested (orange not tested) and the summed vector is highly selective (bias = 0.496) with a preferred color angle of 65.22° (yellow-orange). Overall, there is a high degree of consistency between the neuronal and optical estimates of hue preference and hue selectivity.

Fig. 2.

Optical and electrophysiological analysis of hue selectivity. A: high-magnification view of the cortical surface indicating the location of 5 penetrations within the peak hue response map (penetrations C, F, G, H, and I) and 4 penetrations outside the peak hue map (penetrations A, B, D, and E). B: locations of the electrode penetrations and statistically significant peak hue response contours projected onto the color-coded hue response map. C: polar plots of electrophysiological responses to isoluminant hues for 5 penetrations within the peak hue map (left) and 4 penetrations just outside the peak hue map (right). Hue selectivity and preferred color angle are indicated for each recording site. Single (S) or multiunit (M) recordings and stationary (S) or moving (M) stimuli are indicated by the abbreviations SS, SM, MS, and MM. D: average color vector magnitude and preferred color angle across individual recording sites in each penetration. E: penetration average polar plots, hue selectivity (bias), and preferred color angle (hue) calculated by averaging the responses of individual hues across all cells in the penetration, normalizing the responses (black vectors), and then calculating the average color vector (red vector). F: polar plots illustrating the results of the ROI analysis (210 × 210 μm) of single-condition responses from intrinsic optical imaging of responses to isoluminant hues. Case m0103.

Fig. 3.

Penetration average and optical analysis of hue selectivity in relation to the peak hue map. A: location of 4 electrode penetrations relative to the statistically significant peak hue response contours as projected onto the cortical surface in case m005. B: electrode penetrations and peak hue response contours projected onto differential image of orientation preference (45–135°), demonstrating orientation-selective domains located just outside of the peak hue map. C: electrode penetrations and peak hue response contours projected onto the optically determined, vector-based, hue response map. D: close-up of C indicating the positions of electrode penetrations relative to the vector-based hue response map. E: average color vector magnitude and preferred color angle for 2–5 single- or multiunit recording sites in each penetration. F: penetration average polar plots of hue selectivity (bias) and preferred color angle (hue). The red vector indicates the calculated preferred hue and its length indicates the degree of hue selectivity. G: polar plots illustrating the results of the ROI analysis of single-condition responses from intrinsic optical imaging of responses to isoluminant hues. H: differential image of orientation responses (45–135°), demonstrating orientation-selective activity in V2 interstripes flanking a V2 thin stripe in case w13. I: differential image of isoluminant color activations (red-green), demonstrating the color-preferring domain of this V2 thin stripe. J: low-magnification view of the positions of 4 recording sites projected onto the hue response map based on vector summation of isoluminant hue responses. K: high-magnification view of 4 recording sites projected onto the vector-based hue response map from the white box in J. Penetrations A and B were located in regions of low color selectivity, whereas penetrations D and E were located in regions of high color selectivity (large color vector magnitude). L: average hue selectivity (bias) and average preferred hue (color vector angle) calculated across 2–5 recording sites in each penetration. M: polar representation of penetration average hue responses (black vectors) and summed vector (red), indicating the preferred hue (vector angle) and magnitude of hue selectivity (color vector magnitude or bias). N: polar plots illustrating the results of the ROI analysis of single-condition responses from intrinsic optical imaging of responses to isoluminant hues.

Fig. 4.

Analysis of optical and electrophysiological hue selectivity. A: comparison of color vector response magnitudes (hue selectivity) inside vs. outside the statistically significant peak hue response map based on ROI analysis of optical responses (P < 0.00026), penetration average neuronal responses (P < 0.0019), and average neuronal responses (P < 0.0125). B: relationship between color vector magnitudes (hue selectivity) as determined through ROI analysis of optical responses and penetration average neuronal responses. The resultant correlation is strong (r² = 0.718) and highly significant (P < 0.00007). C: bar graph illustrating the difference in preferred color angles for penetration average neuronal responses and ROI analyses of optical responses across all penetrations. The 9 bars on the left represent penetrations inside the peak hue map, whereas the 6 bars on the right represent penetrations outside of the peak hue map. The calculated preferred color angles are highly similar and statistically significant (circular correlation; r_c = 0.507, Z_{r_c} = 1.668; P < 0.045). D: relationship between normalized optical ROI responses and electrophysiological penetration average responses for each stimulus condition across 15 of 17 penetrations. The resultant correlation is highly significant (r² = 0.4539, P < 8.84 × 10⁻¹¹). Penetrations 005c and 005e were excluded due to their weakly modulated responses and their strong negative correlations (see C). The overall correlation is still highly significant if all 17 penetrations are included (r² = −0.1714, P < 0.000742). E: relationship between penetration average hue selectivity (color vector magnitude) and the SD of individual cell's preferred hue (color vector angle). This relationship is significant (P < 0.011 and r² = 0.406), indicating that recording sites from penetrations with high hue selectivity have little variability in their preferred hues, whereas penetrations with low hue selectivity have a high degree of variability in their cell's preferred hues.

Fig. 5.

Schematic representation of hue preference and selectivity in V2 thin stripes. In this model of hue selectivity in V2 thin stripes neurons encountered in electrode penetrations within the statistically significant peak hue maps tend to exhibit robust hue selectivity (larger circles at recording site). Furthermore, neurons within these penetrations tend to prefer the same or similar hues. In contrast, neurons encountered in penetrations outside of the peak hue map tend to exhibit weak or no hue selectivity (small circles) and the calculated preferred hues are more variable from cell to cell.