Perceptual Color Map in Macaque Visual Area V4

Cortical location and dynamics of color-preferring modules in V4 by optical imaging. A, Cranial window covers the cross region of lunate sulcus (LS), superior temporal sulcus (STS), and inferior occipital sulcus (IOS). White frame indicates imaged area, containing the center of V4d and parts of V1, V2. A, Anterior; M, medial. B, Monkey fixated to screen center, as verified by eye tracker, triggering 4 s color (red-green) or orientation grating stimuli (20° × 15°), after which it received juice reward. CCD chip was mechanically coupled to the lens system and the monkey head, with flexible wires connecting it to the camera; thus, it could move slightly with the head without shifting images, giving high image stability. C, Images of the differential maps for color (top) and orientation (below), respectively, from the stimuli onset onward. Darkening regions (contoured) indicate increasing activity (n = 50 trials). D, Average image from color grating; color processing areas (red-green dashed contour) are separated from the orientation zones (black-white dashed contour), consistent with earlier findings (Tanigawa et al., 2010). E, Enlarged view of the boxed region in D: peak responses (75% maxima) inside significantly activated regions (p < 0.01) contoured. Images Gaussian high-pass (σ = 322 μm) and low-pass filtered (σ = 52 μm), frames clipped to ±0.15%. F, Time course of the reflectance change (mean ± SEM) in the differential maps in the peak regions, as in C, during color stimulation (black trace represents red/green grating; gray trace represents blank condition) in two monkeys (Monkeys A and C). Frames from 1.5–5 s (light gray area) were used for the average image in E. Scale bars represent 1 mm.

Characterization of color-induced cortical activity (color maps) in optical imaging data. A–C, Comparison of cortical maps to red and green stimuli (1° × 1° squares on gray background) obtained by different reprocessing methods. A, Blank control. B, Control by white + black. C, Cocktail blank control by all stimulus conditions. Top rows, Unfiltered. Bottom row, Gaussian filtered maps and their effects on the contoured maps. A, There are common activity patches in red and green maps at the bottom left corner (white arrowheads), possibly evoked by the common shape components of the stimuli. This area belongs to the orientation preference area (see Fig. 2C). B, Contours show 75% relative thresholds of the activity areas. D, A hue cluster with a white line crossing the spatial distribution of its peak activity areas. E, Optical signals along the selected cross section (white line in D) in the hue cluster. F, Red lightness cluster with a white line crossing its spatial distribution of the contoured cortical activity patches (peak activity areas). G, Optical signals along the selected cross section (white line in D) in the lightness cluster. E, G, Dotted colored lines indicate the 75% relative threshold for the same-color-induced activity areas; the black dashed lines indicate examples of low arbitrary absolute thresholds.

Hue maps in area V4. A, Bright (saturated) hues: R, red; O, orange; Y, yellow; G, green; A, aqua; B, blue; P, purple, sampled from the hue circle (i.e., maximum cross section of HSL space; Fig. 1B). Controls: K, black; W, white; BG, gray background is 1/5 lightness of white: CIE xyY of (0.31, 0.33, 22.8). B, Fixation to the gray screen (BG) center (white dot), triggered 4 s presentation of 1° × 1° hue square at a preset screen position, which marks the local visual field center of the glob. After a rest (>10 s), new fixation triggered a new hue at the same position. C, Cortical activity patches to seven hues, respectively, as indicated by optical imaging in Monkey A. Each hue evoked multiple patches of activity. Peak responses (75% maxima) inside significantly activated regions (p < 0.05) outlined by corresponding hue contours. Images of Gaussian high-pass (σ = 322 μm) and low-pass filtered (σ = 52 μm) frames, clipped individually to ± 3 SD (n = 45 trials); see details in Materials and Methods. D, Combined map for seven hues. Patches for adjacent hues form clusters: “rainbows of patches.” E–G, Larger views of hue clusters: C_H1, C_H2, and C_H3, respectively. H, Interpolated locations of hue-preferring patches in hue clusters of Monkey A. I–K, Correlation analysis between hue distances to cortical distances. The hue distance and the cortical distance correlate significantly (r, correlation index; n, number of distance measurements between patches). L, The hue map in Monkey B. M, Interpolated locations of hue-preferring patches in hue clusters of Monkey B. N–O, Correlation analysis of its hue clusters. Scale bars, 1 mm.

Surveying the retinotopy of the hue map in V4. A, Local visual field (i.e., the region of the visual field to which each hue cluster was responsive) mapping was performed by presenting 0.5° × 0.5° red or green square (stimulus) on six horizontal and five vertical positions; fovea is 0°. RF centers of color-preferring modules ∼−1.5° below the fixation point (FP). The subfigures show nonfiltered images. B, Three clusters of Monkey A's hue map: C_H1, C_H2, and C_H3, tested in this survey (the same ones as in Fig. 4D). C, Red- and green-preferring patches in cluster I have virtually identical local visual fields. D, Red-preferring patches in clusters C_H1 and C_H3 have different but largely overlapping local visual fields. E, Green-preferring patches in clusters C_H1 and C_H2 have different but largely overlapping local visual fields. F, Red or green squares of different sizes (0.5°, 1.5°, 4°) presented at the estimated geometric center of the hue map's local visual field evoked comparable optical signals at their corresponding locations. Despite variations in patch sizes in each location (experiments done on different days), their activity did not differ significantly (p > 0.05, two-tailed t test). Scale bars represent 1 mm.

Lightness maps in area V4. A, Colors sampled with different lightness on HSL cone in logarithmic scale. Center points: Rw₂ (pink) between red (R) and white (W); Rw₃ (light pink) between Rw₂ and W; Rk₂ (darken red) between R and black (K); Rk₃ between Rk₂ and K. The same criteria used for green and blue stimuli. B, Activity patches, evoked by reds of varying lightness, shift with decreasing lightness. The 1° × 1° lightness stimuli were presented at the local visual field of the color-biased region in pseudorandom order, as in Figure 3B. Images Gaussian high-pass (σ = 322 μm) and low-pass filtered (σ = 52 μm), frames clipped to ± 3 SD peak responses (75% maxima) in significantly activated regions (p < 0.05) contoured (n = 29 trials). C, Activity patches to red lightness stimuli form three lightness clusters. D, E, Similar lightness clusters for green and blue stimuli, respectively. F, Combined lightness map for red, green, and blue. G, The corresponding interpolated locations of lightness-preferring patches; there is the common branch point for (RGB) lightness values: the central black-patch. H, Correlation analysis between lightness distances to cortical distances for red, green, and blue lightness clusters: C_LR1, C_LG1, and C_LB1, respectively. The logarithmic lightness distance and the cortical distance correlate significantly (r, correlation index; n, number of distance measurements between patches). I, The color lightness map in Monkey B. J, Interpolated locations of its lightness-preferring patches. K, Correlation analysis for its lightness clusters. Scale bars, 1 mm.

Comparison of correlation coefficients when using logarithmic and linear coordinates, in HSL color space. A, B, Examples correlate the lightness distances with the distances between activated cortical patches. The lightness distance between all pairs of tested colors is measured separately in logarithmic and linear coordinates.

Cortical color lightness maps for different colors. A–D, Color lightness maps for orange, yellow, aqua, and purple, respectively. With lightness decreasing, the locations of activated patches shift toward the black-preferring patches. Scale bar, 1 mm.

Representation of color saturation in area V4. A, Unsaturated colors chosen inside HSL cone. Central points: Ru₁₂ is between R and middle gray; Ru₁₃ between Ru₁₂ and middle gray. The same criteria were used for selecting unsaturated green and blue stimuli. B, Maps for red with 1, 1/2, 1/4, 1/8, and 1/16 saturation (S1–S5), respectively, in Monkey A. Images of Gaussian high-pass (σ = 322 μm) and low-pass filtered (σ = 52 μm); same clipping range (± 0.1%) used for every map (n = 45, 35, and 22 trials for R, G, and B stimuli, respectively). C, Peak responses (mean ± SEM) of the activated patches in B. Correlation between peak response intensities and color log saturation approximates linearity (r = −0.938, p < 10⁻⁴). Scale bar, 1 mm.

Cortical representation of unsaturated and darken red. A, Differential maps for unsaturated and darken red. B, Cortical activation decreases when saturation decreases (one-tailed t test). C, Locations of the peak responses shift with decreasing lightness. Data are from Monkey A. Scale bar, 1 mm.

Clusters and stacks in combined maps in globs of area V4. A–D, The combined maps of Monkeys A, B, C, and D, respectively, show individual layouts but similar representational rules for hue and lightness information with each map containing hue and lightness clusters and stacks. E–H, The corresponding interpolated locations of hue-preferring patches in hue clusters, C_H, and lightness-preferring patches in lightness clusters, C_L. Small black or white disks: black- or white-preferring patches, forming end- or branch-points. Light gray rectangles represent orthogonal crossings between hue and lightness clusters. I–L, Stacked patches, S, in the combined maps. Red stacks represent S_R, red disks; blue stacks represent S_B, blue disks; unique stacks represent S_U, light gray disks. Scale bar, 1 mm. Although in Mk.B some stacks appear next to or over vessels, this did not lower the image quality much (see Materials and Methods).

Examples of spatial density analysis for patches in Monkey A (A–E) and Monkey B (F–J). A, F, Contoured color maps. Contours for all test colors were superimposed on the blood vessel background. B, G, The centers of all contours (in A,F) were plotted as white points. C, H, Spatial density map, showing the center points of all patches. These maps use 3 × 3 pixel (77 × 77 μm) binning for each pixel (in B, G) given in arbitrary units. D, I, Smooth spatial density maps derived from C and H, using Gaussian low-pass filter (σ = 26 μm). E, J, Red points in these maps represent peaks in the maps D and I, respectively; 5 SDs are used as threshold. These peaks indicate “stacks,” where many patches concentrate. Scale bar, 1 mm.

Reproducibility of the color maps in V4. A, B, Difference maps to red stimulus in Monkey A, on day 91 and day 97. These maps were calculated by using Equation 3. Peak responses (75% maxima) inside significantly activated regions (one-tailed t test, p < 0.05, n = 35 trials) outlined by red contours. C, Difference map, calculated by subtracting response to red on day 97 from response to red on day 91, revealed no significant regions (two-tailed t test, p < 0.05, n = 35 trials). Peak response contours from day 91 and day 97 are superimposed on this map to easy comparison. D–F, Another example of the reproducibility test in Monkey D, using green stimulus (n = 34 trials), produced similar results. A–F, The maps were unfiltered. Clipping range for all the map was as follows: −0.1% to 0.1%. Scale bar, 1 mm.

Cortical map for (near-) equiluminant colors makes up only a small section of Monkey A's full color map (compare Fig. 10A). A, The map displays cortical activity patches (peak activity areas), evoked by seven hues (red, orange, yellow, green, aqua, blue, and purple) of relatively similar luminance values (22.7, 17.0, 27.4, 20.9, 25.4, 15.2, and 11.0 cd/m², respectively; Table 1). The map shows chromatic hue order but not as clearly as “rainbows of patches,” which form hue clusters to bright saturated hues (compare Fig. 3D). B, Cortical locations of patch centers representing equiluminant red, green, and blue (20 cd/m²) were approximated from the recorded lightness clusters (see Materials and Methods). Because of linear cortical mapping of logarithmic lightness values (compare Fig. 6A), the approximated patch centers for equiluminant red, green, and blue are very close to the measured patch centers of the corresponding near-equiluminant colors (22.7, 20.9, and 15.2 cd/m², respectively; marked by crosses and pointed by arrows). Therefore, the map of peak activity areas of near-equiluminant colors in A is likely to provide an accurate approximation of the corresponding equiluminant color map in globs. To highlight the color map's linear representation of logarithmic luminance values, few other estimated patch center positions for darker (lower luminance) reds, greens, and blues are also indicated by arrows. Scale bar, 1 mm.

Neural responses, measured through microelectrode recordings, correlate with optical imaging signals. A, Locations of the microelectrode recordings, marked with + in respect to the corresponding optically measured color maps in Monkey A. B, Action potentials at electrode pt2, located in a red area, are mostly evoked by dark red and reds with greater lightness. After 60–150 ms delay from the stimulus onset, the firing peaks transiently before settling at steady-state level. Average firing rate (±SD) for each color, obtained from recordings to 15–20 repetitions, show color-specific variations. C, Action potentials at electrode pt6 are mostly evoked by pink, purple, and reds with greater lightness. Interestingly, this recording site showed enhanced firing (opponency) after green and yellow stimulation. D, The normalized color tuning measured at each recording site compared with the corresponding optical signals. Color-induced intensity of the optical signal was taken from its grayscale difference maps (e.g., Figure 3C) as the average of 3 × 3 image pixels at the point where each electrode resided. E, Correlation between the neuronal responses and the optical signals (p < 10⁻⁴); includes all data from D. Scale bar, 1 mm.