A map for horizontal disparity in monkey V2

Abstract

The perception of visual depth is determined by integration of spatial disparities of inputs from the two eyes. Single cells in visual cortex of monkeys are known to respond to specific binocular disparities; however, little is known about their functional organization. We now show, using intrinsic signal optical imaging and single-unit physiology, that, in the thick stripe compartments of the second visual area (V2), there is a clustered organization of Near cells and Far cells, and moreover, there are topographic maps for Near to Far disparities within V2. Our findings suggest that maps for visual disparity are calculated in V2, and demonstrate parallels in functional organization between the thin, pale, and thick stripes of V2.

Figure 1. Localization of the disparity response in the thick stripes of V2

(A) A section stained for cytochrome oxidase showing the positions of thin (red arrow heads) and thick (a black arrow head) stripes of V2. (B) Enlarged part in red box of (A). (C) Percentage of pixels in V1 and in the thin, pale, and thick stripes of V2 with significant (p < 0.05) response to RDS. More pixels in thick stripes (n = 5) responded to depth stimuli than in the pale or thin stripes within V2 or in V1 (p < 10⁻⁶, t test). Error bars, ± SEM. (D) Ocular dominance map in V1 (left eye minus right eye) reveals V1/V2 border (horizontal line). (E) Orientation map (differential response, horizontal vs. vertical gratings). (F) Thin stripes are determined by the areas which prefer color to luminance. Note that regions with color preference (thin stripes) have poor orientation preference. The gray region is out of field of view as camera was moved to slightly different location for the color run. (G) Difference between binocular stimuli (dark pixels) and monocular stimuli (light pixels) reveal the position of the thick stripe (cf. Ts’o et al 2001). (H) RDS disparity map. Sum of all Near and Far. (I) White pixels are those with significant responses to RDS (compared to responses to uncorrelated stereograms, t test, p < 0.05). Scale bar: 1 mm (A) and (B). Scale bar for (B) applies to (D)–(I). A, anterior; M, medial.

Figure 2. Disparity topography in V2

(A) Differential image between all Near (dark pixels) and all Far (light pixels) stimuli. Black dashed line, border of V1–V2. (B)–(H). Single condition images evoked by three Near stimuli with disparities of 0.34°(B), 0.17°(C), and 0.085°(D), Zero (E), and three Far stimuli of 0.085°(F), 0.17°(G) and 0.34°(H). Positions of two crosses are constant through (A)–(I). The outlined regions in (B)–(H) show areas with significantly greater response to RDS than uncorrelated stereograms (p < 0.05, t test). As described by ellipse fits, the lengths of these domains in (B)–(H) are 802, 831, 856, 933, 1216, 690, and 918 µm, respectively. Widths are 431, 428, 350, 437, 370, 549, and 298µm, respectively. (I) Summary showing overlay of three disparity contours (red: 0.34° near, green: zero, blue: 0.34° far). (J) Optical image of response to uncorrelated random dots (vs. Blank. A streak of white activity (upper right corner) is due to blood vessel noise). Grayscale: magnitude of imaged response in percent reflectance. Color scale: near to far disparity. Scale bars in A, B: 1 mm. A, anterior; L, lateral.

Figure 3. Disparity topography in V2: a second case

(A) Differential image between all Near (dark pixels) and all Far (light pixels) stimuli. Dotted box: region shown in B–K. Black dashed line: V1/V2 border. (B–H), Single condition disparity images: −0.34°(B), −0.17°(C), −0.085°(D), zero (E), +0.085°(F), +0.17°(G), and +0.34°(H). Three activation domains are labeled 1, 2, and 3 in B. Color outlines: regions of significant activation (p < 0.05, t test). (I–K), Summary topographies of domains 1 (I), 2 (J), and 3 (K). Conventions same as Figure 2. Scale bars: 1 mm. A, anterior; L, lateral.

Figure 4. Overlap and distance measurements support topography

(A) Percent overlap between pairs of disparity domains. Percent overlap predicts delta disparity: the greater the overlap the more similar the disparity. (B) Distance between centers of mass of disparity domains. Distance predicts delta disparity: smaller distances predict similar disparity. Numbers of domain pairs are indicated by numbers in bars. Since no two disparity domains have Δdisparity larger than 1.1°, the largest bin shown is 1.1° of disparity difference. (C–E), average length, width, and length-width ratio of All (black, n = 123), Near (red, n = 45), Zero (green, n = 50), Far (blue, n = 28) from 9 cases. Error bars, ± SEM.

Figure 5. Comparison between neuronal and optical signals

(A) Four electrode-recording locations (marked by colored squares) within the color-coded disparity domains (see color scale bar). (B) Example consistent with columnar organization. Disparity tuning of four neurons recorded within a single vertical penetration. Red lines: Gaussian fit. Blue triangles: preferred disparity. Normalized optical (C) and neural (D) disparity tuning curves at each of 4 locations in A. Dashed vertical lines in C–D: zero disparity. (E), scatter plot for each pair of optical (abscissa) and neuronal (ordinate) signals in C–D, showing significant correlation (robust regression, r = 0.80, p < 0.01). Scatter plot for disparity preference (F) and disparity tuning width (G) obtained from optical and neuronal signals from 3 cases did both tests (n = 27). Disparity preferences are similar (p > 0.4, paired t test) while tuning widths tend to be wider than optical signals (see histograms at upper right corners, p < 0.01, paired t test). Different marker shapes are neurons recorded from different monkeys. For detailed optical and neuronal tuning curves, see Supplementary materials (Supplementary Figure S5). Thick lines are diagonals. Scale bars: 1 mm (A), 0.25° (D). Error bars, ± SEM.

Figure 6. Relationship between orientation domains and disparity domains

(A) The orientation selectivity of areas with significant response to any disparity tested (same case as shown in Figure 1). The preferred orientations are shown (color wheel). (B) Percentage of pixels (of the disparity selective pixels) at each of the 0°, 45°, 90°, and 135° orientations. Within disparity selective pixels, across all cases, the average percentage of areas covered by each orientation was not significantly different from 25% (all p > 0.5, t test). (C) Statistical results of the average percentage of pixels in an orientation domain covered by different disparity domains. Based on a balanced two-ways ANOVA, where the factors were disparity, orientation, and their interaction, there is no significant influence from orientation or from disparity (both p > 0.8) or between them (p > 0.9). (D) Averaged disparity tuning strength within orientation preference domains. No significant difference was found between horizontal and 45°, 90°, or 135° orientation preference domains (all p > 0.5, t test, n = 9). Error bars, ± SEM. Scale bar: 1 mm (A).

Figure 7

Depiction of possible organization in V2 where orientation and disparity parameters are orthogonally represented.