Interdigitated Color- and Disparity-Selective Columns within Human Visual Cortical Areas V2 and V3.

UNLABELLED

In nonhuman primates (NHPs), secondary visual cortex (V2) is composed of repeating columnar stripes, which are evident in histological variations of cytochrome oxidase (CO) levels. Distinctive "thin" and "thick" stripes of dark CO staining reportedly respond selectively to stimulus variations in color and binocular disparity, respectively. Here, we first tested whether similar color-selective or disparity-selective stripes exist in human V2. If so, available evidence predicts that such stripes should (1) radiate "outward" from the V1-V2 border, (2) interdigitate, (3) differ from each other in both thickness and length, (4) be spaced ∼3.5-4 mm apart (center-to-center), and, perhaps, (5) have segregated functional connections. Second, we tested whether analogous segregated columns exist in a "next-higher" tier area, V3. To answer these questions, we used high-resolution fMRI (1 × 1 × 1 mm(3)) at high field (7 T), presenting color-selective or disparity-selective stimuli, plus extensive signal averaging across multiple scan sessions and cortical surface-based analysis. All hypotheses were confirmed. V2 stripes and V3 columns were reliably localized in all subjects. The two stripe/column types were largely interdigitated (e.g., nonoverlapping) in both V2 and V3. Color-selective stripes differed from disparity-selective stripes in both width (thickness) and length. Analysis of resting-state functional connections (eyes closed) showed a stronger correlation between functionally alike (compared with functionally unlike) stripes/columns in V2 and V3. These results revealed a fine-scale segregation of color-selective or disparity-selective streams within human areas V2 and V3. Together with prior evidence from NHPs, this suggests that two parallel processing streams extend from visual subcortical regions through V1, V2, and V3.

SIGNIFICANCE STATEMENT

In current textbooks and reviews, diagrams of cortical visual processing highlight two distinct neural-processing streams within the first and second cortical areas in monkeys. Two major streams consist of segregated cortical columns that are selectively activated by either color or ocular interactions. Because such cortical columns are so small, they were not revealed previously by conventional imaging techniques in humans. Here we demonstrate that such segregated columnar systems exist in humans. We find that, in humans, color versus binocular disparity columns extend one full area further, into the third visual area. Our approach can be extended to reveal and study additional types of columns in human cortex, perhaps including columns underlying more cognitive functions.