The functional organization of orientation maps in owl monkey V1 and V2 revealed by optical imaging of intrinsic signals

Abstract

This study examined the organization of orientation preference in visual areas V1 and V2 of the nocturnal simian owl monkey (Aotus trivirgatus) using optical imaging of intrinsic signals. Owl monkeys are of interest because they have well developed cytochrome oxidase (CO) blobs in V1 and CO stripes in V2, but lack color vision. Polar maps of orientation preference were constructed by vector summation of single-condition maps acquired during the presentation of 4 or 8 angles of square wave grating stimuli. These maps were then compared to the patterns of CO staining in V1 and V2. As reported in other species, the V1 map contained regions where orientation preference changed linearly (linear zones) and regions where orientation preference was organized radially (pinwheels). Linear zones were prominent along the V1/V2 border and iso-orientation contour lines in the linear zones tended to intersect the border at right angles. Pinwheels occurred at a density of ∼ 8 pinwheels/mm2 in V1. In V2, alternating regions of high and low orientation selectivity were observed that may correspond to regions of light and dark CO staining, respectively. Within the regions of high selectivity, orientation preference was arranged in a manner similar to that found in V1, including both linear zones and pinwheel centers. However, within V2 individual iso-orientation domains were larger and the density of pinwheels (∼3.3 pinwheels/mm2) was about half of that found in V1. The organization of V2 into bands of high and low selectivity for orientation in owl monkey suggests that, as in diurnal primates, these bands segregate higher-order properties but in the absence of color vision. Overall, the organization of orientation preference in V1 and V2 of owl monkeys shows many features in common with the organization described in other simian primates. (Supported by EY01778, EY08126, HD15052, RR13947)