Functional Organization of Visual Cortex in the Owl Monkey

Abstract

In this study, we compared the organization of orientation preference in visual areas V1, V2, and V3. Within these visual areas, we also quantified the relationship between orientation preference and cytochrome oxidase (CO) staining patterns. V1 maps of orientation preference contained both pinwheels and linear zones. The location of CO blobs did not relate in a systematic way to maps of orientation; although, as in other primates, there were approximately twice as many pinwheels as CO blobs. V2 contained bands of high and low orientation selectivity. The bands of high orientation selectivity were organized into pinwheels and linear zones, but iso-orientation domains were twice as large as those in V1. Quantitative comparisons between bands containing high or low orientation selectivity and CO dark and light bands suggested that at least four functional compartments exist in V2, CO dense bands with either high or low orientation selectivity, and CO light bands with either high or low selectivity. We also demonstrated that two functional compartments exist in V3, with zones of high orientation selectivity corresponding to CO dense areas and zones of low orientation selectivity corresponding to CO pale areas. Together with previous findings, these results suggest that the modular organization of V1 is similar across primates and indeed across most mammals. V2 organization in owl monkeys also appears similar to that of other simians but different from that of prosimians and other mammals. Finally, V3 of owl monkeys shows a compartmental organization for orientation selectivity that remains to be demonstrated in other primates.

Unequal representation of cardinal vs. oblique orientations in the middle temporal visual area

“…In owl monkeys, lesions and deactivations of V1 rendered MT unresponsive to visual stimuli (24,38). However, reanalysis of the orientation preference maps from our previous study revealed only a small and inconsistent overrepresentation of cardinal orientations in the region of V1 representing 0-10°eccen-tricity in owl monkeys, whereas more peripheral portions of V1 were unavailable for imaging (23). In the bush baby a consistent anisotropy was found in V1 by using optical imaging but only for the 0-3°representation and not beyond this eccentricity (X.X., T. J. Anderson, and V.A.C., unpublished observations).…”

“…As shown in Fig. 1 a-c, orientation domains in MT of owl monkeys were organized very much like those of V1 (23), with clear isoorientation domains ( Fig. 1 a and b) and continuous representation of a series of pinwheels and linear zones (Fig.…”

“…1c). The average isoorientation domain sizes in MT [0.136 Ϯ 0.075 (mean Ϯ SD) mm 2 , n ϭ 48, measured from three cases], however, are much larger than those in V1 (0.076 Ϯ 0.046 mm 2 ) of owl monkeys (23). Moreover, the MT isoorientation domains consisted of subdomains preferring motion in one direction and the opposite direction (17,18).…”

“…All animals were handled according to an approved protocol from the Vanderbilt University Animal Care and Use Committee. Animals were prepared for surgery, paralyzed, and anesthetized as described elsewhere (18,23,24,39). Five hemispheres were imaged in this study; three of them yielded high-quality functional maps.…”

“…Optical imaging and analysis, visual stimuli, and histological reconstruction procedures were performed as described in detail in previous studies (18,23,24,39). Briefly, intrinsic optical imaging signals were acquired with the Imager 2001 differential videoenhancement imaging system and VDAQ͞NT data acquisition software (Optical Imaging, Mountainside, NJ).…”