Laminar, columnar and topographic aspects of ocular dominance in the primary visual cortex of Cebus monkeys

Abstract

The representation of the two eyes in striate cortex (V1) of Cebus monkeys was studied by electrophysiological single-unit recordings in normal animals and by morphometric analysis of the pattern of ocular dominance (OD) stripes, as revealed by cytochrome oxidase histochemistry in V1 flat-mounts of enucleated animals. Single-unit recordings revealed that the large majority of V1 neurons respond to the stimulation of either eye but are more strongly activated by one of them. As in other species of monkey, neurons with preference for the stimulation of the same eye are grouped in columns 300-400 microns wide, spanning all cortical layers. Monocular neurons are clustered in layer IVc, specially in its deeper half (IVc-beta), and constitute less than 10% of the population of other layers. Neurons with equal responses to each eye are more commonly found in layer V than elsewhere in V1. In the supragranular layers and in granular layer IVc-alpha neurons strongly dominated by one of the eyes tend to be broadly tuned for orientation, while binocularly balanced neurons tend to be sharply tuned for this parameter. No such correlation was detected in the infragranular layers, and most neurons in layer IVc-beta responded regardless of stimulus orientation. Ocular dominance stripes are present throughout most of V1 as long, parallel or bifurcating bands alternately dominated by the ipsi- or the contralateral eye. They are absent from the cortical representations of the blind spot and the monocular crescent. The domains of each eye occupy nearly equal portions of the surface of binocular V1, except for the representation of the periphery, where the contralateral eye has a larger domain, and a narrow strip along the border of V1 with V2, where either eye may predominate. The orderliness of the pattern of stripes and the relationship between stripe arrangement and the representation of the visual meridians vary with eccentricity and polar angle but follow the same rules in different animals. These results demonstrate that the laminar, columnar and topographic distribution of neurons with different degrees of OD in V1 is qualitatively similar in New- and Old World monkeys of similar sizes and suggest that common ancestry, rather than parallel evolution, may account for the OD phenotypes of contemporaneous simians.