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Optical Imaging of Contextual Interactions in V1 of the Behaving Monkey

¹The Rockefeller University; and ²Department of Neuroscience, Columbia University, New York, New York

Submitted 5 August 2008; accepted in final form 5 July 2009

Abstract

Interactions in primary visual cortex (V1) between simple visual elements such as short bar segments are believed to underlie our ability to easily integrate contours and segment surfaces. We used intrinsic signal optical imaging in alert fixating macaques to measure the strength and cortical distribution of V1 interactions among collinear bars. A single short bar stimulus produced a broad-peaked hill of activation (the optical point spread) covering multiple orientation hypercolumns in V1. Flanking the bar stimulus with a pair of identical collinear bars led to a strong nonlinear suppression in the optical signal. This nonlinearity was strongest over the center bar region, with a spatial distribution that cannot be explained by a simple gain control. It was a function of the relative orientation and separation of the bar stimuli in a manner tuned sharply for collinearity, being strongest for immediately adjacent bars lying on a smooth contour. These results suggest intracortical interactions playing a major role in determining V1 activation by smooth extended contours. Our finding that the interaction is primarily suppressive when imaged optically, which presumably reflects the combined inhibitory and excitatory inputs, suggests a complex interplay between these cortical inputs leading to the collinear facilitation seen in the spiking response of V1 neurons. This disjuncture between the facilitation seen in spiking and the suppression in imaging also suggests that cortical representations of complex stimuli involve interactions that need to be studied over extended networks and may be hard to deduce from the responses of individual neurons.