Intracortical Origins of Interocular Suppression in the Visual Cortex

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Abstract
The response of neurons in the primary visual cortex to an optimally oriented grating is usually suppressed quite dramatically when a second grating of, for example, orthogonal orientation is superimposed. Such “cross-orientation suppression” has been implicated in the generation of cortical orientation selectivity and local response normalization. Until recently, little experimental evidence was available concerning the neurophysiological substrate of this phenomenon, although an involvement of intracortical inhibition was commonly assumed. However, Freeman et al. (2002) proposed that cortical cross-orientation suppression is caused by suppression in the thalamus and depression at geniculocortical synapses. Here, we examine a dichoptic form of cross-orientation suppression, termed interocular suppression and thought to be involved in binocular rivalry (Sengpiel et al., 1995a). We show that its dependency on the drift rate of the suppressing stimulus is consistent with a cortical origin; unlike monocular cross-orientation suppression, it cannot be evoked by very fast-moving stimuli. Moreover, we find that previous adaptation to the orthogonal stimulus essentially eliminates interocular suppression. Because adaptation is a cortical phenomenon, this result also argues in favor of a cortical locus of suppression, again unlike monocular cross-orientation suppression, which is not affected by adaptation to the suppressor (Freeman et al., 2002). Finally, interocular suppression is greatly reduced in the presence of the GABA antagonist bicuculline. Together, our study demonstrates that interocular suppression is substantially different from monocular cross-orientation suppression and is mediated by inhibitory circuitry within the visual cortex.