Pattern adaptation and cross-orientation interactions in the primary visual cortex

Abstract

The responsiveness of neurons in the primary visual cortex (V1) is substantially reduced after a few seconds of visual stimulation with an effective pattern. This phenomenon, called pattern adaptation, is uniquely cortical and is the likely substrate of a variety of perceptual after-effects. While adaptation to a given pattern reduces the responses of V1 neurons to all subsequently viewed test patterns, this reduction shows some specificity, being strongest when the adapting and test patterns are identical. This specificity may indicate that adaptation affects the interaction between groups of neurons that are jointly activated by the adapting stimulus. We investigated this possibility by studying the effects of adaptation to visual patterns containing one or both of two orientations—the preferred orientation for a cell, and the orientation orthogonal to it. Because neurons in the primary visual cortex are sharply tuned for orientation, stimulation with orthogonal orientations excites two largely distinct populations of neurons. With intracellular recordings of the membrane potential of cat V1 neurons, we found that adaptation to the orthogonal orientation alone does not evoke the hyperpolarization that is typical of adaptation to the preferred orientation. With extracellular recordings of the firing rate of macaque V1 neurons, we found that the responses were not reduced by adaptation to the orthogonal orientation alone nearly as much as by adaptation to the preferred orientation. In the macaque we also studied the effects of adaptation to plaids containing both the preferred and the orthogonal orientations. We found that adaptation to these stimuli could modify the interactions between orientations. It increased the amount of cross-orientation suppression displayed by some cells, even turning some cells that showed cross-orientation facilitation when adapted to a blank stimulus into cells that show cross-orientation suppression. This result suggests that pattern adaptation can affect the interaction between the groups of neurons tuned to the orthogonal orientations, either by increasing their mutual inhibition or by decreasing their mutual excitation.