Nonlinear combination of binocular signals in macaque cortex

Abstract

We studied the principles by which contrast signals are combined binocularly in visual areas V1 and V2. We recorded the responses of single-units to drifting sinusoidal gratings of optimal spatial frequency and orientation. We first found the relative spatial phases of the gratings that maximized and minimized the responses to binocular stimulation. Then, using pairs of moving gratings in one or other of these relative phases, we measured the responses to all possible pairings of 8 levels of contrast spanning the full range in each eye. This provided two sets of 64 responses that defined binocular contrast-response surfaces. Using each contrast-response surface, we examined whether or not the effects of contrast variation in one eye were independent of the contrast presented to the other eye. By identifying iso-response contours in a contrast response surface, we could characterize input nonlinearities; by comparing the amplitudes of responses to binocular stimuli with the sum of responses to the components presented separately, we could characterize output nonlinearities. Units in both V1 and V2 commonly demonstrated binocular interactions that implied both input and output nonlinearities. For constant amplitude of response, less net contrast was needed when it was distributed across both eyes than when delivered via one eye. We also found that the response to a pair of gratings presented concurrently to both eyes often did not equal the sum of the responses to each of the gratings presented alone. These failures of response summation were often expressed as a form of super-additivity, in which the response to the pair of gratings exceeded the sum of the responses to individual ones, but sometimes we observed a destructive interference. Our finding of super-additivity contrasts with previous descriptions of linear summation, and would not be expected from psychophysical observations on binocular combination.

Footnotes

 Supported by EY04440, EY06745, EY06638, EY13079.