Suppression of optokinesis in the reafferent direction during pursuit eye movements

When tracking with the eyes an object moving against a textured background, the background retinal image moves in the opposite direction to the smooth pursuit eye movement. Optokinetic responses, such as optokinetic nystagmus (OKN) or ocular tracking, to this reafferent signal must be suppressed to sustain pursuit of the object-of-interest. We varied the contrast of a brief background motion to tell apart two plausible accounts of the suppression of optokinesis during pursuit; a visuomotor gain modulation account, which predicts that ocular tracking of background motion is suppressed in the same proportion at irrespective of contrast, and a sensory attenuation account, which predicts that larger contrasts are needed to elicit the same response. Unexpectedly, neither account fits ocular tracking in the reafferent signal direction. The combination of contrast-dependent gating, with maximal suppression observed with higher contrasts, and visuomotor gain modulation, provides a good fit for most observers data. Contrast-dependent gating promotes visuomotor stability in response to most salient signals, as a likely adaptation to the statistics of the environment. Significance statementFor humans to be able to track small moving objects, there is a need for a mechanism to cancel optokinesis, that is reflexive eye movements towards prevalent visual motion. We show that this cancellation is not a simple "volume-control" reduction of responses to motion signals, as expected. This suppression also involves contrast-dependent gating, meaning that most salient signals are not allowed to modify the ongoing movement. This additional component could have arisen from an adaptation to image statistics of motion signals prevalent in natural environments.