Postmicrosaccadic Enhancement of Slow Eye Movements

Abstract

Active sensation poses unique challenges to sensory systems because moving the sensor necessarily alters the input sensory stream. Sensory input quality is additionally compromised if the sensor moves rapidly, as during rapid eye movements, making the period immediately after the movement critical for recovering reliable sensation. Here, we studied this immediate postmovement interval for the case of microsaccades during fixation, which rapidly jitter the "sensor" exactly when it is being voluntarily stabilized to maintain clear vision. We characterized retinal-image slip in monkeys immediately after microsaccades by analyzing postmovement ocular drifts. We observed enhanced ocular drifts by up to ~28% relative to premicrosaccade levels, and for up to ~50 ms after movement end. Moreover, we used a technique to trigger full-field image motion contingent on real-time microsaccade detection, and we used the initial ocular following response to this motion as a proxy for changes in early visual motion processing caused by microsaccades. When the full-field image motion started during microsaccades, ocular following was strongly suppressed, consistent with detrimental retinal effects of the movements. However, when the motion started after microsaccades, there was up to ~73% increase in ocular following speed, suggesting an enhanced motion sensitivity. These results suggest that the interface between even the smallest possible saccades and "fixation" includes a period of faster than usual image slip, as well as an enhanced responsiveness to image motion, and that both of these phenomena need to be considered when interpreting the pervasive neural and perceptual modulations frequently observed around the time of microsaccades.