Head-Eye Coordination at a Microscopic Scale

Abstract

Humans explore static visual scenes by alternating rapid eye movements (saccades) with periods of slow and incessant eye drifts [1-3]. These drifts are commonly believed to be the consequence of physiological limits in maintaining steady gaze, resulting in Brownian-like trajectories [4-7], which are almost independent in the two eyes [8-10]. However, because of the technical difficulty of recording minute eye movements, most knowledge on ocular drift comes from artificial laboratory conditions, in which the head of the observer is strictly immobilized. Little is known about eye drift during natural head-free fixation, when microscopic head movements are also continually present [11-13]. We have recently observed that the power spectrum of the visual input to the retina during ocular drift is largely unaffected by fixational head movements [14]. Here we elucidate the mechanism responsible for this invariance. We show that, contrary to common assumption, ocular drift does not move the eyes randomly, but compensates for microscopic head movements, thereby yielding highly correlated movements in the two eyes. This compensatory behavior is extremely fast, persists with one eye patched, and results in image motion trajectories that are only partially correlated on the two retinas. These findings challenge established views of how humans acquire visual information. They show that ocular drift is precisely controlled, as long speculated [15], and imply the existence of neural mechanisms that integrate minute multimodal signals.