Summary
Eye position changes subtly even when perfect gaze fixation is attempted [1-5]. Such “fixational” eye movement comes in two primary flavors: microsaccades, which resemble large saccades [6-8] and rapidly shift gaze position by a minute amount; and ocular position drifts, which are even smaller and slower movements [1, 2, 4, 5, 9-13]. The mechanisms for generating and influencing microsaccades have received much attention [6, 14, 15]. Despite contrary ideas in the past century, a now accepted property of microsaccades is that, like larger saccades, they are not random but are very systematically [16-24] and rapidly [19-21, 25, 26] influenced by peripheral as well as foveal visual stimuli, among other factors [14, 27]. In stark contrast, the brain mechanisms for controlling ocular position drifts are unknown; these movements continue to be thought of as random, often being modeled as random walk processes [28-32]. Here we used precise eye tracking in three well trained rhesus macaque monkeys to show that ocular position drifts can exhibit highly systematic stimulus-driven modulations in both speed and direction. These modulations have a very short latency, and they are stimulus-tuned, binocular, and independent of convergence responses or starting eye positions. Their amplitudes are sufficient to move images across individual cone photoreceptors in the fovea or multiple rod photoreceptors in some peripheral zones. Our results, coupled with evidence that drift statistics adapt to a variety of behavioral task constraints [13, 26, 33-35], strongly motivate deeper research into the neurophysiological mechanisms controlling incessant ocular position drifts in between saccades.