PROJECT SUMMARY Human eyes are never at rest. Gaze redirections normally occur 2-3 times/second, separating periods of small, incessant eye movements. At first glance, the function of eye movements seems obvious: they are necessary to bring and maintain the object of interest within the foveola, the highest acuity region of the retina. However, an overwhelming body of evidence, in part coming from our NIH-funded research, indicates that this view is simplistic and that, by reformatting a spatial scene into a spatiotemporal stimulus on the retina, eye movements serve fundamental visual functions beyond just orienting the foveola. Here we test several new hypotheses concerning less-obvious but equally critical roles for three main kinds of eye movements: saccades, pursuit, and fixational drift (the eye jitter that continually occurs during fixation). The research strategy consists of evaluating the effect of eye movements on the retinal input and the resulting consequences for neural coding, perception, and control. The experiments rely on state-of-the-art high-resolution measurements of human eye movements and gaze-contingent control of retinal stimulation. All experiments are supported by mathematical modeling of visual input signals and neural modeling of their encoding consequences. Aim 1 focuses on the physiological alternation between saccades and fixational drift. Stereotyped, saccade-induced transients are followed by stereotyped, but distinct, periods of Brownian-like jitter of the retinal image. Our preliminary analyses show that this alternation repackages the energy of natural scenes into different spatiotemporal formats, cyclically varying amplification and spectral distribution within the temporal sensitivity bandwidth of retinal neurons. The predicted outcomes are oculomotor-driven dynamics of visual sensitivity, discrimination, and form perception during natural post- saccadic fixation, which we will quantify and test. Aim 2 focuses on the saccades themselves. We predict that, as a consequence of a saccade, the spectral density of the visual input effective in driving retinal neurons at fixation onset is equalized up to a cut-off spatial frequency that depends on the saccade amplitude. This effect further constrains visual dynamics and implies that visual coding during early fixation depends on the amplitude of the preceding saccade. It also suggests that the visual system can exploit this tuning according to the task. We will test these predictions by isolating the contributions of saccade transients in a variety of low- and high-level visual tasks. Aim 3 further generalizes these ideas. Building on our modeling work, it examines whether fixational drift can also be adjusted to tune visual sensitivity to the task demands, and whether the alternation between pursuit movements and “catch-up” saccades during visual tracking plays a role similar to that of saccade/drift cycle for static targets. All our hypotheses are supported by preliminary d...