Fixational eye movements as active sensation for high visual acuity

Abstract

Perception and action are inherently entangled: our world view is shaped by how we explore and navigate our environment through complex and variable self-motion. Even when fixating on a stable stimulus, our eyes undergo small, involuntary movements. Fixational eye movements (FEM) render a stable world jittery on our retinae, which contributes noise to neural coding. Yet, empirical evidence suggests that FEM help rather than harm human perception of fine detail. Here, we elucidate this paradox by uncovering under which conditions FEM improve or impair retinal coding and human acuity. We combine theory and experiment: model accuracy is directly compared to that of healthy human subjects in a visual acuity task. Acuity is modeled by applying an ideal Bayesian classifier to simulations of retinal spiking activity in the presence of FEM. In addition, empirical FEM are monitored using high-resolution eye-tracking by an adaptive optics scanning laser ophthalmoscope. While FEM introduce noise, they also effectively pre-process visual inputs to facilitate retinal information encoding. Based on an interplay of these mechanisms, our model predicts a relation between visual acuity, FEM amplitude, and single-trial stimulus size that quantitatively accounts for experimental observations and captures the beneficial effect of FEM. Moreover, we observe that human subjects FEM statistics vary with stimulus size, and our model suggests that changing eye motion amplitude, as the subjects indeed do, enhances acuity as compared to maintaining eye motion size constant. Overall, our findings indicate that perception benefits from action even at the fine and noise-dominated spatio-temporal scale of FEM. Significance StatementPerception is inherently active: we need to move our eyes to see the world around us. Yet our eyes also undergo tiny, unconscious movements that can blur out fine visual details. Paradoxically, previous work suggested that these small movements aid fine detail perception. Here, we investigate this paradox to uncover in which contexts small eye movements help or harm visual acuity. Comparing a model of retinal responses with recordings of human visual acuity, we elucidate the mechanisms by which and conditions in which small eye movements support fine detail discrimination. Our results also suggest that varying eye movement amplitude according to stimulus size enhances retinal coding, highlighting that perception is active even at the level of very fine eye movements.