Closed loop motor-sensory dynamics in human vision

Abstract

Vision is obtained with a continuous motion of the eyes. The kinematic analysis of eye motion, during any visual or ocular task, typically reveals two (kinematic) components: saccades, which quickly replace the visual content in the retinal fovea, and drifts, which slowly scan the image after each saccade. While the saccadic exchange of regions of interest (ROIs) is commonly considered to be included in motor-sensory closed-loops, it is commonly assumed that drifts function in an open-loop manner, that is, independent of the concurrent visual input. Accordingly, visual perception is assumed to be based on a sequence of open-loop processes, each initiated by a saccade-triggered retinal snapshot. Here we directly challenged this assumption by testing the dependency of drift kinematics on concurrent visual inputs using real-time gaze-contingent-display. Our results demonstrate a dependency of the trajectory on the concurrent visual input, convergence of speed to condition-specific values and maintenance of selected drift-related motor-sensory controlled variables, all strongly indicative of drifts being included in a closed-loop brain-world process, and thus suggesting that vision is inherently a closed-loop process. Author summaryOur eyes do not function like cameras; it has long been known that we are actively scanning our visual environment in order to see. Moreover, it is commonly accepted that our fast eye movements, saccades, are controlled by the brain and are affected by the sensory input. However, our slow eye movements, the ocular drifts, are often ignored when visual acquisition is analyzed. Accordingly, visual processing is typically assumed to be based on computations performed on saccade-triggered snapshots of the retinal state. Our work strongly challenges this model and provides significant evidence for an alternative model, a cybernetic one. We show that the dynamics of the ocular drifts do not allow, and cannot be explained by, open loop visual acquisition. Instead, our results suggest that visual acquisition is part of a closed-loop process, which dynamically and continuously links the brain to its environment.