Task-dependent head-eye coordination during natural fixation

Abstract

Humans acquire visual information by continually moving their eyes and head. Pioneering studies reported that, during natural fixation, head-eye coordination is tuned according to the task to yield a suitable amount of retinal image motion (Steinman, 1986). But what type of motion is suited for a given task? Recent experiments indicate that structuring the temporal luminance flow impinging onto the retina is an important function of eye movements. In high-acuity tasks, observers tune their fixational eye drifts so that the luminance modulations delivered within the range of temporal sensitivity enhance high spatial frequencies (Intoy & Rucci, 2020). To resolve minute eye movements, in these previous experiments, the head of the observer was strictly immobilized. Here we use a new custom device to examine how retinal image motion varies across tasks during natural head-free fixation. We recorded head and eye movements by means of scleral coils and passive markers, using an apparatus that integrated a motion capture system (OptiTrack) with a specially designed coil system with three highly uniform, oscillating, magnetic fields. Human observers (N=8) conducted a set of natural tasks, which included visual search, sorting objects by color, an acuity test, and sustained fixation on markers. Our results confirm that head-eye fixational coordination changes systematically across tasks. Critically, we show that changes in motor activity alter the information content of visual input signals by modulating the distribution of spatial frequency power delivered within the bandwidth of human temporal sensitivity. That is, humans jointly coordinate fixational head and eye movements according to the tasks’ demands in ways that emphasize the relevant spatial frequency range in the temporal luminance flow. These results indicate that that task-dependent tuning of head-eye coordination effectively acts as a selection mechanism in spatial frequency.