Human eye-head co-ordination in natural exploration

Abstract

During natural behavior humans continuously adjust their gaze by moving head and eyes, yielding rich dynamics of the retinal input. Sensory coding models, however, typically assume visual input as smooth or a sequence of static images interleaved by volitional gaze shifts. Are these assumptions valid during free exploration behavior in natural environments? We used an innovative technique to simultaneously record gaze and head movements in humans, who freely explored various environments (forest, train station, apartment). Most movements occur along the cardinal axes, and the predominance of vertical or horizontal movements depends on the environment. Eye and head movements co-occur more frequently than their individual statistics predicts under an independence assumption. The majority of co-occurring movements point in opposite directions, consistent with a gaze-stabilizing role of eye movements. Nevertheless, a substantial fraction of eye movements point in the same direction as co-occurring head movements. Even under the very most conservative assumptions, saccadic eye movements alone cannot account for these synergistic movements. Hence nonsaccadic eye movements that interact synergistically with head movements to adjust gaze cannot be neglected in natural visual input. Natural retinal input is continuously dynamic, and cannot be faithfully modeled as a mere sequence of static frames with interleaved large saccades.