Vision and vestibular adaptation.

This article summarizes six recent degree-of-freedom studies of visual-vestibular interaction during natural activities and relates the findings to canal-otolith interactions evaluated during eccentric axis rotations. Magnetic search coils were used to measure angular eye and head movements of young and elderly subjects. A flux gate magnetometer was used to measure three-dimensional head translation. Three activities were studied: standing quietly, walking in place, and running in place. Each activity was evaluated with three viewing conditions: a visible target viewed normally, a remembered target in darkness, and a visible target viewed with x2 binocular telescopic spectacles. Canal-otolith interaction was assessed with passive, whole-body, transient, and steady-state rotations in pitch and yaw at multiple frequencies about axes that were either oculocentric or eccentric to the eyes. For each rotational axis, subjects regarded visible and remembered targets located at various distances. Horizontal and vertical angular vestibulo-ocular reflexes were demonstrable in all subjects during standing, walking, and running. When only angular gains were considered, gains in both darkness and during normal vision were less than 1.0 and were generally lower in elderly than in young subjects. Magnified vision with x2 telescopic spectacles produced only small gain increases as compared with normal vision. During walking and running all subjects exhibited significant mediolateral and dorsoventral head translations that were antiphase locked to yaw and pitch head movements, respectively. These head translations and rotations have mutually compensating effects on gaze in a target plane for typical viewing distances and allow angular vestibulo-ocular reflex gains of less than 1.0 to be optimal for gaze stabilization during natural activities. During passive, whole-body eccentric pitch and yaw head rotations, vestibulo-ocular reflex gain was modulated as appropriate to stabilize gaze on targets at the distances used. This modulation was evident within the first 80 msec of onset of head movement, too early to be caused by immediate visual tracking. Modeling suggests a linear interaction between canal signals and otolith signals scaled by the inverse of target distance. Vestibulo-ocular reflex performance appears to be adapted to stabilize gaze during translational and rotational perturbations that occur during natural activities, as is appropriate for relevant target distances. Although immediate visual tracking contributes little to gaze stabilization during natural activities, visual requirements determine the performance of vestibulo-ocular reflexes arising from both canals and otoliths.