Gaze stabilization and dynamic visual acuity across human locomotion speeds

Gaze stabilization during human locomotion requires precise coordination between eye and head movements to maintain visual acuity. Yet how the resultant eye-head coordination patterns relate to visual performance remains incompletely understood. Here, we investigated how locomotion-dependent changes in head-eye coordination relate to dynamic visual acuity (DVA) across walking and running speeds (0.4-2.4 m/s). Twenty-eight healthy participants walked or ran on a treadmill while fixating a visual target, with simultaneous recordings of eye movements (video-oculography), head kinematics (motion capture), and DVA using an adaptive Landolt-C task. We assessed three complementary gaze stabilization mechanisms reflecting compensation of head rotations, compensation of head translations by head rotations, and compensation of head translations by combined eye-head movements, and calculated their gain and phase characteristics and resultant retinal image slip across gait cycles. With increasing locomotion speed, DVA progressively declined, alongside a pronounced, plane-specific reorganization of head-eye coordination. While horizontal eye movements continued to oppose head rotations across locomotion speeds, vertical eye movements progressively shifted from opposing to moving in phase with head rotations, indicating a transition from compensatory to synergistic coordination. This reorganization was closely linked to increasing translational head motion and was most strongly associated with visual performance. Retinal image slip increased with speed, particularly vertically, and was strongly related to DVA. These findings demonstrate that gaze stabilization during locomotion is driven by speed- and plane-dependent eye-head coordination patterns, with vertical head kinematics and the effectiveness of their compensation by eye-head coordination being key determinants of visual acuity.