Vestibular Function Drives Gaze Stability in Locomoting Macaques

Abstract

Stable gaze is essential for effective navigation, yet during locomotion each stride generates phasic head movements that can destabilize the visual scene. The vestibular system is well positioned to counter these disturbances by sensing head motion and rapidly generating reflexive compensatory eye movements, but its specific contribution to gaze stabilization during locomotion is not well understood. To directly test the vestibular system's contribution during walking, we compared gait and gaze kinematics in male and female rhesus macaques with normal vestibular function and those with chronic bilateral vestibular loss (BVL) during treadmill walking at multiple speeds and during overground locomotion. We found that BVL animals showed systematic gait abnormalities, including markedly increased gait variability across conditions. Gaze stabilization deficits were equally pronounced: normal monkeys effectively stabilized gaze across conditions, whereas BVL animals exhibited reduced and more variable eye movements that failed to compensate for head motion. Vestibular loss increased the magnitude of reorienting eye movements, consistent with an increased tolerance for gaze position error. Extending established oculomotor models to incorporate intrinsic noise and elevated error thresholds reproduced these behavioral signatures, revealing that chronic vestibular loss drives a fundamental recalibration of gaze control strategies. Together, these findings demonstrate that vestibular input provides a central scaffold for stabilizing gaze and gait during natural locomotion and establish essential behavioral benchmarks for future neural, rehabilitative, and prosthetic interventions.