Rapid switching of vestibulo-motor pathways through voluntary eyelid closure in primates

Understanding how the brain adjusts movement control based on context is key to explaining adaptive behavior. The vestibulo-ocular reflex (VOR), with its well-defined circuitry, demonstrates adaptability-its primary role in stabilizing vision is suppressed when gaze redirection is required but remains resilient even in complete darkness. Here, we investigated VOR responses during intentional eye closure, when the need for visual stabilization is volitionally removed. Using scleral search coils, we measured human VOR responses and found a rapid ~36-90% reduction across movement directions when participants voluntarily closed their eyes, indicating a broad disruption of VOR pathways. This attenuation coincided with eyelid closure and persisted until the eyes reopened. Parallel experiments in monkeys confirmed these findings, ruling out mechanical factors and revealing a conserved neural mechanism across primates. Moreover, attempts to open restrained eyelids increased VOR gains, suggesting that motor commands for eye opening influence vestibular processing even without eyelid movement. These results demonstrate rapid, sustained VOR suppression linked to eyelid motor control, highlighting an energy-efficient neural strategy that dynamically adjusts sensory-motor processing when visual stabilization is certain to be unnecessary.