Selective suppression of the vestibulo-ocular reflex during human locomotion

In lower vertebrates, gaze stabilization during locomotion is at least partially driven by a direct coupling of spinal locomotor commands with extraocular motor signals. To what extent locomotor feed-forward mechanisms contribute to gaze stabilization during human locomotion is yet unknown. In principle, the feasibility of a feed-forward regulation of gaze during locomotion should critically depend on the spatiotemporal coupling between body and head kinematics and hence the internal predictability of head movements (HMP). The present study thus investigated whether changes in eye-head coordination during human locomotion can be explained by concurrent changes in HMP.

Eye and head movements were recorded at different locomotor speeds in light and darkness to obtain the gain and phase of the horizontal and vertical angular VOR (aVOR). Potential correlations between aVOR performance and HMP were analyzed in dependence of locomotor speed and gait cycle phase.

Horizontal aVOR responses persisted independent of locomotor speed. In contrast, with increasing locomotor speed vertical eye-head coordination switched from a VOR-driven compensatory mode to a synergistic behavior where head and eyes move in phase. Concurrently, vertical HMP increased with faster locomotion. Furthermore, modulations in vertical aVOR gain across the gait cycle corresponded to simultaneous alterations in vertical HMP.

The vertical aVOR appears to be suppressed during faster walking and running, whereas at the same time, the predictability of resultant head movements increases. This suggests that during stereotyped human locomotion, internal feed-forward commands supplement or even suppress sensory feedback to mediate gaze stabilization in the vertical plane.