Strategies for Gaze Stabilization Critically Depend on Locomotor Speed

Locomotion involves complex combinations of translational and rotational head movements. For gaze stability, this necessitates the interplay of angular and linear vestibulo-ocular reflexes (VOR) as well as the integration of visual feedback about the desired viewing distance. Furthermore, gaze stabilizing systems must be able to cope with vast differences in head motion brought about by changing locomotor speeds and patterns (walking vs. running). The present study investigated horizontal and vertical angular VOR (aVOR) and linear gaze stabilization (lGS) as well as compensation for linear head movements by angular counter rotation of the head during treadmill walking and running at different velocities (0.4 to 2.4 m/s) while fixating either a close (0.5 m) or distant (2.0 m) target. In the horizontal plane, the aVOR predominated throughout all locomotor speeds, whereas the compensation of linear translations was highly variable and generally insufficient. In contrast, in the vertical plane, eye and angular head motion steadily became more in phase with increasing locomotor speed, which served to optimize linear motion compensation. Furthermore, the timing of the vertical aVOR became more automated and independent of visual feedback during faster locomotion. Thus, horizontal and vertical gaze stabilization strategies appear to be considerably different. Whereas horizontal gaze control is likely governed by passive sensorimotor reflexes throughout all locomotor speeds, vertical gaze stabilization switches to an automated feed-forward control at faster locomotion. This switch is presumably driven by efference copies from spinal locomotor commands that were previously shown to govern gaze stabilization in animal models during stereotypic locomotion.