Predictive mechanisms of head-eye coordination and vestibulo-ocular reflex suppression in humans

Abstract

Head and eye movements of human subjects have been recorded during head-free pursuit in the horizontal plane of a target executing sinusoidal motion at a frequency of 0.26 to 0.78 Hz and a peak velocity of +/- 96 degrees/s. The target was not presented continuously but was exposed for brief durations of 120 to 320 ms as it passed through the centre of the visual field at peak velocity. This technique allowed the timing of each response to be assessed in relation to the onset of target appearance. During the first 3 to 4 target presentations, there was a progressive buildup of both head velocity and the smooth component of gaze velocity, while, simultaneously, the responses became more phase-advanced with respect to target onset. In the steady state, similar temporal response trajectories were observed for head and gaze velocity, which were initiated approximately 500 ms prior to target onset, rose to a peak that increased with the duration of target exposure, and then decayed with a time constant of 0.5 to 1 s. Whenever the target failed to appear as expected, the gaze and head velocity trajectories continued to be made, indicating that predictive suppression of the vestibulo-ocular reflex (VOR) was taking place in darkness. In a further experiment, subjects attempted to suppress the VOR during whole body oscillation at 0.2 or 0.4 Hz on a turntable by fixating a head-fixed target that appeared for 10 to 160 ms at the time of peak head velocity. Again, VOR suppression was initiated prior to target appearance in the same manner as for natural head movements, and when the target suddenly disappeared but rotation continued, predictive VOR suppression was observed in darkness. The similarity of these predictive effects to those obtained previously for head-fixed pursuit provides further support for the hypothesis that both pursuit and visual suppression of the VOR are controlled primarily by identical visual feedback mechanisms.