Short-term adaptation of the phase of the vestibulo-ocular reflex (VOR) in normal human subjects

We investigated the effects of short-term vestibulo-ocular reflex (VOR) adaptation on the gain and phase of the VOR, and on eccentric gaze-holding in darkness, in five normal human subjects. For 1 h, subjects sat in a chair that rotated sinusoidally at 0.2 Hz while surrounded by a visual stimulus (optokinetic drum). The drum was rotated relative to the chair, to require a VOR with either a phase lead or lag of 45 deg (with respect to a compensatory phase of zero) with no change in gain, or a gain of 1.7 or 0.5 with no change in phase. Immediately before and after each training session, VOR gain and phase were measured in the dark with 0.2 Hz sinusoidal rotation. Gaze-holding was evaluated following 20 deg eccentric saccades in darkness. Adaptation paradigms that called only for a phase lead produced an adapted VOR with 33% of the required amount of phase change, a 20% decrease in VOR gain, and an increased centripetal drift after eccentric saccades made in darkness. Adaptation paradigms that called for a phase lag produced an adapted VOR with 29% of the required amount of phase change, no significant change in VOR gain, and a centrifugal drift after eccentric saccades. Adaptation paradigms requiring a gain of 1.7 produced a 15% increase in VOR gain with small increases in phase and in centripetal drift. Adaptation paradigms requiring a gain of 0.5 produced a 31% decrease in VOR gain with a 6 deg phase lag and a centrifugal drift. The changes in drift and phase were well correlated across all adaptation paradigms; the changes in phase and gain were not. We attribute the effects on phase and gaze-holding to changes in the time constant of the velocity-to-position ocular motor neural integrator. Phase leads and the corresponding centripetal drift are due to a leaky integrator, and phase lags and the corresponding centrifugal drift are due to an unstable integrator. These results imply that in the short-term adaptation paradigm used here, the control of drift and VOR phase are tightly coupled through the neural integrator, whereas VOR gain is controlled by another mechanism.