Optimal Human Passive Vestibulo-Ocular Reflex Adaptation Does Not Rely on Passive Training

The vestibulo-ocular reflex (VOR) is the main vision-stabilising system during rapid head movements in humans. A visual-vestibular mismatch stimulus can be used to train or adapt the VOR response because it induces a retinal image slip error signal that drives VOR motor learning. The training context has been shown to affect VOR adaptation. We sought to determine whether active (self-generated) versus passive (externally imposed) head rotation vestibular training would differentially affect adaptation and short-term retention of the active and passive VOR responses. Ten subjects were tested, each over six separate 1.5-h sessions. We compared active versus passive head impulse (transient, rapid head rotations with peak velocity ~ 150 °/s) VOR adaptation training lasting 15 min with the VOR gain challenged to increment, starting at unity, by 0.1 every 90 s towards one side only (this adapting side was randomised to be either left or right). The VOR response was tested/measured in darkness at 10-min intervals, 20-min intervals, and two single 60-min interval sessions for 1 h post-training. The training was active or passive for the 10- and 20-min interval sessions, but only active for the two single 60-min interval sessions. The mean VOR response increase due to training was ~ 10 % towards the adapting side versus ~2 % towards the non-adapting side. There was no difference in VOR adaptation and retention between active and passive VOR training. The only factor to affect retention was exposure to a de-adaptation stimulus. These data suggest that active VOR adaptation training can be used to optimally adapt the passive VOR and that adaptation is completely retained over 1 h as long as there is no visual feedback signal driving de-adaptation.