Smooth pursuit adaptation (SPA) exhibits features useful to compensate changes in the properties of the smooth pursuit eye movement system due to usage

Smooth-pursuit adaptation (SPA) refers to the fact that pursuit gain in the early, still open-loop response phase of the pursuit eye movement can be adjusted based on experience. For instance, if the target moves initially at a constant velocity for ~100–200 ms and then steps to a higher velocity, subjects learn to up-regulate the pursuit gain associated with the initial target velocity (gain-increase SPA) in order to reduce the retinal error resulting from the velocity step. Correspondingly, a step to a lower target velocity leads to a decrease in gain (gain-decrease SPA). In this study we demonstrate that the increase in peak eye velocity during gain-increase SPA is a consequence of expanding the duration of the eye acceleration profile while the decrease in peak velocity during gain-decrease SPA results from reduced peak eye acceleration but unaltered duration. Furthermore, we show that carrying out stereotypical smooth pursuit eye movements elicited by constant velocity target ramps for several hundred trials (=test of pursuit resilience) leads to a clear drop in initial peak acceleration, a reflection of oculomotor and/or cognitive fatigue. However, this drop in acceleration gets compensated by an increase in the duration of the acceleration profile, thereby keeping initial pursuit gain constant. The compensatory expansion of the acceleration profile in the pursuit resilience experiment is reminiscent of the one leading to gain-increase SPA, suggesting that both processes tap one and the same neuronal mechanism warranting a precise acceleration-duration trade-off. Finally, we show that the ability to adjust acceleration duration during pursuit resilience depends on the integrity of the oculomotor vermis (OMV) as indicated by the complete loss of the duration adjustment following a surgical lesion of the OMV in one rhesus monkey we could study.