Abstract
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.
Highlights
Smooth pursuit eye movements (SPEM) are used to stabilize the image of a moving object of interest on the fovea, allowing the observer to deploy the advantages of foveal vision for the scrutiny of the object in motion
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
Previous studies made similar observations for different velocity steps suggesting that kinematic changes associated with Smooth-pursuit adaptation (SPA) prevail across a wide velocity range (Takagi et al, 2000; Dash et al, 2013)
Summary
Smooth pursuit eye movements (SPEM) are used to stabilize the image of a moving object of interest on the fovea, allowing the observer to deploy the advantages of foveal vision for the scrutiny of the object in motion. The first 100–150 ms of the SPEM are driven by uncompensated retinal target image motion In other words, they reflect an open-loop response whose size depends solely on the visual target motion signal and a gain parameter that specifies the mapping of the visual information onto the motor response. The target moves at a constant velocity for ∼100–200 ms whereupon it steps to a different velocity In reaction to these velocity steps initial SPEM velocity changes such as to draw eye velocity evoked by the initial target velocity nearer to the target velocity after the velocity step. The stereotypic steps in target velocity able to evoke SPA hardly occur outside the laboratory This leads to the question what the ecological role of SPA might be? If patients with one paretic eye are asked to view with that eye while the healthy one is covered, after a few days of habituation, the normal eye may exhibit an increased SPEM
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