A triple distinction of cerebellar function for oculomotor learning and fatigue compensation

by Jana Masselink, Alexis Cheviet, Caroline Froment-Tilikete, Denis Pélisson, Markus Lappe

The cerebellum implements error-based motor learning via synaptic gain adaptation of an inverse model, i.e. the mapping of a spatial movement goal onto a motor command. Recently, we modeled the motor and perceptual changes during learning of saccadic eye movements, showing that learning is actually a threefold process. Besides motor recalibration of (1) the inverse model, learning also comprises perceptual recalibration of (2) the visuospatial target map and (3) of a forward dynamics model that estimates the saccade size from corollary discharge. Yet, the site of perceptual recalibration remains unclear. Here we dissociate cerebellar contributions to the three stages of learning by modeling the learning data of eight cerebellar patients and eight healthy controls. Results showed that cerebellar pathology restrains short-term recalibration of the inverse model while the forward dynamics model is well informed about the reduced saccade change. Adaptation of the visuospatial target map trended in learning direction only in control subjects, yet without reaching significance. Moreover, some patients showed a tendency for uncompensated oculomotor fatigue caused by insufficient upregulation of saccade duration. According to our model, this could induce long-term perceptual compensation, consistent with the overestimation of target eccentricity found in the patients’ baseline data. We conclude that the cerebellum mediates short-term adaptation of the inverse model, especially by control of saccade duration, while the forward dynamics model was not affected by cerebellar pathology.