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

Abstract

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 (Masselink & Lappe, 2021). Besides motor recalibration of the inverse model (1), learning also comprises per-ceptual recalibration of the visuospatial target map (2) and of a forward dynamics model that estimates the saccade size from corollary discharge (3). 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 visuospatial target map and of the inverse model while the forward dynamics model is well informed about the reduced saccade change. Moreover, patients showed 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 visuospatial target map and of the inverse model, especially by control of saccade duration. The forward dynamics model and long-term perceptual learning are computed outside of the cerebellum.