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

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. Author summaryAchieving a fine-grained understanding of how the cerebellum continuously recalibrates our movements is an ongoing challenge in sensorimotor neuroscience. Recently, we showed that recalibration of saccadic eye movements does not only operate in motor space, i.e. by adjusting the motor command, but also in external and internal visual space, i.e. by adjusting the spatial representation of the target and the internal saccade size. For this purpose, (1) we developed a paradigm that allowed us to monitor changes of the internal saccade size estimated from trans-saccadic target localizations, and (2) we unified the three learning processes in one computational modeling framework. Here we apply this approach to the saccade learning data of patients with a neurodegenerative cerebellar disease. First, we dissociate the cerebellar role in recalibration of the three sites of learning. Second, we show how learning is transposed to saccade kinematics. Third, we provide first insights into the perceptual consequences of cerebellar pathology that, according to our model, may be a mechanism to recover from disease-specific motor deficits. Our modeling framework may help to dissociate the contribution of specific sensorimotor areas to adaptive behavior as well as to improve the understanding of learning deficits and compensatory strategies in the clinical context.