Spontaneous, synchronized, and corrective timing behavior in cerebellar lesion patients

Abstract

To successfully navigate through and interact with a dynamic environment it is necessary to acquire and use adequate temporal information to guide behavior. Apart from several areas in the cerebral cortex and cortico-striatal networks, the cerebellum has been proposed to engage in the processing of temporal information. Damage to the cerebellum can impair precise event-based temporal processing in motor and non-motor behavior. To further substantiate cerebellar contributions to temporal processing and to explore its specific role in adapting to a dynamic environment, we investigated sensorimotor temporal processing in ten patients with cerebellar lesions and a corresponding number of healthy matched controls. Experimental tasks included simple self-paced repetitive finger-tapping (spontaneous motor tempo), temporally non-adaptive (isochronous pacing) and adaptive (tempo-changing pacing) sensorimotor synchronization with auditory sequences (synchronization-continuation tapping), and a perceptual tempo judgment. The results indicate that patients’ performance diverges systematically from controls on several measures. Cerebellar patients demonstrate more variable self-paced tapping, larger negative asynchronies when synchronizing with isochronous pacing sequences, altered automatic error correction responses to tempo changes (phase correction), and decreased perceptual sensitivity to these perturbations, especially for small accelerations. These findings confirm imprecise temporal processing in cerebellar patients, and hint at a specific impairment in the tens-of-milliseconds range preceding critical events, in line with a temporally predictive account of cerebellar function. Moreover, this cerebellar profile complements previous findings concerning dysfunctional temporal processing in basal ganglia patients assessed with the same experimental setup, suggesting structural and functional differentiation within an integrative temporal processing network.