Human Cortico-Cerebellar Dynamics During Motor Error Processing After Stroke

The cerebellum acts as a forward internal model to predict motor outcomes, compare them with sensory feedback, and generate prediction errors that refine prediction accuracy. Our physiological understanding of cerebellar function during motor control derives predominantly from animal experiments and clinical observations in patients with disorders of the cerebellum or its connections with the cerebrum and spinal cord. Here, we report a human electrophysiology-based investigation of cerebello-thalamo-cortical pathway activity during motor error detection and correction. Participants performed a computerized motor oddball task while synchronized electrophysiological recordings were collected from cerebellar dentate (DN) using depth electrodes and scalp electroencephalography (EEG). The task involved moving a 2-D ball on a screen toward a predetermined target at 40% (standard trials) or 20% (oddball trials) of their maximum voluntary contraction. Six participants completed an average of 239 trials, with oddball trials randomly occurring with a 30% frequency. At the cortex, oddball trials exhibited significantly greater centro-parietal error positivity and fronto-centro-parietal desynchronization during error correction, predominantly in the alpha and low beta frequency bands. DN examination also revealed greater alpha and low beta desynchronization during error correction. Lastly, oddball trials showed significantly greater cortico-cerebellar coherence during error correction in the same frequency bands with bidirectional interaction between the cortex and DN. These findings expand on the cortico-cerebello-cortical physiology of human motor control and provide cues for designing interventions aimed at alleviating the functional burdens of acquired injuries of the central nervous system.