Neural and behavioral entrainment to auditory rhythmic perturbations in persons with cerebellar impairment

Abstract

The cerebellum plays a key role in temporal processing, as demonstrated by sensorimotor synchronization paradigms. This study extends findings by investigating behavioral and neural adaptation to unpredictable auditory perturbations. Sixteen persons with cerebellar impairment and sixteen healthy controls performed a listening (60 seconds) and a finger-tapping task (465 seconds) to a metronome set at 1.67 Hz: the first 60 seconds were without perturbations, followed by 40 perturbations (+/- 10% period changes). Event-related frequency adjustments (ERFA) were derived from finger-tapping and electroencephalography recordings, yielding 3 event-related frequency adjustments: one behavioral and two neural (perceptual and sensorimotor components). Mean behavioral adaptation to the perturbations was similar in both groups (P < 0.001). Neural tracking was evident in the sensorimotor component but not in the perceptual component in both groups, for both positive (P = 0.005) and negative (P = 0.003) directions. Neural tracking was significantly reduced in persons with cerebellar impairment compared to healthy controls, particularly in response to negative perturbation in the sensorimotor component (P = 0.02). Persons with cerebellar impairment demonstrates spared yet dissociative adaptation with intact behavioral yet hindered neural dynamics. The results suggest parallel yet distinct mechanisms for processing covert and overt responses underlying sensorimotor adaptation. Findings indicate a potential use of spared behavioral adaptation mechanisms in the rehabilitation of persons with cerebellar impairment through rhythm-based interventions.