Neural and behavioral dynamics of encoding, production and synchronization with external rhythms in subcortical lesion patients

Abstract

Acting in and adapting to a dynamically changing environment necessitates precise encoding of the timing of unfolding sensory events in our environment, and to time of our own (re-)actions to them. Cerebellar (CE) and basal ganglia (BG) circuitries play fundamental and complementary roles in timing processes. While the CE seems to encode the precise timing of sensory events (when an event occurs), the BG engage in generating temporal predictions (when a next event occurs). However, their contributions are rarely investigated in combination, as it is generally difficult to record data from respective patient groups in parallel. Here we investigated the causal roles of CE and BG in sensory and sensorimotor timing processes. Healthy controls and patients with CE or BG lesions listened to isochronous auditory sequences while their EEG was recorded and later performed a tapping synchronization task. We assessed intra- and inter-individual variabilities, as well as group differences, using event-related responses, delta-band inter-trial phase-coherence and acceleration dynamics while tuning to the stimulation frequency (Sf). CE and BG lesions increased variability in ERP latency and reduced the coherence of delta-band activity. CE but not BG lesions further impacted the stability of delta-band oscillations while tuning to the Sf. These findings show a causal link between subcortical lesions and the capacity to encode and synchronize ongoing neural activity with temporal regularities in the acoustic environment, but do not fully dissociate the specific contributions of the BG and the CE to processing sound in isochronous contexts.