Basal ganglia and cerebellar lesions causally impact the neural encoding of temporal regularities

基底神经节和小脑病变会对时间规律的神经编码产生因果影响

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Abstract

Acting in and adapting to a dynamically changing environment necessitates to precisely encode thetimingof sensory events, and totimeour 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 use precise timing (whenan event occurs) and temporal intervals to generate temporal predictions (whena next event occurs), the BG uses relative timing to extract the beat in rhythmic sequences. As it is generally difficult to record data from respective patient groups in parallel, CE and BG contributions to timing processes are rarely investigated in combination. Here, we let healthy controls and patients with CE or BG lesions listen to isochronous auditory sequences while their EEG was recorded. We assessed intra- and inter-individual variabilities, as well as group differences, using event-related potentials (ERP), 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 theSf. 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. While moststandardmetrics of neural entrainment do not dissociate specific contributions of BG and CE to sound processing in isochronous sequences, the newly introduced 'stability' metric isolated distinct changes in delta-band tuning dynamics in CE patients. This observation highlights the fundamental role of the CE in generating and maintaining stable neural representations of event onsets in the sensory environment.

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