Greater movement-type selectivity in the striatum than in the cerebellum during rhythm processing

During rhythm perception, accurate processing of temporal structure is essential for predicting when a stimulus will occur and for preparing appropriate actions. Subcortical circuits, particularly the cerebellum and basal ganglia, are known to play central roles in temporal processing, yet how neuronal activity in these structures supports sensory prediction and action preparation remains unclear. Specifically, it is unknown whether timing-related signals during rhythm perception are linked to specific movements or are movement invariant. To address this issue, we recorded single-neuron activity from the cerebellar dentate nucleus and the caudate nucleus while four monkeys (three males and one female) performed a rhythmic timing task. Animals observed isochronously presented visual stimuli and reported either a stimulus omission or a color deviation by generating an eye or hand movement. Behavioral performance indicated that the saccade task was more demanding, with a higher rate of premature responses, particularly during omission detection. Neurons in both structures exhibited periodic modulation during stimulus repetition, but with distinct properties. In the dentate nucleus, rhythmic activity was less dependent on movement type, whereas striatal neurons exhibited stronger movement-type selectivity. Population decoding further revealed that striatal activity more accurately predicted movement type, whereas cerebellar activity more accurately represented stimulus timing, and these temporal representations generalized more readily across movement types. These findings suggest that rhythmic activity in the striatum is more closely linked to motor preparation, whereas cerebellar activity provides a more movement-invariant representation that may contribute to the formation of an internal model of rhythmic stimulus sequence. Significance statement When we perceive rhythm, our body often moves in synchrony. Previous studies have shown that the cerebellum and striatum are active during rhythm perception even without overt movement, possibly because the brain is periodically preparing or rehearsing movements. We recorded single-neuron activity in monkeys while they predicted the timing of regularly flashing visual stimuli. Neurons in the cerebellum exhibited robust rhythmic modulation that predicted stimulus timing and was relatively independent of the upcoming movement. In contrast, periodic activity in the striatum varied depending on whether an eye or hand movement was being prepared. These results shed light on how the brain represents rhythm and may help explain rhythm-related impairments in neurological disorders such as Parkinson’s disease and cerebellar ataxia.