A model of rhythm production and rhythmic auditory stimulation in healthy and Parkinsonian basal ganglia

In fMRI experiments, the basal ganglia is consistently activated by rhythmic action and sensorimotor synchronization to a metronome, and conditions like Parkinson’s Disease that affect basal ganglia and its dopaminergic modulation are experimentally seen to affect performance on both types of task. However, it is not clear what role this circuit or dopaminergic modulation play during rhythm production and synchronization tasks. Here, we propose that the basal ganglia may specify, maintain, and adapt the tempo with which rhythmic action (e.g. finger tapping or walking) is performed. We build a model based on previous “action selection” models of the cortico-basal-ganglia loop, altered such that cortico-basal-ganglia loops correspond not to distinct actions but to a continuum of possible action tempi. During rhythm production, an initial tempo is selected by cortical input, and rhythmic action can be automatized to continue in the absence of cortical input if tonic dopamine levels in striatum are sufficiently high. When striatal dopamine is reduced, our model reproduces two key features of dopamine deprivation in Parkinson’s disease: freezing of gait, and increased variation in produced intertap intervals during rhythmic tapping. By reanalyzing data from a recent experiment with Parkinsonian patients, we confirm the model’s prediction that increased interval variability should be largely attributable to increased tempo drift (rather than, e.g., increased timekeeper noise). This model of rhythm production is the first to invoke specific features of basal ganglia circuitry. It augments existing models of action selection in basal ganglia with the addition of continuous action parameters, and in doing so provides a starting point for further modeling of action timing and rhythm in the motor system. It offers a new model of the mechanism by which rhythmic auditory stimulation supports gait in Parkinson’s patients, and makes a new, testable prediction about sensorimotor synchronization under conditions of low tonic dopamine.