Functionally separated networks for self-paced and externally-cued motor execution in Parkinson's disease: Evidence from deep brain recordings in humans

Spatially segregated cortico-basal ganglia networks have been proposed for the control of goal-directed and habitual behavior. In Parkinson's disease, selective loss of dopaminergic neurons regulating sensorimotor (habitual) behavior might therefore predominantly cause deficits in habitual motor control, whereas control of goal-directed movement is relatively preserved. Following this hypothesis, we examined the electrophysiology of cortico-basal ganglia networks in Parkinson patients emulating habitual and goal-directed motor control during self-paced and externally-cued finger tapping, respectively, while simultaneously recording local field potentials in the subthalamic nucleus (STN) and surface EEG. Only externally-cued movements induced a pro-kinetic event-related beta-desynchronization, whereas beta-oscillations were continuously suppressed during self-paced movements. Connectivity analysis revealed higher synchronicity (phase-locking value) between the STN and central electrodes during self-paced and higher STN to frontal phase-locking during externally-cued movements. Our data provide direct electrophysiological support for the existence of functionally segregated cortico-basal ganglia networks controlling motor behavior in Parkinson patients, and corroborate the assumption of Parkinson patients being shifted from habitual towards goal-directed behavior.