Abstract
We investigated the effect of acute levodopa administration on movement-related cortical oscillations and movement velocity in Parkinson's disease (PD). Patients with PD on and off medication and age- and sex-matched healthy controls performed a ballistic upper limb flexion movement as fast and accurately as possible while cortical oscillations were recorded with high-density electroencephalography. Patients off medication were also studied using task-based functional magnetic resonance imaging (fMRI) using a force control paradigm. Percent signal change of functional activity during the force control task was calculated for the putamen and subthalamic nucleus (STN) contralateral to the hand tested. We found that patients with PD off medication had an exaggerated movement-related beta-band (13–30 Hz) desynchronization in the supplementary motor area (SMA) compared to controls. In PD, spectral power in the beta-band was correlated with movement velocity. Following an acute dose of levodopa, we observed that the beta-band desynchronization in the SMA was reduced in PD, and was associated with increased movement velocity and increased voltage of agonist muscle activity. Further, using fMRI we found that the functional activity in the putamen and STN in the off medication state, was related to how responsive that cortical oscillations in the SMA of PD were to levodopa. Collectively, these findings provide the first direct evaluation of how movement-related cortical oscillations relate to movement velocity during the ballistic phase of movement in PD and demonstrate that functional brain activity in the basal ganglia pathways relate to the effects of dopaminergic medication on cortical neuronal oscillations during movement.
Highlights
Since the time of Woodworth's seminal studies in motor behavior, we have known that the two key phases in the performance of a voluntary movement are the ballistic phase and the corrective phase (Woodworth, 1899)
We found that greater functional magnetic resonance imaging (fMRI) blood oxygen level dependent (BOLD) signal in the putamen and subthalamic nucleus (STN) in the unmedicated state predicted a greater response of betaband cortical activity to dopaminergic medication
We showed in the current study how basal ganglia fMRI activity from the direct and indirect pathway is related to levodopa-induced changes in neuronal oscillations within the supplementary motor area (SMA) in Parkinson's disease (PD)
Summary
Since the time of Woodworth's seminal studies in motor behavior, we have known that the two key phases in the performance of a voluntary movement are the ballistic phase and the corrective phase (Woodworth, 1899). The acceleration and magnitude of the initial EMG burst has been shown to scale with movement velocity (Gottlieb et al, 1989). In patients with PD who perform a ballistic movement, the typical triphasic pattern is altered, with fractionated agonist EMG bursts that are marked by reduced agonist burst duration and magnitude, and an increase in the number of triphasic burst cycles. Dopaminergic medication and deep brain stimulation (DBS) of the subthalamic nucleus (STN) have been shown to increase the voltage of the first agonist burst and reduce fractionation of agonist activity (Hallett et al, 1975; Pfann et al, 2001; Vaillancourt et al, 2004). While there has been considerable focus on EMG activity during a ballistic movement, we know far less about how brain activity changes during a ballistic movement in patients with PD
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