Abstract
In Parkinson's disease patients in the OFF medication state, basal ganglia local field potentials exhibit changes in beta and gamma oscillations that correlate with reduced voluntary movement, manifested as rigidity and akinesia. However, magnetoencephalography and low-resolution electrocorticography (ECoG) studies in Parkinson's patients suggest that changes in sensorimotor cortical oscillations differ from those of the basal ganglia. To more clearly define the role of sensorimotor cortex oscillatory activity in Parkinson's, we performed intraoperative, high-resolution (4 mm spacing) ECoG recordings in 10 Parkinson's patients (2 females, ages 47–72) undergoing deep brain stimulation (DBS) lead placement in the awake, OFF medication state. We analyzed ECoG potentials during a computer-controlled reaching task designed to separate movement preparation from movement execution and compared findings to similar invasive recordings in eight patients with essential tremor (3 females, ages 59–78), a condition not associated with rigidity or akinesia. We show that (1) cortical beta spectral power at rest does not differ between Parkinson's and essential tremor patients (p = 0.85), (2) early motor preparation in Parkinson's patients in the OFF medication state is associated with a larger beta desynchronization compared to patients with essential tremor (p = 0.0061), and (3) cortical broadband gamma power is elevated in Parkinson's patients compared to essential tremor patients during both rest and task recordings (p = 0.004). Our findings suggest an oscillatory profile in sensorimotor cortex of Parkinson's patients that, in contrast to the basal ganglia, may act to promote movement to oppose the anti-kinetic bias of the dopamine-depleted state.
Highlights
Recent theories describing the network dynamics of abnormal movement patterns, such as rigidity and akinesia, in Parkinson’s disease emphasize the role of pathological oscillatory synchronization of distributed neuronal populations
We primarily focused our analysis on two frequency bands: beta frequency (13–30 Hz) and broadband gamma frequency (70–200 Hz)
Using low-resolution ECoG (1 contact/gyrus), we previously reported an increase in broadband gamma power at rest in Parkinson’s patients relative to those with essential tremor and dystonia (Crowell et al, 2012)
Summary
Recent theories describing the network dynamics of abnormal movement patterns, such as rigidity and akinesia, in Parkinson’s disease emphasize the role of pathological oscillatory synchronization of distributed neuronal populations. Broadband high gamma activity in motor cortex is associated with movement generation (Crone et al, 1998a) and this frequency range is elevated in PD motor cortex compared to other disorders (Crowell et al, 2012) Taken together, these frequency band changes in the OFF medication state have been suggested as a possible basis for the symptoms of bradykinesia and bradyphrenia, that is, reduced motor and cognitive flexibility in Parkinson’s patients (Engel and Fries, 2010; Jenkinson et al, 2013). These frequency band changes in the OFF medication state have been suggested as a possible basis for the symptoms of bradykinesia and bradyphrenia, that is, reduced motor and cognitive flexibility in Parkinson’s patients (Engel and Fries, 2010; Jenkinson et al, 2013) It is not clear whether these changes are specific to basal ganglia or occur in parallel in other parts of the basal ganglia-thalamocortical motor loop. In comparison to patients with essential tremor, the study showed that Parkinson’s patients in the OFF medication state have elevated cortical broadband gamma power during the stop phase of the task, no major differences in beta power during the stop or move phases were observed (Crowell et al, 2012)
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