Cortical and Subthalamic Nucleus Spectral Changes During Limb Movements in Parkinson's Disease Patients with and Without Dystonia

Abstract

Background Dystonia is an understudied motor feature of Parkinson's disease (PD). Although considerable efforts have focused on brain oscillations related to the cardinal symptoms of PD, whether dystonia is associated with specific electrophysiological features is unclear. Objective The objective of this study was to investigate subcortical and cortical field potentials at rest and during contralateral hand and foot movements in patients with PD with and without dystonia. Methods We examined the prevalence and distribution of dystonia in patients with PD undergoing deep brain stimulation surgery. During surgery, we recorded intracranial electrophysiology from the motor cortex and directional electrodes in the subthalamic nucleus (STN) both at rest and during self‐paced repetitive contralateral hand and foot movements. Wavelet transforms and mixed models characterized changes in spectral content in patients with and without dystonia. Results Dystonia was highly prevalent at enrollment (61%) and occurred most commonly in the foot. Regardless of dystonia status, cortical recordings display beta (13–30 Hz) desynchronization during movements versus rest, while STN signals show increased power in low frequencies (6.0 ± 3.3 and 4.2 ± 2.9 Hz peak frequencies for hand and foot movements, respectively). Patients with PD with dystonia during deep brain stimulation surgery displayed greater M1 beta power at rest and STN low‐frequency power during movements versus those without dystonia. Conclusions Spectral power in motor cortex and STN field potentials differs markedly during repetitive limb movements, with cortical beta desynchronization and subcortical low‐frequency synchronization, especially in patients with PD with dystonia. Greater knowledge on field potential dynamics in human motor circuits can inform dystonia pathophysiology in PD and guide novel approaches to therapy. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society

Subthalamic Nucleus Stimulation–Induced Local Field Potential Changes in Dystonia

“…Despite the postoperative stun effect as a potential confounder in this study, our results are confirmed by a previous report that did not find increased theta power in the STN of dystonia patients, which could be due to differences in input between the GPi and STN 35 . Another recent study indicates that dystonia‐related spectral changes in the STN may be more prominent during voluntary movements; however, this study investigated dystonia as a motor sign of PD instead of isolated dystonia 36 …”

“…35 Another recent study indicates that dystonia-related spectral changes in the STN may be more prominent during voluntary movements; however, this study investigated dystonia as a motor sign of PD instead of isolated dystonia. 36 Contrary to the prominent beta peaks in STN that are a hallmark of PD, 37,38 we did not observe a clear beta peak in the STN of dystonic patients (Fig. 1C), despite other studies showing beta activity in the STN of dystonic patients at rest 35 and subthalamic beta peaks in patients with obsessive compulsive disorder.…”

“…PSDs of both the baseline and all DBS blocks were normalized to the mean power between 1 and 95 Hz of the baseline PSD. Percentage change in the power relative to the baseline for three frequency ranges was calculated: beta (13-35 Hz), low gamma (36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48), and high gamma (52-80 Hz).…”

Pointing in the right direction: Motor improvements with directional versus circular DBS

“…Given the mixed findings from various groups, correlations between local field potentials and motor efficacy should be studied prospectively in larger samples and with chronic recordings >4 weeks after implant. Importantly, even if beta cannot consistently inform selection of directional contacts, it is nevertheless an important component of field potential signals arising from central motor circuits 37,38 and still might prove useful as a control signal for adaptive stimulation. 39 Also, the asymmetric 1-3-3-1 design of first generation directional electrodes complicates interpretation because the surface area of the ring contacts (1 and 8) differs substantially from the smaller directional contact segments.…”

Differential cognitive effects of unilateral left and right subthalamic nucleus deep brain stimulation for Parkinson disease

“…Motor symptom asymmetry is a defining clinical feature of PD. Our routine clinical practice is to treat the most severely affected hemibody with unilateral DBS, followed by staged surgery on the opposite side of the brain (when, and if, needed) [24][25][26][27][28] . The same neurosurgeons (BG, JNB) implanted a 1-3-3-1 directional lead (Boston Scientific Vercise DBS system, Natick MA, USA, FDA IDE# G170063) at the STN target under local anesthesia with the patient fully awake.…”