Longitudinal Recordings Reveal Transient Increase of Alpha/Low-Beta Power in the Subthalamic Nucleus Associated With the Onset of Parkinsonian Rest Tremor

Abstract

Functional magnetic resonance imaging studies suggest that different subcortico-cortical circuits control different aspects of Parkinsonian rest tremor. The basal ganglia were proposed to drive tremor onset, and the cerebellum was suggested to be responsible for tremor maintenance (“dimmer-switch” hypothesis). Although several electrophysiological correlates of tremor have been described, it is currently unclear whether any of these is specific to tremor onset or maintenance. In this study, we present data from a single patient measured repeatedly within 2 years after implantation of a deep brain stimulation (DBS) system capable of recording brain activity from the target. Local field potentials (LFPs) from the subthalamic nucleus and the scalp electroencephalogram were recorded 1 week, 3 months, 6 months, 1 year, and 2 years after surgery. Importantly, the patient suffered from severe rest tremor of the lower limbs, which could be interrupted voluntarily by repositioning the feet. This provided the unique opportunity to record many tremor onsets in succession. We found that tremor onset and tremor maintenance were characterized by distinct modulations of subthalamic oscillations. Alpha/low-beta power increased transiently immediately after tremor onset. In contrast, beta power was continuously suppressed during tremor maintenance. Tremor maintenance was additionally associated with subthalamic and cortical power increases around individual tremor frequency. To our knowledge, this is the first evidence of distinct subthalamic LFP modulations in tremor onset and tremor maintenance. Our observations suggest the existence of an acceleration signal for Parkinsonian rest tremor in the basal ganglia, in line with the “dimmer-switch” hypothesis.

Subthalamic-Cortical Network Reorganization during Parkinson’s Tremor

“…While tremor has previously been found to decrease β coherence between STN and motor cortex (Qasim et al, 2016) while increasing θ coherence (Hirschmann et al, 2013), we demonstrated directed θ phase interactions from STN to motor cortex specifically during tremor onset. While a previous case study of tremor onset displayed local STN and cortical α/β power changes with tremor onset (Hirschmann et al, 2019), we show here that STN and motor cortical θ activity are directionally linked. We also demonstrated that during sustained tremor, the STN-motor cortex θ phase slope relationship reversed, suggesting the θ influence over sustained tremor shifted source from STN to cortex.…”

High density microelectrode recording predicts span of therapeutic tissue activation volumes in subthalamic deep brain stimulation for Parkinson disease

“…Stein and Bar-Gad [14] suggest that perhaps a single physiologically important oscillation is captured by both alpha and beta bands, in concordance with the high covariance of alpha and beta observed in our data, which the model corrects for using the interaction term. There also exists some evidence that the two bands together are directly linked to presentation of parkinsonian tremor [54]. Similar phenomena may also explain inclusion of the high gamma-HFO interaction in the LASSO model.…”

Debugging Adaptive Deep Brain Stimulation for Parkinson's Disease

“…Indeed, several studies report a decrease in beta activity during parkinsonian tremor for reasons that are obscure. [49][50][51][52] Accordingly, it might be supposed that adaptive DBS should fail to treat parkinsonian tremor. The surprise is that this is only true in a minority of cases.…”