Levodopa Modulates Functional Connectivity in the Upper Beta Band Between Subthalamic Nucleus and Muscle Activity in Tonic and Phasic Motor Activity Patterns in Parkinson’s Disease
Introduction: Striatal dopamine depletion disrupts basal ganglia function and causes Parkinson’s disease (PD). The pathophysiology of the dopamine-dependent relationship between basal ganglia signaling and motor control, however, is not fully understood. We obtained simultaneous recordings of local...
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doaj-59e5ba61409c4900b1dfa4e75ed2d5d22020-11-25T03:06:03ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612019-07-011310.3389/fnhum.2019.00223449169Levodopa Modulates Functional Connectivity in the Upper Beta Band Between Subthalamic Nucleus and Muscle Activity in Tonic and Phasic Motor Activity Patterns in Parkinson’s DiseaseUri E. Ramirez Pasos0Frank Steigerwald1Martin M. Reich2Cordula Matthies3Jens Volkmann4René Reese5René Reese6Department of Neurology, University Hospital Würzburg, Würzburg, GermanyDepartment of Neurology, University Hospital Würzburg, Würzburg, GermanyDepartment of Neurology, University Hospital Würzburg, Würzburg, GermanyDepartment of Neurosurgery, University Hospital Würzburg, Würzburg, GermanyDepartment of Neurology, University Hospital Würzburg, Würzburg, GermanyDepartment of Neurology, University Hospital Würzburg, Würzburg, GermanyDepartment of Neurology, University of Rostock, Rostock, GermanyIntroduction: Striatal dopamine depletion disrupts basal ganglia function and causes Parkinson’s disease (PD). The pathophysiology of the dopamine-dependent relationship between basal ganglia signaling and motor control, however, is not fully understood. We obtained simultaneous recordings of local field potentials (LFPs) from the subthalamic nucleus (STN) and electromyograms (EMGs) in patients with PD to investigate the impact of dopaminergic state and movement on long-range beta functional connectivity between basal ganglia and lower motor neurons.Methods: Eight PD patients were investigated 3 months after implantation of a deep brain stimulation (DBS)-system capable of recording LFPs via chronically-implanted leads (Medtronic, ACTIVA PC+S®). We analyzed STN spectral power and its coherence with EMG in the context of two different movement paradigms (tonic wrist extension vs. alternating wrist extension and flexion) and the effect of levodopa (L-Dopa) intake using an unbiased data-driven approach to determine regions of interest (ROI).Results: Two ROIs capturing prominent coherence within a grand average coherogram were identified. A trend of a dopamine effect was observed for the first ROI (50–150 ms after movement start) with higher STN-EMG coherence in medicated patients. Concerning the second ROI (300–500 ms after movement start), an interaction effect of L-Dopa medication and movement task was observed with higher coherence in the isometric contraction task compared to alternating movements in the medication ON state, a pattern which was reversed in L-Dopa OFF.Discussion: L-Dopa medication may normalize functional connectivity between remote structures of the motor system with increased upper beta coherence reflecting a physiological restriction of the amount of information conveyed between remote structures. This may be necessary to maintain simple movements like isometric contraction. Our study adds dynamic properties to the complex interplay between STN spectral beta power and the nucleus’ functional connectivity to remote structures of the motor system as a function of movement and dopaminergic state. This may help to identify markers of neuronal activity relevant for more individualized programming of DBS therapy.https://www.frontiersin.org/article/10.3389/fnhum.2019.00223/fullParkinson’s diseasesubthalamic nucleusdeep brain stimulationlocal field potentialsdopaminemovement |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Uri E. Ramirez Pasos Frank Steigerwald Martin M. Reich Cordula Matthies Jens Volkmann René Reese René Reese |
spellingShingle |
Uri E. Ramirez Pasos Frank Steigerwald Martin M. Reich Cordula Matthies Jens Volkmann René Reese René Reese Levodopa Modulates Functional Connectivity in the Upper Beta Band Between Subthalamic Nucleus and Muscle Activity in Tonic and Phasic Motor Activity Patterns in Parkinson’s Disease Frontiers in Human Neuroscience Parkinson’s disease subthalamic nucleus deep brain stimulation local field potentials dopamine movement |
author_facet |
Uri E. Ramirez Pasos Frank Steigerwald Martin M. Reich Cordula Matthies Jens Volkmann René Reese René Reese |
author_sort |
Uri E. Ramirez Pasos |
title |
Levodopa Modulates Functional Connectivity in the Upper Beta Band Between Subthalamic Nucleus and Muscle Activity in Tonic and Phasic Motor Activity Patterns in Parkinson’s Disease |
title_short |
Levodopa Modulates Functional Connectivity in the Upper Beta Band Between Subthalamic Nucleus and Muscle Activity in Tonic and Phasic Motor Activity Patterns in Parkinson’s Disease |
title_full |
Levodopa Modulates Functional Connectivity in the Upper Beta Band Between Subthalamic Nucleus and Muscle Activity in Tonic and Phasic Motor Activity Patterns in Parkinson’s Disease |
title_fullStr |
Levodopa Modulates Functional Connectivity in the Upper Beta Band Between Subthalamic Nucleus and Muscle Activity in Tonic and Phasic Motor Activity Patterns in Parkinson’s Disease |
title_full_unstemmed |
Levodopa Modulates Functional Connectivity in the Upper Beta Band Between Subthalamic Nucleus and Muscle Activity in Tonic and Phasic Motor Activity Patterns in Parkinson’s Disease |
title_sort |
levodopa modulates functional connectivity in the upper beta band between subthalamic nucleus and muscle activity in tonic and phasic motor activity patterns in parkinson’s disease |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Human Neuroscience |
issn |
1662-5161 |
publishDate |
2019-07-01 |
description |
Introduction: Striatal dopamine depletion disrupts basal ganglia function and causes Parkinson’s disease (PD). The pathophysiology of the dopamine-dependent relationship between basal ganglia signaling and motor control, however, is not fully understood. We obtained simultaneous recordings of local field potentials (LFPs) from the subthalamic nucleus (STN) and electromyograms (EMGs) in patients with PD to investigate the impact of dopaminergic state and movement on long-range beta functional connectivity between basal ganglia and lower motor neurons.Methods: Eight PD patients were investigated 3 months after implantation of a deep brain stimulation (DBS)-system capable of recording LFPs via chronically-implanted leads (Medtronic, ACTIVA PC+S®). We analyzed STN spectral power and its coherence with EMG in the context of two different movement paradigms (tonic wrist extension vs. alternating wrist extension and flexion) and the effect of levodopa (L-Dopa) intake using an unbiased data-driven approach to determine regions of interest (ROI).Results: Two ROIs capturing prominent coherence within a grand average coherogram were identified. A trend of a dopamine effect was observed for the first ROI (50–150 ms after movement start) with higher STN-EMG coherence in medicated patients. Concerning the second ROI (300–500 ms after movement start), an interaction effect of L-Dopa medication and movement task was observed with higher coherence in the isometric contraction task compared to alternating movements in the medication ON state, a pattern which was reversed in L-Dopa OFF.Discussion: L-Dopa medication may normalize functional connectivity between remote structures of the motor system with increased upper beta coherence reflecting a physiological restriction of the amount of information conveyed between remote structures. This may be necessary to maintain simple movements like isometric contraction. Our study adds dynamic properties to the complex interplay between STN spectral beta power and the nucleus’ functional connectivity to remote structures of the motor system as a function of movement and dopaminergic state. This may help to identify markers of neuronal activity relevant for more individualized programming of DBS therapy. |
topic |
Parkinson’s disease subthalamic nucleus deep brain stimulation local field potentials dopamine movement |
url |
https://www.frontiersin.org/article/10.3389/fnhum.2019.00223/full |
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