Parkinsonism alters beta burst dynamics across the basal ganglia-motor cortical network

Ying Yu, David Escobar Sanabria, Jing Wang, Claudia M. Hendrix, Jianyu Zhang, Shane D. Nebeck, Alexia M. Amundson, Zachary B. Busby, Devyn L. Bauer, Matthew D. Johnson, Luke A. Johnson, Jerrold L. Vitek

Research output: Contribution to journalArticlepeer-review

Abstract

Elevated synchronized oscillatory activity in the beta band has been hypothesized to be a pathophysiological marker of Parkinson's disease (PD). Recent studies have suggested that parkinsonism is closely associated with increased amplitude and duration of beta burst activity in the subthalamic nucleus (STN). How beta burst dynamics are altered from the normal to parkinsonian state across the basal ganglia-thalamocortical (BGTC) motor network, however, remains unclear. In this study, we simultaneously recorded local field potential activity from the STN, internal segment of the globus pallidus (GPi), and primary motor cortex (M1) in three female rhesus macaques, and characterized how beta burst activity changed as the animals transitioned from normal to progressively more severe parkinsonian states. Parkinsonism was associated with an increased incidence of beta bursts with longer duration and higher amplitude in the low beta band (8-20 Hz) in both the STN and GPi, but not in M1. We observed greater concurrence of beta burst activity, however, across all recording sites (M1, STN, and GPi) in PD. The simultaneous presence of low beta burst activity across multiple nodes of the BGTC network that increased with severity of PD motor signs provides compelling evidence in support of the hypothesis that low beta synchronized oscillations play a significant role in the underlying pathophysiology of PD. Given its immersion throughout the motor circuit, we hypothesize that this elevated beta-band activity interferes with spatial-temporal processing of information flow in the BGTC network that contributes to the impairment of motor function in PD.

Original languageEnglish (US)
Pages (from-to)2274-2286
Number of pages13
JournalJournal of Neuroscience
Volume41
Issue number10
DOIs
StatePublished - Mar 10 2021

Bibliographical note

Funding Information:
This work was supported by National Institutes of Health/National Institute of Neurological Disorders and Stroke Grants R01 NS058945, R01 NS037019, R01 NS110613, P50 NS098573, R37 NS077657; and by the MnDRIVE (Minnesota’s Discovery, Research and Innovation Economy) Brain Conditions Program and Engdahl Family Foundation. Correspondence should be addressed to Jerrold L. Vitek at vitek004@umn.edu. https://doi.org/10.1523/JNEUROSCI.1591-20.2021 Copyright © 2021 the authors

Publisher Copyright:
© 2021 Society for Neuroscience. All rights reserved.

Keywords

  • Burst coupling
  • Low beta burst
  • Mptp
  • Nonhuman primate
  • Parkinson's disease
  • Temporal dynamics

PubMed: MeSH publication types

  • Journal Article

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