High-Frequency Oscillations in the Pallidum: A Pathophysiological Biomarker in Parkinson's Disease?

Luke A. Johnson, Joshua E. Aman, Ying Yu, David Escobar Sanabria, Jing Wang, Meghan Hill, Rajiv Dharnipragada, Remi Patriat, Mark Fiecas, Laura Li, Lauren E. Schrock, Scott E. Cooper, Matthew D. Johnson, Michael C. Park, Noam Harel, Jerrold L. Vitek

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Background: Abnormal oscillatory neural activity in the beta-frequency band (13–35 Hz) is thought to play a role in Parkinson's disease (PD); however, increasing evidence points to alterations in high-frequency ranges (>100 Hz) also having pathophysiological relevance. Objectives: Studies have found that power in subthalamic nucleus (STN) high-frequency oscillations is increased with dopaminergic medication and during voluntary movements, implicating these brain rhythms in normal basal ganglia function. The objective of this study was to investigate whether similar signaling occurs in the internal globus pallidus (GPi), a nucleus increasingly used as a target for deep brain stimulation (DBS) for PD. Methods: Spontaneous and movement-related GPi field potentials were recorded from DBS leads in 5 externalized PD patients on and off dopaminergic medication, as well as from 3 rhesus monkeys before and after the induction of parkinsonism with the neurotoxin 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine. Results: In the parkinsonian condition, we identified a prominent oscillatory peak centered at 200–300 Hz that increased during movement. In patients the magnitude of high-frequency oscillation modulation was negatively correlated with bradykinesia. In monkeys, high-frequency oscillations were mostly absent in the naive condition but emerged after the neurotoxin 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine. In patients, spontaneous high-frequency oscillations were significantly attenuated on-medication. Conclusions: Our findings provide evidence in support of the hypothesis that exaggerated, movement-modulated high-frequency oscillations in the GPi are pathophysiological features of PD. These findings suggest that the functional role(s) of high-frequency oscillations may differ between the STN and GPi and motivate additional investigations into their relationship to motor control in normal and diseased states.

Original languageEnglish (US)
Pages (from-to)1332-1341
Number of pages10
JournalMovement Disorders
Volume36
Issue number6
Early online dateApr 13 2021
DOIs
StatePublished - Jun 2021

Bibliographical note

Funding Information:
This work was supported by the Udall Center for Excellence in Parkinson's Disease, National Institutes of Health, National Institute of Neurological Disorders and Stroke P50‐NS098573, R01‐NS094206, R01‐NS058945, R01‐NS037019, R01‐NS110613, P30‐NS076408, P41‐EB027061; University of Minnesota's NIH Clinical and Translational Science Award UL1TR002494; MnDRIVE (Minnesota's Discovery, Research and Innovation Economy) Brain Conditions Program; Engdahl Family Foundation; the Kurt B. Seydow Dystonia Foundation. Funding agencies:

Publisher Copyright:
© 2021 International Parkinson and Movement Disorder Society

Keywords

  • Parkinson's disease
  • deep brain stimulation
  • high-frequency oscillations
  • internal globus pallidus
  • local field potentials

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

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