Slow-wave sleep dysfunction in mild parkinsonism is associated with excessive beta and reduced delta oscillations in motor cortex

Ajay K. Verma, Bharadwaj Nandakumar, Kit Acedillo, Ying Yu, Ethan Marshall, David Schneck, Mark Fiecas, Jing Wang, Colum D. MacKinnon, Michael J. Howell, Jerrold L. Vitek, Luke A. Johnson

Research output: Contribution to journalArticlepeer-review

Abstract

Increasing evidence suggests slow-wave sleep (SWS) dysfunction in Parkinson’s disease (PD) is associated with faster disease progression, cognitive impairment, and excessive daytime sleepiness. Beta oscillations (8–35 Hz) in the basal ganglia thalamocortical (BGTC) network are thought to play a role in the development of cardinal motor signs of PD. The role cortical beta oscillations play in SWS dysfunction in the early stage of parkinsonism is not understood, however. To address this question, we used a within-subject design in a nonhuman primate (NHP) model of PD to record local field potentials from the primary motor cortex (MC) during sleep across normal and mild parkinsonian states. The MC is a critical node in the BGTC network, exhibits pathological oscillations with depletion in dopamine tone, and displays high amplitude slow oscillations during SWS. The MC is therefore an appropriate recording site to understand the neurophysiology of SWS dysfunction in parkinsonism. We observed a reduction in SWS quantity (p = 0.027) in the parkinsonian state compared to normal. The cortical delta (0.5–3 Hz) power was reduced (p = 0.038) whereas beta (8–35 Hz) power was elevated (p = 0.001) during SWS in the parkinsonian state compared to normal. Furthermore, SWS quantity positively correlated with delta power (r = 0.43, p = 0.037) and negatively correlated with beta power (r = −0.65, p < 0.001). Our findings support excessive beta oscillations as a mechanism for SWS dysfunction in mild parkinsonism and could inform the development of neuromodulation therapies for enhancing SWS in people with PD.

Original languageEnglish (US)
Article number1338624
JournalFrontiers in Neuroscience
Volume18
DOIs
StatePublished - 2024

Bibliographical note

Publisher Copyright:
Copyright © 2024 Verma, Nandakumar, Acedillo, Yu, Marshall, Schneck, Fiecas, Wang, MacKinnon, Howell, Vitek and Johnson.

Keywords

  • beta oscillations
  • delta oscillations
  • local field potential
  • motor cortex
  • MPTP
  • Parkinson’s disease
  • sleep-wake disturbances

PubMed: MeSH publication types

  • Journal Article

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