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Multi-night cortico-basal recordings reveal mechanisms of NREM slow-wave suppression and spontaneous awakenings in Parkinson’s disease

Author

Listed:
  • Md Fahim Anjum

    (University California San Francisco)

  • Clay Smyth

    (University California San Francisco)

  • Rafael Zuzuárregui

    (University California San Francisco
    San Francisco Veteran’s Affairs Medical Center)

  • Derk Jan Dijk

    (University of Surrey
    Care Research and Technology Centre at Imperial College, London and The University of Surrey)

  • Philip A. Starr

    (University California San Francisco)

  • Timothy Denison

    (University of Oxford)

  • Simon Little

    (University California San Francisco)

Abstract

Sleep disturbance is a prevalent and disabling comorbidity in Parkinson’s disease (PD). We performed multi-night (n = 57) at-home intracranial recordings from electrocorticography and subcortical electrodes using sensing-enabled Deep Brain Stimulation (DBS), paired with portable polysomnography in four PD participants and one with cervical dystonia (clinical trial: NCT03582891). Cortico-basal activity in delta increased and in beta decreased during NREM (N2 + N3) versus wakefulness in PD. DBS caused further elevation in cortical delta and decrease in alpha and low-beta compared to DBS OFF state. Our primary outcome demonstrated an inverse interaction between subcortical beta and cortical slow-wave during NREM. Our secondary outcome revealed subcortical beta increases prior to spontaneous awakenings in PD. We classified NREM vs. wakefulness with high accuracy in both traditional (30 s: 92.6 ± 1.7%) and rapid (5 s: 88.3 ± 2.1%) data epochs of intracranial signals. Our findings elucidate sleep neurophysiology and impacts of DBS on sleep in PD informing adaptive DBS for sleep dysfunction.

Suggested Citation

  • Md Fahim Anjum & Clay Smyth & Rafael Zuzuárregui & Derk Jan Dijk & Philip A. Starr & Timothy Denison & Simon Little, 2024. "Multi-night cortico-basal recordings reveal mechanisms of NREM slow-wave suppression and spontaneous awakenings in Parkinson’s disease," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46002-7
    DOI: 10.1038/s41467-024-46002-7
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    1. Zixiao Yin & Ruoyu Ma & Qi An & Yichen Xu & Yifei Gan & Guanyu Zhu & Yin Jiang & Ning Zhang & Anchao Yang & Fangang Meng & Andrea A. Kühn & Hagai Bergman & Wolf-Julian Neumann & Jianguo Zhang, 2023. "Pathological pallidal beta activity in Parkinson’s disease is sustained during sleep and associated with sleep disturbance," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Brian C Ross, 2014. "Mutual Information between Discrete and Continuous Data Sets," PLOS ONE, Public Library of Science, vol. 9(2), pages 1-5, February.
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