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Wake slow waves in focal human epilepsy impact network activity and cognition

Author

Listed:
  • Laurent Sheybani

    (University College London
    University College London Hospitals NHS Foundation Trust
    NIHR University College London Hospitals Biomedical Research Centre)

  • Umesh Vivekananda

    (University College London
    University College London Hospitals NHS Foundation Trust
    NIHR University College London Hospitals Biomedical Research Centre)

  • Roman Rodionov

    (University College London
    University College London Hospitals NHS Foundation Trust
    NIHR University College London Hospitals Biomedical Research Centre)

  • Beate Diehl

    (University College London
    University College London Hospitals NHS Foundation Trust
    NIHR University College London Hospitals Biomedical Research Centre)

  • Fahmida A. Chowdhury

    (University College London
    University College London Hospitals NHS Foundation Trust
    NIHR University College London Hospitals Biomedical Research Centre)

  • Andrew W. McEvoy

    (University College London
    University College London Hospitals NHS Foundation Trust
    NIHR University College London Hospitals Biomedical Research Centre)

  • Anna Miserocchi

    (University College London
    University College London Hospitals NHS Foundation Trust
    NIHR University College London Hospitals Biomedical Research Centre)

  • James A. Bisby

    (University College London)

  • Daniel Bush

    (University College London)

  • Neil Burgess

    (University College London
    University College London)

  • Matthew C. Walker

    (University College London
    University College London Hospitals NHS Foundation Trust
    NIHR University College London Hospitals Biomedical Research Centre)

Abstract

Slow waves of neuronal activity are a fundamental component of sleep that are proposed to have homeostatic and restorative functions. Despite this, their interaction with pathology is unclear and there is only indirect evidence of their presence during wakefulness. Using intracortical recordings from the temporal lobe of 25 patients with epilepsy, we demonstrate the existence of local wake slow waves (LoWS) with key features of sleep slow waves, including a down-state of neuronal firing. Consistent with a reduction in neuronal activity, LoWS were associated with slowed cognitive processing. However, we also found that LoWS showed signatures of a homeostatic relationship with interictal epileptiform discharges (IEDs): exhibiting progressive adaptation during the build-up of network excitability before an IED and reducing the impact of subsequent IEDs on network excitability. We therefore propose an epilepsy homeostasis hypothesis: that slow waves in epilepsy reduce aberrant activity at the price of transient cognitive impairment.

Suggested Citation

  • Laurent Sheybani & Umesh Vivekananda & Roman Rodionov & Beate Diehl & Fahmida A. Chowdhury & Andrew W. McEvoy & Anna Miserocchi & James A. Bisby & Daniel Bush & Neil Burgess & Matthew C. Walker, 2023. "Wake slow waves in focal human epilepsy impact network activity and cognition," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42971-3
    DOI: 10.1038/s41467-023-42971-3
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    References listed on IDEAS

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    1. Thomas Andrillon & Angus Burns & Teigane Mackay & Jennifer Windt & Naotsugu Tsuchiya, 2021. "Predicting lapses of attention with sleep-like slow waves," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Reto Huber & M. Felice Ghilardi & Marcello Massimini & Giulio Tononi, 2004. "Local sleep and learning," Nature, Nature, vol. 430(6995), pages 78-81, July.
    3. Catherine A. Schevon & Shennan A. Weiss & Guy McKhann & Robert R. Goodman & Rafael Yuste & Ronald G. Emerson & Andrew J. Trevelyan, 2012. "Evidence of an inhibitory restraint of seizure activity in humans," Nature Communications, Nature, vol. 3(1), pages 1-11, January.
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    1. Marcello Massimini & Maurizio Corbetta & Maria V. Sanchez-Vives & Thomas Andrillon & Gustavo Deco & Mario Rosanova & Simone Sarasso, 2024. "Sleep-like cortical dynamics during wakefulness and their network effects following brain injury," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

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