An electrophysiological marker of arousal level in humans

  1. Janna Desiree Lendner  Is a corresponding author
  2. Randolph F Helfrich
  3. Bryce A Mander
  4. Luis Romundstad
  5. Jack J Lin
  6. Matthew P Walker
  7. Pal G Larsson
  8. Robert T Knight
  1. University of California, Berkeley, United States
  2. University of Tübingen, Germany
  3. University of California, Irvine, United States
  4. University of Oslo, Norway
  5. Univsersity of Oslo, Norway

Abstract

Deep non-rapid eye movement sleep (NREM) and general anesthesia with propofol are prominent states of reduced arousal linked to the occurrence of synchronized oscillations in the electroencephalogram (EEG). Although rapid eye movement (REM) sleep is also associated with diminished arousal levels, it is characterized by a desynchronized, 'wake-like' EEG. This observation implies that reduced arousal states are not necessarily only defined by synchronous oscillatory activity. Using intracranial and surface EEG recordings in four independent data sets, we demonstrate that the 1/f spectral slope of the electrophysiological power spectrum, which reflects the non-oscillatory, scale-free component of neural activity, delineates wakefulness from propofol anesthesia, NREM and REM sleep. Critically, the spectral slope discriminates wakefulness from REM sleep solely based on the neurophysiological brain state. Taken together, our findings describe a common electrophysiological marker that tracks states of reduced arousal, including different sleep stages as well as anesthesia in humans.

Data availability

Source data files have been updated and are provided here:Lendner, Janna (2020), An Electrophysiological Marker of Arousal Level in Humans, UC Berkeley, Dataset, https://doi.org/10.6078/D1NX1V

The following data sets were generated

Article and author information

Author details

  1. Janna Desiree Lendner

    Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States
    For correspondence
    janna.lendner@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1967-6110
  2. Randolph F Helfrich

    Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8045-3111
  3. Bryce A Mander

    Psychiatry and Human Behavior, University of California, Irvine, Irvine, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Luis Romundstad

    Anesthesiology, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  5. Jack J Lin

    Neurology, University of California, Irvine, Irvine, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Matthew P Walker

    Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Pal G Larsson

    Neurosurgery, Univsersity of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.
  8. Robert T Knight

    Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (LE 3863/2-1)

  • Janna Desiree Lendner

National Institute of Neurological Disorders and Stroke (R37NS21135)

  • Robert T Knight

Deutsche Forschungsgemeinschaft (HE 8329/2-1)

  • Randolph F Helfrich

National Institute of Mental Health (R01AG03116408)

  • Matthew P Walker

National Institute of Mental Health (RF1AG05401901)

  • Matthew P Walker

National Institute of Mental Health (RF1AG05410601)

  • Matthew P Walker

National Institute of Mental Health (F32-AG039170)

  • Bryce A Mander

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: We collected four independent datasets for this study to assess the neurophysiological basis of states of reduced arousal, namely sleep and general anesthesia.Study 1 - Anesthesia scalp EEG: All participants were informed and provided written consent in accordance with the local ethics committee (Regional Committees for Medical and Health Research Ethics in Oslo case number 2012/2015 and extension 2012/2015-8).Study 2 - Anesthesia intracranial EEG: All participants were informed and provided written consent in accordance with the local ethics committee (Regional Committees for Medical and Health Research Ethics in Oslo case number 2012/2015 and extension 2012/2015-8).Study 3 - Sleep scalp EEG: All participants were informed and provided written consent in accordance with the local ethics committee (Berkeley Committee for Protection of Human Subjects Protocol Number 2010-01-595).Study 4 - Sleep intracranial EEG: All patients provided informed consent according to the local ethics committees of the University of California at Berkeley and at Irvine (University of California at Berkeley Committee for the Protection of Human Subjects Protocol Number 2010-01-520; University of California at Irvine Institutional Review Board Protocol Number 2014-1522, UCB relies on UCI Reliance Number 1817) and gave their written consent before data collection.

Reviewing Editor

  1. Saskia Haegens, Columbia University College of Physicians and Surgeons, United States

Version history

  1. Received: January 12, 2020
  2. Accepted: July 6, 2020
  3. Accepted Manuscript published: July 28, 2020 (version 1)
  4. Version of Record published: July 31, 2020 (version 2)

Copyright

© 2020, Lendner et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Janna Desiree Lendner
  2. Randolph F Helfrich
  3. Bryce A Mander
  4. Luis Romundstad
  5. Jack J Lin
  6. Matthew P Walker
  7. Pal G Larsson
  8. Robert T Knight
(2020)
An electrophysiological marker of arousal level in humans
eLife 9:e55092.
https://doi.org/10.7554/eLife.55092

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