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Opposing brain signatures of sleep in task-based and resting-state conditions

Author

Listed:
  • Mohamed Abdelhack

    (Centre for Addiction and Mental Health)

  • Peter Zhukovsky

    (Centre for Addiction and Mental Health
    McLean Hospital)

  • Milos Milic

    (Centre for Addiction and Mental Health)

  • Shreyas Harita

    (Centre for Addiction and Mental Health
    University of Toronto)

  • Michael Wainberg

    (Centre for Addiction and Mental Health
    University of Toronto
    University of Toronto
    Sinai Health)

  • Shreejoy J. Tripathy

    (Centre for Addiction and Mental Health
    Centre for Addiction and Mental Health
    University of Toronto
    University of Toronto)

  • John D. Griffiths

    (Centre for Addiction and Mental Health
    Centre for Addiction and Mental Health
    University of Toronto
    University of Toronto)

  • Sean L. Hill

    (Centre for Addiction and Mental Health
    Centre for Addiction and Mental Health
    University of Toronto
    University of Toronto)

  • Daniel Felsky

    (Centre for Addiction and Mental Health
    University of Toronto
    University of Toronto
    University of Toronto)

Abstract

Sleep and depression have a complex, bidirectional relationship, with sleep-associated alterations in brain dynamics and structure impacting a range of symptoms and cognitive abilities. Previous work describing these relationships has provided an incomplete picture by investigating only one or two types of sleep measures, depression, or neuroimaging modalities in parallel. We analyze the correlations between brainwide neural signatures of sleep, cognition, and depression in task and resting-state data from over 30,000 individuals from the UK Biobank and Human Connectome Project. Neural signatures of insomnia and depression are negatively correlated with those of sleep duration measured by accelerometer in the task condition but positively correlated in the resting-state condition. Our results show that resting-state neural signatures of insomnia and depression resemble that of rested wakefulness. This is further supported by our finding of hypoconnectivity in task but hyperconnectivity in resting-state data in association with insomnia and depression. These observations dispute conventional assumptions about the neurofunctional manifestations of hyper- and hypo-somnia, and may explain inconsistent findings in the literature.

Suggested Citation

  • Mohamed Abdelhack & Peter Zhukovsky & Milos Milic & Shreyas Harita & Michael Wainberg & Shreejoy J. Tripathy & John D. Griffiths & Sean L. Hill & Daniel Felsky, 2023. "Opposing brain signatures of sleep in task-based and resting-state conditions," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43737-7
    DOI: 10.1038/s41467-023-43737-7
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    References listed on IDEAS

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    1. Matthew F. Glasser & Timothy S. Coalson & Emma C. Robinson & Carl D. Hacker & John Harwell & Essa Yacoub & Kamil Ugurbil & Jesper Andersson & Christian F. Beckmann & Mark Jenkinson & Stephen M. Smith , 2016. "A multi-modal parcellation of human cerebral cortex," Nature, Nature, vol. 536(7615), pages 171-178, August.
    2. Leonhard Schilbach & Veronika I Müller & Felix Hoffstaedter & Mareike Clos & Roberto Goya-Maldonado & Oliver Gruber & Simon B Eickhoff, 2014. "Meta-Analytically Informed Network Analysis of Resting State fMRI Reveals Hyperconnectivity in an Introspective Socio-Affective Network in Depression," PLOS ONE, Public Library of Science, vol. 9(4), pages 1-9, April.
    3. Scott Marek & Brenden Tervo-Clemmens & Finnegan J. Calabro & David F. Montez & Benjamin P. Kay & Alexander S. Hatoum & Meghan Rose Donohue & William Foran & Ryland L. Miller & Timothy J. Hendrickson &, 2022. "Reproducible brain-wide association studies require thousands of individuals," Nature, Nature, vol. 603(7902), pages 654-660, March.
    4. Vladyslav V. Vyazovskiy & Umberto Olcese & Erin C. Hanlon & Yuval Nir & Chiara Cirelli & Giulio Tononi, 2011. "Local sleep in awake rats," Nature, Nature, vol. 472(7344), pages 443-447, April.
    5. Marco Fabbri & Alessia Beracci & Monica Martoni & Debora Meneo & Lorenzo Tonetti & Vincenzo Natale, 2021. "Measuring Subjective Sleep Quality: A Review," IJERPH, MDPI, vol. 18(3), pages 1-50, January.
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