IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43737-7.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43737-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43737-7?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    4. 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.
    5. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Martin Gell & Simon B. Eickhoff & Amir Omidvarnia & Vincent Küppers & Kaustubh R. Patil & Theodore D. Satterthwaite & Veronika I. Müller & Robert Langner, 2024. "How measurement noise limits the accuracy of brain-behaviour predictions," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Andrew D. Grotzinger & Travis T. Mallard & Zhaowen Liu & Jakob Seidlitz & Tian Ge & Jordan W. Smoller, 2023. "Multivariate genomic architecture of cortical thickness and surface area at multiple levels of analysis," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Dardo Tomasi & Nora D. Volkow, 2024. "Associations between handedness and brain functional connectivity patterns in children," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    4. Golia Shafiei & Ben D. Fulcher & Bradley Voytek & Theodore D. Satterthwaite & Sylvain Baillet & Bratislav Misic, 2023. "Neurophysiological signatures of cortical micro-architecture," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Valentina Pacella & Victor Nozais & Lia Talozzi & Majd Abdallah & Demian Wassermann & Stephanie J. Forkel & Michel Thiebaut de Schotten, 2024. "The morphospace of the brain-cognition organisation," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    6. Meike D. Hettwer & Lena Dorfschmidt & Lara M. C. Puhlmann & Linda M. Jacob & Casey Paquola & Richard A. I. Bethlehem & Edward T. Bullmore & Simon B. Eickhoff & Sofie L. Valk, 2024. "Longitudinal variation in resilient psychosocial functioning is associated with ongoing cortical myelination and functional reorganization during adolescence," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Audrey C. Luo & Valerie J. Sydnor & Adam Pines & Bart Larsen & Aaron F. Alexander-Bloch & Matthew Cieslak & Sydney Covitz & Andrew A. Chen & Nathalia Bianchini Esper & Eric Feczko & Alexandre R. Franc, 2024. "Functional connectivity development along the sensorimotor-association axis enhances the cortical hierarchy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Arielle S. Keller & Adam R. Pines & Sheila Shanmugan & Valerie J. Sydnor & Zaixu Cui & Maxwell A. Bertolero & Ran Barzilay & Aaron F. Alexander-Bloch & Nora Byington & Andrew Chen & Gregory M. Conan &, 2023. "Personalized functional brain network topography is associated with individual differences in youth cognition," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    9. Lukas L Imbach & Esther Werth & Ulf Kallweit & Johannes Sarnthein & Thomas E Scammell & Christian R Baumann, 2012. "Inter-Hemispheric Oscillations in Human Sleep," PLOS ONE, Public Library of Science, vol. 7(11), pages 1-10, November.
    10. Matthew Rosenblatt & Link Tejavibulya & Rongtao Jiang & Stephanie Noble & Dustin Scheinost, 2024. "Data leakage inflates prediction performance in connectome-based machine learning models," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    11. Leon D. Lotter & Amin Saberi & Justine Y. Hansen & Bratislav Misic & Casey Paquola & Gareth J. Barker & Arun L. W. Bokde & Sylvane Desrivières & Herta Flor & Antoine Grigis & Hugh Garavan & Penny Gowl, 2024. "Regional patterns of human cortex development correlate with underlying neurobiology," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    12. Haewon Nam & Chongwon Pae & Jinseok Eo & Maeng-Keun Oh & Hae-Jeong Park, 2021. "Inter-species cortical registration between macaques and humans using a functional network property under a spherical demons framework," PLOS ONE, Public Library of Science, vol. 16(10), pages 1-22, October.
    13. Arno Klein & Satrajit S Ghosh & Forrest S Bao & Joachim Giard & Yrjö Häme & Eliezer Stavsky & Noah Lee & Brian Rossa & Martin Reuter & Elias Chaibub Neto & Anisha Keshavan, 2017. "Mindboggling morphometry of human brains," PLOS Computational Biology, Public Library of Science, vol. 13(2), pages 1-40, February.
    14. Ann Hillier & Ryan P Kelly & Terrie Klinger, 2016. "Narrative Style Influences Citation Frequency in Climate Change Science," PLOS ONE, Public Library of Science, vol. 11(12), pages 1-12, December.
    15. Manish Saggar & James M. Shine & Raphaël Liégeois & Nico U. F. Dosenbach & Damien Fair, 2022. "Precision dynamical mapping using topological data analysis reveals a hub-like transition state at rest," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    16. Casey Paquola & Reinder Vos De Wael & Konrad Wagstyl & Richard A I Bethlehem & Seok-Jun Hong & Jakob Seidlitz & Edward T Bullmore & Alan C Evans & Bratislav Misic & Daniel S Margulies & Jonathan Small, 2019. "Microstructural and functional gradients are increasingly dissociated in transmodal cortices," PLOS Biology, Public Library of Science, vol. 17(5), pages 1-28, May.
    17. Peter Zhukovsky & Earvin S. Tio & Gillian Coughlan & David A. Bennett & Yanling Wang & Timothy J. Hohman & Diego A. Pizzagalli & Benoit H. Mulsant & Aristotle N. Voineskos & Daniel Felsky, 2024. "Genetic influences on brain and cognitive health and their interactions with cardiovascular conditions and depression," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    18. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    19. Gustavo Deco & Diego Vidaurre & Morten L. Kringelbach, 2021. "Revisiting the global workspace orchestrating the hierarchical organization of the human brain," Nature Human Behaviour, Nature, vol. 5(4), pages 497-511, April.
    20. David J. Whiteside & Negin Holland & Kamen A. Tsvetanov & Elijah Mak & Maura Malpetti & George Savulich & P. Simon Jones & Michelle Naessens & Matthew A. Rouse & Tim D. Fryer & Young T. Hong & Frankli, 2023. "Synaptic density affects clinical severity via network dysfunction in syndromes associated with frontotemporal lobar degeneration," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43737-7. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.