IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32840-w.html
   My bibliography  Save this article

The human thalamus orchestrates neocortical oscillations during NREM sleep

Author

Listed:
  • Thomas Schreiner

    (Ludwig-Maximilians-Universität München)

  • Elisabeth Kaufmann

    (Ludwig-Maximilians-Universität München)

  • Soheyl Noachtar

    (Ludwig-Maximilians-Universität München)

  • Jan-Hinnerk Mehrkens

    (Ludwig-Maximilians-Universität München)

  • Tobias Staudigl

    (Ludwig-Maximilians-Universität München)

Abstract

A hallmark of non-rapid eye movement sleep is the coordinated interplay of slow oscillations (SOs) and sleep spindles. Traditionally, a cortico-thalamo-cortical loop is suggested to coordinate these rhythms: neocortically-generated SOs trigger spindles in the thalamus that are projected back to neocortex. Here, we used intrathalamic recordings from human epilepsy patients to test this canonical interplay. We show that SOs in the anterior thalamus precede neocortical SOs (peak −50 ms), whereas concurrently-recorded SOs in the mediodorsal thalamus are led by neocortical SOs (peak +50 ms). Sleep spindles, detected in both thalamic nuclei, preceded their neocortical counterparts (peak −100 ms) and were initiated during early phases of thalamic SOs. Our findings indicate an active role of the anterior thalamus in organizing sleep rhythms in the neocortex and highlight the functional diversity of thalamic nuclei in humans. The thalamic coordination of sleep oscillations could have broad implications for the mechanisms underlying memory consolidation.

Suggested Citation

  • Thomas Schreiner & Elisabeth Kaufmann & Soheyl Noachtar & Jan-Hinnerk Mehrkens & Tobias Staudigl, 2022. "The human thalamus orchestrates neocortical oscillations during NREM sleep," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32840-w
    DOI: 10.1038/s41467-022-32840-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32840-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-32840-w?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. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    2. Thomas Schreiner & Marit Petzka & Tobias Staudigl & Bernhard P. Staresina, 2021. "Endogenous memory reactivation during sleep in humans is clocked by slow oscillation-spindle complexes," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    3. Guillaume Viejo & Adrien Peyrache, 2020. "Precise coupling of the thalamic head-direction system to hippocampal ripples," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    4. Rachel A. Mak-McCully & Matthieu Rolland & Anna Sargsyan & Chris Gonzalez & Michel Magnin & Patrick Chauvel & Marc Rey & Hélène Bastuji & Eric Halgren, 2017. "Coordination of cortical and thalamic activity during non-REM sleep in humans," Nature Communications, Nature, vol. 8(1), pages 1-11, August.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Thomas Schreiner & Benjamin J. Griffiths & Merve Kutlu & Christian Vollmar & Elisabeth Kaufmann & Stefanie Quach & Jan Remi & Soheyl Noachtar & Tobias Staudigl, 2024. "Spindle-locked ripples mediate memory reactivation during human NREM sleep," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Thomas Schreiner & Marit Petzka & Tobias Staudigl & Bernhard P. Staresina, 2023. "Respiration modulates sleep oscillations and memory reactivation in humans," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Layton Lamsam & Brett Gu & Mingli Liang & George Sun & Kamren J. Khan & Kevin N. Sheth & Lawrence J. Hirsch & Christopher Pittenger & Alfred P. Kaye & John H. Krystal & Eyiyemisi C. Damisah, 2024. "The human claustrum tracks slow waves during sleep," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

    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. Thomas Schreiner & Benjamin J. Griffiths & Merve Kutlu & Christian Vollmar & Elisabeth Kaufmann & Stefanie Quach & Jan Remi & Soheyl Noachtar & Tobias Staudigl, 2024. "Spindle-locked ripples mediate memory reactivation during human NREM sleep," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Joshua M. Diamond & Julio I. Chapeton & Weizhen Xie & Samantha N. Jackson & Sara K. Inati & Kareem A. Zaghloul, 2024. "Focal seizures induce spatiotemporally organized spiking activity in the human cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Kyerl Park & Yoonsoo Yeo & Kisung Shin & Jeehyun Kwag, 2024. "Egocentric neural representation of geometric vertex in the retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Jennifer B Tennessen & Marla M Holt & Brianna M Wright & M Bradley Hanson & Candice K Emmons & Deborah A Giles & Jeffrey T Hogan & Sheila J Thornton & Volker B Deecke, 2023. "Divergent foraging strategies between populations of sympatric matrilineal killer whales," Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(3), pages 373-386.
    5. Thomas Schreiner & Marit Petzka & Tobias Staudigl & Bernhard P. Staresina, 2023. "Respiration modulates sleep oscillations and memory reactivation in humans," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    6. Douglas Feitosa Tomé & Sadra Sadeh & Claudia Clopath, 2022. "Coordinated hippocampal-thalamic-cortical communication crucial for engram dynamics underneath systems consolidation," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Celia M. Gagliardi & Marc E. Normandin & Alexandra T. Keinath & Joshua B. Julian & Matthew R. Lopez & Manuel-Miguel Ramos-Alvarez & Russell A. Epstein & Isabel A. Muzzio, 2024. "Distinct neural mechanisms for heading retrieval and context recognition in the hippocampus during spatial reorientation," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    8. Alireza Saeedi & Kun Wang & Ghazaleh Nikpourian & Andreas Bartels & Nikos K. Logothetis & Nelson K. Totah & Masataka Watanabe, 2024. "Brightness illusions drive a neuronal response in the primary visual cortex under top-down modulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    9. Arthur Pewsey & Eduardo García-Portugués, 2021. "Recent advances in directional statistics," TEST: An Official Journal of the Spanish Society of Statistics and Operations Research, Springer;Sociedad de Estadística e Investigación Operativa, vol. 30(1), pages 1-58, March.
    10. César Henrique Mattos Pires & Felipe M. Pimenta & Carla A. D'Aquino & Osvaldo R. Saavedra & Xuerui Mao & Arcilan T. Assireu, 2020. "Coastal Wind Power in Southern Santa Catarina, Brazil," Energies, MDPI, vol. 13(19), pages 1-23, October.
    11. Alexis T Baria & Brian Maniscalco & Biyu J He, 2017. "Initial-state-dependent, robust, transient neural dynamics encode conscious visual perception," PLOS Computational Biology, Public Library of Science, vol. 13(11), pages 1-29, November.
    12. Matthijs J. Warrens & Bunga C. Pratiwi, 2016. "Kappa Coefficients for Circular Classifications," Journal of Classification, Springer;The Classification Society, vol. 33(3), pages 507-522, October.
    13. Lombard, F. & Hawkins, Douglas M. & Potgieter, Cornelis J., 2017. "Sequential rank CUSUM charts for angular data," Computational Statistics & Data Analysis, Elsevier, vol. 105(C), pages 268-279.
    14. Masataka Sawayama & Shin'ya Nishida, 2018. "Material and shape perception based on two types of intensity gradient information," PLOS Computational Biology, Public Library of Science, vol. 14(4), pages 1-40, April.
    15. Aguiar-Conraria, Luis & Martins, Manuel M.F. & Soares, Maria Joana, 2018. "Estimating the Taylor rule in the time-frequency domain," Journal of Macroeconomics, Elsevier, vol. 57(C), pages 122-137.
    16. Assaf Breska & Leon Y Deouell, 2017. "Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment," PLOS Biology, Public Library of Science, vol. 15(2), pages 1-30, February.
    17. Sunny Nigam & Russell Milton & Sorin Pojoga & Valentin Dragoi, 2023. "Adaptive coding across visual features during free-viewing and fixation conditions," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    18. Chinnakkaruppan Adaikkan & Justin Joseph & Georgios Foustoukos & Jun Wang & Denis Polygalov & Roman Boehringer & Steven J. Middleton & Arthur J. Y. Huang & Li-Huei Tsai & Thomas J. McHugh, 2024. "Silencing CA1 pyramidal cells output reveals the role of feedback inhibition in hippocampal oscillations," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Daniel S. Kluger & Carina Forster & Omid Abbasi & Nikos Chalas & Arno Villringer & Joachim Gross, 2023. "Modulatory dynamics of periodic and aperiodic activity in respiration-brain coupling," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    20. Manuela Costa & Diego Lozano-Soldevilla & Antonio Gil-Nagel & Rafael Toledano & Carina R. Oehrn & Lukas Kunz & Mar Yebra & Costantino Mendez-Bertolo & Lennart Stieglitz & Johannes Sarnthein & Nikolai , 2022. "Aversive memory formation in humans involves an amygdala-hippocampus phase code," Nature Communications, Nature, vol. 13(1), pages 1-16, 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:13:y:2022:i:1:d:10.1038_s41467-022-32840-w. 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.