IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v10y2019i1d10.1038_s41467-019-11444-x.html
   My bibliography  Save this article

Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans

Author

Listed:
  • Randolph F. Helfrich

    (UC Berkeley)

  • Janna D. Lendner

    (UC Berkeley
    University Medical Center Hamburg Eppendorf)

  • Bryce A. Mander

    (UC Irvine)

  • Heriberto Guillen

    (UC Irvine)

  • Michelle Paff

    (UC Irvine)

  • Lilit Mnatsakanyan

    (UC Irvine)

  • Sumeet Vadera

    (UC Irvine)

  • Matthew P. Walker

    (UC Berkeley
    UC Berkeley)

  • Jack J. Lin

    (UC Irvine
    Henry Samueli School of Engineering)

  • Robert T. Knight

    (UC Berkeley
    UC Berkeley)

Abstract

How are memories transferred from short-term to long-term storage? Systems-level memory consolidation is thought to be dependent on the coordinated interplay of cortical slow waves, thalamo-cortical sleep spindles and hippocampal ripple oscillations. However, it is currently unclear how the selective interaction of these cardinal sleep oscillations is organized to support information reactivation and transfer. Here, using human intracranial recordings, we demonstrate that the prefrontal cortex plays a key role in organizing the ripple-mediated information transfer during non-rapid eye movement (NREM) sleep. We reveal a temporally precise form of coupling between prefrontal slow-wave and spindle oscillations, which actively dictates the hippocampal-neocortical dialogue and information transfer. Our results suggest a model of the human sleeping brain in which rapid bidirectional interactions, triggered by the prefrontal cortex, mediate hippocampal activation to optimally time subsequent information transfer to the neocortex during NREM sleep.

Suggested Citation

  • Randolph F. Helfrich & Janna D. Lendner & Bryce A. Mander & Heriberto Guillen & Michelle Paff & Lilit Mnatsakanyan & Sumeet Vadera & Matthew P. Walker & Jack J. Lin & Robert T. Knight, 2019. "Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-11444-x
    DOI: 10.1038/s41467-019-11444-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-019-11444-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-019-11444-x?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
    ---><---

    Citations

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


    Cited by:

    1. Xunda Wang & Alex T. L. Leong & Shawn Z. K. Tan & Eddie C. Wong & Yilong Liu & Lee-Wei Lim & Ed X. Wu, 2023. "Functional MRI reveals brain-wide actions of thalamically-initiated oscillatory activities on associative memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    2. 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.
    3. Anli A. Liu & Simon Henin & Saman Abbaspoor & Anatol Bragin & Elizabeth A. Buffalo & Jordan S. Farrell & David J. Foster & Loren M. Frank & Tamara Gedankien & Jean Gotman & Jennifer A. Guidera & Kari , 2022. "A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. 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.
    5. Haoxin Zhang & Ivan Skelin & Shiting Ma & Michelle Paff & Lilit Mnatsakanyan & Michael A. Yassa & Robert T. Knight & Jack J. Lin, 2024. "Awake ripples enhance emotional memory encoding in the human brain," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Jan Weber & Anne-Kristin Solbakk & Alejandro O. Blenkmann & Anais Llorens & Ingrid Funderud & Sabine Leske & Pål Gunnar Larsson & Jugoslav Ivanovic & Robert T. Knight & Tor Endestad & Randolph F. Helf, 2024. "Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior," Nature Communications, Nature, vol. 15(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:10:y:2019:i:1:d:10.1038_s41467-019-11444-x. 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.

    We have no bibliographic references for this item. You can help adding them by using 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.