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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
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    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. 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.
    3. 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.
    4. 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.
    5. 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.

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