IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48816-x.html
   My bibliography  Save this article

Prefrontal coding of learned and inferred knowledge during REM and NREM sleep

Author

Listed:
  • Kareem Abdou

    (University of Toyama
    University of Toyama
    Cairo University
    University of Toyama)

  • Masanori Nomoto

    (University of Toyama
    University of Toyama
    University of Toyama
    Japan Agency for Medical Research and Development (AMED))

  • Mohamed H. Aly

    (University of Toyama
    University of Toyama
    University of Toyama
    The British University in Egypt)

  • Ahmed Z. Ibrahim

    (University of Toyama
    University of Toyama
    Cairo University
    University of Toyama)

  • Kiriko Choko

    (University of Toyama
    University of Toyama
    University of Toyama)

  • Reiko Okubo-Suzuki

    (University of Toyama
    University of Toyama
    University of Toyama)

  • Shin-ichi Muramatsu

    (Jichi Medical University
    The University of Tokyo)

  • Kaoru Inokuchi

    (University of Toyama
    University of Toyama
    University of Toyama)

Abstract

Idling brain activity has been proposed to facilitate inference, insight, and innovative problem-solving. However, it remains unclear how and when the idling brain can create novel ideas. Here, we show that cortical offline activity is both necessary and sufficient for building unlearned inferential knowledge from previously acquired information. In a transitive inference paradigm, male C57BL/6J mice gained the inference 1 day after, but not shortly after, complete training. Inhibiting the neuronal computations in the anterior cingulate cortex (ACC) during post-learning either non-rapid eye movement (NREM) or rapid eye movement (REM) sleep, but not wakefulness, disrupted the inference without affecting the learned knowledge. In vivo Ca2+ imaging suggests that NREM sleep organizes the scattered learned knowledge in a complete hierarchy, while REM sleep computes the inferential information from the organized hierarchy. Furthermore, after insufficient learning, artificial activation of medial entorhinal cortex-ACC dialog during only REM sleep created inferential knowledge. Collectively, our study provides a mechanistic insight on NREM and REM coordination in weaving inferential knowledge, thus highlighting the power of idling brain in cognitive flexibility.

Suggested Citation

  • Kareem Abdou & Masanori Nomoto & Mohamed H. Aly & Ahmed Z. Ibrahim & Kiriko Choko & Reiko Okubo-Suzuki & Shin-ichi Muramatsu & Kaoru Inokuchi, 2024. "Prefrontal coding of learned and inferred knowledge during REM and NREM sleep," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48816-x
    DOI: 10.1038/s41467-024-48816-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48816-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48816-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
    ---><---

    References listed on IDEAS

    as
    1. Masanori Nomoto & Emi Murayama & Shuntaro Ohno & Reiko Okubo-Suzuki & Shin-ichi Muramatsu & Kaoru Inokuchi, 2022. "Hippocampus as a sorter and reverberatory integrator of sensory inputs," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Khaled Ghandour & Noriaki Ohkawa & Chi Chung Alan Fung & Hirotaka Asai & Yoshito Saitoh & Takashi Takekawa & Reiko Okubo-Suzuki & Shingo Soya & Hirofumi Nishizono & Mina Matsuo & Makoto Osanai & Masaa, 2019. "Orchestrated ensemble activities constitute a hippocampal memory engram," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    3. Ullrich Wagner & Steffen Gais & Hilde Haider & Rolf Verleger & Jan Born, 2004. "Sleep inspires insight," Nature, Nature, vol. 427(6972), pages 352-355, January.
    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. Smith, Vernon L., 2005. "Behavioral economics research and the foundations of economics," Journal of Behavioral and Experimental Economics (formerly The Journal of Socio-Economics), Elsevier, vol. 34(2), pages 135-150, March.
    2. Masakazu Agetsuma & Issei Sato & Yasuhiro R. Tanaka & Luis Carrillo-Reid & Atsushi Kasai & Atsushi Noritake & Yoshiyuki Arai & Miki Yoshitomo & Takashi Inagaki & Hiroshi Yukawa & Hitoshi Hashimoto & J, 2023. "Activity-dependent organization of prefrontal hub-networks for associative learning and signal transformation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    3. Hamed Tajedin & Hamed Tajedin & Mohammad Keyhani, 2019. "A Theory of Digital Firm-Designed Markets: Defying Knowledge Constraints with Crowds and Marketplaces," Strategy Science, INFORMS, vol. 4(4), pages 323-342, December.
    4. Kosha J. Mehta, 2022. "Effect of sleep and mood on academic performance—at interface of physiology, psychology, and education," Palgrave Communications, Palgrave Macmillan, vol. 9(1), pages 1-13, December.
    5. Mathias Basner & Uwe Siebert, 2010. "Markov Processes for the Prediction of Aircraft Noise Effects on Sleep," Medical Decision Making, , vol. 30(2), pages 275-289, March.
    6. Dolan, Paul & Metcalfe, Robert, 2012. "The relationship between innovation and subjective wellbeing," Research Policy, Elsevier, vol. 41(8), pages 1489-1498.
    7. Heather C. Ratigan & Seetha Krishnan & Shai Smith & Mark E. J. Sheffield, 2023. "A thalamic-hippocampal CA1 signal for contextual fear memory suppression, extinction, and discrimination," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Masanori Nomoto & Emi Murayama & Shuntaro Ohno & Reiko Okubo-Suzuki & Shin-ichi Muramatsu & Kaoru Inokuchi, 2022. "Hippocampus as a sorter and reverberatory integrator of sensory inputs," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Guohong Helen Han & P. D. Harms & Yuntao Bai, 2017. "Nightmare Bosses: The Impact of Abusive Supervision on Employees’ Sleep, Emotions, and Creativity," Journal of Business Ethics, Springer, vol. 145(1), pages 21-31, September.
    10. Amanda J. Williamson & Martina Battisti & Michael Leatherbee & J. Jeffrey Gish, 2019. "Rest, Zest, and My Innovative Best: Sleep and Mood as Drivers of Entrepreneurs’ Innovative Behavior," Entrepreneurship Theory and Practice, , vol. 43(3), pages 582-610, May.
    11. Richard Curtin, 2021. "Nonconscious cognitive reasoning: A neglected ability shaping economic behavior," Journal of Behavioral Economics for Policy, Society for the Advancement of Behavioral Economics (SABE), vol. 5(S3), pages 35-43, October.
    12. Hiuyan Lau & Sara E Alger & William Fishbein, 2011. "Relational Memory: A Daytime Nap Facilitates the Abstraction of General Concepts," PLOS ONE, Public Library of Science, vol. 6(11), pages 1-6, November.
    13. Sprugnoli, Giulia & Rossi, Simone & Emmendorfer, Alexandra & Rossi, Alessandro & Liew, Sook-Lei & Tatti, Elisa & di Lorenzo, Giorgio & Pascual-Leone, Alvaro & Santarnecchi, Emiliano, 2017. "Neural correlates of Eureka moment," Intelligence, Elsevier, vol. 62(C), pages 99-118.
    14. Eelco V van Dongen & Jan-Willem Thielen & Atsuko Takashima & Markus Barth & Guillén Fernández, 2012. "Sleep Supports Selective Retention of Associative Memories Based on Relevance for Future Utilization," PLOS ONE, Public Library of Science, vol. 7(8), pages 1-6, August.

    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:15:y:2024:i:1:d:10.1038_s41467-024-48816-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.

    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.