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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
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    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.
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