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

Kareem Abdou, Masanori Nomoto, Mohamed H. Aly, Ahmed Z. Ibrahim, Kiriko Choko, Reiko Okubo-Suzuki, Shin-ichi Muramatsu and Kaoru Inokuchi ()
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Kareem Abdou: University of Toyama
Masanori Nomoto: University of Toyama
Mohamed H. Aly: University of Toyama
Ahmed Z. Ibrahim: University of Toyama
Kiriko Choko: University of Toyama
Reiko Okubo-Suzuki: University of Toyama
Shin-ichi Muramatsu: Jichi Medical University
Kaoru Inokuchi: University of Toyama

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-48816-x

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