Isolated theta waves originating from the midline thalamus trigger memory reactivation during NREM sleep in mice

Qin Xiao, Minmin Lu, Xiaolong Zhang, Jiangheng Guan, Xin Li, Ruyi Wen, Na Wang, Ling Qian, Yixiang Liao, Zehui Zhang, Xiang Liao, Chenggang Jiang, Faguo Yue, Shuancheng Ren, Jianxia Xia, Jun Hu, Fenlan Luo (), Zhian Hu () and Chao He ()
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Qin Xiao: Third Military Medical University
Minmin Lu: Third Military Medical University
Xiaolong Zhang: Third Military Medical University
Jiangheng Guan: General Hospital of Chinese PLA Central Theater Command
Xin Li: Third Military Medical University
Ruyi Wen: Third Military Medical University
Na Wang: Third Military Medical University
Ling Qian: Third Military Medical University
Yixiang Liao: Third Military Medical University
Zehui Zhang: College of Basic Medical Sciences of Jilin University
Xiang Liao: Chongqing University
Chenggang Jiang: Chongqing Health Center for Women and Children
Faguo Yue: Bishan Hospital of Chongqing Medical University
Shuancheng Ren: Third Military Medical University
Jianxia Xia: Third Military Medical University
Jun Hu: Third Military Medical University
Fenlan Luo: Third Military Medical University
Zhian Hu: Third Military Medical University
Chao He: Third Military Medical University

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract During non-rapid eye movement (NREM) sleep, neural ensembles in the entorhinal-hippocampal circuit responsible for encoding recent memories undergo reactivation to facilitate the process of memory consolidation. This reactivation is widely acknowledged as pivotal for the formation of stable memory and its impairment is closely associated with memory dysfunction. To date, the neural mechanisms driving the reactivation of neural ensembles during NREM sleep remain poorly understood. Here, we show that the neural ensembles in the medial entorhinal cortex (MEC) that encode spatial experiences exhibit reactivation during NREM sleep. Notably, this reactivation consistently coincides with isolated theta waves. In addition, we found that the nucleus reuniens (RE) in the midline thalamus exhibits typical theta waves during NREM sleep, which are highly synchronized with those occurring in the MEC in male mice. Closed-loop optogenetic inhibition of the RE-MEC pathway specifically suppressed these isolated theta waves, resulting in impaired reactivation and compromised memory consolidation following a spatial memory task in male mice. The findings suggest that theta waves originating from the ventral midline thalamus play a role in initiating memory reactivation and consolidation during sleep.

Date: 2024
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DOI: 10.1038/s41467-024-53522-9

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