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  3. Homeostatic Shrinkage of Dendritic Spines Requires Melatonin Type 3 Receptor Activation During Sleep

Homeostatic Shrinkage of Dendritic Spines Requires Melatonin Type 3 Receptor Activation During Sleep

  • Adv Sci (Weinh). 2024 Aug 9:e2400253. doi: 10.1002/advs.202400253.
Shiyin Li 1,  Xin Li 1 2,  Minmin Lu 1,  Quanhui Chen 1,  Di Yao 3 4,  Xiaoqian Yu 4,  Zhen Li 4,  Woo-Ping Ge 4,  Na Wang 1,  Jiehua Jin 1,  Yaling Wang 1,  Yixiang Liao 1,  Fenlan Luo 1,  Jie Yan 1,  Xuedan Chen 5,  Chenggang Jiang 6,  Faguo Yue 7,  Dong Gao 8,  Xiangdong Tang 9,  Hong Guo 5,  Yanjiang Wang 10 11,  Xiaowei Chen 11 12,  Jianxia Xia 1,  Min Xu 13,  Shuancheng Ren 1,  Chao He 1,  Zhian Hu 1 11
Affiliations

Affiliations

  • 1 Department of Physiology, Institute of Brain and Intelligence, Third Military Medical University, Chongqing, 400038, China.
  • 2 School of Basic Medical Sciences and IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing, 100084, China.
  • 3 School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.
  • 4 Chinese Institute for Brain Research, Beijing, 102206, China.
  • 5 Department of Medical Genetics, College of Basic Medical Sciences, Third Military Medical University, Chongqing, 400038, China.
  • 6 Department of Sleep and Psychology, Chongqing Health Center for Women and Children, Chongqing, 401147, China.
  • 7 Sleep and Psychology Center, Bishan Hospital of Chongqing Medical University, Chongqing, 402760, China.
  • 8 Department of Sleep and Psychology, The Fifth People's Hospital of Chongqing, Chongqing, 400062, China.
  • 9 Sleep Medicine Center, Laboratory of Anaesthesia and Critical Care Medicine, Translational Neuroscience Center, West China Hospital, Sichuan University, Chengdu, 610041, China.
  • 10 Department of Neurology, Daping Hospital, Third Military Medical University, Chongqing, 400042, China.
  • 11 Chongqing Institute for Brain and Intelligence, Guangyang Bay Laboratory, Chongqing, 400064, China.
  • 12 Brain Research Center, Institute of Brain and Intelligence, Third Military Medical University, Chongqing, 400038, China.
  • 13 Institute of Neuroscience，Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, 200031, China.
PMID: 39119847 DOI: 10.1002/advs.202400253
Abstract

High-frequency oscillatory activity in cognition-related neural circuits during wakefulness consistently induces the growth of dendritic spines and axonal terminals. Although these structural changes are essential for cognitive functions, it is hypothesized that if these newly expanded structures fail to establish functional connections, they may become superfluous. Sleep is believed to facilitate the reduction of such redundant structures to maintain neural homeostasis. However, the mechanisms underlying this pruning process during sleep remain poorly understood. In this study, that melatonin type 3 receptors (MT3Rs) are selectively expressed in the stellate neurons of the medial entorhinal cortex (MEC) is demonstrated, an area where high melatonin levels are detected during sleep. Activation of MT3Rs during sleep initiates the shrinkage of dendritic spines in stellate neurons by downregulating neural network activity and dephosphorylating synaptic proteins in the MEC. This process is disrupted when MT3R expression is knocked down or when MT3Rs are blocked during sleep. Notably, interference with MT3Rs in the MEC during sleep impairs the acquisition of spatial memory but does not affect object memory acquisition following sleep. These findings reveal novel molecular mechanisms involving melatonin and MT3Rs in the regulation of dendritic spine shrinkage during sleep, which is crucial for the acquisition and consolidation of spatial memory.

Keywords

medial entorhinal cortex; melatonin; sleep; spatial memory.

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