journal article·2024-10Open access

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

Shiyin Li, Xin Li, Minmin Lu, Quanhui Chen, Di Yao, Xiaoqian Yu, Zhen Li, Woo‐ping Ge, Na Wang, Jiehua Jin, Yaling Wang, Yixiang Liao, Fenlan Luo, Jie Yan, Xuedan Chen, Chenggang Jiang, Faguo Yue, Dong Gao, Xiangdong Tang, Hong Guo, Yanjiang Wang, Xiaowei Chen, Jianxia Xia, Min Xu, Shuancheng Ren, Chao He, Zhian Hu

Advanced Science· Volume 11· Issue 38

Abstract

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.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Sleep and Wakefulness Research · Circadian rhythm and melatonin · Photoreceptor and optogenetics research

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Physiology Institute of Brain and Intelligence Third Military Medical University Chongqing 400038 China

School of Basic Medical Sciences and IDG/McGovern Institute for Brain Research Tsinghua University Beijing 100084 China

School of Basic Medical Sciences Capital Medical University Beijing 100069 China

Chinese Institute for Brain Research Beijing 102206 China

Department of Medical Genetics College of Basic Medical Sciences Third Military Medical University Chongqing 400038 China

Department of Sleep and Psychology Chongqing Health Center for Women and Children Chongqing 401147 China

Sleep and Psychology Center Bishan Hospital of Chongqing Medical University Chongqing 402760 China

Department of Sleep and Psychology The Fifth People's Hospital of Chongqing Chongqing 400062 China

Sleep Medicine Center Laboratory of Anaesthesia and Critical Care Medicine Translational Neuroscience Center West China Hospital Sichuan University Chengdu 610041 China

Department of Neurology Daping Hospital Third Military Medical University Chongqing 400042 China

Chongqing Institute for Brain and Intelligence Guangyang Bay Laboratory Chongqing 400064 China

Brain Research Center Institute of Brain and Intelligence Third Military Medical University Chongqing 400038 China

Institute of Neuroscience,Center for Excellence in Brain Science and Intelligence Technology Chinese Academy of Sciences Shanghai 200031 China

Funding

National Natural Science Foundation of China

References (74)

Show source-provided references
1. 10.1126/science.124909810.1126/science.1249098 ↗
2. 10.1038/nrn130110.1038/nrn1301 ↗
3. 10.1038/nrn325810.1038/nrn3258 ↗
4. 10.1126/science.aao070210.1126/science.aao0702 ↗
5. 10.1126/science.aat149310.1126/science.aat1493 ↗
6. 10.1016/j.brainresbull.2003.09.00410.1016/j.brainresbull.2003.09.004 ↗
7. 10.1126/science.aai835510.1126/science.aai8355 ↗
8. 10.1126/science.aah598210.1126/science.aah5982 ↗
9. 10.1126/science.120283910.1126/science.1202839 ↗
10. 10.1007/s12264-019-00453-x10.1007/s12264-019-00453-x ↗
11. 10.1016/j.smrv.2004.08.00110.1016/j.smrv.2004.08.001 ↗
12. 10.5664/jcsm.2708310.5664/jcsm.27083 ↗
13. 10.1177/074873041559175310.1177/0748730415591753 ↗
14. 10.1016/j.drudis.2014.04.01410.1016/j.drudis.2014.04.014 ↗
15. 10.1124/jpet.118.25326010.1124/jpet.118.253260 ↗
16. 10.1016/j.febslet.2004.10.08310.1016/j.febslet.2004.10.083 ↗
17. 10.1523/ENEURO.0067-20.202010.1523/ENEURO.0067-20.2020 ↗
18. 10.1523/JNEUROSCI.2808-10.201010.1523/JNEUROSCI.2808-10.2010 ↗
19. 10.1038/nn.465310.1038/nn.4653 ↗
20. 10.1038/nrn.2016.2110.1038/nrn.2016.21 ↗
21. 10.1093/cercor/bhx14510.1093/cercor/bhx145 ↗
22. 10.7554/eLife.3666410.7554/eLife.36664 ↗
23. 10.1210/en.2010-126010.1210/en.2010-1260 ↗
24. 10.1080/07420528.2019.162437310.1080/07420528.2019.1624373 ↗
25. 10.3390/ijms22241324010.3390/ijms222413240 ↗
26. 10.1523/JNEUROSCI.2676-11.201110.1523/JNEUROSCI.2676-11.2011 ↗
27. 10.1016/j.bbr.2013.01.00810.1016/j.bbr.2013.01.008 ↗
28. 10.1111/jpi.1236010.1111/jpi.12360 ↗
29. 10.1111/j.1600-079X.2011.00931.x10.1111/j.1600-079X.2011.00931.x ↗
30. 10.1002/cne.2476410.1002/cne.24764 ↗
31. 10.1111/j.1460-9568.2010.07270.x10.1111/j.1460-9568.2010.07270.x ↗
32. 10.1038/nrn269910.1038/nrn2699 ↗
33. Tu X. · Sci. Rep.‐Uk · 2020 · 10
34. 10.1093/cercor/bhu32210.1093/cercor/bhu322 ↗
35. 10.1016/j.neuron.2009.06.02210.1016/j.neuron.2009.06.022 ↗
36. 10.1111/j.1365-2826.2010.02063.x10.1111/j.1365-2826.2010.02063.x ↗
37. 10.1126/science.aat251210.1126/science.aat2512 ↗
38. 10.1126/scisignal.aaf671610.1126/scisignal.aaf6716 ↗
39. 10.1038/s41586-018-0218-810.1038/s41586-018-0218-8 ↗
40. 10.1172/JCI12577110.1172/JCI125771 ↗
41. 10.1038/s41586-021-04125-710.1038/s41586-021-04125-7 ↗
42. 10.7554/eLife.8300810.7554/eLife.83008 ↗
43. 10.1016/j.smrv.2005.05.00210.1016/j.smrv.2005.05.002 ↗
44. 10.1007/s00018-017-2609-710.1007/s00018-017-2609-7 ↗
45. 10.1007/s00018-017-2616-810.1007/s00018-017-2616-8 ↗
46. 10.1111/jpi.1202610.1111/jpi.12026 ↗
47. Kerenyi N. A. · Cell Mol. Biol. Incl. Cyto. Enzymol. · 1979 · 25 · 259
48. 10.1021/bi050202d10.1021/bi050202d ↗
49. 10.5152/eurasianjmed.2015.026710.5152/eurasianjmed.2015.0267 ↗
50. 10.1523/JNEUROSCI.1243-20.202010.1523/JNEUROSCI.1243-20.2020 ↗
51. 10.1124/molpharm.120.00010510.1124/molpharm.120.000105 ↗
52. 10.1073/pnas.170576811410.1073/pnas.1705768114 ↗
53. 10.1146/annurev-pharmtox-010814-12474210.1146/annurev-pharmtox-010814-124742 ↗
54. 10.1016/j.tips.2005.06.00610.1016/j.tips.2005.06.006 ↗
55. 10.1111/jpi.1222410.1111/jpi.12224 ↗
56. 10.1007/s10571-009-9447-610.1007/s10571-009-9447-6 ↗
57. 10.1126/science.124122410.1126/science.1241224 ↗
58. 10.1016/j.neuron.2023.10.01210.1016/j.neuron.2023.10.012 ↗
59. 10.1126/science.abb055610.1126/science.abb0556 ↗
60. 10.1002/hipo.2074510.1002/hipo.20745 ↗
61. 10.1016/j.exger.2009.02.00210.1016/j.exger.2009.02.002 ↗
62. 10.1016/j.bbr.2013.01.00810.1016/j.bbr.2013.01.008 ↗
63. 10.1111/bph.1411610.1111/bph.14116 ↗
64. 10.1111/sbr.1203910.1111/sbr.12039 ↗
65. Archer S. · Sleep · 2007 · 30 · A54
66. 10.1016/j.cell.2015.07.01810.1016/j.cell.2015.07.018 ↗
67. 10.1007/s12264-017-0111-810.1007/s12264-017-0111-8 ↗
68. 10.1007/s12264-023-01080-310.1007/s12264-023-01080-3 ↗
69. Wang Y. · Neurosci. Bull. · 2023 · 201
70. 10.1016/j.bbr.2015.02.04010.1016/j.bbr.2015.02.040 ↗
71. 10.1371/journal.pone.008356110.1371/journal.pone.0083561 ↗
72. 10.1016/j.jpain.2009.05.00510.1016/j.jpain.2009.05.005 ↗
73. 10.1038/s41586-018-0716-810.1038/s41586-018-0716-8 ↗
74. 10.1007/s12264-020-00625-010.1007/s12264-020-00625-0 ↗