Selective engram coreactivation in idling brain inspires implicit learning

被引:18
作者
Aly, Mohamed H. [1 ,2 ,3 ,4 ]
Abdou, Kareem [1 ,2 ,3 ,5 ]
Okubo-Suzuki, Reiko [1 ,2 ,3 ]
Nomoto, Masanori [1 ,2 ,3 ]
Inokuchi, Kaoru [1 ,2 ,3 ]
机构
[1] Univ Toyama, Res Ctr Idling Brain Sci, Toyama 9300194, Japan
[2] Univ Toyama, Grad Sch Med & Pharmaceut Sci, Dept Biochem, Toyama 9300194, Japan
[3] Univ Toyama, Japan Sci & Technol Agcy JST, Core Res Evolutionary Sci & Technol Crest, Toyama 9300194, Japan
[4] British Univ Egypt, Fac Pharm, Pharmacol Dept, Cairo 11837, Egypt
[5] Cairo Univ, Fac Pharm, Dept Biochem, Cairo 11562, Egypt
基金
日本科学技术振兴机构; 日本学术振兴会;
关键词
knowledge assimilation; idling brain; engram; sleep; implicit learning; ANTERIOR CINGULATE CORTEX; NEURAL MECHANISMS; MEMORY REPLAY; SLEEP; HIPPOCAMPAL; REPRESENTATION; CONSOLIDATION; REACTIVATION; ASSOCIATION; INTEGRATION;
D O I
10.1073/pnas.2201578119
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Passive priming of prior knowledge to assimilate ongoing experiences underlies advanced cognitive processing. However, the necessary neural dynamics of memory assimilation remains elusive. Uninstructed brain could also show boosted creativity, particularly after idling states, yet it remains unclear whether the idling brain can spontaneously spark relevant knowledge assimilations. We established a paradigm that links/separates context-dependent memories according to geometrical similarities. Mice exploring one of four contexts 1 d before undergoing contextual fear conditioning in a square context showed a gradual fear transfer to preexposed geometrically relevant contexts the next day, but not after 15 min. Anterior cingulate cortex neurons representing relevant, rather than distinct, memories were significantly coreactivated during postconditioning sleep only, before their selective integration the next day during testing. Disrupting sleep coreactivations prevented assimilation while preserving recent memory consolidation. Thus, assimilating pertinent memories during sleep through coreactivation of their respective engrams represents the neural underpinnings of sleep-triggered implicit cortical learning.
引用
收藏
页数:12
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共 46 条
[1]  
Abdou K, 2023, bioRxiv, DOI [10.1101/2021.04.08.439095, 10.1101/2021.04.08.439095, DOI 10.1101/2021.04.08.439095]
[2]   Synapse-specific representation of the identity of overlapping memory engrams [J].
Abdou, Kareem ;
Shehata, Mohammad ;
Choko, Kiriko ;
Nishizono, Hirofumi ;
Matsuo, Mina ;
Muramatsu, Shin-ichi ;
Inokuchi, Kaoru .
SCIENCE, 2018, 360 (6394) :1227-1231
[3]   Pcdhβ deficiency affects hippocampal CA1 ensemble activity and contextual fear discrimination [J].
Asai, Hirotaka ;
Ohkawa, Noriaki ;
Saitoh, Yoshito ;
Ghandour, Khaled ;
Murayama, Emi ;
Nishizono, Hirofumi ;
Matsuo, Mina ;
Hirayama, Teruyoshi ;
Kaneko, Ryosuke ;
Muramatsu, Shin-ichi ;
Yagi, Takeshi ;
Inokuchi, Kaoru .
MOLECULAR BRAIN, 2020, 13 (01)
[4]   Neuronal Computation Underlying Inferential Reasoning in Humans and Mice [J].
Barron, Helen C. ;
Reeve, Hayley M. ;
Koolschijn, Renee S. ;
Perestenko, Pavel, V ;
Shpektor, Anna ;
Nili, Hamed ;
Rothaermel, Roman ;
Campo-Urriza, Natalia ;
O'Reilly, Jill X. ;
Bannerman, David M. ;
Behrens, Timothy E. J. ;
Dupret, David .
CELL, 2020, 183 (01) :228-+
[5]   Online evaluation of novel choices by simultaneous representation of multiple memories [J].
Barron, Helen C. ;
Dolan, Raymond J. ;
Behrens, Timothy E. J. .
NATURE NEUROSCIENCE, 2013, 16 (10) :1492-+
[6]   Utility of the Idling Brain: Abstraction of New Knowledge [J].
Buzsaki, Gyorgy ;
Fernandez-Ruiz, Antonio .
CELL, 2019, 178 (03) :513-515
[7]   The Role of Sleep in Forming a Memory Representation of a Two-Dimensional Space [J].
Coutanche, Marc N. ;
Gianessi, Carol A. ;
Chanales, Avi J. H. ;
Willison, Kate W. ;
Thompson-Schill, Sharon L. .
HIPPOCAMPUS, 2013, 23 (12) :1189-1197
[8]   Explicit memory creation during sleep demonstrates a causal role of place cells in navigation [J].
de lavilleon, Gaetan ;
Lacroix, Marie Masako ;
Rondi-Reig, Laure ;
Benchenane, Karim .
NATURE NEUROSCIENCE, 2015, 18 (04) :493-+
[9]   Sleep enhances category learning [J].
Djonlagic, Ina ;
Rosenfeld, Andrew ;
Shohamy, Daphna ;
Myers, Catherine ;
Gluck, Mark ;
Stickgold, Robert .
LEARNING & MEMORY, 2009, 16 (12) :751-755
[10]   Involvement of the anterior cingulate cortex in formation, consolidation, and reconsolidation of recent and remote contextual fear memory [J].
Einarsson, Einar Oe. ;
Nader, Karim .
LEARNING & MEMORY, 2012, 19 (10) :449-452