Contributions of repeated learning to memory in humans: insights from single-neuron recordings in the hippocampus and amygdala

doi:10.1093/cercor/bhae244

	Contributions of repeated learning to memory in humans: insights from single-neuron recordings in the hippocampus and amygdala
	Xiao, Xinyu1,2 ; Li, Jin3 ; Cao, Dan2 ; Zhang, Jiaqi1,2 ; Jiang, Tianzi1,2,4,5,6
发表期刊	CEREBRAL CORTEX
ISSN	1047-3211
	2024-06-10
卷号	34 期号:6 页码:9
通讯作者	Jiang, Tianzi(jiangtz@nlpr.ia.ac.cn)
摘要	Despite the well-established phenomenon of improved memory performance through repeated learning, studies investigating the associated neural mechanisms have yielded complex and sometimes contradictory findings, and direct evidence from human neuronal recordings has been lacking. This study employs single-neuron recordings with exceptional spatial-temporal resolution, combined with representational similarity analysis, to explore the neural dynamics within the hippocampus and amygdala during repeated learning. Our results demonstrate that in the hippocampus, repetition enhances both representational specificity and fidelity, with these features predicting learning times. Conversely, the amygdala exhibits heightened representational specificity and fidelity during initial learning but does not show improvement with repetition, suggesting functional specialization of the hippocampus and amygdala during different stages of the learning repetition. Specifically, the hippocampus appears to contribute to sustained engagement necessary for benefiting from repeated learning, while the amygdala may play a role in the representation of novel items. These findings contribute to a comprehensive understanding of the intricate interplay between these brain regions in memory processes.Significance statement For over a century, understanding how repetition contributes to memory enhancement has captivated researchers, yet direct neuronal evidence has been lacking, with a primary focus on the hippocampus and a neglect of the neighboring amygdala. Employing advanced single-neuron recordings and analytical techniques, this study unveils a nuanced functional specialization within the amygdala-hippocampal circuit during various learning repetition. The results highlight the hippocampus's role in sustaining engagement for improved memory with repetition, contrasting with the amygdala's superior ability in representing novel items. This exploration not only deepens our comprehension of memory enhancement intricacies but also sheds light on potential interventions to optimize learning and memory processes.
关键词	repeated learning single-neuron recordings representational similarity analysis hippocampus amygdala
DOI	10.1093/cercor/bhae244
关键词[WOS]	PATTERN SEPARATION ; REPRESENTATIONS ; SIMILARITY
收录类别	SCI
语种	英语
资助项目	STI2030-Major Projects[2021ZD0200200] ; National Natural Science Foundation of China[32271085] ; National Natural Science Foundation of China[62327805] ; Key Research Project of Zhejiang Lab[2022KI0AC02] ; Key Research Project of Zhejiang Lab[2022ND0AN01]
项目资助者	STI2030-Major Projects ; National Natural Science Foundation of China ; Key Research Project of Zhejiang Lab
WOS研究方向	Neurosciences & Neurology
WOS类目	Neurosciences
WOS记录号	WOS:001242388200004
出版者	OXFORD UNIV PRESS INC
引用统计
文献类型	期刊论文
条目标识符	http://ir.ia.ac.cn/handle/173211/58671
专题	脑图谱与类脑智能实验室_脑网络组研究
通讯作者	Jiang, Tianzi
作者单位	1.Chinese Acad Sci, Inst Automat, Tianzi Jiang Brainnetome Ctr, Beijing 100190, Peoples R China 2.Univ Chinese Acad Sci, Sch Artificial Intelligence, Beijing 100049, Peoples R China 3.Capital Normal Univ, Sch Psychol, Beijing 100048, Peoples R China 4.Res Ctr Augmented Intelligence, Zhejiang Lab, Hangzhou 311100, Peoples R China 5.Xiaoxiang Inst Brain Hlth, Yongzhou 425000, Hunan, Peoples R China 6.Yongzhou Cent Hosp, Yongzhou 425000, Hunan, Peoples R China
第一作者单位	中国科学院自动化研究所
通讯作者单位	中国科学院自动化研究所
推荐引用方式 GB/T 7714	Xiao, Xinyu,Li, Jin,Cao, Dan,et al. Contributions of repeated learning to memory in humans: insights from single-neuron recordings in the hippocampus and amygdala[J]. CEREBRAL CORTEX,2024,34(6):9.
APA	Xiao, Xinyu,Li, Jin,Cao, Dan,Zhang, Jiaqi,&Jiang, Tianzi.(2024).Contributions of repeated learning to memory in humans: insights from single-neuron recordings in the hippocampus and amygdala.CEREBRAL CORTEX,34(6),9.
MLA	Xiao, Xinyu,et al."Contributions of repeated learning to memory in humans: insights from single-neuron recordings in the hippocampus and amygdala".CEREBRAL CORTEX 34.6(2024):9.