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Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing

Both the hippocampus and amygdala are involved in working memory (WM) processing. However, their specific role in WM is still an open question. Here, we simultaneously recorded intracranial EEG from the amygdala and hippocampus of epilepsy patients while performing a WM task, and compared their repr...

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Autores principales: Li, Jin, Cao, Dan, Yu, Shan, Xiao, Xinyu, Imbach, Lukas, Stieglitz, Lennart, Sarnthein, Johannes, Jiang, Tianzi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10203226/
https://www.ncbi.nlm.nih.gov/pubmed/37217494
http://dx.doi.org/10.1038/s41467-023-38571-w
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author Li, Jin
Cao, Dan
Yu, Shan
Xiao, Xinyu
Imbach, Lukas
Stieglitz, Lennart
Sarnthein, Johannes
Jiang, Tianzi
author_facet Li, Jin
Cao, Dan
Yu, Shan
Xiao, Xinyu
Imbach, Lukas
Stieglitz, Lennart
Sarnthein, Johannes
Jiang, Tianzi
author_sort Li, Jin
collection PubMed
description Both the hippocampus and amygdala are involved in working memory (WM) processing. However, their specific role in WM is still an open question. Here, we simultaneously recorded intracranial EEG from the amygdala and hippocampus of epilepsy patients while performing a WM task, and compared their representation patterns during the encoding and maintenance periods. By combining multivariate representational analysis and connectivity analyses with machine learning methods, our results revealed a functional specialization of the amygdala-hippocampal circuit: The mnemonic representations in the amygdala were highly distinct and decreased from encoding to maintenance. The hippocampal representations, however, were more similar across different items but remained stable in the absence of the stimulus. WM encoding and maintenance were associated with bidirectional information flow between the amygdala and the hippocampus in low-frequency bands (1–40 Hz). Furthermore, the decoding accuracy on WM load was higher by using representational features in the amygdala during encoding and in the hippocampus during maintenance, and by using information flow from the amygdala during encoding and that from the hippocampus during maintenance, respectively. Taken together, our study reveals that WM processing is associated with functional specialization and interaction within the amygdala-hippocampus circuit.
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spelling pubmed-102032262023-05-24 Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing Li, Jin Cao, Dan Yu, Shan Xiao, Xinyu Imbach, Lukas Stieglitz, Lennart Sarnthein, Johannes Jiang, Tianzi Nat Commun Article Both the hippocampus and amygdala are involved in working memory (WM) processing. However, their specific role in WM is still an open question. Here, we simultaneously recorded intracranial EEG from the amygdala and hippocampus of epilepsy patients while performing a WM task, and compared their representation patterns during the encoding and maintenance periods. By combining multivariate representational analysis and connectivity analyses with machine learning methods, our results revealed a functional specialization of the amygdala-hippocampal circuit: The mnemonic representations in the amygdala were highly distinct and decreased from encoding to maintenance. The hippocampal representations, however, were more similar across different items but remained stable in the absence of the stimulus. WM encoding and maintenance were associated with bidirectional information flow between the amygdala and the hippocampus in low-frequency bands (1–40 Hz). Furthermore, the decoding accuracy on WM load was higher by using representational features in the amygdala during encoding and in the hippocampus during maintenance, and by using information flow from the amygdala during encoding and that from the hippocampus during maintenance, respectively. Taken together, our study reveals that WM processing is associated with functional specialization and interaction within the amygdala-hippocampus circuit. Nature Publishing Group UK 2023-05-22 /pmc/articles/PMC10203226/ /pubmed/37217494 http://dx.doi.org/10.1038/s41467-023-38571-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Li, Jin
Cao, Dan
Yu, Shan
Xiao, Xinyu
Imbach, Lukas
Stieglitz, Lennart
Sarnthein, Johannes
Jiang, Tianzi
Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing
title Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing
title_full Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing
title_fullStr Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing
title_full_unstemmed Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing
title_short Functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing
title_sort functional specialization and interaction in the amygdala-hippocampus circuit during working memory processing
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10203226/
https://www.ncbi.nlm.nih.gov/pubmed/37217494
http://dx.doi.org/10.1038/s41467-023-38571-w
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