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Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization

Neutral events preceding emotional experiences can be better remembered, likely by assigning them as significant to guide possible use in future. Yet, the neurobiological mechanisms of how emotional learning enhances memory for past mundane events remain unclear. By two behavioral studies and one fu...

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Detalles Bibliográficos
Autores principales: Zhu, Yannan, Zeng, Yimeng, Ren, Jingyuan, Zhang, Lingke, Chen, Changming, Fernandez, Guillen, Qin, Shaozheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9815824/
https://www.ncbi.nlm.nih.gov/pubmed/36476501
http://dx.doi.org/10.7554/eLife.60190
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author Zhu, Yannan
Zeng, Yimeng
Ren, Jingyuan
Zhang, Lingke
Chen, Changming
Fernandez, Guillen
Qin, Shaozheng
author_facet Zhu, Yannan
Zeng, Yimeng
Ren, Jingyuan
Zhang, Lingke
Chen, Changming
Fernandez, Guillen
Qin, Shaozheng
author_sort Zhu, Yannan
collection PubMed
description Neutral events preceding emotional experiences can be better remembered, likely by assigning them as significant to guide possible use in future. Yet, the neurobiological mechanisms of how emotional learning enhances memory for past mundane events remain unclear. By two behavioral studies and one functional magnetic resonance imaging study with an adapted sensory preconditioning paradigm, we show rapid neural reactivation and connectivity changes underlying emotion-charged retroactive memory enhancement. Behaviorally, emotional learning retroactively enhanced initial memory for neutral associations across the three studies. Neurally, emotional learning potentiated trial-specific reactivation of overlapping neural traces in the hippocampus and stimulus-relevant neocortex. It further induced rapid hippocampal-neocortical functional reorganization supporting such retroactive memory benefit, as characterized by enhanced hippocampal-neocortical coupling modulated by the amygdala during emotional learning, and a shift of hippocampal connectivity from stimulus-relevant neocortex to distributed transmodal prefrontal-parietal areas at post-learning rests. Together, emotional learning retroactively promotes memory integration for past neutral events through stimulating trial-specific reactivation of overlapping representations and reorganization of associated memories into an integrated network to foster its priority for future use.
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spelling pubmed-98158242023-01-06 Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization Zhu, Yannan Zeng, Yimeng Ren, Jingyuan Zhang, Lingke Chen, Changming Fernandez, Guillen Qin, Shaozheng eLife Neuroscience Neutral events preceding emotional experiences can be better remembered, likely by assigning them as significant to guide possible use in future. Yet, the neurobiological mechanisms of how emotional learning enhances memory for past mundane events remain unclear. By two behavioral studies and one functional magnetic resonance imaging study with an adapted sensory preconditioning paradigm, we show rapid neural reactivation and connectivity changes underlying emotion-charged retroactive memory enhancement. Behaviorally, emotional learning retroactively enhanced initial memory for neutral associations across the three studies. Neurally, emotional learning potentiated trial-specific reactivation of overlapping neural traces in the hippocampus and stimulus-relevant neocortex. It further induced rapid hippocampal-neocortical functional reorganization supporting such retroactive memory benefit, as characterized by enhanced hippocampal-neocortical coupling modulated by the amygdala during emotional learning, and a shift of hippocampal connectivity from stimulus-relevant neocortex to distributed transmodal prefrontal-parietal areas at post-learning rests. Together, emotional learning retroactively promotes memory integration for past neutral events through stimulating trial-specific reactivation of overlapping representations and reorganization of associated memories into an integrated network to foster its priority for future use. eLife Sciences Publications, Ltd 2022-12-08 /pmc/articles/PMC9815824/ /pubmed/36476501 http://dx.doi.org/10.7554/eLife.60190 Text en © 2022, Zhu et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Zhu, Yannan
Zeng, Yimeng
Ren, Jingyuan
Zhang, Lingke
Chen, Changming
Fernandez, Guillen
Qin, Shaozheng
Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
title Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
title_full Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
title_fullStr Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
title_full_unstemmed Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
title_short Emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
title_sort emotional learning retroactively promotes memory integration through rapid neural reactivation and reorganization
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9815824/
https://www.ncbi.nlm.nih.gov/pubmed/36476501
http://dx.doi.org/10.7554/eLife.60190
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