Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval

Emotional memories require coordinated activity of the amygdala and hippocampus. Human intracranial recordings have shown that formation of aversive memories involves an amygdala theta-hippocampal gamma phase code. Yet, the mechanisms engaged during translation of aversive experiences into memories...

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Authors: Costa, Manuela|||0000-0001-6251-7900, Pacheco Estefan, Daniel|||0000-0003-2253-5172, Gil-Nagel, Antonio|||0000-0003-4515-0793, Toledano, Rafael|||0000-0002-9387-1088, Imbach, Lukas|||0000-0002-6135-8642, Sarnthein, Johannes|||0000-0001-9141-381X, Strange, Bryan A.|||0000-0001-6476-4091
Format: article
Publication Date:2025
Country:España
Institution:Universitat Autònoma de Barcelona
Repository:Dipòsit Digital de Documents de la UAB
Language:English
OAI Identifier:oai:ddd.uab.cat:320225
Online Access:https://ddd.uab.cat/record/320225
https://dx.doi.org/urn:doi:10.1038/s41467-025-61928-2
Access Level:Open access
Keyword:Amygdala
Hippocampus
id ES_a374d5979edfcb7a52f7e243fcdb426d
oai_identifier_str oai:ddd.uab.cat:320225
network_acronym_str ES
network_name_str España
repository_id_str
spelling Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrievalCosta, Manuela|||0000-0001-6251-7900Pacheco Estefan, Daniel|||0000-0003-2253-5172Gil-Nagel, Antonio|||0000-0003-4515-0793Toledano, Rafael|||0000-0002-9387-1088Imbach, Lukas|||0000-0002-6135-8642Sarnthein, Johannes|||0000-0001-9141-381XStrange, Bryan A.|||0000-0001-6476-4091AmygdalaHippocampusEmotional memories require coordinated activity of the amygdala and hippocampus. Human intracranial recordings have shown that formation of aversive memories involves an amygdala theta-hippocampal gamma phase code. Yet, the mechanisms engaged during translation of aversive experiences into memories and subsequent retrieval remain unclear. Directly recording from human amygdala and hippocampus, here we show that hippocampal gamma activity increases for correctly remembered aversive scenes. Crucially, patterns of amygdala high amplitude gamma activity at encoding are reactivated in the hippocampus, but not amygdala, during both aversive encoding and retrieval. Trial-specific hippocampal gamma patterns showing highest representational similarity with amygdala activity at encoding are reactivated in the hippocampus during aversive retrieval. This reactivation process occurs against a background of gamma activity that is otherwise decorrelated between encoding and retrieval. Thus, phasic hippocampal gamma responses track the retrieval of aversive memories, with activity patterns apparently entrained by the amygdala during encoding. 22025-01-0120252025-01-01Articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://ddd.uab.cat/record/320225https://dx.doi.org/urn:doi:10.1038/s41467-025-61928-2reponame:Dipòsit Digital de Documents de la UABinstname:Universitat Autònoma de BarcelonaInglésengEuropean Commission https://doi.org/10.13039/501100000780 819814open accesshttp://purl.org/coar/access_right/c_abf2Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, i la comunicació pública de l'obra, sempre que no sigui amb finalitats comercials, i sempre que es reconegui l'autoria de l'obra original. No es permet la creació d'obres derivades.https://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:ddd.uab.cat:3202252026-06-06T12:50:31Z
dc.title.none.fl_str_mv Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval
title Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval
spellingShingle Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval
Costa, Manuela|||0000-0001-6251-7900
Amygdala
Hippocampus
title_short Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval
title_full Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval
title_fullStr Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval
title_full_unstemmed Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval
title_sort Human hippocampal reactivation of amygdala encoding-related gamma patterns during aversive memory retrieval
dc.creator.none.fl_str_mv Costa, Manuela|||0000-0001-6251-7900
Pacheco Estefan, Daniel|||0000-0003-2253-5172
Gil-Nagel, Antonio|||0000-0003-4515-0793
Toledano, Rafael|||0000-0002-9387-1088
Imbach, Lukas|||0000-0002-6135-8642
Sarnthein, Johannes|||0000-0001-9141-381X
Strange, Bryan A.|||0000-0001-6476-4091
author Costa, Manuela|||0000-0001-6251-7900
author_facet Costa, Manuela|||0000-0001-6251-7900
Pacheco Estefan, Daniel|||0000-0003-2253-5172
Gil-Nagel, Antonio|||0000-0003-4515-0793
Toledano, Rafael|||0000-0002-9387-1088
Imbach, Lukas|||0000-0002-6135-8642
Sarnthein, Johannes|||0000-0001-9141-381X
Strange, Bryan A.|||0000-0001-6476-4091
author_role author
author2 Pacheco Estefan, Daniel|||0000-0003-2253-5172
Gil-Nagel, Antonio|||0000-0003-4515-0793
Toledano, Rafael|||0000-0002-9387-1088
Imbach, Lukas|||0000-0002-6135-8642
Sarnthein, Johannes|||0000-0001-9141-381X
Strange, Bryan A.|||0000-0001-6476-4091
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Amygdala
Hippocampus
topic Amygdala
Hippocampus
description Emotional memories require coordinated activity of the amygdala and hippocampus. Human intracranial recordings have shown that formation of aversive memories involves an amygdala theta-hippocampal gamma phase code. Yet, the mechanisms engaged during translation of aversive experiences into memories and subsequent retrieval remain unclear. Directly recording from human amygdala and hippocampus, here we show that hippocampal gamma activity increases for correctly remembered aversive scenes. Crucially, patterns of amygdala high amplitude gamma activity at encoding are reactivated in the hippocampus, but not amygdala, during both aversive encoding and retrieval. Trial-specific hippocampal gamma patterns showing highest representational similarity with amygdala activity at encoding are reactivated in the hippocampus during aversive retrieval. This reactivation process occurs against a background of gamma activity that is otherwise decorrelated between encoding and retrieval. Thus, phasic hippocampal gamma responses track the retrieval of aversive memories, with activity patterns apparently entrained by the amygdala during encoding.
publishDate 2025
dc.date.none.fl_str_mv 2
2025-01-01
2025
2025-01-01
dc.type.none.fl_str_mv Article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://ddd.uab.cat/record/320225
https://dx.doi.org/urn:doi:10.1038/s41467-025-61928-2
url https://ddd.uab.cat/record/320225
https://dx.doi.org/urn:doi:10.1038/s41467-025-61928-2
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv European Commission https://doi.org/10.13039/501100000780 819814
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by-nc-nd/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Dipòsit Digital de Documents de la UAB
instname:Universitat Autònoma de Barcelona
instname_str Universitat Autònoma de Barcelona
reponame_str Dipòsit Digital de Documents de la UAB
collection Dipòsit Digital de Documents de la UAB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,812429

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