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Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala

Extinction memory retrieval is influenced by spatial contextual information that determines responding to conditioned stimuli (CS). However, it is poorly understood whether contextual representations are imbued with emotional values to support memory selection. Here, we performed activity-dependent...

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Autores principales: Nguyen, Robin, Koukoutselos, Konstantinos, Forro, Thomas, Ciocchi, Stéphane
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Association for the Advancement of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10413664/
https://www.ncbi.nlm.nih.gov/pubmed/37256958
http://dx.doi.org/10.1126/sciadv.adg4881
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author Nguyen, Robin
Koukoutselos, Konstantinos
Forro, Thomas
Ciocchi, Stéphane
author_facet Nguyen, Robin
Koukoutselos, Konstantinos
Forro, Thomas
Ciocchi, Stéphane
author_sort Nguyen, Robin
collection PubMed
description Extinction memory retrieval is influenced by spatial contextual information that determines responding to conditioned stimuli (CS). However, it is poorly understood whether contextual representations are imbued with emotional values to support memory selection. Here, we performed activity-dependent engram tagging and in vivo single-unit electrophysiological recordings from the ventral hippocampus (vH) while optogenetically manipulating basolateral amygdala (BLA) inputs during the formation of cued fear extinction memory. During fear extinction when CS acquire safety properties, we found that CS-related activity in the vH reactivated during sleep consolidation and was strengthened upon memory retrieval. Moreover, fear extinction memory was facilitated when the extinction context exhibited precise coding of its affective zones. Last, these activity patterns along with the retrieval of the fear extinction memory were dependent on glutamatergic transmission from the BLA during extinction learning. Thus, fear extinction memory relies on the formation of contextual and stimulus safety representations in the vH instructed by the BLA.
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spelling pubmed-104136642023-08-11 Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala Nguyen, Robin Koukoutselos, Konstantinos Forro, Thomas Ciocchi, Stéphane Sci Adv Neuroscience Extinction memory retrieval is influenced by spatial contextual information that determines responding to conditioned stimuli (CS). However, it is poorly understood whether contextual representations are imbued with emotional values to support memory selection. Here, we performed activity-dependent engram tagging and in vivo single-unit electrophysiological recordings from the ventral hippocampus (vH) while optogenetically manipulating basolateral amygdala (BLA) inputs during the formation of cued fear extinction memory. During fear extinction when CS acquire safety properties, we found that CS-related activity in the vH reactivated during sleep consolidation and was strengthened upon memory retrieval. Moreover, fear extinction memory was facilitated when the extinction context exhibited precise coding of its affective zones. Last, these activity patterns along with the retrieval of the fear extinction memory were dependent on glutamatergic transmission from the BLA during extinction learning. Thus, fear extinction memory relies on the formation of contextual and stimulus safety representations in the vH instructed by the BLA. American Association for the Advancement of Science 2023-05-31 /pmc/articles/PMC10413664/ /pubmed/37256958 http://dx.doi.org/10.1126/sciadv.adg4881 Text en Copyright © 2023 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). https://creativecommons.org/licenses/by-nc/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license (https://creativecommons.org/licenses/by-nc/4.0/) , which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.
spellingShingle Neuroscience
Nguyen, Robin
Koukoutselos, Konstantinos
Forro, Thomas
Ciocchi, Stéphane
Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala
title Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala
title_full Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala
title_fullStr Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala
title_full_unstemmed Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala
title_short Fear extinction relies on ventral hippocampal safety codes shaped by the amygdala
title_sort fear extinction relies on ventral hippocampal safety codes shaped by the amygdala
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10413664/
https://www.ncbi.nlm.nih.gov/pubmed/37256958
http://dx.doi.org/10.1126/sciadv.adg4881
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