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Odor modulates the temporal dynamics of fear memory consolidation

Systems consolidation (SC) theory proposes that recent, contextually rich memories are stored in the hippocampus (HPC). As these memories become remote, they are believed to rely more heavily on cortical structures within the prefrontal cortex (PFC), where they lose much of their contextual detail a...

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Autores principales: Grella, Stephanie L., Fortin, Amanda H., McKissick, Olivia, Leblanc, Heloise, Ramirez, Steve
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7079569/
https://www.ncbi.nlm.nih.gov/pubmed/32179657
http://dx.doi.org/10.1101/lm.050690.119
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author Grella, Stephanie L.
Fortin, Amanda H.
McKissick, Olivia
Leblanc, Heloise
Ramirez, Steve
author_facet Grella, Stephanie L.
Fortin, Amanda H.
McKissick, Olivia
Leblanc, Heloise
Ramirez, Steve
author_sort Grella, Stephanie L.
collection PubMed
description Systems consolidation (SC) theory proposes that recent, contextually rich memories are stored in the hippocampus (HPC). As these memories become remote, they are believed to rely more heavily on cortical structures within the prefrontal cortex (PFC), where they lose much of their contextual detail and become schematized. Odor is a particularly evocative cue for intense remote memory recall and despite these memories being remote, they are highly contextual. In instances such as posttraumatic stress disorder (PTSD), intense remote memory recall can occur years after trauma, which seemingly contradicts SC. We hypothesized that odor may shift the organization of salient or fearful memories such that when paired with an odor at the time of encoding, they are delayed in the de-contextualization process that occurs across time, and retrieval may still rely on the HPC, where memories are imbued with contextually rich information, even at remote time points. We investigated this by tagging odor- and non-odor-associated fear memories in male c57BL/6 mice and assessed recall and c-Fos expression in the dorsal CA1 (dCA1) and prelimbic cortex (PL) 1 or 21 d later. In support of SC, our data showed that recent memories were more dCA1-dependent whereas remote memories were more PL-dependent. However, we also found that odor influenced this temporal dynamic, biasing the memory system from the PL to the dCA1 when odor cues were present. Behaviorally, inhibiting the dCA1 with activity-dependent DREADDs had no effect on recall at 1 d and unexpectedly caused an increase in freezing at 21 d. Together, these findings demonstrate that odor can shift the organization of fear memories at the systems level.
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spelling pubmed-70795692020-04-01 Odor modulates the temporal dynamics of fear memory consolidation Grella, Stephanie L. Fortin, Amanda H. McKissick, Olivia Leblanc, Heloise Ramirez, Steve Learn Mem Research Systems consolidation (SC) theory proposes that recent, contextually rich memories are stored in the hippocampus (HPC). As these memories become remote, they are believed to rely more heavily on cortical structures within the prefrontal cortex (PFC), where they lose much of their contextual detail and become schematized. Odor is a particularly evocative cue for intense remote memory recall and despite these memories being remote, they are highly contextual. In instances such as posttraumatic stress disorder (PTSD), intense remote memory recall can occur years after trauma, which seemingly contradicts SC. We hypothesized that odor may shift the organization of salient or fearful memories such that when paired with an odor at the time of encoding, they are delayed in the de-contextualization process that occurs across time, and retrieval may still rely on the HPC, where memories are imbued with contextually rich information, even at remote time points. We investigated this by tagging odor- and non-odor-associated fear memories in male c57BL/6 mice and assessed recall and c-Fos expression in the dorsal CA1 (dCA1) and prelimbic cortex (PL) 1 or 21 d later. In support of SC, our data showed that recent memories were more dCA1-dependent whereas remote memories were more PL-dependent. However, we also found that odor influenced this temporal dynamic, biasing the memory system from the PL to the dCA1 when odor cues were present. Behaviorally, inhibiting the dCA1 with activity-dependent DREADDs had no effect on recall at 1 d and unexpectedly caused an increase in freezing at 21 d. Together, these findings demonstrate that odor can shift the organization of fear memories at the systems level. Cold Spring Harbor Laboratory Press 2020-04 /pmc/articles/PMC7079569/ /pubmed/32179657 http://dx.doi.org/10.1101/lm.050690.119 Text en © 2020 Grella et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article, published in Learning & Memory, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research
Grella, Stephanie L.
Fortin, Amanda H.
McKissick, Olivia
Leblanc, Heloise
Ramirez, Steve
Odor modulates the temporal dynamics of fear memory consolidation
title Odor modulates the temporal dynamics of fear memory consolidation
title_full Odor modulates the temporal dynamics of fear memory consolidation
title_fullStr Odor modulates the temporal dynamics of fear memory consolidation
title_full_unstemmed Odor modulates the temporal dynamics of fear memory consolidation
title_short Odor modulates the temporal dynamics of fear memory consolidation
title_sort odor modulates the temporal dynamics of fear memory consolidation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7079569/
https://www.ncbi.nlm.nih.gov/pubmed/32179657
http://dx.doi.org/10.1101/lm.050690.119
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