Cargando…

Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories

Intrusive memories often take the form of distressing images that emerge into a person's awareness, unbidden. A fundamental goal of clinical neuroscience is to understand the mechanisms allowing people to control these memory intrusions and reduce their emotional impact. Mnemonic control engage...

Descripción completa

Detalles Bibliográficos
Autores principales: Gagnepain, Pierre, Hulbert, Justin, Anderson, Michael C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5511877/
https://www.ncbi.nlm.nih.gov/pubmed/28559378
http://dx.doi.org/10.1523/JNEUROSCI.2732-16.2017
_version_ 1783250408567734272
author Gagnepain, Pierre
Hulbert, Justin
Anderson, Michael C.
author_facet Gagnepain, Pierre
Hulbert, Justin
Anderson, Michael C.
author_sort Gagnepain, Pierre
collection PubMed
description Intrusive memories often take the form of distressing images that emerge into a person's awareness, unbidden. A fundamental goal of clinical neuroscience is to understand the mechanisms allowing people to control these memory intrusions and reduce their emotional impact. Mnemonic control engages a right frontoparietal network that interrupts episodic retrieval by modulating hippocampal activity; less is known, however, about how this mechanism contributes to affect regulation. Here we report evidence in humans (males and females) that stopping episodic retrieval to suppress an unpleasant image triggers parallel inhibition of mnemonic and emotional content. Using fMRI, we found that regulation of both mnemonic and emotional content was driven by a shared frontoparietal inhibitory network and was predicted by a common profile of medial temporal lobe downregulation involving the anterior hippocampus and the amygdala. Critically, effective connectivity analysis confirmed that reduced amygdala activity was not merely an indirect consequence of hippocampal suppression; rather, both the hippocampus and the amygdala were targeted by a top-down inhibitory control signal originating from the dorsolateral prefrontal cortex. This negative coupling was greater when unwanted memories intruded into awareness and needed to be purged. Together, these findings support the broad principle that retrieval suppression is achieved by regulating hippocampal processes in tandem with domain-specific brain regions involved in reinstating specific content, in an activity-dependent fashion. SIGNIFICANCE STATEMENT Upsetting events sometimes trigger intrusive images that cause distress and that may contribute to psychiatric disorders. People often respond to intrusions by suppressing their retrieval, excluding them from awareness. Here we examined whether suppressing aversive images might also alter emotional responses to them, and the mechanisms underlying such changes. We found that the better people were at suppressing intrusions, the more it reduced their emotional responses to suppressed images. These dual effects on memory and emotion originated from a common right prefrontal cortical mechanism that downregulated the hippocampus and amygdala in parallel. Thus, suppressing intrusions affected emotional content. Importantly, participants who did not suppress intrusions well showed increased negative affect, suggesting that suppression deficits render people vulnerable to psychiatric disorders.
format Online
Article
Text
id pubmed-5511877
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Society for Neuroscience
record_format MEDLINE/PubMed
spelling pubmed-55118772017-08-08 Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories Gagnepain, Pierre Hulbert, Justin Anderson, Michael C. J Neurosci Research Articles Intrusive memories often take the form of distressing images that emerge into a person's awareness, unbidden. A fundamental goal of clinical neuroscience is to understand the mechanisms allowing people to control these memory intrusions and reduce their emotional impact. Mnemonic control engages a right frontoparietal network that interrupts episodic retrieval by modulating hippocampal activity; less is known, however, about how this mechanism contributes to affect regulation. Here we report evidence in humans (males and females) that stopping episodic retrieval to suppress an unpleasant image triggers parallel inhibition of mnemonic and emotional content. Using fMRI, we found that regulation of both mnemonic and emotional content was driven by a shared frontoparietal inhibitory network and was predicted by a common profile of medial temporal lobe downregulation involving the anterior hippocampus and the amygdala. Critically, effective connectivity analysis confirmed that reduced amygdala activity was not merely an indirect consequence of hippocampal suppression; rather, both the hippocampus and the amygdala were targeted by a top-down inhibitory control signal originating from the dorsolateral prefrontal cortex. This negative coupling was greater when unwanted memories intruded into awareness and needed to be purged. Together, these findings support the broad principle that retrieval suppression is achieved by regulating hippocampal processes in tandem with domain-specific brain regions involved in reinstating specific content, in an activity-dependent fashion. SIGNIFICANCE STATEMENT Upsetting events sometimes trigger intrusive images that cause distress and that may contribute to psychiatric disorders. People often respond to intrusions by suppressing their retrieval, excluding them from awareness. Here we examined whether suppressing aversive images might also alter emotional responses to them, and the mechanisms underlying such changes. We found that the better people were at suppressing intrusions, the more it reduced their emotional responses to suppressed images. These dual effects on memory and emotion originated from a common right prefrontal cortical mechanism that downregulated the hippocampus and amygdala in parallel. Thus, suppressing intrusions affected emotional content. Importantly, participants who did not suppress intrusions well showed increased negative affect, suggesting that suppression deficits render people vulnerable to psychiatric disorders. Society for Neuroscience 2017-07-05 /pmc/articles/PMC5511877/ /pubmed/28559378 http://dx.doi.org/10.1523/JNEUROSCI.2732-16.2017 Text en Copyright © 2017 Gagnepain et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Gagnepain, Pierre
Hulbert, Justin
Anderson, Michael C.
Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories
title Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories
title_full Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories
title_fullStr Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories
title_full_unstemmed Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories
title_short Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories
title_sort parallel regulation of memory and emotion supports the suppression of intrusive memories
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5511877/
https://www.ncbi.nlm.nih.gov/pubmed/28559378
http://dx.doi.org/10.1523/JNEUROSCI.2732-16.2017
work_keys_str_mv AT gagnepainpierre parallelregulationofmemoryandemotionsupportsthesuppressionofintrusivememories
AT hulbertjustin parallelregulationofmemoryandemotionsupportsthesuppressionofintrusivememories
AT andersonmichaelc parallelregulationofmemoryandemotionsupportsthesuppressionofintrusivememories