Emotional arousal impairs association-memory: roles of amygdala and hippocampus

Emotional arousal is well-known to enhance memory for individual items or events, whereas it can impair association memory. The neural mechanism of this association memory impairment by emotion is not known: In response to emotionally arousing information, amygdala activity may interfere with hippoc...

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Main Authors: Madan, Christopher R., Fujiwara, Esther, Caplan, Jeremy B., Sommer, Tobias
Format: Article
Published: Elsevier 2017
Online Access:https://eprints.nottingham.ac.uk/49064/
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author Madan, Christopher R.
Fujiwara, Esther
Caplan, Jeremy B.
Sommer, Tobias
author_facet Madan, Christopher R.
Fujiwara, Esther
Caplan, Jeremy B.
Sommer, Tobias
author_sort Madan, Christopher R.
building Nottingham Research Data Repository
collection Online Access
description Emotional arousal is well-known to enhance memory for individual items or events, whereas it can impair association memory. The neural mechanism of this association memory impairment by emotion is not known: In response to emotionally arousing information, amygdala activity may interfere with hippocampal associative encoding (e.g., via prefrontal cortex). Alternatively, emotional information may be harder to unitize, resulting in reduced availability of extra-hippocampal medial temporal lobe support for emotional than neutral associations. To test these opposing hypotheses, we compared neural processes underlying successful and unsuccessful encoding of emotional and neutral associations. Participants intentionally studied pairs of neutral and negative pictures (Experiments 1–3). We found reduced association-memory for negative pictures in all experiments, accompanied by item-memory increases in Experiment 2. High-resolution fMRI (Experiment 3) indicated that reductions in associative encoding of emotional information are localizable to an area in ventral-lateral amygdala, driven by attentional/salience effects in the central amygdala. Hippocampal activity was similar during both pair types, but a left hippocampal cluster related to successful encoding was observed only for negative pairs. Extra-hippocampal associative memory processes (e.g., unitization) were more effective for neutral than emotional materials. Our findings suggest that reduced emotional association memory is accompanied by increases in activity and functional coupling within the amygdala. This did not disrupt hippocampal association-memory processes, which indeed were critical for successful emotional association memory formation.
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spelling nottingham-490642020-05-04T18:58:32Z https://eprints.nottingham.ac.uk/49064/ Emotional arousal impairs association-memory: roles of amygdala and hippocampus Madan, Christopher R. Fujiwara, Esther Caplan, Jeremy B. Sommer, Tobias Emotional arousal is well-known to enhance memory for individual items or events, whereas it can impair association memory. The neural mechanism of this association memory impairment by emotion is not known: In response to emotionally arousing information, amygdala activity may interfere with hippocampal associative encoding (e.g., via prefrontal cortex). Alternatively, emotional information may be harder to unitize, resulting in reduced availability of extra-hippocampal medial temporal lobe support for emotional than neutral associations. To test these opposing hypotheses, we compared neural processes underlying successful and unsuccessful encoding of emotional and neutral associations. Participants intentionally studied pairs of neutral and negative pictures (Experiments 1–3). We found reduced association-memory for negative pictures in all experiments, accompanied by item-memory increases in Experiment 2. High-resolution fMRI (Experiment 3) indicated that reductions in associative encoding of emotional information are localizable to an area in ventral-lateral amygdala, driven by attentional/salience effects in the central amygdala. Hippocampal activity was similar during both pair types, but a left hippocampal cluster related to successful encoding was observed only for negative pairs. Extra-hippocampal associative memory processes (e.g., unitization) were more effective for neutral than emotional materials. Our findings suggest that reduced emotional association memory is accompanied by increases in activity and functional coupling within the amygdala. This did not disrupt hippocampal association-memory processes, which indeed were critical for successful emotional association memory formation. Elsevier 2017-08-01 Article PeerReviewed Madan, Christopher R., Fujiwara, Esther, Caplan, Jeremy B. and Sommer, Tobias (2017) Emotional arousal impairs association-memory: roles of amygdala and hippocampus. NeuroImage, 156 . pp. 14-28. ISSN 1095-9572 http://www.sciencedirect.com/science/article/pii/S1053811917303841 doi:10.1016/j.neuroimage.2017.04.065 doi:10.1016/j.neuroimage.2017.04.065
spellingShingle Madan, Christopher R.
Fujiwara, Esther
Caplan, Jeremy B.
Sommer, Tobias
Emotional arousal impairs association-memory: roles of amygdala and hippocampus
title Emotional arousal impairs association-memory: roles of amygdala and hippocampus
title_full Emotional arousal impairs association-memory: roles of amygdala and hippocampus
title_fullStr Emotional arousal impairs association-memory: roles of amygdala and hippocampus
title_full_unstemmed Emotional arousal impairs association-memory: roles of amygdala and hippocampus
title_short Emotional arousal impairs association-memory: roles of amygdala and hippocampus
title_sort emotional arousal impairs association-memory: roles of amygdala and hippocampus
url https://eprints.nottingham.ac.uk/49064/
https://eprints.nottingham.ac.uk/49064/
https://eprints.nottingham.ac.uk/49064/