Dissociating retrieval success from incidental encoding activity during emotional memory retrieval, in the medial temporal lobe

Andrea T. Shafer, Florin Dolcos

Research output: Contribution to journalArticle

Abstract

The memory-enhancing effect of emotion has been linked to the engagement of emotion- and memory-related medial temporal lobe (MTL) regions (amygdala-AMY; hippocampus-HC; parahippocampus-PHC), during both encoding and retrieval. However, recognition tasks used to investigate the neural correlates of retrieval make it difficult to distinguish MTL engagement linked to retrieval success (RS) from that linked to incidental encoding success (ES) during retrieval. This issue has been investigated for retrieval of non-emotional memories, but not for emotional memory retrieval. To address this, we used event-related functional MRI in conjunction with an emotional distraction and two episodic memory tasks (one testing memory for distracter items and the other testing memory for new/lure items presented in the first memory task). This paradigm allowed for dissociation of MTL activity specifically linked to RS from that linked to both RS and incidental ES during retrieval. There were two novel findings regarding the neural correlates of emotional memory retrieval. First, greater emotional RS was identified bilaterally in AMY, HC, and PHC. However, AMY activity was most impacted when accounting for ES activity, as only RS activity in left AMY was dissociated from ES activity during retrieval, whereas portions of HC and PHC showing greater emotional RS were largely uninvolved in ES. Second, an earlier and more anteriorly spread response (left AMY and bilateral HC, PHC) was linked to greater emotional RS activity, whereas a later and more posteriorly localized response (right posterior PHC) was linked to greater neutral RS activity. These findings shed light on MTL mechanisms subserving the memory-enhancing effect of emotion at retrieval.

Original languageEnglish (US)
Article number177
JournalFrontiers in Behavioral Neuroscience
Volume8
Issue numberJUNE
DOIs
StatePublished - Jun 3 2014

Fingerprint

Temporal Lobe
Emotions
Episodic Memory
Amygdala
Hippocampus
Magnetic Resonance Imaging

Keywords

  • Affect
  • Episodic memory
  • Incidental learning
  • Recollection
  • Successful retrieval

ASJC Scopus subject areas

  • Neuropsychology and Physiological Psychology
  • Cognitive Neuroscience
  • Behavioral Neuroscience

Cite this

@article{6e823f16d2274b2dac967514b5359bd2,
title = "Dissociating retrieval success from incidental encoding activity during emotional memory retrieval, in the medial temporal lobe",
abstract = "The memory-enhancing effect of emotion has been linked to the engagement of emotion- and memory-related medial temporal lobe (MTL) regions (amygdala-AMY; hippocampus-HC; parahippocampus-PHC), during both encoding and retrieval. However, recognition tasks used to investigate the neural correlates of retrieval make it difficult to distinguish MTL engagement linked to retrieval success (RS) from that linked to incidental encoding success (ES) during retrieval. This issue has been investigated for retrieval of non-emotional memories, but not for emotional memory retrieval. To address this, we used event-related functional MRI in conjunction with an emotional distraction and two episodic memory tasks (one testing memory for distracter items and the other testing memory for new/lure items presented in the first memory task). This paradigm allowed for dissociation of MTL activity specifically linked to RS from that linked to both RS and incidental ES during retrieval. There were two novel findings regarding the neural correlates of emotional memory retrieval. First, greater emotional RS was identified bilaterally in AMY, HC, and PHC. However, AMY activity was most impacted when accounting for ES activity, as only RS activity in left AMY was dissociated from ES activity during retrieval, whereas portions of HC and PHC showing greater emotional RS were largely uninvolved in ES. Second, an earlier and more anteriorly spread response (left AMY and bilateral HC, PHC) was linked to greater emotional RS activity, whereas a later and more posteriorly localized response (right posterior PHC) was linked to greater neutral RS activity. These findings shed light on MTL mechanisms subserving the memory-enhancing effect of emotion at retrieval.",
keywords = "Affect, Episodic memory, Incidental learning, Recollection, Successful retrieval",
author = "Shafer, {Andrea T.} and Florin Dolcos",
year = "2014",
month = "6",
day = "3",
doi = "10.3389/fnbeh.2014.00177",
language = "English (US)",
volume = "8",
journal = "Frontiers in Behavioral Neuroscience",
issn = "1662-5153",
publisher = "Frontiers Research Foundation",
number = "JUNE",

}

TY - JOUR

T1 - Dissociating retrieval success from incidental encoding activity during emotional memory retrieval, in the medial temporal lobe

AU - Shafer, Andrea T.

AU - Dolcos, Florin

PY - 2014/6/3

Y1 - 2014/6/3

N2 - The memory-enhancing effect of emotion has been linked to the engagement of emotion- and memory-related medial temporal lobe (MTL) regions (amygdala-AMY; hippocampus-HC; parahippocampus-PHC), during both encoding and retrieval. However, recognition tasks used to investigate the neural correlates of retrieval make it difficult to distinguish MTL engagement linked to retrieval success (RS) from that linked to incidental encoding success (ES) during retrieval. This issue has been investigated for retrieval of non-emotional memories, but not for emotional memory retrieval. To address this, we used event-related functional MRI in conjunction with an emotional distraction and two episodic memory tasks (one testing memory for distracter items and the other testing memory for new/lure items presented in the first memory task). This paradigm allowed for dissociation of MTL activity specifically linked to RS from that linked to both RS and incidental ES during retrieval. There were two novel findings regarding the neural correlates of emotional memory retrieval. First, greater emotional RS was identified bilaterally in AMY, HC, and PHC. However, AMY activity was most impacted when accounting for ES activity, as only RS activity in left AMY was dissociated from ES activity during retrieval, whereas portions of HC and PHC showing greater emotional RS were largely uninvolved in ES. Second, an earlier and more anteriorly spread response (left AMY and bilateral HC, PHC) was linked to greater emotional RS activity, whereas a later and more posteriorly localized response (right posterior PHC) was linked to greater neutral RS activity. These findings shed light on MTL mechanisms subserving the memory-enhancing effect of emotion at retrieval.

AB - The memory-enhancing effect of emotion has been linked to the engagement of emotion- and memory-related medial temporal lobe (MTL) regions (amygdala-AMY; hippocampus-HC; parahippocampus-PHC), during both encoding and retrieval. However, recognition tasks used to investigate the neural correlates of retrieval make it difficult to distinguish MTL engagement linked to retrieval success (RS) from that linked to incidental encoding success (ES) during retrieval. This issue has been investigated for retrieval of non-emotional memories, but not for emotional memory retrieval. To address this, we used event-related functional MRI in conjunction with an emotional distraction and two episodic memory tasks (one testing memory for distracter items and the other testing memory for new/lure items presented in the first memory task). This paradigm allowed for dissociation of MTL activity specifically linked to RS from that linked to both RS and incidental ES during retrieval. There were two novel findings regarding the neural correlates of emotional memory retrieval. First, greater emotional RS was identified bilaterally in AMY, HC, and PHC. However, AMY activity was most impacted when accounting for ES activity, as only RS activity in left AMY was dissociated from ES activity during retrieval, whereas portions of HC and PHC showing greater emotional RS were largely uninvolved in ES. Second, an earlier and more anteriorly spread response (left AMY and bilateral HC, PHC) was linked to greater emotional RS activity, whereas a later and more posteriorly localized response (right posterior PHC) was linked to greater neutral RS activity. These findings shed light on MTL mechanisms subserving the memory-enhancing effect of emotion at retrieval.

KW - Affect

KW - Episodic memory

KW - Incidental learning

KW - Recollection

KW - Successful retrieval

UR - http://www.scopus.com/inward/record.url?scp=84921999263&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84921999263&partnerID=8YFLogxK

U2 - 10.3389/fnbeh.2014.00177

DO - 10.3389/fnbeh.2014.00177

M3 - Article

AN - SCOPUS:84921999263

VL - 8

JO - Frontiers in Behavioral Neuroscience

JF - Frontiers in Behavioral Neuroscience

SN - 1662-5153

IS - JUNE

M1 - 177

ER -