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.

Highlights

  • Investigations on the impact of emotion on memory have shown that emotion enhances memory (Bradley et al, 1992; Christianson, 1992; Chiu et al, 2013), and that this enhancement is associated with increased engagement of emotion and memory related medial temporal lobe (MTL) regions

  • The present study addressed this issue by using functional magnetic resonance imaging in conjunction with an experimental design that allowed for the dissociation of MTL involvement in retrieval success from incidental encoding success, during the retrieval of emotional memories

  • AMY activity was most impacted when accounting for encoding success activity, as only retrieval success activity in the left but not right AMY was dissociated from encoding success activity during retrieval, whereas the portions of HC and PHC showing greater emotional retrieval success activity were largely uninvolved in encoding success

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Summary

Introduction

Investigations on the impact of emotion on memory have shown that emotion enhances memory (Bradley et al, 1992; Christianson, 1992; Chiu et al, 2013), and that this enhancement is associated with increased engagement of emotion (amygdala, AMY) and memory (hippocampus, HC and parahippocampus, PHC) related medial temporal lobe (MTL) regions This increased engagement is observed during both encoding (Dolcos et al, 2004; McGaugh, 2004; Dolcos and Denkova, 2008; Murty et al, 2011) and retrieval (Sharot et al, 2004; Dolcos et al, 2005; Kensinger and Schacter, 2005; Sergerie et al, 2006; Smith et al, 2006); reviewed in Dolcos et al (2012). The present study addressed this issue by using functional magnetic resonance imaging (fMRI) in conjunction with an experimental design that allowed for the dissociation of MTL involvement in retrieval success from incidental encoding success, during the retrieval of emotional memories

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