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      Neural Correlates of Opposing Effects of Emotional Distraction on Working Memory and Episodic Memory: An Event-Related fMRI Investigation

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          Abstract

          A fundamental question in the emotional memory literature is why emotion enhances memory in some conditions but disrupts memory in other conditions. For example, separate studies have shown that emotional stimuli tend to be better remembered in long-term episodic memory (EM), whereas emotional distracters tend to impair working memory (WM) maintenance. The first goal of this study was to directly compare the neural correlates of EM enhancement (EME) and WM impairing (WMI) effects, and the second goal was to explore individual differences in these mechanisms. During event-related functional magnetic resonance imaging (fMRI), participants maintained faces in WM while being distracted by emotional or neutral pictures presented during the delay period. EM for the distracting pictures was tested after scanning and was used to identify successful encoding activity for the picture distracters. The first goal yielded two findings: (1) emotional pictures that disrupted face WM but enhanced subsequent EM were associated with increased amygdala (AMY) and hippocampal activity (ventral system) coupled with reduced dorsolateral PFC (dlPFC) activity (dorsal system); (2) trials in which emotion enhanced EM without disrupting WM were associated with increased ventrolateral PFC activity. The ventral-dorsal switch can explain EME and WMI, while the ventrolateral PFC effect suggests a coping mechanism. The second goal yielded two additional findings: (3) participants who were more susceptible to WMI showed greater amygdala increases and PFC reductions; (4) AMY activity increased and dlPFC activity decreased with measures of attentional impulsivity. Taken together, these results clarify the mechanisms linking the enhancing and impairing effects of emotion on memory, and provide insights into the role of individual differences in the impact of emotional distraction.

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          Most cited references37

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          Distracted and confused?: selective attention under load.

          The ability to remain focused on goal-relevant stimuli in the presence of potentially interfering distractors is crucial for any coherent cognitive function. However, simply instructing people to ignore goal-irrelevant stimuli is not sufficient for preventing their processing. Recent research reveals that distractor processing depends critically on the level and type of load involved in the processing of goal-relevant information. Whereas high perceptual load can eliminate distractor processing, high load on "frontal" cognitive control processes increases distractor processing. These findings provide a resolution to the long-standing early and late selection debate within a load theory of attention that accommodates behavioural and neuroimaging data within a framework that integrates attention research with executive function.
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            Emotion regulation and memory: the cognitive costs of keeping one's cool.

            An emerging literature has begun to document the affective consequences of emotion regulation. Little is known, however, about whether emotion regulation also has cognitive consequences. A process model of emotion suggests that expressive suppression should reduce memory for emotional events but that reappraisal should not. Three studies tested this hypothesis. Study 1 experimentally manipulated expressive suppression during film viewing, showing that suppression led to poorer memory for the details of the film. Study 2 manipulated expressive suppression and reappraisal during slide viewing. Only suppression led to poorer slide memory. Study 3 examined individual differences in typical expressive suppression and reappraisal and found that suppression was associated with poorer self-reported and objective memory but that reappraisal was not. Together, these studies suggest that the cognitive costs of keeping one's cool may vary according to how this is done.
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              Brain systems mediating cognitive interference by emotional distraction.

              Flexible behavior depends on our ability to cope with distracting stimuli that can interfere with the attainment of goals. Emotional distracters can be particularly disruptive to goal-oriented behavior, but the neural systems through which these detrimental effects are mediated are not known. We used event-related functional magnetic resonance imaging to investigate the effect of emotional and nonemotional distracters on a delayed-response working memory (WM) task. As expected, this task evoked robust activity during the delay period in typical WM regions (dorsolateral prefrontal cortex and lateral parietal cortex). Presentation of emotional distracters during the delay interval evoked strong activity in typical emotional processing regions (amygdala and ventrolateral prefrontal cortex) while simultaneously evoking relative deactivation of the WM regions and impairing WM performance. These results provide the first direct evidence that the detrimental effect of emotional distracters on ongoing cognitive processes entails the interaction between a dorsal neural system associated with "cold" executive processing and a ventral system associated with "hot" emotional processing.
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                Author and article information

                Journal
                Front Psychol
                Front Psychol
                Front. Psychol.
                Frontiers in Psychology
                Frontiers Media S.A.
                1664-1078
                06 June 2013
                2013
                : 4
                : 293
                Affiliations
                [1] 1Psychology Department, University of Illinois at Urbana-Champaign , Urbana, IL, USA
                [2] 2Neuroscience Program, University of Illinois at Urbana-Champaign , Urbana, IL, USA
                [3] 3Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign , Urbana, IL, USA
                [4] 4Center for Cognitive Neuroscience, Duke University , Durham, NC, USA
                [5] 5Department of Psychological Sciences, Vanderbilt University , Nashville, TN, USA
                [6] 6Department of Psychology, University of California Davis , Davis, CA, USA
                [7] 7Department of Psychiatry, University of Alberta , Edmonton, AB, Canada
                [8] 8Brain Imaging and Analysis Center, Duke University , Durham, NC, USA
                [9] 9Department of Psychology, Yale University , New Haven, CT, USA
                Author notes

                Edited by: Mara Mather, University of Southern California, USA

                Reviewed by: Bjoern Rasch, University of Zurich, Switzerland; Alan Anticevic, Yale University, USA; Atsuko Takashima, Radboud University Nijmegen, Netherlands

                *Correspondence: Florin Dolcos, Affective, Cognitive, and Clinical Neuroscience Lab, Department of Psychology and the Neuroscience Program, Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, 405 North Mathews Avenue, Urbana, IL 61801, USA e-mail: fdolcos@ 123456illinois.edu

                This article was submitted to Frontiers in Emotion Science, a specialty of Frontiers in Psychology.

                Article
                10.3389/fpsyg.2013.00293
                3674478
                23761770
                56ecf2a8-7e3e-46c7-bcc6-45ba3d0d2764
                Copyright © 2013 Dolcos, Iordan, Kragel, Stokes, Campbell, McCarthy and Cabeza.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                History
                : 18 December 2012
                : 07 May 2013
                Page count
                Figures: 5, Tables: 2, Equations: 0, References: 64, Pages: 16, Words: 12749
                Categories
                Psychology
                Original Research

                Clinical Psychology & Psychiatry
                emotional interference,emotional control,emotional memory,amy,hc,vlpfc,dlpfc

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