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Neural correlates of opposing effects of emotional distraction on working memory and episodic memory: an event-related FMRI investigation.

Dolcos F, Iordan AD, Kragel J, Stokes J, Campbell R, McCarthy G, Cabeza R - Front Psychol (2013)

Bottom Line: EM for the distracting pictures was tested after scanning and was used to identify successful encoding activity for the picture distracters.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.

View Article: PubMed Central - PubMed

Affiliation: Psychology Department, University of Illinois at Urbana-Champaign , Urbana, IL , USA ; Neuroscience Program, University of Illinois at Urbana-Champaign , Urbana, IL , USA ; Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign , Urbana, IL , USA.

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.

No MeSH data available.


Related in: MedlinePlus

Increased right vlPFC activity linked to coping with emotional distraction and enhanced EM. Right vlPFC showed increased activity to emotional distracters associated with WM success and later remembered relative to both neutral distracters associated with WM success (red blob) and emotional distracters associated with WM impairment (green blob). A positive correlation was also identified between activity in this right vlPFC area and WM performance for emotional distraction (white blob; see Results). In contrast, the left inferior frontal cortex showed increased activity to emotional distracters associated with WM success relative to emotional distracters associated with WM impairment, independent of whether they were later remembered or not (Talairach coordinates: x = −46, y = 8, z = 22; not shown). This suggests a hemispheric dissociation between brain activity involved in coping with emotional distraction (left vlPFC) and linking coping mechanisms with increased subsequent EM for the distracting information (right vlPFC). The bar graph shows contrast estimates for the peak voxel in right vlPFC for the comparison between emotional and neutral stimuli associated with WM success and later remembered (Talairach coordinates: x = 43, y = 23, z = 14). The scatter plot shows the co-variation between brain activity and WM performance, as extracted from the peak voxel of the green blob (Talairach coordinates: x = 47, y = 24, z = 7). The activation maps are superimposed on a high-resolution brain image displayed in sagittal view (x indicates the Talairach coordinate on the left-right axis of the brain). vlPFC, ventrolateral PFC; Emo/Neu WM-R and EM-R, emotional/neutral distracters that did not impair WM and were later remembered. Error bars represent standard errors of means.
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Figure 3: Increased right vlPFC activity linked to coping with emotional distraction and enhanced EM. Right vlPFC showed increased activity to emotional distracters associated with WM success and later remembered relative to both neutral distracters associated with WM success (red blob) and emotional distracters associated with WM impairment (green blob). A positive correlation was also identified between activity in this right vlPFC area and WM performance for emotional distraction (white blob; see Results). In contrast, the left inferior frontal cortex showed increased activity to emotional distracters associated with WM success relative to emotional distracters associated with WM impairment, independent of whether they were later remembered or not (Talairach coordinates: x = −46, y = 8, z = 22; not shown). This suggests a hemispheric dissociation between brain activity involved in coping with emotional distraction (left vlPFC) and linking coping mechanisms with increased subsequent EM for the distracting information (right vlPFC). The bar graph shows contrast estimates for the peak voxel in right vlPFC for the comparison between emotional and neutral stimuli associated with WM success and later remembered (Talairach coordinates: x = 43, y = 23, z = 14). The scatter plot shows the co-variation between brain activity and WM performance, as extracted from the peak voxel of the green blob (Talairach coordinates: x = 47, y = 24, z = 7). The activation maps are superimposed on a high-resolution brain image displayed in sagittal view (x indicates the Talairach coordinate on the left-right axis of the brain). vlPFC, ventrolateral PFC; Emo/Neu WM-R and EM-R, emotional/neutral distracters that did not impair WM and were later remembered. Error bars represent standard errors of means.

Mentions: Analyses contrasting activity for the emotional and neutral distracters that did not impair WM performance but were later remembered (i.e., Emo WM-R and EM-R > Neu WM-R and EM-R) identified increased activity in a right vlPFC region (red blob in Figure 3; see also Table 2). Importantly, activity in this vlPFC region overlapped with areas associated with successful coping with emotional distraction, as revealed by greater activity to emotional distracters associated with WM success than to those that impaired WM (i.e., Emo WM-R and EM-R > Emo WM-F and EM-R; see green blob in Figure 3). Moreover, investigation of brain-behavior relationships showed a positive correlation between activity in these right vlPFC areas, in response to emotional vs. neutral distracters associated with WM success and later remembered, and WM performance for emotional distracters (r = 0.63, p = 0.003; Talairach coordinates: x = 47, y = 24, z = 7; see the white blob in Figure 3). Specifically, consistent with a role of this region in coping with emotional distraction, participants who showed increased vlPFC activity also had higher WM performance in the presence of emotional distraction.


Neural correlates of opposing effects of emotional distraction on working memory and episodic memory: an event-related FMRI investigation.

Dolcos F, Iordan AD, Kragel J, Stokes J, Campbell R, McCarthy G, Cabeza R - Front Psychol (2013)

Increased right vlPFC activity linked to coping with emotional distraction and enhanced EM. Right vlPFC showed increased activity to emotional distracters associated with WM success and later remembered relative to both neutral distracters associated with WM success (red blob) and emotional distracters associated with WM impairment (green blob). A positive correlation was also identified between activity in this right vlPFC area and WM performance for emotional distraction (white blob; see Results). In contrast, the left inferior frontal cortex showed increased activity to emotional distracters associated with WM success relative to emotional distracters associated with WM impairment, independent of whether they were later remembered or not (Talairach coordinates: x = −46, y = 8, z = 22; not shown). This suggests a hemispheric dissociation between brain activity involved in coping with emotional distraction (left vlPFC) and linking coping mechanisms with increased subsequent EM for the distracting information (right vlPFC). The bar graph shows contrast estimates for the peak voxel in right vlPFC for the comparison between emotional and neutral stimuli associated with WM success and later remembered (Talairach coordinates: x = 43, y = 23, z = 14). The scatter plot shows the co-variation between brain activity and WM performance, as extracted from the peak voxel of the green blob (Talairach coordinates: x = 47, y = 24, z = 7). The activation maps are superimposed on a high-resolution brain image displayed in sagittal view (x indicates the Talairach coordinate on the left-right axis of the brain). vlPFC, ventrolateral PFC; Emo/Neu WM-R and EM-R, emotional/neutral distracters that did not impair WM and were later remembered. Error bars represent standard errors of means.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 3: Increased right vlPFC activity linked to coping with emotional distraction and enhanced EM. Right vlPFC showed increased activity to emotional distracters associated with WM success and later remembered relative to both neutral distracters associated with WM success (red blob) and emotional distracters associated with WM impairment (green blob). A positive correlation was also identified between activity in this right vlPFC area and WM performance for emotional distraction (white blob; see Results). In contrast, the left inferior frontal cortex showed increased activity to emotional distracters associated with WM success relative to emotional distracters associated with WM impairment, independent of whether they were later remembered or not (Talairach coordinates: x = −46, y = 8, z = 22; not shown). This suggests a hemispheric dissociation between brain activity involved in coping with emotional distraction (left vlPFC) and linking coping mechanisms with increased subsequent EM for the distracting information (right vlPFC). The bar graph shows contrast estimates for the peak voxel in right vlPFC for the comparison between emotional and neutral stimuli associated with WM success and later remembered (Talairach coordinates: x = 43, y = 23, z = 14). The scatter plot shows the co-variation between brain activity and WM performance, as extracted from the peak voxel of the green blob (Talairach coordinates: x = 47, y = 24, z = 7). The activation maps are superimposed on a high-resolution brain image displayed in sagittal view (x indicates the Talairach coordinate on the left-right axis of the brain). vlPFC, ventrolateral PFC; Emo/Neu WM-R and EM-R, emotional/neutral distracters that did not impair WM and were later remembered. Error bars represent standard errors of means.
Mentions: Analyses contrasting activity for the emotional and neutral distracters that did not impair WM performance but were later remembered (i.e., Emo WM-R and EM-R > Neu WM-R and EM-R) identified increased activity in a right vlPFC region (red blob in Figure 3; see also Table 2). Importantly, activity in this vlPFC region overlapped with areas associated with successful coping with emotional distraction, as revealed by greater activity to emotional distracters associated with WM success than to those that impaired WM (i.e., Emo WM-R and EM-R > Emo WM-F and EM-R; see green blob in Figure 3). Moreover, investigation of brain-behavior relationships showed a positive correlation between activity in these right vlPFC areas, in response to emotional vs. neutral distracters associated with WM success and later remembered, and WM performance for emotional distracters (r = 0.63, p = 0.003; Talairach coordinates: x = 47, y = 24, z = 7; see the white blob in Figure 3). Specifically, consistent with a role of this region in coping with emotional distraction, participants who showed increased vlPFC activity also had higher WM performance in the presence of emotional distraction.

Bottom Line: EM for the distracting pictures was tested after scanning and was used to identify successful encoding activity for the picture distracters.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.

View Article: PubMed Central - PubMed

Affiliation: Psychology Department, University of Illinois at Urbana-Champaign , Urbana, IL , USA ; Neuroscience Program, University of Illinois at Urbana-Champaign , Urbana, IL , USA ; Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign , Urbana, IL , USA.

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.

No MeSH data available.


Related in: MedlinePlus