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Neural signatures of the response to emotional distraction: a review of evidence from brain imaging investigations.

Iordan AD, Dolcos S, Dolcos F - Front Hum Neurosci (2013)

Bottom Line: First, the response to emotional distraction is associated with opposing patterns of activity in a ventral "hot" affective system (HotEmo, showing increased activity) and a dorsal "cold" executive system (ColdEx, showing decreased activity).Second, coping with emotional distraction involves top-down control in order to counteract the bottom-up influence of emotional distraction, and involves interactions between the amygdala and the prefrontal cortex.Third, both the response to and coping with emotional distraction are influenced by individual differences affecting emotional sensitivity and distractibility, which are linked to alterations of both HotEmo and ColdEx neural systems.

View Article: PubMed Central - PubMed

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

ABSTRACT
Prompt responses to emotional, potentially threatening, stimuli are supported by neural mechanisms that allow for privileged access of emotional information to processing resources. The existence of these mechanisms can also make emotional stimuli potent distracters, particularly when task-irrelevant. The ability to deploy cognitive control in order to cope with emotional distraction is essential for adaptive behavior, while reduced control may lead to enhanced emotional distractibility, which is often a hallmark of affective disorders. Evidence suggests that increased susceptibility to emotional distraction is linked to changes in the processing of emotional information that affect both the basic response to and coping with emotional distraction, but the neural correlates of these phenomena are not clear. The present review discusses emerging evidence from brain imaging studies addressing these issues, and highlights the following three aspects. First, the response to emotional distraction is associated with opposing patterns of activity in a ventral "hot" affective system (HotEmo, showing increased activity) and a dorsal "cold" executive system (ColdEx, showing decreased activity). Second, coping with emotional distraction involves top-down control in order to counteract the bottom-up influence of emotional distraction, and involves interactions between the amygdala and the prefrontal cortex. Third, both the response to and coping with emotional distraction are influenced by individual differences affecting emotional sensitivity and distractibility, which are linked to alterations of both HotEmo and ColdEx neural systems. Collectively, the available evidence identifies specific neural signatures of the response to emotional challenge, which are fundamental to understanding the mechanisms of emotion-cognition interactions in healthy functioning, and the changes linked to individual variation in emotional distractibility and susceptibility to affective disorders.

No MeSH data available.


Related in: MedlinePlus

Evidence for the role of lateral PFC in coping with distracting emotions. (A) Brain regions showing enhanced functional coupling with the amygdala during processing of emotional distraction—ventrolateral prefrontal cortex (vlPFC)/inferior frontal cortex (IFC) highlighted. (B) Hemispheric asymmetry in the vlPFC/IFC during successful coping with emotional distraction. (C) Enhanced correlation between vlPFC activity and subjective emotional distractibility scores. Taken together, these findings suggest a hemispheric asymmetry in the IFC with respect to its role in actually coping with distraction (left vlPFC/IFC) vs. coping with the subjective feeling of being distracted (right vlPFC/IFC). Correct/Incorrect, Remembered/Forgotten items in the WM task; R, Right; L, Left. Adapted from Dolcos and McCarthy (2006) and Dolcos et al. (2006), with permission.
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Figure 5: Evidence for the role of lateral PFC in coping with distracting emotions. (A) Brain regions showing enhanced functional coupling with the amygdala during processing of emotional distraction—ventrolateral prefrontal cortex (vlPFC)/inferior frontal cortex (IFC) highlighted. (B) Hemispheric asymmetry in the vlPFC/IFC during successful coping with emotional distraction. (C) Enhanced correlation between vlPFC activity and subjective emotional distractibility scores. Taken together, these findings suggest a hemispheric asymmetry in the IFC with respect to its role in actually coping with distraction (left vlPFC/IFC) vs. coping with the subjective feeling of being distracted (right vlPFC/IFC). Correct/Incorrect, Remembered/Forgotten items in the WM task; R, Right; L, Left. Adapted from Dolcos and McCarthy (2006) and Dolcos et al. (2006), with permission.

Mentions: Functional connectivity analyses of data from the Dolcos and McCarthy study provided evidence for enhanced positive coupling between AMY and vlPFC/IFC during processing of emotional distraction (Figure 5A). In turn, the engagement of IFC leads to successful coping with emotional distraction, as reflected in greater activity to correct vs. incorrect trials in the WM task, despite the presence of emotional distraction (Dolcos et al., 2006). Further investigation of activity in these PFC regions provided evidence clarifying the consequences of their engagement in coping with emotional distraction (Figure 5B). The engagement of the AMY can be seen as having the role of an “emotional detector” that signals the PFC about the presence of emotional, potentially distracting, stimuli and thus the need to control their possible detrimental effects on cognitive performance (Dolcos et al., 2006). Anatomical evidence of substantial AMY–vlPFC connections (Amaral et al., 1992) supports this interpretation, and hence it is reasonable to posit that enhanced functional connectivity between the AMY and IFC reflects processing that originates in the AMY. Of all the lateral PFC regions, which are generally sparsely connected to the AMY, the IFC/vlPFC provides the most substantial connections, thus making it the best candidate among the lateral PFC regions to potentially exert direct control over AMY (Ray and Zald, 2012; see also Pessoa, 2010). Our interpretation is consistent with the idea that AMY is signaling the emotional relevance of the stimuli to PFC regions, such as ventrolateral and ventromedial PFC, which are integrating and interpreting them according to the current goals, and “taking” context-appropriate decisions which may dampen the emotional experience and benefit WM processing (Wager et al., 2008; Chuah et al., 2010; Denkova et al., under review). As described below, investigation of IFC activity in response to task-irrelevant emotional distraction provided further evidence consistent with this idea. These findings complement the results of emotion regulation studies typically identifying negative correlations between the levels of activity in PFC and AMY regions (e.g., Ochsner et al., 2004; see also Ray and Zald, 2012 for a review).


Neural signatures of the response to emotional distraction: a review of evidence from brain imaging investigations.

Iordan AD, Dolcos S, Dolcos F - Front Hum Neurosci (2013)

Evidence for the role of lateral PFC in coping with distracting emotions. (A) Brain regions showing enhanced functional coupling with the amygdala during processing of emotional distraction—ventrolateral prefrontal cortex (vlPFC)/inferior frontal cortex (IFC) highlighted. (B) Hemispheric asymmetry in the vlPFC/IFC during successful coping with emotional distraction. (C) Enhanced correlation between vlPFC activity and subjective emotional distractibility scores. Taken together, these findings suggest a hemispheric asymmetry in the IFC with respect to its role in actually coping with distraction (left vlPFC/IFC) vs. coping with the subjective feeling of being distracted (right vlPFC/IFC). Correct/Incorrect, Remembered/Forgotten items in the WM task; R, Right; L, Left. Adapted from Dolcos and McCarthy (2006) and Dolcos et al. (2006), with permission.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3672684&req=5

Figure 5: Evidence for the role of lateral PFC in coping with distracting emotions. (A) Brain regions showing enhanced functional coupling with the amygdala during processing of emotional distraction—ventrolateral prefrontal cortex (vlPFC)/inferior frontal cortex (IFC) highlighted. (B) Hemispheric asymmetry in the vlPFC/IFC during successful coping with emotional distraction. (C) Enhanced correlation between vlPFC activity and subjective emotional distractibility scores. Taken together, these findings suggest a hemispheric asymmetry in the IFC with respect to its role in actually coping with distraction (left vlPFC/IFC) vs. coping with the subjective feeling of being distracted (right vlPFC/IFC). Correct/Incorrect, Remembered/Forgotten items in the WM task; R, Right; L, Left. Adapted from Dolcos and McCarthy (2006) and Dolcos et al. (2006), with permission.
Mentions: Functional connectivity analyses of data from the Dolcos and McCarthy study provided evidence for enhanced positive coupling between AMY and vlPFC/IFC during processing of emotional distraction (Figure 5A). In turn, the engagement of IFC leads to successful coping with emotional distraction, as reflected in greater activity to correct vs. incorrect trials in the WM task, despite the presence of emotional distraction (Dolcos et al., 2006). Further investigation of activity in these PFC regions provided evidence clarifying the consequences of their engagement in coping with emotional distraction (Figure 5B). The engagement of the AMY can be seen as having the role of an “emotional detector” that signals the PFC about the presence of emotional, potentially distracting, stimuli and thus the need to control their possible detrimental effects on cognitive performance (Dolcos et al., 2006). Anatomical evidence of substantial AMY–vlPFC connections (Amaral et al., 1992) supports this interpretation, and hence it is reasonable to posit that enhanced functional connectivity between the AMY and IFC reflects processing that originates in the AMY. Of all the lateral PFC regions, which are generally sparsely connected to the AMY, the IFC/vlPFC provides the most substantial connections, thus making it the best candidate among the lateral PFC regions to potentially exert direct control over AMY (Ray and Zald, 2012; see also Pessoa, 2010). Our interpretation is consistent with the idea that AMY is signaling the emotional relevance of the stimuli to PFC regions, such as ventrolateral and ventromedial PFC, which are integrating and interpreting them according to the current goals, and “taking” context-appropriate decisions which may dampen the emotional experience and benefit WM processing (Wager et al., 2008; Chuah et al., 2010; Denkova et al., under review). As described below, investigation of IFC activity in response to task-irrelevant emotional distraction provided further evidence consistent with this idea. These findings complement the results of emotion regulation studies typically identifying negative correlations between the levels of activity in PFC and AMY regions (e.g., Ochsner et al., 2004; see also Ray and Zald, 2012 for a review).

Bottom Line: First, the response to emotional distraction is associated with opposing patterns of activity in a ventral "hot" affective system (HotEmo, showing increased activity) and a dorsal "cold" executive system (ColdEx, showing decreased activity).Second, coping with emotional distraction involves top-down control in order to counteract the bottom-up influence of emotional distraction, and involves interactions between the amygdala and the prefrontal cortex.Third, both the response to and coping with emotional distraction are influenced by individual differences affecting emotional sensitivity and distractibility, which are linked to alterations of both HotEmo and ColdEx neural systems.

View Article: PubMed Central - PubMed

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

ABSTRACT
Prompt responses to emotional, potentially threatening, stimuli are supported by neural mechanisms that allow for privileged access of emotional information to processing resources. The existence of these mechanisms can also make emotional stimuli potent distracters, particularly when task-irrelevant. The ability to deploy cognitive control in order to cope with emotional distraction is essential for adaptive behavior, while reduced control may lead to enhanced emotional distractibility, which is often a hallmark of affective disorders. Evidence suggests that increased susceptibility to emotional distraction is linked to changes in the processing of emotional information that affect both the basic response to and coping with emotional distraction, but the neural correlates of these phenomena are not clear. The present review discusses emerging evidence from brain imaging studies addressing these issues, and highlights the following three aspects. First, the response to emotional distraction is associated with opposing patterns of activity in a ventral "hot" affective system (HotEmo, showing increased activity) and a dorsal "cold" executive system (ColdEx, showing decreased activity). Second, coping with emotional distraction involves top-down control in order to counteract the bottom-up influence of emotional distraction, and involves interactions between the amygdala and the prefrontal cortex. Third, both the response to and coping with emotional distraction are influenced by individual differences affecting emotional sensitivity and distractibility, which are linked to alterations of both HotEmo and ColdEx neural systems. Collectively, the available evidence identifies specific neural signatures of the response to emotional challenge, which are fundamental to understanding the mechanisms of emotion-cognition interactions in healthy functioning, and the changes linked to individual variation in emotional distractibility and susceptibility to affective disorders.

No MeSH data available.


Related in: MedlinePlus