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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

Summary of activations in brain regions associated with the ventral HotEmo system (red) and the dorsal ColdEx system (blue). The figure shows peak activation voxels from areas showing increased (red) and decreased (blue) activity to emotional distraction, as identified by the studies featured in Table 1. The white geometric shapes identify peak voxels from regions associated with coping with emotional distraction, in women and men. Specifically, for the female subjects, the rhombi identify peak activation voxels from bilateral inferior frontal areas controlling for the subjective “feeling of being distracted” (Dolcos and McCarthy, 2006). The triangles identify peak activation voxels from left inferior frontal areas controlling for the objective impact of emotional distraction (Dolcos et al., 2006, 2013; Denkova et al., 2010); and the square identifies the peak activation voxel from a left dlPFC area linked to increased performance in the presence of emotional distraction (Dolcos et al., 2008). For the male subjects, the stars identify peak activation voxels in right dorsal frontal areas linked to increased performance in the presence of emotional distraction (Iordan et al., 2013a). The peak activation voxels are superimposed on a high resolution brain image displayed in a tridimensional view using MRIcro (www.mccauslandcenter.sc.edu/mricro/mricro/). R, Right; L, Left.
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Figure 10: Summary of activations in brain regions associated with the ventral HotEmo system (red) and the dorsal ColdEx system (blue). The figure shows peak activation voxels from areas showing increased (red) and decreased (blue) activity to emotional distraction, as identified by the studies featured in Table 1. The white geometric shapes identify peak voxels from regions associated with coping with emotional distraction, in women and men. Specifically, for the female subjects, the rhombi identify peak activation voxels from bilateral inferior frontal areas controlling for the subjective “feeling of being distracted” (Dolcos and McCarthy, 2006). The triangles identify peak activation voxels from left inferior frontal areas controlling for the objective impact of emotional distraction (Dolcos et al., 2006, 2013; Denkova et al., 2010); and the square identifies the peak activation voxel from a left dlPFC area linked to increased performance in the presence of emotional distraction (Dolcos et al., 2008). For the male subjects, the stars identify peak activation voxels in right dorsal frontal areas linked to increased performance in the presence of emotional distraction (Iordan et al., 2013a). The peak activation voxels are superimposed on a high resolution brain image displayed in a tridimensional view using MRIcro (www.mccauslandcenter.sc.edu/mricro/mricro/). R, Right; L, Left.

Mentions: Another recent study investigating the effects of more specific emotional distracters (i.e., anxiety-inducing angry faces), as opposed to those inducing a general emotional distraction involved in previous studies (i.e., IAPS pictures), found similar brain imaging effects (Denkova et al., 2010). Confirming that the manipulation worked in inducing anxiety, participants had significantly higher levels of state anxiety after the completion of the task compared to the beginning of the study. These findings show that similar dissociable patterns of activity in the ColdEx and HotEmo systems are also produced by relatively mild distracters (negative facial expressions) inducing specific emotions (anxiety; see also Grillon and Charney, 2011). Moreover, preliminary findings from an investigation that manipulated other emotional properties of task-irrelevant distracters (arousal: high vs. low, and valence: positive vs. negative) suggest that similar brain activity effects may also be observed in the case of positive distraction (Iordan et al., 2013b). Finally, other investigations using similar (Anticevic et al., 2010; Diaz et al., 2011; Oei et al., 2012) or different tasks (e.g., “emotional odd-ball task,” Yamasaki et al., 2002; Wang et al., 2005; “emotional interrupt task,” Mitchell et al., 2008), and evidence from clinical research (Morey et al., 2009; Anticevic et al., 2011) also support this dorso-ventral dissociation in response to emotional distraction, thus pointing to the replicability and generalizability of these findings (see Table 1 and Figure 10).


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)

Summary of activations in brain regions associated with the ventral HotEmo system (red) and the dorsal ColdEx system (blue). The figure shows peak activation voxels from areas showing increased (red) and decreased (blue) activity to emotional distraction, as identified by the studies featured in Table 1. The white geometric shapes identify peak voxels from regions associated with coping with emotional distraction, in women and men. Specifically, for the female subjects, the rhombi identify peak activation voxels from bilateral inferior frontal areas controlling for the subjective “feeling of being distracted” (Dolcos and McCarthy, 2006). The triangles identify peak activation voxels from left inferior frontal areas controlling for the objective impact of emotional distraction (Dolcos et al., 2006, 2013; Denkova et al., 2010); and the square identifies the peak activation voxel from a left dlPFC area linked to increased performance in the presence of emotional distraction (Dolcos et al., 2008). For the male subjects, the stars identify peak activation voxels in right dorsal frontal areas linked to increased performance in the presence of emotional distraction (Iordan et al., 2013a). The peak activation voxels are superimposed on a high resolution brain image displayed in a tridimensional view using MRIcro (www.mccauslandcenter.sc.edu/mricro/mricro/). R, Right; L, Left.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 10: Summary of activations in brain regions associated with the ventral HotEmo system (red) and the dorsal ColdEx system (blue). The figure shows peak activation voxels from areas showing increased (red) and decreased (blue) activity to emotional distraction, as identified by the studies featured in Table 1. The white geometric shapes identify peak voxels from regions associated with coping with emotional distraction, in women and men. Specifically, for the female subjects, the rhombi identify peak activation voxels from bilateral inferior frontal areas controlling for the subjective “feeling of being distracted” (Dolcos and McCarthy, 2006). The triangles identify peak activation voxels from left inferior frontal areas controlling for the objective impact of emotional distraction (Dolcos et al., 2006, 2013; Denkova et al., 2010); and the square identifies the peak activation voxel from a left dlPFC area linked to increased performance in the presence of emotional distraction (Dolcos et al., 2008). For the male subjects, the stars identify peak activation voxels in right dorsal frontal areas linked to increased performance in the presence of emotional distraction (Iordan et al., 2013a). The peak activation voxels are superimposed on a high resolution brain image displayed in a tridimensional view using MRIcro (www.mccauslandcenter.sc.edu/mricro/mricro/). R, Right; L, Left.
Mentions: Another recent study investigating the effects of more specific emotional distracters (i.e., anxiety-inducing angry faces), as opposed to those inducing a general emotional distraction involved in previous studies (i.e., IAPS pictures), found similar brain imaging effects (Denkova et al., 2010). Confirming that the manipulation worked in inducing anxiety, participants had significantly higher levels of state anxiety after the completion of the task compared to the beginning of the study. These findings show that similar dissociable patterns of activity in the ColdEx and HotEmo systems are also produced by relatively mild distracters (negative facial expressions) inducing specific emotions (anxiety; see also Grillon and Charney, 2011). Moreover, preliminary findings from an investigation that manipulated other emotional properties of task-irrelevant distracters (arousal: high vs. low, and valence: positive vs. negative) suggest that similar brain activity effects may also be observed in the case of positive distraction (Iordan et al., 2013b). Finally, other investigations using similar (Anticevic et al., 2010; Diaz et al., 2011; Oei et al., 2012) or different tasks (e.g., “emotional odd-ball task,” Yamasaki et al., 2002; Wang et al., 2005; “emotional interrupt task,” Mitchell et al., 2008), and evidence from clinical research (Morey et al., 2009; Anticevic et al., 2011) also support this dorso-ventral dissociation in response to emotional distraction, thus pointing to the replicability and generalizability of these findings (see Table 1 and Figure 10).

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