Edited by: Alexander J. Shackman, University of Maryland, USA
Reviewed by: Alexander J. Shackman, University of Maryland, USA; Katherine E. Vytal, National Institutes of Health, USA
*Correspondence: F. Dolcos, Psychology Department, Neuroscience Program, The Beckman Institute for Advanced Science and Technology, University of Illinois at Urbana-Champaign, 405 North Mathews Avenue, Urbana, IL 61801, USA e-mail:
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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 (
Emotion and cognition are two complexly intertwined, yet distinct facets of human behavior. Emotion has often been compared to a “double-edged sword,” as it can exert both beneficial and deleterious influences on our cognition and behavior. For example, we may experience enhanced memory for emotional events, but could also be more distracted by emotional stimuli that interfere with our goals. These effects have been linked to prioritization of emotional information, possibly due to its enhanced evolutionary value, as at a basic level these phenomena depend on neural mechanisms that allow timely detection, identification, and privileged processing of stimuli and situations that are important for survival (e.g., finding food, avoiding predators; Hansen and Hansen,
Although the enhancing effects of emotion on cognitive functions such as memory, where emotion tends to be task-relevant, have been the focus of extensive research (see Dolcos et al.,
The present review discusses emerging evidence from brain imaging studies investigating the neural correlates of the detrimental impact of transient emotional distraction on goal-oriented processing and the neural correlates of coping with such distraction. The discussion focuses primarily on findings from studies using delayed-response working memory (WM) tasks and similar dual-task paradigms with emotional distraction, which allowed a clear dissociation of the fMRI signal in brain regions involved in cognitive and emotional processing. Although, overall, the focus in the present review is on the effect of transiently-induced emotional responses, in some cases investigations identified more complex combinations of effects, involving transient emotional responses, longer-lasting states, and trait-like aspects. For matters of conciseness, the present paper does not provide an in-depth discussion of evidence from studies employing perceptual, conflict resolution, and emotion regulation paradigms, which are also methodologically different (see Banich et al.,
The focus will be on the following three main aspects: (1) We will first discuss evidence concerning the neural circuitry underlying the impact of emotional distraction, focusing on the interplay between two major neural systems: a ventral system associated with “hot” emotional processing (
Investigations of the neural circuitry underlying the detrimental impact of emotional distraction complement the research investigating the neural correlates of the enhancing effect of emotion (reviewed in Dolcos et al.,
Models of affective-cognitive interactions inspired by clinical studies point to dysfunctional interactions between a dorsal executive neural system (
Findings from recent studies investigating the neural correlates of cognitive interference by emotional distraction in healthy participants provide evidence that interactions between the
Using this paradigm, the study by Dolcos and McCarthy (
Follow-up investigations (Dolcos et al.,
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.,
Dolcos and McCarthy ( |
F | WM with distraction | Faces | IAPS pictures | Decreased WM performance for Emo | Yes | Dorsal: PCC | Incr vlPFC activity associated with lower distractibility index | N/A |
Ventral: sgACC, Ins, HC | |||||||||
Dolcos et al. ( |
F | WM with distraction | Faces | IAPS pictures | Decreased WM performance for Emo | Yes | N/A | Incr AMY-IFC/vlPFC coupling | N/A |
Incr L IFC/vlPFC for correct trials | |||||||||
Dolcos et al. ( |
F | WM with distraction | Faces | IAPS pictures | Subset of subjects showing decreased WM performance for Emo | Yes | Dorsal: SPC | Incr L dlPFC for subjects showing increased performance | Incr dlPFC for Face distracters |
Ventral: sgACC, MFC, HC | |||||||||
Morey et al. ( |
F + M, PTSD vs. CON | WM with distraction | Faces | Combat-related pictures | Decreased WM performance for PTSD group | Yes | Ventral: TP | N/A | Incr AMY, vlPFC, FG for Combat in PTSD group |
Decr dlPFC for Combat and Neu in PTSD group | |||||||||
Chuah et al. ( |
F + M | WM with distraction | Faces | IAPS pictures | Decreased WM performance for Emo | Yes | Dorsal: dACC | Incr AMY-mPFC and AMY-dlPFC connectivity associated with better WM performance | Incr AMY associated with lower WM performance for Emo |
Decreased WM performance after sleep deprivation | Ventral: Ins | ||||||||
Denkova et al. ( |
F | WM with distraction | Faces | Morphed angry faces | Decreased WM performance for Emo | Yes |
Dorsal: dmPFC | Incr L vlPFC and dmPFC associated with increased WM performance | Incr L FG associated with increased social anxiety |
Ventral: vmPFC | Incr R FG associated with lower WM performance for Emo | ||||||||
Iordan et al. ( |
F + M | WM with distraction | Faces | Morphed angry faces | Decreased WM performance for Emo in F | Yes |
Dorsal: dmPFC | Incr L vlPFC associated with increased WM performance in F | Incr L FG to Emo in F, associated with lower WM performance |
Ventral: vmPFC | |||||||||
Incr R dlPFC associated with increased WM performance in M | Incr sgACC in F | ||||||||
Dolcos et al. ( |
F | WM with distraction | Faces | IAPS pictures | Subset of subjects showing decreased WM performance to Emo | Yes | Dorsal: SPL | Incr L vlPFC for correct trials | Incr AMY and decr dlPFC in subjects showing impaired WM to Emo |
Ventral: mPFC, Ins, HC | Incr R vlPFC associated with WM success for subsequently remembered Emo distracters | Incr AMY associated with higher AI scores | |||||||
Incr dlPFC associated with lower AI scores | |||||||||
Anticevic et al. ( |
F + M | WM with distraction | Shapes | IAPS pictures | Decreased WM performance for Emo | Yes | Dorsal: aPFC | Incr R aPFC and R vlPFC for correct trials | Decr aPFC and dlPFC associated with increased WM performance |
Ventral: OFC | |||||||||
Incr AMY associated with decreased WM performance for all distracter types | |||||||||
Incr AMY-dlPFC negative coupling during task, compared to rest-state | |||||||||
Oei et al. ( |
M | WM with distraction | Letters | IAPS pictures | Decreased WM performance and slower RT for Emo | Yes | Dorsal: aPFC | N/A | Incr ventral regions for stressed group |
Ventral: Ins, TP | |||||||||
Yamasaki et al. ( |
F + M | Emotional odd-ball | N/A | IAPS pictures | Slower RT to Emo | Yes | N/A | N/A | Incr rACC to both Emo and targets |
Wang et al. ( |
F + M, MDD vs. CON | Emotional odd-ball | N/A | Commercial and in-house pictures | Slower RT to target-after-Emo | Yes | Dorsal: dACC, PCC | Incr ACC to target-after-Emo and incr R IFC to target-after-Neu in CON | Decr executive regions in MDD |
Slower RT for MDD, esp. to target-after-Emo | Ventral: Ins, sub-regional specificity in IFC | Incr R IFC associated with faster RT in MDD |
Collectively, these findings are consistent with the idea that the outcome of task-irrelevant emotional distraction depends on dynamic interactions between neural systems that allow the ability to stay focused on task-relevant information and systems involved in the processing of emotional information that may compete with the available processing resources. Possibly as a result of their salience, emotional distracters may produce a
The opposing responses observed in the
The dorsal-ventral dissociation in the neural response to emotional distraction has been observed not only in the larger neural systems (i.e.,
Noteworthy, the dorsal-ventral distinction is primarily a functional dissociation based on the opposing response to emotional distraction in identified typical cognitive/executive and emotion processing regions. In addition to this general dissociation, there are also exceptions, reflecting sub-regional specificity. For example, certain dorsal sub-regions show an increased response to emotional distraction (e.g., BA6/9; Dolcos et al.,
In summary, studies investigating the neural correlates of the basic response to emotional distraction point to an interplay between two major neural systems: a ventral system, associated with “hot” emotional processing (
Brain imaging studies in which emotional information was presented as task-irrelevant distraction also provided evidence regarding the neural correlates of coping with distracting emotions. A series of investigations from our group and from others (Dolcos and McCarthy,
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
Investigation of vlPFC/IFC activity in the two areas showing increased coupling with AMY in response to emotional distraction revealed a hemispheric asymmetry in this region, concerning its involvement in
Overall, these findings are consistent with evidence pointing to vlPFC as a site of cross-modal inhibition, generally associated with inhibitory processes (Aron et al.,
Noteworthy, other investigations also point to the involvement of other brain regions, such as the ACC and dlPFC, in coping with emotional distraction. Regarding the ACC, the evidence consistent with the involvement of the ventral/rostral ACC in emotional conflict resolution also supports a role for this region in coping with irrelevant emotions (Bush et al.,
In summary, the extant evidence concerning the neural correlates of coping with distracting emotion highlights the role of lateral PFC regions, particularly the left ventrolateral PFC, in diminishing the
Investigation of individual differences is an important topic in the corpus of research examining emotion-cognition interactions (see Dolcos et al.,
The same study that identified the specificity of dlPFC engagement in response to emotional distraction (Dolcos et al.,
Regarding the basic response to emotional distraction, Dolcos et al. (
Results from the same investigation also provided further support for the role of the left vlPFC/IFC in successful coping with emotional distraction, and revealed an interesting hemispheric dissociation between brain activity linked to the short-term vs. long-term impact of emotional distraction on WM and episodic memory (EM), respectively (Dolcos et al.,
Relationships between brain activity and personality-related differences were identified not only for traits reflecting general aspects of cognitive/executive and affective processing, but also for traits reflecting differences in processing and experiencing of specific emotions, such as anxiety. Complementing previous evidence showing that anxiety modulates the response to threat conveyed by social stimuli (e.g., angry faces) in primary emotion processing regions (AMY; e.g., Evans et al.,
In addition, medial prefrontal regions associated with experiencing of emotion (e.g., ventromedial PFC—vmPFC) showed increased overall activity and positive correlations with trait anxiety scores, whereas lateral regions associated with executive functions (e.g., dlPFC) showed decreased overall activity and negative correlations with trait anxiety scores (Denkova et al.,
Overall, the results of these investigations suggest that individual differences in general cognitive/executive control (e.g., attentional impulsivity) and general and specific emotional sensitivity (e.g., anxiety) are linked to neural changes indexing increased sensitivity to emotional distraction, reflected in exacerbated activity in
Available evidence has shown that in addition to enhanced emotional competence (Kring and Gordon,
The study by Iordan et al. (
Interestingly, a specific pattern of sensitivity to emotional distraction was also revealed in men, who showed increased sensitivity in regions of the
The same investigation also identified sex differences linked to the engagement of mechanisms to cope with emotional distraction. Results revealed a dorsal-ventral hemispheric dissociation within the lateral PFC, with the left ventral PFC being linked to individual differences in WM performance in women, and the right dorsal PFC being linked to individual differences in men (Figure
In summary, available evidence points to the role of individual differences in both the basic response to and coping with task-irrelevant emotions, suggesting that increased sensitivity to emotional distraction is associated with a pattern of activity characterized by both greater
The present review discussed evidence regarding the neural correlates of the response to emotional distraction, as provided by fMRI studies focusing on three main topics: (1) the neural circuitry underlying the basic response linked to a detrimental impact of emotional distraction, (2) the neural mechanisms of coping with emotional distraction, and (3) the role of individual differences in these phenomena. Overall, the extant evidence points to specific neural signatures of the response to emotional challenge (summarized in Table
Regarding (2),
Despite a rapidly-growing body of literature providing clarification into the neural correlates of the response to emotional distraction, a number of issues are still unclear. Below, we briefly introduce them in relation to the topics covered in the present review.
An important open question refers to the role of emotional valence and arousal in the impact of emotional distraction. For instance, the majority of studies investigating the impact of task-irrelevant emotional distraction on performance in short-term/working memory tasks have used high-arousing negative distracters, and hence it is not known whether similar effects are also produced by positive distracters, or further dissociations linked to emotional arousal and valence exist. Given that positive and negative emotions have evolved to subserve different functions, it is reasonable to expect that their impact as distracters may be associated with different neural mechanisms, which may partially overlap with the mechanisms underlying the more general effect of emotional arousal. Only a limited number of studies have used stimuli with different emotional properties (i.e., arousal and valence) as task-irrelevant distracters, and the results so far have been mixed (Erk et al.,
Regarding the neural correlates of coping with emotional distraction, an important open question refers to understanding the role of different types of emotional control and their associated neural correlates. Although evidence from studies investigating the response to emotional distraction shows that the impact of task-irrelevant emotions is modulated by inhibitory mechanisms deployed in order to cope with distracting emotions (Dolcos and McCarthy,
Another open question refers to the role of individual differences in the impact of emotional distraction on different cognitive processes, other than WM. Although recent evidence reconciled a long-standing debate regarding whether the processing of emotional stimuli is automatic or depends on available attentional resources (Shafer et al.,
Investigations of the role of individual differences in the response to emotional distraction may prove informative not only for understanding features of individual variation in healthy subjects, but also changes associated with clinical conditions. Recent evidence suggests that dysfunctional alterations in factors influencing emotional sensitivity and susceptibility to emotional distraction, along with changes in the associated neural correlates, could play an important role in mental disorders affecting both emotional and cognitive domains, such as post-traumatic stress disorder (PTSD; Morey et al.,
Regarding the larger context of the impact of emotion on cognition, although a substantial corpus of research (reviewed in Dolcos et al.,
Finally, manipulations involving other types of distraction, emerging from the engagement of other systems, such as long-term memory, could complement present evidence emphasizing the impact of transient visual distracters. This could also expand our present understanding of the role of individual differences in order to include a greater repertoire of responses and establish further links with changes occurring in clinical disorders. For example, clinical research has linked increased susceptibility to recollecting negative events with both symptom severity and cognitive impairment in emotional disorders such as depression and PTSD (e.g., Davis and Nolen-Hoeksema,
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Financial support to authors during the preparation of this manuscript was provided by the University of Illinois. A. D. Iordan was supported by a Beckman Institute Graduate Fellowship.