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Randomized Controlled Trial
. 2010 Nov 30;5(11):e14150.
doi: 10.1371/journal.pone.0014150.

The impact of anxiety-inducing distraction on cognitive performance: a combined brain imaging and personality investigation

Ekaterina Denkova  1 , Gloria Wong, Sanda Dolcos, Keen Sung, Lihong Wang, Nicholas Coupland, Florin Dolcos
Affiliations
Randomized Controlled Trial

The impact of anxiety-inducing distraction on cognitive performance: a combined brain imaging and personality investigation

Ekaterina Denkova et al. PLoS One. .

Abstract

Background: Previous investigations revealed that the impact of task-irrelevant emotional distraction on ongoing goal-oriented cognitive processing is linked to opposite patterns of activation in emotional and perceptual vs. cognitive control/executive brain regions. However, little is known about the role of individual variations in these responses. The present study investigated the effect of trait anxiety on the neural responses mediating the impact of transient anxiety-inducing task-irrelevant distraction on cognitive performance, and on the neural correlates of coping with such distraction. We investigated whether activity in the brain regions sensitive to emotional distraction would show dissociable patterns of co-variation with measures indexing individual variations in trait anxiety and cognitive performance.

Methodology/principal findings: Event-related fMRI data, recorded while healthy female participants performed a delayed-response working memory (WM) task with distraction, were investigated in conjunction with behavioural measures that assessed individual variations in both trait anxiety and WM performance. Consistent with increased sensitivity to emotional cues in high anxiety, specific perceptual areas (fusiform gyrus--FG) exhibited increased activity that was positively correlated with trait anxiety and negatively correlated with WM performance, whereas specific executive regions (right lateral prefrontal cortex--PFC) exhibited decreased activity that was negatively correlated with trait anxiety. The study also identified a role of the medial and left lateral PFC in coping with distraction, as opposed to reflecting a detrimental impact of emotional distraction.

Conclusions: These findings provide initial evidence concerning the neural mechanisms sensitive to individual variations in trait anxiety and WM performance, which dissociate the detrimental impact of emotion distraction and the engagement of mechanisms to cope with distracting emotions. Our study sheds light on the neural correlates of emotion-cognition interactions in normal behaviour, which has implications for understanding factors that may influence susceptibility to affective disorders, in general, and to anxiety disorders, in particular.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Diagram of the WM Task with Anxiety-Inducing Distraction.
Functional magnetic resonance imaging (fMRI) data were recorded while subjects performed a working memory (WM) task for faces, with distraction presented during the delay interval between the memoranda and probes. To increase the impact, the novel distracters were morphed. The WM performance was measured using a recognition memory task, in which participants indicated by pushing a button whether single-face probes were part of the memoranda (Old = 1) or not (New = 2), and then they indicated the level of confidence (LOC) in their responses by pushing one of three buttons (1 = Low, 2 = Medium, 3 = High). All stimuli were presented in colour. Written informed consent for photograph publication was obtained for all faces illustrated in the figure that are not part of the standardized NimStim Face Stimulus Set.
Figure 2
Figure 2. The detrimental effect of transient anxiety-inducing distraction on WM performances was reflected in responses with the highest level of confidence (LOC3).
A two-way ANOVA on corrected recognition scores (% Hits – % FAs) yielded a significant level of confidence (LOC1, LOC2, LOC3) x distracter type (emotional, neutral, scrambled) interaction (F ,  = 8.57; p<0.00002), and post-hoc analyses showed that the emotional distraction had an impairing effect only on LOC3, with the emotional distracters being associated with lower level of performance compared to both neutral (p<0.02) and scrambled distracters (p<0.0005). Emo = Emotional Distracter; Neu  =  Neutral Distracters; Scr  =  Scrambled Distracters; FAs  =  False Alarms; WM  =  Working Memory. Error bars represent standard errors.
Figure 3
Figure 3. Opposite patterns of activity and co-variation in the ventral vs. dorsal neural systems in the presence of anxiety-inducing distracters.
Consistent with a bottom-up effect of emotional distraction on brain activity, ventral regions associated with perception (FG, bottom panels) and experiencing of emotion (vmPFC, middle panels) showed increased overall activity (red blobs) and positive correlations with anxiety scores (white blobs within the red blobs), whereas dorsal regions associated with executive functions (e.g., dlPFC, top panels) showed decreased overall activity (blue blobs) and negative correlations with anxiety scores (white blobs within the blue blobs). Because in the FG the correlation was specific for social anxiety, whereas in the vmPFC it was larger for general anxiety (see Table 3), the scatterplots on the right side of the figure are based on the corresponding correlations of the signal extracted from the ROIs with the LSAS and STAI-T scores, respectively. In the vmPFC, the positive correlation was specific for the emotional distraction - i.e., the correlation was significant for the emotional but not for the neutral distracters, and the difference between these two correlations was also significant (see Table 3). In the dlPFC, although in the whole ROI (white blob) the negative correlation was not statistically greater for the emotional distracters (see Table 3), a restricted area within this ROI (the black blob within the white blob) showed specificity for the emotional distracters. As illustrated in the top right scatterplot, the correlation was significant for the emotional but not for the neutral distracters, and the difference between these two correlations was also significant (t = −1.92; p = 0.04). A similar pattern was also observed in the dmPFC (not shown). The activation and conjunction/correlation maps are superimposed on high resolution brain images displayed in coronal views (y indicates the Talairach coordinate on the anterior-posterior axis of the brain). The line graphs on the left side panels illustrate the time courses of the fMRI signal, as extracted from the ROIs meeting the triple conjunction criteria (the white blobs), on a TR-by-TR basis (1 TR = 2 seconds). FG  =  Fusiform Gyrus; vmPFC  =  Ventro-medial Prefrontal Cortex; dlPFC  =  Dorso-lateral Prefrontal Cortex; L =  Left; R =  Right; TR  =  Repetition Time.
Figure 4
Figure 4. Co-variation between activity in the right fusiform gyrus (FG) and individual differences in WM performance.
Consistent with a bottom-up impact of emotional distraction on cognitive performance, the right FG showed increased overall activity (red blob) and negative correlation with the LOC3 WM performance (the white blob within the red blob). The negative correlation, illustrated in the right side scatterplot was specific for the emotional distracters (see Table 4). The middle panel illustrates the activation and correlation maps superimposed on high resolution brain images, displayed in coronal view. The line graph in the left side panel illustrates the time course of fMRI signal, as extracted from the whole ROI meeting the triple conjunction criteria, on a TR-by-TR basis.
Figure 5
Figure 5. Evidence for the role of the PFC in coping with emotional distraction.
Regions in the dorso-medial and left lateral PFC showed positive correlations with the LOC3 WM performance (white blobs within the blue blobs), despite showing overall decreased activity (blue blobs) in the presence of emotional distraction. In both cases, the correlations were significant only for the emotional distracters, and in the dmPFC the correlation for emotional distracter was also statistically greater than for the neutral distracters (see Table 4). The line graphs in the left side panels illustrate the time course of fMRI signal, as extracted from the whole ROIs meeting the triple conjunction criteria, on TR-by-TR. The activation and correlation maps are superimposed on high resolution brain images displayed in coronal views.
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