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, 26 (7), 2072-9

Brain Systems Mediating Cognitive Interference by Emotional Distraction

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Brain Systems Mediating Cognitive Interference by Emotional Distraction

Florin Dolcos et al. J Neurosci.

Erratum in

  • J Neurosci. 2006 Mar 8;26(10):2839

Abstract

Flexible behavior depends on our ability to cope with distracting stimuli that can interfere with the attainment of goals. Emotional distracters can be particularly disruptive to goal-oriented behavior, but the neural systems through which these detrimental effects are mediated are not known. We used event-related functional magnetic resonance imaging to investigate the effect of emotional and nonemotional distracters on a delayed-response working memory (WM) task. As expected, this task evoked robust activity during the delay period in typical WM regions (dorsolateral prefrontal cortex and lateral parietal cortex). Presentation of emotional distracters during the delay interval evoked strong activity in typical emotional processing regions (amygdala and ventrolateral prefrontal cortex) while simultaneously evoking relative deactivation of the WM regions and impairing WM performance. These results provide the first direct evidence that the detrimental effect of emotional distracters on ongoing cognitive processes entails the interaction between a dorsal neural system associated with "cold" executive processing and a ventral system associated with "hot" emotional processing.

Figures

Figure 1.
Figure 1.
Diagram of the working memory task showing the event order and trial types. Three categories of trials, defined by the type of distracters presented during the delay interval, were involved. Each trial contained two distracters of the same type, which were consecutively presented for 3 s. Subjects were instructed to encode and maintain the memoranda into working memory, look at the distracters, and then indicate by pressing a response button whether the probes were part of the memoranda (1, yes; 2, no).
Figure 2.
Figure 2.
Brain-behavior relationship showing the direct link between brain activity and memory performance. A, As illustrated by the bar graph of the corrected recognition scores (Hits-FAs), emotional distracters had the most detrimental effect on working memory performance. B, Paralleling this behavioral pattern, emotional distracters had the most disrupting effect on the activity during the delay period in brain regions typically associated with active maintenance of task-relevant information in working memory (e.g., dlPFC). C, Mirroring these effects, emotional distracters had the most enhancing effect in brain regions typically associated with emotional processing (e.g., amygdala). Hits, Correctly identified old probes; FAs, incorrectly identified new probes (false alarms). Error bars represent SEM.
Figure 3.
Figure 3.
Dorsoventral dissociable patterns of activity in the presence of emotional distracters. Emotional distracters produced the most disrupting effect on the activity during the delay period in a set of dorsal brain regions associated with cold executive processes (the blue blobs) while producing the most enhancing effect on activity in a set of ventral brain regions associated with hot emotional processing (the red blobs). The central image shows activation maps of the direct contrasts between the most versus least distracting conditions (i.e., emotional vs scrambled), superimposed on a high-resolution brain image displayed in a lateral view of the right hemisphere. The colored horizontal bars at the bottom of the brain image indicate the gradients of the t values for the activation maps displayed. The line graphs show the time courses of activity in representative dorsal and ventral brain regions (indicated by color-coded arrows). The gray rectangular boxes above the x-axes indicate the onset and duration of the memoranda, distracters, and probes, respectively. FFG, Fusiform gyrus.
Figure 4.
Figure 4.
Right-lateralized patterns of frontal activity in the processing of emotional distracters. Consistent with the role of the right hemisphere in the processing of negative emotions, emotional distracters were associated with a right-lateralized pattern of activity, which was more pronounced in the lateral prefrontal cortex. The activation maps displayed in a coronal view show greater effects of emotional distracters in the right (R) hemisphere than in the left (L) hemisphere. For display purposes, a higher t threshold was used, and hence only activity in the right hemisphere is shown. However, emotional distracters also produced significant effects in the left hemisphere (Table 1) (bar graphs). The bar graphs illustrate the peak delay differences in brain activity between the three experimental conditions in the right versus left hemispheres. The ANOVAs confirming this right-lateralized pattern are performed on percentage signal changes in the MR signal extracted from functionally defined ROIs, which were traced in homologes dorsal and ventral regions from both hemispheres. Error bars represent SEM.
Figure 5.
Figure 5.
Greater correlation between the vlPFC activity and the distractibility scores for emotional than for neutral distracters. The left panel shows a subregion of the right vlPFC (BA 45; Talairach coordinates: x = 60, y = 18, z = 18), the activity of which in the presence of emotional distracters highly correlated with the subjective scores for distractibility. Similar effects were also identified in the left hemisphere (BA 45/46; Talairach coordinates: x = −50, y = 27, z = 13), in which the same correlations were significant for emotional distracters (r = −0.68; p < 0.005) but not for the neutral distracters (r = −0.001; p > 0.99). The correlation map was obtained by calculating across-subject voxel-based correlations on the MR signal from the vlPFC voxels that showed greater activity during the delay period for emotional than for neutral distracters at p < 0.005 (t > 3.0). The scatter plots illustrate the results of the correlations calculated on the averaged MR signal extracted from clusters of voxels showing significant correlations at p < 0.005 (R > 0.64). The colored horizontal bar at the bottom of the brain image indicates the gradients of the R values in the correlation map.

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