Opposing influences of emotional and non-emotional distracters upon sustained prefrontal cortex activity during a delayed-response working memory task
Introduction
Studies investigating the neural correlates of delayed-response working memory (WM) tasks have demonstrated sustained activity in the dorsolateral prefrontal cortex (dlPFC) regions that spans the interval between the memoranda and the probe stimulus. Several groups have associated the presence of this sustained activity with working memory maintenance (Courtney, Ungerleider, Keil, & Haxby, 1997; Curtis & D’Esposito, 2003; Funahashi, Bruce, & Goldman-Rakic, 1993; Goldman-Rakic, 1995; Smith & Jonides, 1999), although others have suggested that this activity might reflect other processes such as the maintenance of a preparatory set, mental timing, or the control of distraction (Jha & McCarthy, 2000). Task-irrelevant stimuli presented during the delay period typically interfere with WM performance, and so the effect of such distracters on sustained activation in delayed-response tasks has generated considerable interest. Indeed, evidence from recent functional neuroimaging studies suggests that sustained activity in the dlPFC is affected by distraction, but the nature of this effect has not been consistent.
One study from our group has shown that the presence of emotional distracters in the delay interval was associated with impairments in WM performance and a marked decrease in sustained activity to below prestimulus baseline levels (Dolcos & McCarthy, 2006). This finding suggests that, possibly because of their relevance for survival, emotional stimuli can capture and divert attention, and thus may reallocate processing resources from task-relevant to task-irrelevant emotional stimuli. Other evidence from studies using non-emotional distracters (e.g., Yoon, Curtis, & D’Esposito, 2006) suggests that such effects are not specific to emotional distraction per se, and that similar decreases in sustained activation occur with memoranda-confusable non-emotional distracters (e.g., novel face presented as distracters in a WM task for faces). However, when our group tested memoranda-confusable neutral distracters (Dolcos, Miller, Kragel, Jha, & McCarthy, 2007), we found the expected impairments in memory performance, but increased not decreased dlPFC activity.
While the similar decreases in dlPFC-sustained activity in the studies of Dolcos and McCarthy (2006) and Yoon et al. (2006) that used different types of distracters suggests the operation of similar neural mechanisms mediating the effects of task-irrelevant distraction, the contradictory findings from Dolcos et al. (2007) suggest that the same behavioral outcome might occur through different mechanisms. However, because these contradictory effects were observed in different studies, using different subjects and analytical strategies, their comparability is open to question.
A possible explanation for these contradictory findings is that the dlPFC may show a subregional specificity with respect to its involvement in operations that are generally engaged in the processing of distraction, and/or are differentially sensitive to the nature of distraction. It is not clear whether the opposing effects of distraction type upon dlPFC-sustained activity (compare Dolcos & McCarthy, 2006 with Dolcos et al., 2007) modulate delay activity in the same dlPFC regions, or in different regions linked to the nature of distraction. As Dolcos et al. (2007) used an anatomical region of interest (ROI) analysis, it is possible that the ROIs may have summed brain activity over subpopulations of voxels with different activation profiles. Investigation of these issues has relevance for understanding the alterations in neural mechanisms that lead to general impairment of cognitive control (e.g., observed in frontal patients and in healthy and clinical aging Chao & Knight, 1995; Richer et al., 1993, Shimamura, 2000), and to the impairment in the ability to control emotional distraction (e.g., observed in mood and anxiety disorders, Mayberg et al., 1999; Watts, MacLeod, & Morris, 1988).
The goal of the present study, therefore, was to directly compare the effect of memoranda-confusable and memoranda-nonconfusable emotional distracters on delay activity in the dlPFC. Event-related functional magnetic resonance imaging (fMRI) data were acquired while subjects performed a delayed-response item recognition working memory task for faces. Distracters presented during the delay interval were either faces that were cropped and posed similarly as the faces comprising the memoranda (confusable distracters) or scenes with strong emotional content (nonconfusable distracters). Additional control distracters were also included. Based on evidence from our prior studies that separately investigated this issue (Dolcos & McCarthy, 2006; Dolcos et al., 2007), we predicted that the memoranda-confusable distracters would increase dlPFC-sustained activity while the memoranda-nonconfusable emotional distracters would decrease dlPFC-sustained activity. Of critical interest was whether these predicated opposing patterns of sustained activity would occur in the same or different areas of the dlPFC.
Section snippets
Subjects
Analyses were performed on data from fourteen healthy young (19–30 years of age) right-handed adults from Duke University community who participated in the study. Because other investigators have reported gender differences in the processing of emotional information (Lang, Greenwald, Bradley, & Hamm, 1993; Shields, 1991), we restricted our study to female participants to maintain homogeneity of the subject sample. The experimental protocol was approved by the Institutional Review Board at Duke
Emotional intensity ratings
As expected, subjects rated emotional distracters as more emotional than the neutral distracters. The average scores for emotional intensity (1 = lowest, 4 = highest) as rated by the participants were 2.8 (S.D. = 0.3) for the emotional distracters and 1.1 (S.D. = 0.1) for the neutral distracters. Pairwise comparison of the rating scores was highly significant (t(10) = 21.22, p < 0.00001), thus confirming that the subjects’ rating scores were consistent with the normative scores.
Working memory performance
The percentages of probes
Discussion
The present study investigated the influence of different forms of distraction upon sustained activation in prefrontal cortex during the delay interval of a delayed item recognition working memory task. Consistent with our prior findings, the study identified dlPFC areas that showed opposing patterns of activity to memoranda-confusable (increased activity) and memoranda-nonconfusable emotional distracters (decreased activity). The opposite patterns were not observed. The present study also
Conclusions
In summary, the present study provides evidence concerning the role of the dlPFC in processing task-irrelevant distracters, and identified specific PFC regions that are sensitive to the nature of distraction and linked with differences in performance in the presence of memoranda-confusable and memoranda-nonconfusable emotional distraction. The present findings suggest that the pattern of decreased delay activity observed reflects the reallocation of executive control resources by emotional
Acknowledgements
This research was supported by the grants R01-MH05286, P01-NS41328, and P50-MH60451. GM was supported by a DVA Senior Research Career Scientist Award and by a DVA Mental Illness Research, Education, and Clinical Center (MIRECC). FD was supported by a Post-Doctoral Fellowship from the Natural Sciences and Engineering Research Council of Canada (NSERC) and a Young Investigator Award from the National Alliance for Research on Schizophrenia and Depression (NARSAD). The authors wish to thank Jordan
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Current address: Department of Psychiatry, University of Alberta, Edmonton, Alta., Canada. Tel.: +1 780 492 8657.