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Negative affect moderates the effect of social rejection on frontal and anterior cingulate cortex activation in borderline personality disorder.

ABSTRACT: Patients with borderline personality disorder (BPD) have a heightened sensitivity to social exclusion. Experimental manipulations have produced inconsistent findings and suggested that baseline negative affect (NA) might influence the experience of exclusion. We administered a standardized social exclusion protocol (Cyberball paradigm) in BPD (n = 39) and age-matched and sex-matched healthy controls (n = 29) to investigate the association of NA on social exclusion and activation in brain regions previously implicated in this paradigm. Compared with controls, patients with BPD showed higher activation during social exclusion in the anterior cingulate cortex (ACC), the medial prefrontal cortex (mPFC), and in the right precuneus. Prescan NA ratings were associated with higher brain activation in the ACC and mPFC over all conditions, and post hoc t tests revealed that differences between the groups were only significant when controlling for NA. Brain activation during exclusion was correlated with NA separately for each group. Only BPD patients showed a significant association of NA and exclusion related precuneus activation (r = .52 p = .001). Additionally, BPD patients experienced less feelings of belonging compared with a healthy control (HC) group during inclusion and exclusion, although they estimated their ball possessions significantly higher than did the HC. These findings suggest that baseline NA has a crucial impact on Cyberball-related brain activation. The results underscore the importance of considering levels of NA in social exclusion protocols for participants high in this trait.

SUBMITTER: Wrege JS

PROVIDER: S-EPMC6785570 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Negative affect moderates the effect of social rejection on frontal and anterior cingulate cortex activation in borderline personality disorder.

Wrege Johannes Sebastian JS Ruocco Anthony Charles AC Euler Sebastian S Preller Katrin H KH Busmann Mareike M Meya Louisa L Schmidt André A Lang Undine E UE Borgwardt Stefan S Walter Marc M

Cognitive, affective & behavioral neuroscience 20191001 5

Patients with borderline personality disorder (BPD) have a heightened sensitivity to social exclusion. Experimental manipulations have produced inconsistent findings and suggested that baseline negative affect (NA) might influence the experience of exclusion. We administered a standardized social exclusion protocol (Cyberball paradigm) in BPD (n = 39) and age-matched and sex-matched healthy controls (n = 29) to investigate the association of NA on social exclusion and activation in brain regions ...[more]

PMID: 31165440

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Project description:OBJECTIVE:The anterior cingulate cortex (ACC) is critical for both stress and inhibitory control processes and has been implicated in childhood trauma. This prospective study tested the hypothesis that early trauma moderates the association between inhibitory control during late childhood and ACC stress reactivity during adolescence. METHOD:Sixty-four adolescents were stratified into higher- or lower-childhood-trauma groups. Inhibitory control was indicated by fewer errors on a Stroop Color-Word task. Personalized stress cues during functional magnetic resonance imaging assessed neural correlates of stress in adolescents. RESULTS:Using a priori-defined anterior (rCZa) and posterior rostral cingulate zones of the ACC, associated with Stroop Color-Word task performance in prior meta-analyses, Stroop errors correlated inversely with activation in the rCZa during stress-cue exposure (r?=?-.23, p?=?.04). Childhood trauma moderated the association between Stroop errors and rCZa stress reactivity (interaction?=?-1.26, p?=?.02, 95%CI?=?-2.33,-0.20), where Stroop errors were inversely associated with brain activation among those with higher childhood trauma (simple slopes?=?-.83, p?=?.007, 95%CI?=?-1.40,-0.25). Low stress-related rCZa activation inversely (R2?=?0.19, b?=?-0.43, p?=?.001, 95%CI?=?-4.11,-1.06) and Stroop errors directly (R2?=?0.09, b?=?0.27, p?=?.048, 95%CI?=?0.02, 5.8) associated with baseline subjective anxiety while controlling for childhood trauma. CONCLUSIONS:This is the first study to demonstrate a moderating role of childhood trauma on the relationship between inhibitory control and stress-related ACC activation. Childhood trauma may portend neurodevelopmental changes that impede recruitment of control-associated ACC-functioning during distress, which may relate to dysregulation of stress-induced affective responses. Further work is needed to elucidate relationships between childhood trauma and addictive behaviors precipitated by stress.

Project description:Working memory is critically involved in ignoring emotional distraction while maintaining goal-directed behavior. Antagonistic interactions between brain regions implicated in emotion processing, e.g., amygdala, and brain regions involved in cognitive control, e.g., dorsolateral and dorsomedial prefrontal cortex (dlPFC, dmPFC), may play an important role in coping with emotional distraction. We previously reported prolonged reaction times associated with amygdala hyperreactivity during emotional distraction in interpersonally traumatized borderline personality disorder (BPD) patients compared to healthy controls (HC): Participants performed a working memory task, while neutral versus negative distractors (interpersonal scenes from the International Affective Picture System) were presented. Here, we re-analyzed data from this study using psychophysiological interaction analysis. The bilateral amygdala and bilateral dorsal anterior cingulate cortex (dACC) were defined as seed regions of interest. Whole-brain regression analyses with reaction times and self-reported increase of dissociation were performed. During emotional distraction, reduced amygdala connectivity with clusters in the left dorsolateral and ventrolateral PFC was observed in the whole group. Compared to HC, BPD patients showed a stronger coupling of both seeds with a cluster in the right dmPFC and stronger positive amygdala connectivity with bilateral (para)hippocampus. Patients further demonstrated stronger positive dACC connectivity with left posterior cingulate, insula, and frontoparietal regions during emotional distraction. Reaction times positively predicted amygdala connectivity with right dmPFC and (para)hippocampus, while dissociation positively predicted amygdala connectivity with right ACC during emotional distraction in patients. Our findings suggest increased attention to task-irrelevant (emotional) social information during a working memory task in interpersonally traumatized patients with BPD.

Dataset Information

Negative affect moderates the effect of social rejection on frontal and anterior cingulate cortex activation in borderline personality disorder.

Publications

Negative affect moderates the effect of social rejection on frontal and anterior cingulate cortex activation in borderline personality disorder.

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