Amygdala and dorsal anterior cingulate connectivity during an emotional working memory task in borderline personality disorder patients with interpersonal trauma history

Annegret Krause-Utz^1,2*, Bernet M. Elzinga^3,4, Nicole Y. L. Oei^5,6, Christian Paret^2,7, Inga Niedtfeld^1,2, Philip Spinhoven^3,4, Martin Bohus^1,2 and Christian Schmahl^1,2

• ¹Department of Psychosomatic Medicine and Psychotherapy, Central Institute of Mental Health, Mannheim, Germany
• ²Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
• ³Institute of Psychology, Leiden University, Leiden, Netherlands
• ⁴Leiden Institute for Brain and Cognition (LIBC), Leiden, Netherlands
• ⁵Addiction, Development and Psychopathology (ADAPT) Lab, Department of Psychology, University of Amsterdam, Amsterdam, Netherlands
• ⁶Amsterdam Brain and Cognition (ABC), University of Amsterdam, Amsterdam, Netherlands
• ⁷Department of Neuroimaging, Central Institute of Mental Health, Mannheim, Germany

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.