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Interpersonal early-life trauma alters amygdala connectivity and sustained attention performance.

ABSTRACT: INTRODUCTION:Interpersonal early life trauma (I-ELT) is associated with a myriad of functional impairments in adulthood, increased risk of drug addiction, and neuropsychiatric disorders. While deficits in emotional regulation and amygdala functioning are well characterized, deficits in general cognitive functioning have also been documented. However, the neural underpinnings of cognitive dysfunction in adults with a history of I-ELT and the potential relationship between amygdala-based functional connectivity and behavioral performance are currently poorly understood. This study examined how I-ELT affects the cognitive and neural mechanisms supporting sustained attention. METHODS:A total of 66 Veterans (18 with and 48 without a history of I-ELT) completed a nonemotional sustained attention task during functional MRI. RESULTS:The individuals with I-ELT showed significant impairments in sustained attention (i.e., higher error rates, greater response variability). This cohort exhibited increased amygdala functional connectivity with the prefrontal cortex and decreased functional connectivity with the parahippocampal gyrus when compared to those without I-ELT. These connections were significantly correlated with individual differences in sustained attention performance. Notably, classification analyses revealed that the pattern of amygdala connectivity across the whole brain was able to classify I-ELT status with 70% accuracy. CONCLUSION:These results provide evidence of a lasting negative impact for those with a history of I-ELT on sustained attention ability. They also highlight a critical role for amygdala functioning in cognitive control and sustained attention for those with a history of I-ELT, which may underlie the observed attention deficits in clinical assessments and cognitive tests involving both emotional and nonemotional stimuli.

SUBMITTER: Fortenbaugh FC

PROVIDER: S-EPMC5434189 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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Interpersonal early-life trauma alters amygdala connectivity and sustained attention performance.

Fortenbaugh Francesca C FC Corbo Vincent V Poole Victoria V McGlinchey Regina R Milberg William W Salat David D DeGutis Joseph J Esterman Michael M

Brain and behavior 20170410 5

<h4>Introduction</h4>Interpersonal early life trauma (I-ELT) is associated with a myriad of functional impairments in adulthood, increased risk of drug addiction, and neuropsychiatric disorders. While deficits in emotional regulation and amygdala functioning are well characterized, deficits in general cognitive functioning have also been documented. However, the neural underpinnings of cognitive dysfunction in adults with a history of I-ELT and the potential relationship between amygdala-based f ...[more]

PMID: 28523226

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Project description:BackgroundCerebral blood flow (CBF) is critically important in the overall maintenance of brain health, and disruptions in normal flow have been linked to the degradation of the brain's structural integrity and function. Recent studies have highlighted the potential role of CBF as a link between psychiatric disorders and brain integrity. Although interpersonal early life trauma (IP-ELT) is a risk factor for the development of psychiatric disorders and has been linked to disruptions in brain structure and function, the mechanisms through which IP-ELT alters brain integrity and development remain unclear. The goal of this study was to understand whether IP-ELT was associated with alterations in CBF assessed during adulthood. Further, because the cognitive implications of perfusion disruptions in IP-ELT are also unclear, this study sought to investigate the relationship between IP-ELT, perfusion, and cognition.Methods179 Operations Enduring Freedom/Iraqi Freedom/New Dawn (OEF/OIF/OND) Veterans and military personnel completed pseudo-continuous arterial spin labeling (pCASL) imaging, clinical interviews, the Traumatic Life Events Questionnaire (TLEQ), and a battery of neuropsychological tests that were used to derive attention, memory, and executive function cognitive composite scores. To determine whether individuals were exposed to an IP-ELT, events on the TLEQ that specifically queried interpersonal trauma before the age of 18 were tallied for each individual. Analyses compared individuals who reported an interpersonal IP-ELT (IP-ELT+, n = 48) with those who did not (IP-ELT-, n = 131).ResultsWhole brain analyses revealed that IP-ELT+ individuals had significantly greater CBF in the right inferior/middle temporal gyrus compared to those in the IP-ELT- group, even after controlling for age, sex, and posttraumatic stress disorder (PTSD). Further, perfusion in the right inferior/middle temporal gyrus significantly mediated the relationship between IP-ELT and memory, not attention or executive function, such that those with an IP-ELT had greater perfusion, which, in turn, was associated with poorer memory. Examination of other clinical variables such as current PTSD diagnosis and severity as well as the interaction between IP-ELT and PTSD yielded no significant effects.ConclusionsThese results extend prior work demonstrating an association between ELT and cerebral perfusion by suggesting that increased CBF may be an important neural marker with cognitive implications in populations at risk for psychiatric disorders.

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.

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Interpersonal early-life trauma alters amygdala connectivity and sustained attention performance.

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Interpersonal early-life trauma alters amygdala connectivity and sustained attention performance.

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