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

Francesca C Fortenbaugh,Michael Esterman,Vincent Corbo,Regina Mcglinchey,William Milberg,David Salat,Joseph Degutis,Victoria Poole

doi:10.1002/brb3.684

Abstract

IntroductionInterpersonal 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.MethodsA total of 66 Veterans (18 with and 48 without a history of I‐ELT) completed a nonemotional sustained attention task during functional MRI.ResultsThe 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.ConclusionThese 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.

Highlights

Interpersonal early life trauma (I-ELT) is associated with a myriad of functional impairments in adulthood, increased risk of drug addiction, and neuropsychiatric disorders
We examined the connectivity of the amygdala during a sustained attention task in groups of Veterans with and without exposure to interpersonal early life trauma, defined as physical/sexual abuse or witnessing family violence before the age of eighteen
Our findings suggest that individuals exposed to I-ELT show general deficits in sustained attention to stimuli without emotional valence

Summary

| INTRODUCTION

Converging evidence points to a lasting impact of trauma experienced during sensitive periods in childhood (Anda et al, 2006), with developmental trajectories occurring pre/periadolescence irremediably altered by exposure to significant stress (Bergman, Larsen, & Mueller, 1986; Mullen, Martin, Anderson, Romans, & Herbison, 1996; Perry, Pollard, Blakley, Baker, & Vigilante, 1995; Tottenham & Sheridan, 2010). Functional imaging studies have further shown that, when processing emotional stimuli (e.g., angry faces), I-ELT was associated with increased activity in the amygdala (Bremner et al, 2005; Grant, Cannistraci, Hollon, Gore, & Shelton, 2011; Maheu et al, 2010), and with decreased activity of the hippocampus (Bremner et al, 1999; Bremner et al, 2003; Carrion, Haas, Garrett, Song, & Reiss, 2010) and anterior cingulate cortex (Bremner, Vythilingam, Vermetten, Southwick, McGlashan, Nazeer, et al, 2003; Bremner, et al, 2003; Bremner et al, 2004; Mueller et al, 2010) These studies have been limited by the consistent use of emotional stimuli, preventing assessments of whether I-ELT-related limbic dysfunction potentially impacts more general aspects of cognition. Based on findings in the literature indicating that the amygdala may be structurally and functionally altered following a history of I-ELT, we tested the hypothesis that group-level differences in amygdala functional connectivity exist across the brain and, are related to observed attentional performance differences

| Participants

Findings

| DISCUSSION