Interpersonal early‐life trauma alters amygdala connectivity and sustained attention performance

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.

Interpersonal early life trauma is associated with increased cerebral perfusion and poorer memory performance in post-9/11 veterans

“…There were no significant mediating effects for performance in attention or executive function domains, although attention performance was significantly worse in those with IP-ELT+ . Together, these results add to the growing literature that suggests a putative role of early adversity on brain health and cognition ( Andersen et al, 2008 , Cohen et al, 2006 , Dannlowski et al, 2012 , Fan et al, 2014 , Fortenbaugh et al, 2017 , Gould et al, 2012 , Jedd et al, 2015 , Majer et al, 2010 , Pagliaccio et al, 2015 ).…”

“…Our finding that increased perfusion in the right inferior/middle temporal gyrus mediates the relationship between IP-ELT and memory performance suggests that perfusion in this region may be particularly important in IP-ELT-associated cognitive outcomes. Previous work has found that ELT is associated with a range of cognitive deficits in memory, attention, executive function, and affective processing ( Fortenbaugh et al, 2017 , Gould et al, 2012 , Hedges and Woon, 2011 , Majer et al, 2010 , Pechtel and Pizzagalli, 2011 ).…”

“…A more recent study has shown that both increases and decreases in 13 gray matter regions predicted childhood trauma severity ( Clausen et al, 2019 ). Additional research has shown ELT negatively impacts brain function, with increased functional connectivity and activation in limbic structures during an emotional processing task ( Jedd et al, 2015 ) as well as a sustained attention task ( Fortenbaugh et al, 2017 ) and decreased functional connectivity between amygdalae and prefrontal regions at rest ( Fan et al, 2014 , Pagliaccio et al, 2015 ). Moreover, a recent meta -analysis reported structural and functional abnormalities in association with childhood trauma type ( Cassiers et al, 2018 ), further implicating disruptions to both structure and function in association with ELT.…”

“…ELT has also been separately linked to cognitive performance ( Gould et al, 2012 , Majer et al, 2010 ). Specifically, research suggests that the negative effects of ELT on cognition spans multiple domains, including memory and affective functions as well as sustained attention, and persist well into adulthood after ELT has ceased ( Fortenbaugh et al, 2017 , Hedges and Woon, 2011 , Pechtel and Pizzagalli, 2011 ). Together, this work indicates that perfusion may have important cognitive implications in individuals exposed to ELT.…”

Individual differences in sustained attention are associated with cortical thickness

“…While studies show that the ability to sustain attention is malleable within an individual (e.g., due to motivation, time‐on‐task), there are also stable, trait‐like individual differences in sustained attention ability (Fortenbaugh et al, ; Fortenbaugh, DeGutis, & Esterman, ; Rosenberg, Noonan, DeGutis, & Esterman, ; Unsworth, Redick, Lakey, & Young, ). These differences are particularly apparent in numerous clinical populations (Clark, Iversen, & Goodwin, ; DeGutis et al, ; Fortenbaugh et al, ; Fortenbaugh, Corbo, et al, ; Fortenbaugh, DeGutis, & Esterman, ; Johnson et al, ; Liu et al, ; Vasterling, Brailey, Constans, & Sutker, ) whose deficits in sustained attention have considerable real‐world consequences (Smilek, Carriere, & Cheyne, ). Associations between individual differences in sustained attention and trauma sequelae, such as posttraumatic stress disorder (PTSD), depression, and traumatic brain injury (TBI), make this avenue of research especially relevant for Veteran populations (DeGutis et al, ; Dutra, Marx, McGlinchey, DeGutis, & Esterman, ; Esterman et al, in press).…”