Neurofunctional Abnormalities during Sustained Attention in Severe Childhood Abuse

Abstract

Childhood maltreatment is associated with adverse affective and cognitive consequences including impaired emotion processing, inhibition and attention. However, the majority of functional magnetic resonance imaging (fMRI) studies in childhood maltreatment have examined emotion processing, while very few studies have tested the neurofunctional substrates of cognitive functions and none of attention. This study investigated the association between severe childhood abuse and fMRI brain activation during a parametric sustained attention task with a progressively increasing load of sustained attention in 21 medication-naïve, drug-free young people with a history of childhood abuse controlling for psychiatric comorbidities by including 19 psychiatric controls matched for psychiatric diagnoses, and 27 healthy controls. Behaviorally, the participants exposed to childhood abuse showed increased omission errors in the task which correlated positively trend-wise with the duration of their abuse. Neurofunctionally, the participants with a history of childhood abuse, but not the psychiatric controls, displayed significantly reduced activation relative to the healthy controls during the most challenging attention condition only in typical attention regions including left inferior and dorsolateral prefrontal cortex, insula and temporal areas. We therefore show for the first time that severe childhood abuse is associated with neurofunctional abnormalities in key ventral frontal-temporal sustained attention regions. The findings represent a first step towards the delineation of abuse-related neurofunctional abnormalities in sustained attention, which may help in the development of effective treatments for victims of childhood abuse.

Fig 1. Schematic Representation of the Sustained Attention Task.

Subjects are required to press a right-hand button as soon as they see a timer appear on the screen counting seconds. The counter appears after either predictable short delays of 0.5s in blocks of 3–5 stimuli, or after unpredictable long delays of 2s, 5s or 8s, pseudorandomly interspersed into the blocks of 0.5s delays. The long second delays have a progressively higher load on sustained attention than the short 0.5s delays that are typically anticipated and have a higher load on sensorimotor synchronization.

Fig 2. Group by Delay Interaction Effect on Brain Activation in Healthy Controls, Young People Exposed to Childhood Abuse and Psychiatric Controls.

A) Axial sections showing group by delay interaction effect on brain activation during sustained attention in 27 healthy controls, 21 young people exposed to childhood abuse and 19 psychiatric controls as revealed by F test, p < 0.05 FWE-corrected at the cluster-level. Axial slices are marked with the z coordinate as distance in millimetres from the anterior–posterior commissure. The right side of the image corresponds to the right side of the brain. B) fMRI BOLD contrast values in Cluster 1 left IFC/DLPFC and Cluster 2 left temporal/fusiform gyrus for the healthy control group (green), childhood abuse group (blue) and psychiatric control group (red) during the 8s delay condition. The group with a history of childhood abuse had significantly lower activation in the left IFC/DLPFC cluster (p<0.05) and at a trend-level in the left temporal/fusiform cluster (p = 0.09) compared to heathy controls. There were no significant differences between the psychiatric and healthy controls.

Fig 3. Group by Delay Interaction Effect on Brain Activation during Sustained Attention in an IQ-matched subsample of Healthy Controls, Young People Exposed to Childhood abuse and Psychiatric Controls.

Axial sections showing group by delay interaction effect on brain activation during sustained attention in a subsample of 18 healthy controls, 19 young people exposed to childhood abuse and 19 psychiatric controls matched on IQ, as revealed by F test, p < 0.05 FWE-corrected at the cluster-level. Axial slices are marked with the z coordinate as distance in millimetres from the anterior–posterior commissure. The right side of the image corresponds to the right side of the brain.