Dimensions of childhood adversity have distinct associations with neural systems underlying executive functioning

Abstract

Childhood adversity is associated with increased risk for psychopathology. Neurodevelopmental pathways underlying this risk remain poorly understood. A recent conceptual model posits that childhood adversity can be deconstructed into at least two underlying dimensions, deprivation and threat, that are associated with distinct neurocognitive consequences. This model argues that deprivation (i.e., a lack of cognitive stimulation and learning opportunities) is associated with poor executive function (EF), whereas threat is not. We examine this hypothesis in two studies measuring EF at multiple levels: performance on EF tasks, neural recruitment during EF, and problems with EF in daily life. In Study 1, deprivation (low parental education and child neglect) was associated with greater parent-reported problems with EF in adolescents (N = 169; 13-17 years) after adjustment for levels of threat (community violence and abuse), which were unrelated to EF. In Study 2, low parental education was associated with poor working memory (WM) performance and inefficient neural recruitment in the parietal and prefrontal cortex during high WM load among adolescents (N = 51, 13-20 years) after adjusting for abuse, which was unrelated to WM task performance and neural recruitment during WM. These findings constitute strong preliminary evidence for a novel model of the neurodevelopmental consequences of childhood adversity.

Figure 1

Working memory filtering task. In this spatial delayed match to sample task adapted from McNab and Klingberg (2008), participants were given 1 s to remember either two or four stars (encoding). On 25% of the trials, they were instructed prior to encoding to ignore two yellow stars while remembering the location of two red stars (cue period). After a 2-, 3-, or 4-s delay (delay) where they viewed a white fixation crosshair, they were shown a screen with a single question mark (probe). They pressed one button to indicate if that question mark was in the same place as a star to be remembered and another to indicate that it was not. Stimuli were presented in four runs lasting approximately 9 min each.

Figure 2

Whole-brain associations with parental education. Associations of parental education with neural response to trials involving high > low working memory load. Regions with greater blood oxygen level dependent activation during high > low working memory load as parental education decreased. Cluster-level correction to a cluster level p = .05 was applied in FSL with z >2.3, p <.01 as our voxel-level threshold. Severity of abuse exposure, age, and sex were included as nuisance regressors in all analyses.

Figure 3

Activation in regions of interest and with parental education. Associations of parental education with neural recruitment during high > low working memory load in prefrontal cortex regions of interest: anterior cingulate cortex (ACC), medial frontal gyrus (MFG), and right inferior frontal gyrus (rIFG). Regions of interest were defined structurally using FreeSurfer (see Methods section for details). Parameter estimates were extracted for the contrast of high > low working memory load. Severity of abuse exposure, age, and sex were included as nuisance regressors in all analyses.