Alterations in neural circuits underlying emotion regulation following child maltreatment: a mechanism underlying trauma-related psychopathology

Abstract

Background: Disruptions in neural circuits underlying emotion regulation (ER) may be a mechanism linking child maltreatment with psychopathology. We examined the associations of maltreatment with neural responses during passive viewing of negative emotional stimuli and attempts to modulate emotional responses. We investigated whether the influence of maltreatment on neural activation during ER differed across development and whether alterations in brain function mediated the association between maltreatment and a latent general psychopathology ('p') factor.

Methods: Youth aged 8-16 years with (n = 79) and without (n = 72) exposure to maltreatment completed an ER task assessing neural responses during passive viewing of negative and neutral images and effortful attempts to regulate emotional responses to negative stimuli. P-factor scores were defined by a bi-factor model encompassing internalizing and externalizing psychopathology.

Results: Maltreated youth had greater activation in left amygdala and salience processing regions and reduced activation in multiple regions involved in cognitive control (bilateral superior frontal gyrus, middle frontal gyrus, and dorsal anterior cingulate cortex) when viewing negative v. neutral images than youth without maltreatment exposure. Reduced neural recruitment in cognitive control regions mediated the association of maltreatment with p-factor in whole-brain analysis. Maltreated youth exhibited increasing recruitment with age in ventrolateral prefrontal cortex during reappraisal while control participants exhibited decreasing recruitment with age. Findings were similar after adjusting for co-occurring neglect.

Conclusions: Child maltreatment influences the development of regions associated with salience processing and cognitive control during ER in ways that contribute to psychopathology.

Keywords: Child maltreatment; P-factor; cognitive control network; emotion regulation; fMRI; salience network.

Fig. 1.

Maltreatment exposure and neural recruitment during emotional reactivity. Maltreatment main effects for whole-brain recruitment controlling for SES and race/ethnicity (a) and neglect and race/ethnicity (b), and amygdala recruitment using region of analysis (ROI) (c) during emotional reactivity (Look-Negative>Look-Neutral contrast). Cluster-level correction applied in AFNI, p < 0.005 was the primary threshold, and p < 0.001 was the cluster-level threshold. ROIs were created by masking contrasts of interest (i.e. Look-Negative > Neutral) with a mask of the amygdala from the Harvard–Oxford subcortical atlas (20% threshold; mask pictured).

Fig. 2.

Variation in maltreatment-related neural recruitment across development during emotion regulation. Age by maltreatment moderation controlling for SES and race/ethnicity (a) and neglect and race/ethnicity (b) during emotion regulation (Decrease-Negative > Look-Negative contrast). Cluster-level correction applied in FSL, z > 23 was the primary threshold, and p < 0.01 was the cluster-level threshold.

Fig. 3.

Association of p factor with neural recruitment during emotional reactivity. Cluster-level correction applied in AFNI, p < 0.005 was the primary threshold, and p < 0.001 was the cluster-level threshold.

Fig. 4.

Whole-brain mediation during emotional reactivity. Depicting clusters that significantly mediated the association of child maltreatment with p factor scores during emotional reactivity (Look-Negative > Look-Neutral contrast) controlling for SES and race/ethnicity (a) and neglect and race/ethnicity (b). We used Mediation Effect Parametric Mapping (MEPM) to generate a whole-brain map of mediators with the Wager et al. (2008) Mediation Toolbox. Threshold for significant clusters was p < 0.005 with a minimum of 5 voxels per cluster.