Childhood trauma exposure disrupts the automatic regulation of emotional processing

Abstract

Early-life trauma is one of the strongest risk factors for later emotional psychopathology. Although research in adults highlights that childhood trauma predicts deficits in emotion regulation that persist decades later, it is unknown whether neural and behavioral changes that may precipitate illness are evident during formative, developmental years. This study examined whether automatic regulation of emotional conflict is perturbed in a high-risk urban sample of trauma-exposed children and adolescents. A total of 14 trauma-exposed and 16 age-, sex-, and IQ-matched comparison youth underwent functional MRI while performing an emotional conflict task that involved categorizing facial affect while ignoring an overlying emotion word. Engagement of the conflict regulation system was evaluated at neural and behavioral levels. Results showed that trauma-exposed youth failed to dampen dorsolateral prefrontal cortex activity and engage amygdala-pregenual cingulate inhibitory circuitry during the regulation of emotional conflict, and were less able to regulate emotional conflict. In addition, trauma-exposed youth showed greater conflict-related amygdala reactivity that was associated with diminished levels of trait reward sensitivity. These data point to a trauma-related deficit in automatic regulation of emotional processing, and increase in sensitivity to emotional conflict in neural systems implicated in threat detection. Aberrant amygdala response to emotional conflict was related to diminished reward sensitivity that is emerging as a critical stress-susceptibility trait that may contribute to the emergence of mental illness during adolescence. These results suggest that deficits in conflict regulation for emotional material may underlie heightened risk for psychopathology in individuals that endure early-life trauma.

Figures

Figure 1

Emotional conflict task. Participants were instructed to identify the underlying facial emotion (fearful or happy) while ignoring an overlying emotion word (‘FEAR' or ‘HAPPY'). Trials varied such that emotional distracter words either matched (‘congruent' (C)) or conflicted (‘incongruent' (I)) with the underlying facial expression. Conflict interference was assessed by contrasting incongruent trials with congruent trials. Conflict regulation was isolated by contrasting postincongruent incongruent (iI) with postcongruent incongruent (cI) trials. The task was adapted for children by utilizing an established set of child emotion-face stimuli of varied ethnicities, ages 10–17 years (Egger et al, 2011). Importantly, the stimuli used matched the demographics of our study sample and minimized complex relations inherent in adult face stimuli (Marusak et al, 2013).

Figure 2

Lower emotion conflict regulatory ability in trauma-exposed youth. (a) No group differences were observed in overall accuracy (left) or reaction time (RT; right). (b) Trauma-exposed youth showed lower ability to regulate emotional conflict. (b, left) Positive values indicate a gain in performance for iI relative to cI trials (iI–cI). (b, right) Negative values indicate faster response for iI relative to cI trials (iI–cI). *P≤0.05, two-sample t-test. Error bars represent standard error.

Figure 3

Greater amygdala response to emotional conflict in trauma-exposed youth. Greater conflict-related (I–C) bilateral amygdala activity was observed in trauma relative to comparison participants. Results are displayed for the whole brain at p<0.05 uncorrected (a). The anatomically defined amygdala region from which average signal was extracted (b) to provide group differences shown in (c). *P≤0.05 two-sample t-test. Higher conflict-related amygdala reactivity across the sample mediated the association between trauma exposure and diminished reward sensitivity (d). Error bars represent SEM.

Figure 4

Abnormal regulation of the dorsolateral prefrontal cortex (DLPFC) and disrupted amygdala–pregenual cingulate (pgACC) connectivity in trauma-exposed youth. Increase in DLPFC response is observed in trauma participants (a) and this is related to reduced ability to improve behavioral performance during repeat conflict trials (iI–cI; see Figure 2b). Psychophysiologic interaction functional connectivity analysis showed that only comparison participants showed robust negative connectivity between the amygdala and pgACC during emotional conflict regulation (b). Reduced regulatory connectivity was associated with lower ability of trauma participants to improve reaction time during iI relative to cI trials (iI–cI; see Figure 2b). Whole-brain effects displayed at p<0.01 uncorrected; results are significant at pFWE <0.03.