Atypical Neural Activation During Emotional but Not Nonemotional Response Inhibition in Healthy Young People Exposed to Childhood Maltreatment and Peer Victimization

Abstract

Background

Early-life interpersonal stress, particularly childhood maltreatment (CM), is associated with neurobiological abnormalities and atypical emotion regulation. However, few studies have investigated the neural effects of peer victimization (PV). We examined neural alterations in emotional and nonemotional response inhibition in carefully matched healthy CM and PV groups.

Methods

Functional magnetic resonance imaging data were collected from 113 age- and sex-matched nonclinical/community youths (38 CM, 39 PV, and 36 control) during an emotional (fearful/happy) and nonemotional (letter) Go/NoGo task.

Results

There were no significant group differences in behavioral performance. However, during fearful face inhibition, the CM group exhibited hyperactivation compared with the PV group in a cluster comprising the bilateral calcarine, cuneus, and lingual gyri, which was related to higher parental antipathy in the CM group. Hyperactivation also occurred in limbic-striatal, middle temporal, and cerebellar regions, although at a more liberal threshold. Additionally, there was a trend of PV-specific underactivation in the left middle temporal gyrus during happy inhibition. Despite no significant group differences in nonemotional response inhibition, both the CM and PV groups exhibited greater activation than the control group in default mode network regions during the cognitively low-load LetterGo condition.

Conclusions

These findings suggest that early-life interpersonal stress is associated with atypical neural activation during emotionally driven decision making but not during nonemotional response inhibition, underscoring the importance of examining both “hot” and “cold” decision-making processes. The atypical activation of key emotion-visual processing regions may be a potential mechanism to cope with aversive experiences and may reflect the brain’s attempt to facilitate emotional inhibitory control, particularly in resilient maltreated youths.