Discussion

To our knowledge, this is the first fMRI study on emotional processing in childhood maltreatment and peer victimisation that has used a sizable community youth sample free from psychopathology, medications and drug misuse, and controlled for the number of recent stressors and the timing and duration of early-life stress. This is essential to elucidate the effects of early-life stress from the confounding effects associated with current stressors, psychiatric comorbidities, medications and drug use.^{Reference Lim, Radua and Rubia7}

There were no significant group differences in task performance, and groups differed in brain activation during disgust processing only. For the ROI analysis, both childhood maltreatment and peer victimisation groups had lower activation in the right amygdala and bilateral posterior insula than controls, with reduced left insular activation furthermore being related to increased self-harm in maltreated individuals. Compared with controls, at the whole-brain level, both childhood maltreatment and peer victimisation groups had lower activation in a cluster of predominantly bilateral limbic-thalamic-striatal, precuneus/PCC and fusiform/lingual regions, which was negatively associated with emotional problems in controls, as well as a cluster of somatosensory regions that was associated with increased self-harm in maltreated individuals. The reduced activation of key emotion and sensory processing regions during disgust processing may possibly serve as an avoidance coping mechanism to protect youths who experience early-life stress from distressing emotional responses by blocking the processing of aversive disgust facial expressions, thereby enabling them to achieve equivalent performance with their counterparts who do not experience early-life stress. However, this may increase their vulnerability for affective psychopathology later in life.

Most earlier studies have focused primarily on negative emotions of fear and anger, whereas disgust has been the most understudied of all emotions.^{Reference McNally37} Nonetheless, there is a growing recognition of the role of disgust as a central emotion in trauma-related disorders, and that it can lead to self-disgust.^{Reference Knowles, Cox, Armstrong and Olatunji38} Disgust is a basic emotion and represents an evolutionary adaptive defensive-avoidance response.^{Reference McNally37} Disgust facial expressions signal interpersonal rejection and have been linked to feelings of self-disgust and debasement,^{Reference Giner-Sorolla and Espinosa39} which is a potential mechanism underlying the association between childhood maltreatment and self-harm/suicide risk.^{Reference Mason, James, Andrew and Fox20}

Recent event-related potential findings reported that childhood maltreatment is associated with an automatic early vigilance and a subsequent attentional avoidance of disgust faces in healthy young adults, where attentional avoidance may be a coping strategy adopted by the maltreated individuals to downregulate their experience of disgust and avoid conflicts.^{Reference Hoepfel, Günther, Bujanow, Kersting, Bodenschatz and Suslow40} Therefore, childhood interpersonal trauma such as childhood maltreatment and peer victimisation, which often involve repeated exposure to facial disgust in others signalling rejection, may affect the victim's processing of disgust and further heighten their vulnerability to affective psychopathology, possibly via feelings of (self-) disgust.

Besides its critical role in interoceptive processes, the insula is also relevant in the processing of negative emotions including disgust and fear,^{Reference Gogolla41} which are frequently experienced in childhood interpersonal trauma. Although the anterior part is usually implicated, mounting research also suggests the involvement of the posterior insula in aversive emotion and sensory processing.^{Reference Gehrlach, Dolensek, Klein, Roy Chowdhury, Matthys and Junghänel42} The posterior insula, which has strong projections to the amygdala and is a major cortical convergence site that integrates signals from within and outside the body, has also been implicated as a neuroanatomical hub underlying various psychiatric conditions.^{Reference Goodkind, Eickhoff, Oathes, Jiang, Chang and Jones-Hagata43}

Aberrant amygdala and insula activations have been found to mediate atypical emotion processing of fear and anger in childhood maltreatment^{Reference Hart, Lim, Mehta, Simmons, Mirza and Rubia3,Reference McCrory, De Brito, Kelly, Bird, Sebastian and Mechelli10} and peer victimisation.^{Reference Swartz, Carranza and Knodt17} Recent large-scale transdiagnostic studies also implicated the role of insula in childhood emotional trauma.^{Reference Popovic, Ruef, Dwyer, Antonucci, Eder and Sanfelici44} In addition, a recent meta-analysis found that youths with self-injurious behaviours exhibited insula functional alterations, which may underlie their core symptoms of altered emotion processing and regulation.^{Reference Lai, Jiang, Xu, Luo, Hao and Li45} Thus, the current findings of atypical limbic activation during disgust processing extends earlier findings of altered threat processing in childhood trauma, and underscores the importance of examining disgust processing in early-life interpersonal stress and self-harm. Furthermore, given that individuals with a history of self-injurious behaviours and suicide have higher pain tolerance than controls,^{Reference Kirtley, O'Carroll and O'Connor46} the reduced activation of the limbic and somatosensory regions, which are also part of the pain modulatory brain networks,^{Reference Lalouni, Fust, Bjureberg, Kastrati, Fondberg and Fransson47} may potentially modulate pain perceptions and increase self-harm/suicide risk by lowering pain sensitivity in maltreated youths.

Converging evidence underscores the link between childhood trauma and atypical development of the visual sensory systems that convey adverse experiences. For instance, morphometric studies reported reduced lingual GMV^{Reference Lim, Hart, Mehta, Worker, Simmons and Mirza6} and reduced fractional anisotropy of the inferior longitudinal fasciculus and inferior frontal-occipital fasciculus in childhood maltreatment, where the reduced fractional anisotropy values were associated with greater severity and longer duration of abuse.^{Reference Lim, Hart, Howells, Mehta, Simmons and Mirza48} A recent meta-analysis further suggests that disruption in these visual-emotional processing tracts may underpin the emotional problems commonly observed in childhood trauma.^{Reference Lim, Howells, Radua and Rubia8} Reduced somatosensory GMV in childhood maltreatment has also been reported in a meta-analysis of structural MRI studies of childhood maltreatment^{Reference Lim, Radua and Rubia7} and in recent large-scale transdiagnostic studies.^{Reference Begemann, Schutte, van Dellen, Abramovic, Boks and van Haren49} Thus, the current findings of reduced activation of the visual and somatosensory regions in youths who experience early-life stress, together with structural abnormalities in these regions reported in earlier studies, suggest that the visual sensory systems may be altered by early-life stress exposure.

The PCC and precuneus form part of the default mode network and are involved in self-referential processing and mental representation, with increased activations being associated with distraction from task performance.^{Reference Davey, Pujol and Harrison50} It has been purported that the PCC mediates experiences of identifying with attributes of ourselves.^{Reference Brewer, Garrison and Whitfield-Gabrieli51} Hence, the observed reduced activation of the PCC/precuneus by our early-life stress groups may suggest an attempt to inhibit self-related thinking of highly relevant emotions that are potentially associated with oneself, such as disgust, to stay focused on the current task. PCC/precuneus are also key areas of visuospatial attention^{Reference Cavanna and Trimble52} and a reduced activation could be attributable to reduced attention or suppression of attention to negative emotional stimuli. In line with this, a recent study found that chronically bullied youths exhibited lower precuneus activation than controls in response to viewing cyberbullying stimuli, thereby signalling habituation to the aversive stimuli.^{Reference McLoughlin, Shan, Mohamed, Boyes, Driver and Lagopoulos53} Thus, the reduced precuneus activation observed in our early-life stress groups may also reflect their habituation to facial disgust.

Both childhood maltreatment and peer victimisation groups achieved comparable task performance as controls, but with a shared under-recruitment of task-relevant brain regions during disgust processing; hence, differences in the activated regions cannot be attributed to performance effects. Moreover, we note that our childhood maltreatment and peer victimisation youths represent high-functioning community youths with comparable IQ and socioeconomic status to the controls. Thus, the atypical brain activation patterns and lack of performance deficits in childhood maltreatment and peer victimisation groups may suggest that the two early-life stress groups employed an adaptive or compensatory neural strategy to achieve comparable task performance.

The shared atypical activation patterns observed in both early-life stress groups, who also had comparable psychological and socioeconomic status scores, underscore the detrimental effects of peer victimisation and suggest that negative peer relationships may be as harmful as abusive caregiving. More research attention on the neural correlates of peer victimisation is warranted. Furthermore, it is intriguing to note that reduced activation of key emotion and sensory processing regions was associated with increased self-harm in maltreated individuals only. It has been postulated that feelings of self-disgust and debasement, which have been linked to disgust facial expressions,^{Reference Giner-Sorolla and Espinosa39} may be a potential mechanism underlying increased self-harm/suicide risk in childhood maltreatment.^{Reference Mason, James, Andrew and Fox20} Although we did not directly test for self-disgust and debasement in the current study, a similar mechanism might be at work. Given that harsh parenting exhibited incremental importance over and above peer victimisation on youths’ self-cognition,^{Reference Cole, Sinclair-McBride, Zelkowitz, Bilsk, Roeder and Spinelli22} we propose that, for our childhood maltreatment group, growing up with constant exposure to disgust expressions from caregivers might have detrimentally affected their internal self-schemas, leading to feelings of worthlessness and perceived burdensome, and thereby increasing their vulnerability for self-harm/suicide. Indeed, research has shown that children internalise expectations from parents in their construction of self-concept, and chronic negative parental feedbacks and rejection are linked to internalising symptoms.^{Reference McLeod, Wood and Weisz54} Thus, we postulate that prolonged exposure to disgust faces, which essentially signal rejection, especially from parents from whom a child typically derives a sense of self-worth during early critical developmental stages, may result in the eventual internalisation of a repulsive self-concept. An inward disgust response to one's self-identity may thus potentiate feelings of perceived burdensome and thwarted belongingness, which further heightens self-harm/suicide risk.

Finally, we did not observe atypical activation during anger and fear possessing, possibly because of our more resilient community-based sample compared with earlier studies. The maltreated and bullied youths in our sample are healthy and high-functioning individuals with similar IQ and socioeconomic status as controls, and have depressive and anxiety scores within normative ranges, albeit higher than controls. Therefore, instead of viewing adverse early experiences as factors leading to general developmental deficits per se, the current findings of reduced recruitment of key emotion and sensory processing regions may reflect the brain's attempt to cope by blocking the processing of aversive stimuli and functionally adapt to growing up in hostile environments in ways that promote survival. Nonetheless, we appreciate that prolonged neural overmodulation during disgust processing, despite meeting the immediate contextual demands, may have negative long-term consequences such as hindering the development of appropriate emotion regulation skills, potentially paving the way to affective disorders and self-injurious behaviours.

This study is not without its limitations. First, it is cross-sectional and the findings are still correlational. Second, the use of retrospective self-report data may be subject to recall biases. Third, the results may not be generalisable to the childhood sexual abuse population. Nevertheless, strengths of this study are that all participants were free from psychopathology, medications and drug misuse; their current stressors were assessed and controlled for; the early adverse experiences were carefully substantiated by semi-structured interviews and we used dynamic stimuli that are more realistic representation of real-life emotional expressions. The slight discrepancy in the ROI and whole-brain findings could be because the ROIs were examined without correction for multiple comparisons, whereas the whole-brain analysis was performed using rigid statistics (family-wise error rate correction). Nonetheless, our whole-brain results reinforced the ROI findings of atypical limbic activation in our early-life stress groups, particularly in the right amygdala and posterior insula. Finally, although the generalisability of the results may be restricted to the ‘more resilient’ portion of community youths without any psychiatric disorders, the current findings underscore that individuals exposed to early-life stress do show neural alterations compared with their unexposed counterparts, even in the absence of reported psychopathology.