Early Experience of Threat is Associated with Altered Neural Sensitivity for Facial Expressions in Young Adults with Emerging Psychiatric Symptoms

BACKGROUND: Studies linking childhood adversity with risk for psychopathology suggest a threat-related information processing bias in those exposed. METHODS: We combined frequency-tagging electroencephalography (EEG) and eye-tracking to assess automatic and implicit facial expression processing in young adults aged 16–24 years with emerging psychiatric symptoms and a history of childhood adversity (N = 52) as compared to healthy controls (N = 61). Neural discrimination of angry or happy faces from neutral faces was assessed via an EEG oddball paradigm. Neural salience and preferential looking towards angry versus neutral faces were quantified via an EEG multi-input paradigm with eye-tracking. RESULTS: Participants with adversity showed lower angry-neutral discrimination relative to happy-neutral discrimination, which was specifically related to their threat, but not neglect, experiences. When presenting angry and neutral faces simultaneously, again, they showed similar neural processing, while controls preferentially processed neutral faces, providing convincing neural evidence for threat-safety indiscrimination in adversity. Additionally, while we observed a neural attentional bias towards anger in participants with adversity relative to controls, no such bias was observed from the visual looking patterns, highlighting the superior sensitivity of the frequency-tagging EEG approach in capturing subtle adversity-related alterations in facial expression processing. All these response patterns were unrelated to the presence of psychiatric symptoms. CONCLUSIONS: Our results demonstrate that childhood adversity, in particular threat experiences, is associated with a threat-related information processing bias in young adults. This bias is not only characterized by increased neural salience towards threatening information, but also by decreased neural threat-safety discrimination.