The Influence of Early Life Stress on the Development of Neural Representations during Mentalizing

Early life stress (ELS) is associated with altered social cognition, but the neurodevelopmental mechanisms of this association remain understudied. In the present longitudinal study spanning 20-years, eighty-nine young adults performed the Reading the Mind in the Eyes Test (RMET) with a matched control condition during fMRI. Two ELS indices were inspected separately: a prospective cumulative risk score based on caregiver wellbeing during pregnancy and first year of life, and a retrospective self-report of adverse experiences by the participants in late adolescence. Neural outcomes were characterized by univariate activation, representational similarity analysis (RSA), and inter-subject RSA. Inter-subject RSA tested two pairwise approaches to intersubject similarity in ELS: absolute pairwise difference, and pairwise average. Prospective ELS was associated with better RMET performance, and one region survived correction across 360 cortical regions tested in RSA and IS-RSA: left anterior inferior frontal sulcus. The IS-RSA effect was pairwise average: low-exposure participants shared a more typical neural representational geometry, while high-exposure participants demonstrated increasing neural representational idiosyncrasy. Additionally, higher prospective ELS was associated with weaker RMET-versus-control separation within the same region. Retrospective ELS yielded no behavioral nor neural associations. The present study offers novel findings relating to neural representations of mentalizing using the RMET, alongside their neurodevelopmental susceptibility to ELS. The present study additionally highlights implications relating to the differentiation of mentalizing from lexical-semantic and semantic-control demands for future research.