Pubertal Testosterone and Brain Response to Faces in Young Adulthood: An Interplay between Organizational and Activational Effects in Young Men

Abstract

According to the organizational-activational hypothesis, the organizational effects of testosterone during (prenatal) brain development moderate the activational effects of adult testosterone on behavior. Accumulating evidence supports the notion that adolescence is another period during which sex hormones organize the nervous system. Here we investigate how pubertal sex hormones moderate the activational effects of adult sex hormones on social cognition in humans. To do so, we recruited a sample of young men (n = 507; age, ;19 years) from a longitudinal birth cohort and investigated whether testosterone exposure during adolescence (from 9 to 17 years of age) moderates the relation between current testosterone and brain response to faces in young adulthood, as assessed with functional magnetic resonance imaging (fMRI). Our results showed that the cumulative exposure to testosterone during adolescence moderated the relation between adult testosterone and both the mean fMRI response and functional connectivity (i.e., node strength). Specifically, in participants with low exposure to testosterone during puberty, we observed a positive relationship between current testosterone and the brain response to faces; this was not the case for participants with medium and high pubertal testosterone. Furthermore, we observed a stronger relationship between the brain response and current testosterone in parts of the angry-face network associated with (vs without) motion in the eye region of an observed (angry) face. We speculate that pubertal testosterone modulates the relationship between current testosterone and brain response to social cues carried by the eyes and signaling a potential threat.