Neural and behavioral responses to fearful faces in men transitioning to first-time fatherhood

Fearful facial expressions signal vulnerability and may be especially salient in caregiving contexts. Like women, men undergo neurobiological transformation as they become parents, but no study has focused on how expectant and new fathers process fearful faces. To fill this gap, we administered a behavioral and fMRI emotion perception task to characterize fear responses in men transitioning to fatherhood. First-time fathers completed a forced-choice behavioral emotion recognition task and an fMRI emotion perception task before (n = 38, M_age = 32.33 years) and after (n = 34, M_age = 33.25 years) their child's birth. We examined behavioral fear recognition and neural responses to fearful adult faces prenatally and ~8 months postpartum. Additionally, we examined whether fathers' fear recognition and postpartum bonding difficulties were associated with neural response. Before their child's birth, fathers showed heightened neural activation to fearful expressions (versus rest) in the inferior frontal gyrus, anterior cingulate, insula, amygdala, periaqueductal gray, pre and postcentral gyri, fusiform gyrus, and visual cortex. Fathers who exhibited stronger periaqueductal gray activation towards fearful faces also showed more accurate fear recognition. After their child's birth, fathers responded to fearful faces in many of the same regions, but also showed activation in the dorsal striatum. Higher dorsal striatum activation was associated with fewer father-infant bonding problems. A longitudinal region-of-interest analysis revealed a trend towards increased nucleus accumbens activation to fearful expressions from prenatal to postpartum. An exploratory whole-brain analysis also found that responses to fearful faces increased in the angular gyrus and decreased in the secondary visual cortex over the transition to fatherhood. Consistent with theory proposing caregivers must be willing to approach others in distress, our findings suggest that first-time fathers recruit reward regions in addition to canonical fear processing regions after their child's birth, and that striatal responding to fearful faces is linked with father-child bonding. This is the first longitudinal study to examine fear processing across the transition to fatherhood and provides insight into how men adapt to the fatherhood role.