Mammalian young are born with immature brains and rely on the mother's body and caregiving behavior for maturation of neurobiological systems that sustain adult sociality. However, the parent-child precursors of humans' social brain are unknown. We followed human neonates, who received or were deprived of maternal bodily contact, to adulthood, repeatedly measuring mother-child interactive synchrony. We tested the neural basis of empathic accuracy in adulthood and utilized multivariate techniques to distinguish brain regions sensitive to others' distinct emotions from those globally activated by the vicarious stance. A network comprising the amygdala, insula, and temporal pole underpinned empathic accuracy, which was shaped by mother-child synchrony across development. Synchronous experiences with mother or father in infancy impacted adults' neural empathy, highlighting the benefits of humans' bi-parental rearing. Findings demonstrate the centrality of synchronous caregiving across development for tuning humans' social brain.
Introdunction:Being born a mammal implies that the brain is immature at birth and develops in the context of the mother's body and caregiving behavior. Infants rely on the provisions embedded in the mother's body, such as smell, touch, heat, or movements, and the expression of caregiving behavior for maturation of neurobiological systems that sustain participation in the 2 social world. For mammalian young, therefore, no factor is as critical to brain maturation as the dependence of the infant on its mother, and no feature of ontogeny is as consequential as proximity to mother's body and the experience of synchronous caregiving 1 . Extant research in animal models has shown that breeches in the mother's continuous presence and variability in caregiving behavior carry long-term effects on brain structure and function, particularly on systems that underpin sociality, and the effects are maintained throughout life, altering the adult animal's capacity to coordinate social bonds, manage hardships, and parent the next generation 2,3 . However, while the human brain is slowest to mature and requires the most extended period of dependence, the long-term consequences of parenting on the human social brain are unknown.To date, no study has followed infants from birth to adulthood to test whether variability in maternal contact and synchronous caregiving longitudinally impact social brain functioning in human adults.The human social brain integrates activity of subcortical, paralimbic, and cortical structures to sustain the multi-dimensional task of managing human social life, which requires rapid processing of social inputs, top-down interpretation of others' intent, and coordination of the two into social action in the present moment 4 . The social brain has undergone massive expansion across primate evolution to support humans' exquisite social skills, communicative competencies, and mindreading capacities and it is suggested that Homo sapiens' success over other hominin owes to their empathic abili...