Mammalian young are born with immature brain and rely on the mother’s body and caregiving behavior for maturation of neurobiological systems that sustain adult sociality. While research in animal models indicated the long-term effects of maternal contact and caregiving on the adult brain, little is known about the effects of maternal–newborn contact and parenting behavior on social brain functioning in human adults. We followed human neonates, including premature infants who initially lacked or received maternal–newborn skin-to-skin contact and full-term controls, from birth to adulthood, repeatedly observing mother–child social synchrony at key developmental nodes. We tested the brain basis of affect-specific empathy in young adulthood and utilized multivariate techniques to distinguish brain regions sensitive to others’ distinct emotions from those globally activated by the empathy task. The amygdala, insula, temporal pole (TP), and ventromedial prefrontal cortex (VMPFC) showed high sensitivity to others’ distinct emotions. Provision of maternal–newborn contact enhanced social synchrony across development from infancy and up until adulthood. The experience of synchrony, in turn, predicted the brain’s sensitivity to emotion-specific empathy in the amygdala and insula, core structures of the social brain. Social synchrony linked with greater empathic understanding in adolescence, which was longitudinally associated with higher neural sensitivity to emotion-specific empathy in TP and VMPFC. Findings demonstrate the centrality of synchronous caregiving, by which infants practice the detection and sharing of others’ affective states, for tuning the human social brain, particularly in regions implicated in salience detection, interoception, and mentalization that underpin affect sharing and human attachment.

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...

Reorganization of the maternal brain upon childbirth triggers species-typical maternal social behavior. These brief social moments carry profound effects on the infant's brain and likely have distinct signature in the maternal brain. Utilizing a double-blind, within-subject oxytocin/placebo administration crossover design, mothers' brain was imaged twice using fMRI while observing three naturalistic maternal-infant contexts in the home ecology; 'unavailable', 'unresponsive', and 'social', when mothers engaged in synchronous peek-a-boo play. The social condition elicited greater neural response across the human caregiving network, including amygdala, VTA, hippocampus, insula, ACC, and temporal cortex. Oxytocin impacted neural response primarily to the social condition and attenuated differences between social and non-social stimuli. Greater temporal consistency emerged in the 'social' condition across the two imaging sessions, particularly in insula, amygdala, and TP. Findings describe how mother's brain varies by caregiving experiences and gives salience to moments of social synchrony that support infant social development and brain maturation.