Early life bonding in humans has critical long-term implications for health, productivity, and well-being in society. Nonetheless, neural mechanisms of bonding are typically studied in rodents, and no studies to date had examined the neurochemistry of human social affiliation. This study utilizes a state-of-the-art technology to demonstrate that human maternal bonding is associated with striatal dopamine function and the recruitment of a cortico–striatal–amygdala brain network that supports affiliation. The simultaneous probing of neurochemical responses and whole-brain network function in mothers watching their infants provides a unique observation into an “affiliating brain.” These results advance the mechanistic understanding of human social bonding and promote basic and clinical research in social neuroscience, development, and psychopathology.

Abstract

Research in humans and nonhuman animals indicates that social affiliation, and particularly maternal bonding, depends on reward circuitry. Although numerous mechanistic studies in rodents demonstrated that maternal bonding depends on striatal dopamine transmission, the neurochemistry supporting maternal behavior in humans has not been described so far. In this study, we tested the role of central dopamine in human bonding. We applied a combined functional MRI-PET scanner to simultaneously probe mothers’ dopamine responses to their infants and the connectivity between the nucleus accumbens (NAcc), the amygdala, and the medial prefrontal cortex (mPFC), which form an intrinsic network (referred to as the “medial amygdala network”) that supports social functioning. We also measured the mothers’ behavioral synchrony with their infants and plasma oxytocin. The results of this study suggest that synchronous maternal behavior is associated with increased dopamine responses to the mother’s infant and stronger intrinsic connectivity within the medial amygdala network. Moreover, stronger network connectivity is associated with increased dopamine responses within the network and decreased plasma oxytocin. Together, these data indicate that dopamine is involved in human bonding. Compared with other mammals, humans have an unusually complex social life. The complexity of human bonding cannot be fully captured in nonhuman animal models, particularly in pathological bonding, such as that in autistic spectrum disorder or postpartum depression. Thus, investigations of the neurochemistry of social bonding in humans, for which this study provides initial evidence, are warranted.