Dopamine in the medial amygdala network mediates human bonding

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.arly social bonding with a primary caregiver is necessary for mental and physical health, whereas the absence of such bonding is a clear risk factor for adult illness (1). However, despite potentially enormous implications, to date the science of mother-infant bonding relies mostly on nonhuman animal models.Research on nonhuman animals indicates that maternal bonding involves the nucleus accumbens (NAcc), amygdala, and medial prefrontal cortex (mPFC). In rodents, oxytocin and dopamine act in the amygdala and NAcc (2) to regulate maternal appetitive behaviors. In humans, functional MRI (fMRI) studies have verified that NAcc activity increases consistently when mothers gaze at their infants (3). Moreover, the NAcc and amygdala activity have been linked to the quality of maternal behavior (4). Mothers who were sensitive to their infants' cues for social engagement and who adjusted their own behavior to meet those needs (referred to as "mother-infant synchrony"), showed greater activations in the left NAcc and lower activation in the right amygdala when viewing films of their infants than did nonsynchronous mothers (4). In agreement with the animal studies, oxytocin has been implicated in human maternal behavior, so that synchronous mothers show a stronger link between levels of circulating plasma oxytocin and NAcc fMRI activations when viewing films of their in...

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