title: 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.
authors.affiliation: Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129.
authors.forename: Shir
authors.identifier: 0000-0002-4074-6777
authors.initials: S
authors.lastname: Atzil
authors.affiliation: Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129.
authors.forename: Alexandra
authors.initials: A
authors.lastname: Touroutoglou
authors.affiliation: Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129.|Department of Psychology, Northeastern University, Boston, MA 02115.
authors.forename: Tali
authors.initials: T
authors.lastname: Rudy
authors.affiliation: Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129.
authors.forename: Stephanie
authors.initials: S
authors.lastname: Salcedo
authors.affiliation: Yale Child Study Center, New Haven, CT 06520.|Gonda Brain Research, Bar Ilan University, Ramat Gan 5290002, Israel.
authors.forename: Ruth
authors.initials: R
authors.lastname: Feldman
authors.affiliation: Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129.
authors.forename: Jacob M
authors.initials: JM
authors.lastname: Hooker
authors.affiliation: Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129.|Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114.
authors.forename: Bradford C
authors.initials: BC
authors.lastname: Dickerson
authors.affiliation: Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129.
authors.forename: Ciprian
authors.initials: C
authors.lastname: Catana
authors.affiliation: Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129; l.barrett@neu.edu.|Department of Psychology, Northeastern University, Boston, MA 02115.
authors.forename: Lisa Feldman
authors.initials: LF
authors.lastname: Barrett
mesh_terms: D000328:Adult; D002247:Carbon Isotopes; D063132:Connectome / Q000379:methods; D066276:Corticomedial Nuclear Complex / Q000502:physiology*; D004298:Dopamine / Q000378:metabolism*; D005260:Female; D006801:Humans; D007223:Infant; D008279:Magnetic Resonance Imaging; D008297:Male; D009034:Mother-Child Relations / Q000523:psychology*; D009714:Nucleus Accumbens / Q000502:physiology*; D009769:Object Attachment; D010121:Oxytocin / Q000097:blood; D017397:Prefrontal Cortex / Q000502:physiology*; D020891:Raclopride / Q000008:administration & dosage / Q000493:pharmacokinetics; D017448:Receptors, Dopamine D2 / Q000378:metabolism; D012201:Reward
chemical_list: D002247:Carbon Isotopes; D017448:Receptors, Dopamine D2; D020891:Raclopride; D010121:Oxytocin; D004298:Dopamine
keywords: dopamine; humans; maternal behavior; network connectivity; social affiliation