Attachment Stimuli Trigger Widespread Synchrony across Multiple Brains

Abstract

Infant stimuli elicit a widespread neural and behavioral response in human adults and such massive allocation of resources attests to the evolutionary significance of the primary attachment. Here, we examined whether attachment-related cues also trigger cross-brain concordance, generating greater neural uniformity among individuals. Post-partum mothers were imaged twice in oxytocin/placebo administration design and stimuli included four ecological videos; two of infant/mother alone (Alone) and two mother-infant dyadic contexts (Social). Theory-driven analysis measured cross-brain synchrony in preregistered nodes of the parental caregiving network (PCN), which integrates subcortical structures underpinning mammalian mothering with cortical areas implicated in simulation, mentalization, and emotion regulation, and data-driven analysis assessed brain-wide concordance using whole brain parcellation. Results demonstrated widespread cross-brain synchrony in both the PCN and across the neuroaxis, from primary sensory and somatosensory areas, through insular-cingulate regions, to temporal and prefrontal cortices. The Social context yielded significantly more cross-brain concordance, with PCN's striatum, parahipporcampal gyrus, superior temporal sulcus, anterior cingulate cortex (ACC), and prefrontal cortex displaying cross-brain synchrony only to mother-infant social cues. Moment-by-moment fluctuations in mother-infant social synchrony, ranging from episodes of gaze aversion to rhythmically-coordinated positive bouts, were tracked online by cross-brain concordance in the pre-registered ACC. Findings indicate that social attachment stimuli, representing evolutionary-salient universal cues that require no verbal narrative for immediate comprehension, trigger substantial inter-brain concordance and suggest that the mother-infant bond, an icon standing at the heart of human civilization, may function to glue brains into a unified experience and bind humans into social groups.

Oxytocin receptor function regulates neural signatures of pair bonding and fidelity in the nucleus accumbens

“…Alternatively, the distinct prosocial behavior displayed by stranger-preferring males may impact females' reciprocal social behavior in such a way that males prefer not to continue interacting when given a choice 20 . The predictive relationship between initial social interactions and the fidelity of future bonds in the absence of Oxtr suggests that Oxtr signaling functions to reinforce attachment between mates or even to override other pathways controlling social behaviors in animals with a lower propensity for pair bond formation [81][82][83] . By decorrelating variation in behavior and neural activity during initial social interactions between partners from the social and neural mechanisms that mediate pair bonding between them, Oxtr may have evolved to reduce promiscuity amongst male prairie voles, decrease sexual dimorphism in behavior, and reinforce behaviors that facilitate enduring attachments between mates.…”