Attachment Reminders Trigger Widespread Synchrony across Multiple Brains

• Published in: The Journal of neuroscience 2023-10, Vol.43 (43), p.7213-7225
• Main Authors: Shimon-Raz, Ortal, Yeshurun, Yaara, Ulmer-Yaniv, Adi, Levinkron, Ayelet, Salomon, Roy, Feldman, Ruth
• Format: Article
• Language: English
• Subjects: Attachment; Brain; Cortex (somatosensory); Cues; Infants; Neostriatum; Oxytocin; Parahippocampal gyrus; Resource allocation; Social interactions; Stimuli; Superior temporal sulcus
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.0026-23.2023

Infant stimuli elicit 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 reminders also trigger cross-brain concordance and generate greater neural uniformity, as indicated by intersubject correlation. Human mothers were imaged twice in oxytocin/placebo administration design, and stimuli included four ecological videos of a standard unfamiliar mother and infant: two 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/somatosensory areas, through insular-cingulate regions, to temporal and prefrontal cortices. The Social context yielded significantly more cross-brain concordance, with PCNs striatum, parahippocampal gyrus, superior temporal sulcus, ACC, and PFC displaying cross-brain synchrony only to mother–infant social cues. Moment-by-moment fluctuations in mother–infant social synchrony, ranging from episodes of low synchrony to tightly coordinated positive bouts, were tracked online by cross-brain concordance in the preregistered ACC. Findings indicate that social attachment stimuli, representing evolutionary-salient universal cues that require no verbal narrative, trigger substantial interbrain 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. SIGNIFICANCE STATEMENT Infant stimuli elicit widespread neural response in human adults, attesting to their evolutionary significance, but do they also trigger cross-brain concordance and induce neural uniformity among perceivers? We measured cross-brain synchrony to ecological mother–infant videos. We used theory-driven analysis, measuring cross-brain concordance in the parenting network, and data-driven analysis, assessing brain-wide concordance using whole-brain parcellation. Attachment cues triggered widespread cro