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Attachment Reminders Trigger Widespread Synchrony across Multiple Brains

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 neura...

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Autores principales: Shimon-Raz, Ortal, Yeshurun, Yaara, Ulmer-Yaniv, Adi, Levinkron, Ayelet, Salomon, Roy, Feldman, Ruth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10601370/
https://www.ncbi.nlm.nih.gov/pubmed/37813569
http://dx.doi.org/10.1523/JNEUROSCI.0026-23.2023
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author Shimon-Raz, Ortal
Yeshurun, Yaara
Ulmer-Yaniv, Adi
Levinkron, Ayelet
Salomon, Roy
Feldman, Ruth
author_facet Shimon-Raz, Ortal
Yeshurun, Yaara
Ulmer-Yaniv, Adi
Levinkron, Ayelet
Salomon, Roy
Feldman, Ruth
author_sort Shimon-Raz, Ortal
collection PubMed
description 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 cross-brain concordance in both the parenting network and across the neuroaxis. Moment-by-moment fluctuations in behavioral synchrony were tracked online by cross-brain variability in ACC. Attachment reminders bind humans' brains into a unitary experience and stimuli characterized by social synchrony enhance neural similarity among participants, describing one mechanism by which attachment bonds provide the neural template for the consolidation of social groups.
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spelling pubmed-106013702023-10-27 Attachment Reminders Trigger Widespread Synchrony across Multiple Brains Shimon-Raz, Ortal Yeshurun, Yaara Ulmer-Yaniv, Adi Levinkron, Ayelet Salomon, Roy Feldman, Ruth J Neurosci Research Articles 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 cross-brain concordance in both the parenting network and across the neuroaxis. Moment-by-moment fluctuations in behavioral synchrony were tracked online by cross-brain variability in ACC. Attachment reminders bind humans' brains into a unitary experience and stimuli characterized by social synchrony enhance neural similarity among participants, describing one mechanism by which attachment bonds provide the neural template for the consolidation of social groups. Society for Neuroscience 2023-10-25 /pmc/articles/PMC10601370/ /pubmed/37813569 http://dx.doi.org/10.1523/JNEUROSCI.0026-23.2023 Text en Copyright © 2023 Shimon-Raz et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Shimon-Raz, Ortal
Yeshurun, Yaara
Ulmer-Yaniv, Adi
Levinkron, Ayelet
Salomon, Roy
Feldman, Ruth
Attachment Reminders Trigger Widespread Synchrony across Multiple Brains
title Attachment Reminders Trigger Widespread Synchrony across Multiple Brains
title_full Attachment Reminders Trigger Widespread Synchrony across Multiple Brains
title_fullStr Attachment Reminders Trigger Widespread Synchrony across Multiple Brains
title_full_unstemmed Attachment Reminders Trigger Widespread Synchrony across Multiple Brains
title_short Attachment Reminders Trigger Widespread Synchrony across Multiple Brains
title_sort attachment reminders trigger widespread synchrony across multiple brains
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10601370/
https://www.ncbi.nlm.nih.gov/pubmed/37813569
http://dx.doi.org/10.1523/JNEUROSCI.0026-23.2023
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