Synchronous caregiving from birth to adulthood tunes humans' social brain

Adi Ulmer Yaniv, Roy Salomon, Shani Waidergoren, Ortal Shimon-Raz, Amir Djalovski, Ruth Feldman

Research output: Contribution to journalArticlepeer-review

47 Scopus citations

Abstract

Mammalian young are born with immature brain and rely on the mother's body and caregiving behavior for maturation of neurobiological systems that sustain adult sociality. While research in animal models indicated the long-term effects of maternal contact and caregiving on the adult brain, little is known about the effects of maternal-newborn contact and parenting behavior on social brain functioning in human adults. We followed human neonates, including premature infants who initially lacked or received maternal-newborn skin-to-skin contact and full-term controls, from birth to adulthood, repeatedly observing mother-child social synchrony at key developmental nodes. We tested the brain basis of affect-specific empathy in young adulthood and utilized multivariate techniques to distinguish brain regions sensitive to others' distinct emotions from those globally activated by the empathy task. The amygdala, insula, temporal pole (TP), and ventromedial prefrontal cortex (VMPFC) showed high sensitivity to others' distinct emotions. Provision of maternal-newborn contact enhanced social synchrony across development from infancy and up until adulthood. The experience of synchrony, in turn, predicted the brain's sensitivity to emotion-specific empathy in the amygdala and insula, core structures of the social brain. Social synchrony linked with greater empathic understanding in adolescence, which was longitudinally associated with higher neural sensitivity to emotion-specific empathy in TP and VMPFC. Findings demonstrate the centrality of synchronous caregiving, by which infants practice the detection and sharing of others' affective states, for tuning the human social brain, particularly in regions implicated in salience detection, interoception, and mentalization that underpin affect sharing and human attachment.

Original languageEnglish
Article numbere2012900118
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number14
DOIs
StatePublished - 6 Apr 2021

Bibliographical note

Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.

Funding

ACKNOWLEDGMENTS. We are grateful to the participants and their families for their kind cooperation across the years. R.F. is supported by the Simms/Mann Foundation and the Irving B. Harris Foundation. The initial study was supported by the Irving B. Harris Foundation and the Israel Science Foundation.

FundersFunder number
Irving B. Harris Foundation
Simms/Mann Foundation
Israel Science Foundation

    Keywords

    • Empathy
    • Longitudinal studies
    • Maternal touch
    • Social brain
    • Synchrony

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