Synchronous caregiving from birth to adulthood tunes humans' social brain

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.

Keywords: empathy; longitudinal studies; maternal touch; social brain; synchrony.

Fig. 1.

Birth-to-adulthood longitudinal study design and fMRI paradigm. (A) Three cohorts of infants and parents recruited at birth: full-term (FT) infants and two case-matched neurologically intact premature infants assigned to either Kangaroo Care (KC: infants receiving skin-to-skin contact with mother) or matched controls receiving standard incubator care (SC). Mother–child social synchrony was assessed at 4 mo (SD =1.14), 3 y (SD = 1.38), 12 y (SD = 1.62), and 20 y (SD = 2.01). (B) fMRI empathy paradigm. Example illustrates a pseudorandomized design in which participants were presented with an emotional probe followed by four photos depicting this probe. Participants were asked to empathize with the protagonists, and five blocks per condition were presented.

Fig. 2.

Mother–child synchrony from infancy to adulthood. Individual scores are marked by dots of respective color. Group means are marked by a black circle.

Fig. 3.

Whole-brain maps of affect-specific empathy. (A) Experiment 1: 18 subjects (six from each group, FT, KC, and SC) were randomly chosen for functional localizer. Presented contrast: emotion > scrambled image. Group means were used for ROI definition. (B) Experiment 2: Similar contrast presented for the analysis dataset (n = 78). Note resemblance of activation patterns across samples. All maps are false discovery rate corrected at q < 0.05. Note: Images present left hemisphere. For right hemisphere, see SI Appendix, Fig. S1.

Fig. 4.

RSA across ROIs: Representational similarity was measured subject-by-subject by calculating correlation distance (1 minus Pearson correlation between two vectors of beta values of emotional pair) resulting in three dissimilarity pairs: (A) joy/distress, (B) joy/sadness, (C) and distress/sadness (D) mean dissimilarity levels across all emotional pairs A–C for each ROI. Colored dots show mean dissimilarity levels for each ROI; error bars represent 95% CIs, and gray marks are the noise ceiling bounds. A similar pattern of dissimilarity is observed across emotional pairs. TP and amygdala show highest levels of dissimilarity. (E) Actual ROIs, superimposed on an inflated brain. Color marks the dissimilarity levels according to the color code of A–D.

Fig. 5.

Linear regression between synchrony from infancy to young adulthood and dissimilarity. Regression and correlation values between mean synchrony and mean dissimilarity values in Amygdala (A) and Insula (B). Higher mean synchrony values were related to higher levels of neural dissimilarity.