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.

The Development of a Flexible Bodily Representation: Behavioral Outcomes and Brain Oscillatory Activity During the Rubber Hand Illusion in Preterm and Full-Term School-Age Children

“…In support of this, a recent study showed that lacking bodily contact in the first weeks of life due to prenatal birth affected mother-infant synchrony (Yaniv et al, 2021 ). However, if additional skin-to-skin mother-newborn contact was provided, an increased mother-child synchrony was observed across development impacting the brain’s capacity to empathize with others in adulthood (Yaniv et al, 2021 ). These findings support that early sensory experiences shape the representation of one’s own body as a point of reference for interactions with the external physical and social environment with cascading effects on socio-emotional and cognitive development.…”

“…Thus atypical body-related multisensory integration could affect the development of body ownership and the malleability of one's own bodily representation, impacting higher-order social and cognitive processes, including the understanding of others' actions and emotions (Ropar et al, 2018). In support of this, a recent study showed that lacking bodily contact in the first weeks of life due to prenatal birth affected mother-infant synchrony (Yaniv et al, 2021). However, if additional skin-to-skin mother-newborn contact was provided, an increased motherchild synchrony was observed across development impacting the brain's capacity to empathize with others in adulthood (Yaniv et al, 2021).…”

A Review on the Vagus Nerve and Autonomic Nervous System During Fetal Development: Searching for Critical Windows

“…At birth, the higher cortical networks controlling the ANS increase their connectivity (Schlatterer et al, 2021 ) and, in low-risk newborns at around 1 day of age, coherence between electrocortical activity and brainstem-mediated autonomic tone, especially parasympathetic, can be easily detected (Mulkey et al, 2021 ). Social interactions, including skin-to-skin contact between mother and newborns, help increase ANS maturation as well as stress responsivity and circadian rhythms, in particular in preterm infants (Ulmer Yaniv et al, 2021 ).…”

What Is Social about Autism? The Role of Allostasis-Driven Learning

“…These regions include the subcortical regions in the amygdala, nucleus accumbens (NAcc), and hypothalamus [56][57][58][59], and cortical regions in perception and action cortices [60], limbic cortices in the ventral anterior insula and cingulate cortex [61,62], and other association cortices in the ventromedial prefrontal cortex (vmPFC), ACC, and PCC [63,64]. Moreover, coordinated function and dopamine secretion within these regions is associated with improved social behavior in humans [65][66][67] and non-human mammals [68][69][70].…”