Network integrity of the parental brain in infancy supports the development of children's social competencies

Abstract

The cross-generational transmission of mammalian sociality, initiated by the parent's postpartum brain plasticity and species-typical behavior that buttress offspring's socialization, has not been studied in humans. In this longitudinal study, we measured brain response of 45 primary-caregiving parents to their infant's stimuli, observed parent-infant interactions, and assayed parental oxytocin (OT). Intra- and inter-network connectivity were computed in three main networks of the human parental brain: core limbic, embodied simulation and mentalizing. During preschool, two key child social competencies were observed: emotion regulation and socialization. Parent's network integrity in infancy predicted preschoolers' social outcomes, with subcortical and cortical network integrity foreshadowing simple evolutionary-based regulatory tactics vs complex self-regulatory strategies and advanced socialization. Parent-infant synchrony mediated the links between connectivity of the parent's embodied simulation network and preschoolers' ability to use cognitive/executive emotion regulation strategies, highlighting the inherently dyadic nature of this network and its long-term effects on tuning young to social life. Parent's inter-network core limbic-embodied simulation connectivity predicted children's OT as moderated by parental OT. Findings challenge solipsistic neuroscience perspectives by demonstrating how the parent-offspring interface enables the brain of one human to profoundly impact long-term adaptation of another.

Keywords: embodied simulation; mentalizing; oxytocin; parent-infant synchrony; parental brain.

Fig. 1.

Location of ROIs comprising the core-limbic (red), embodied-simulation (green) and mentalizing (blue) networks, from coronal (A) and sagittal (B) views. dmPFC, dorsomedial prefrontal cortex; Ant. insula, anterior insula; IFG, inferior frontal gyrus; TP, temporal pole; NAcc, nucleus accumbens; GP, globuspallidus; STS, superior temporal sulcus; TPJ, temporoparietal junction; PAG, periaqueductal gray; vmPFC, ventromedial prefrontal cortex; ACC, anterior cingulated cortex. L, left; R, right. The bar graph (C) presents the three networks’ intra-NCI values (±SE; represented by error bars at top) activated by parents’ viewing of their interactions with infants at Time 1, for primary-caregiving mothers (PC-Mothers; n = 20, bright orange) and primary-caregiving fathers (PC-Fathers; n = 25, dark orange).

Fig. 2.

Relations between parent's intra-NCIs and child's emotion regulation, emotionality and social behaviors (Time 2). Proportion values (±SE; represented by error bars at the top) are presented for: child’s simple regulatory behaviors and positive emotionality during positive-emotion-eliciting paradigm and child’s social behavior during parent–child interaction (A); child’s complex regulatory behaviors and negative emotionality during negative-emotion-eliciting paradigm (B); and child’s self-regulatory socialization during socialization situation (C). n = 45. * P< 0.05.

Fig. 3.

Direct and indirect effects of parent’s-NCI on child’s outcomes (Time 2). Standardized regression coefficient for the relations between parent’s embodied-simulation-NCI and child’s complex self-regulation as partially mediated by parent-infant synchrony. Path c shows the standardized regression coefficient for the total (β) and direct (β') effects of embodied-simulation-NC Ion child's complex regulatory behavior (A). Moderation model of parental OT levels on core limbic and embodied simulation-Inter-NCI and child’s OT levels. Path b Model shows the standardized regression coefficient for the interaction (β) and direct (β') effects of core (there was no space) limbic-embodied simulation-Inter-NCI on child's OT levels. Examination of the interaction showed that under condition of high parental OT levels a significant positive correlation was found between parents’core limbic-embodied simulation-inter-NCI and child’s OT (solid line) and was not found under low parental OT levels (broken line). In addition, higher child’s OT levels were positively associated with more frequent child use of complex regulatory strategies. (B). *P< 0.05; **P< 0.01; ***P< 0.001.