The neural development of empathy is sensitive to caregiving and early trauma

Abstract

Empathy is a core human social ability shaped by biological dispositions and caregiving experiences; yet the mechanisms sustaining maturation of the neural basis of empathy are unknown. Here, we followed eighty-four children, including 42 exposed to chronic war-related adversity, across the first decade of life, and assessed parenting, child temperament, and anxiety disorders as contributors to the neural development of empathy. At preadolescence, participants underwent magenetoencephalography while observing others' distress. Preadolescents show a widely-distributed response in structures implicating the overlap of affective (automatic) and cognitive (higher-order) empathy, which is predicted by mother-child synchrony across childhood. Only temperamentally reactive young children growing in chronic adversity, particularly those who later develop anxiety disorders, display additional engagement of neural nodes possibly reflecting hyper-mentalizing and ruminations over the distressing stimuli. These findings demonstrate how caregiving patterns fostering interpersonal resonance, reactive temperament, and chronic adversity combine across early development to shape the human empathic brain.

Fig. 1

Longitudinal study timeline. In T1, at early childhood, child and mother interacted with each other; mother–child synchrony was calculated. In T3*, Psychiatric diagnosis was conducted and child and mother interacted again and the synchrony construct was again computed; hence Maternal Synchrony scores leaned on the T1 and T3 interactions. In T4, neural empathic response to vicarious distress was evaluated using MEG neuroimaging. Illustration of empathy networks is inspired by the comprehensive review of de Waal and Preston. *The Synchrony illustration is adapted and reproduced by permission of Oxford University Press. ^© The Author 2017. All rights reserved. For permissions, please email journals.permissions@oup.com. This figure is not included under the open access license of this publication. The original figure is Fig. 1a—Jonathan Levy, Abraham Goldstein, Ruth Feldman, Perception of social synchrony induces mother–child gamma coupling in the social brain. Soc. Cogn. Affect. Neurosci. 2017; 12 (7): 1036–1046

Fig. 2

Neural empathic response. Preadolescents activated the SMA/MCC (right upper panel) in response to vicarious distress (masked for P_cluster-cor < 0.05), and the color bar represents masked significant t values. This activation was expressed as late alpha-band enhancement (left upper panel). The red blob represents the significant time-frequency window (P_cluster-cor < 0.05), and the color bar conveys the t values. This neural effect of empathy was not significantly different between the two groups (left lower panel), yet mother–child synchrony in early and late childhood mediated (**P_FDR-cor < 0.05) the effects of trauma exposure on this neural effect (right lower panel). In the chart bars, points are laid over a SEM (95% confidence interval)

Fig. 3

Characterizing the Putative Mentalizing activity. a ELS preadolescents activated the putative mentalizing network in T4 significantly stronger than controls did (masked for P_cluster-cor < 0.05), and the color bar conveys masked t values. b Power averages over the network nodes were significantly different between the two groups, particularly those with high negative reactivity in T1. c Individuals with high negative reactivity in T1 developed more internalizing disorders in T3. d Internalizing disorders in T3 explained that mentalizing neural activity, in T4. In the chart bars, points are laid over a SEM (95% confidence interval), and asterisks convey statistically significant effects