Sensitive infant care tunes a frontotemporal interbrain network in adolescence

Abstract

Caregiving plays a critical role in children's cognitive, emotional, and psychological well-being. In the current longitudinal study, we investigated the enduring effects of early maternal behavior on processes of interbrain synchrony in adolescence. Mother-infant naturalistic interactions were filmed when infants were 3-4 months old and interactions were coded for maternal sensitivity and intrusiveness with the Coding Interactive Behavior Manual. In early adolescence (Mean = 12.30, SD = 1.25), mother-adolescent interbrain synchrony was measured using hyperscanning EEG during a naturalistic interaction of positive valence. Guided by previous hyperscanning studies, we focused on interbrain connections within the right frontotemporal interbrain network. Results indicate that maternal sensitivity in early infancy was longitudinally associated with neural synchrony in the right interbrain frontotemporal network. Post-hoc comparisons highlighted enhancement of mother-adolescent frontal-frontal connectivity, a connection that has been implicated in parent-child social communication. In contrast, maternal intrusiveness in infancy was linked with attenuation of interbrain synchrony in the right interbrain frontotemporal network. Sensitivity and intrusiveness are key maternal social orientations that have shown to be individually stable in the mother-child relationship from infancy to adulthood and foreshadow children's positive and negative social-emotional outcomes, respectively. Our findings are the first to demonstrate that these two maternal orientations play a role in enhancing or attenuating the child's interbrain frontotemporal network, which sustains social communication and affiliation. Results suggest that the reported long-term impact of maternal sensitivity and intrusiveness may relate, in part, to its effects on tuning the child's brain to sociality.

Keywords: EEG; Hyperscanning; Maternal sensitivity; Mother-child relationships; Social development; Social neuroscience; Synchrony.

Fig. 1

Procedure and experimental design.

Fig. 2

Visualization of validation analysis conducted on face-to-face relative to control (surrogate data): Higher interbrain synchrony was detected during the face-to-face interactions relative to control (surrogate data). (A) Visualization of the surrogate data (left) compared to the real connectivity values (right). Each node represents a different ROI in the mother and child brains. RT – right temporal, LT – left temporal, RC – right central, LC - left central, RF – right frontal, LF - left frontal. M and C refer to the mother and child, respectively. Darker shades represent greater values of interbrain connectivity (wPLI scores). (B) Visualization of the significant links found in the face-to-face interaction relative to control. A permutation test based on repeated-measures ANOVA revealed a significant advantage for the face-to-face interaction compared to the control condition in facilitating interbrain synchrony in the frontotemporal network (p < 0.001). Further analysis revealed this effect was evident in every possible link between the mother and child frontotemporal network. (C) Visualization of interbrain increase in the face-to-face interaction compared to control, with each dot representing a dyad. Both the overall interbrain across the entire frontotemporal network and the right hemisphere network showed increased synchrony relative to control (p < 0.001).

Fig. 3

Visualization of brain-behavior correlations with the improvement in interbrain synchrony during the face-to-face interaction. The improvement in interbrain synchrony in the face-to-face interaction relative to control (calculated as Δ wPLI) is shown on the Y-axis. (A) Improvement in interbrain synchrony in the right hemisphere network is correlated positively with maternal sensitivity (r = 0.41, p = 0.026), and negatively with maternal intrusiveness (r = -0.37 p = 0.049). (B) The improvement in interbrain synchrony in the mother-left-frontal child-right-temporal is correlated positively with maternal sensitivity (r = 0.42 p = 0.022), and negatively with maternal intrusiveness (r = -0.49 p = 0.007).