Mother-Infant Brain-to-Brain Synchrony Patterns Reflect Caregiving Profiles

Abstract

Biobehavioral synchrony, the coordination of physiological and behavioral signals between mother and infant during social contact, tunes the child's brain to the social world. Probing this mechanism from a two-brain perspective, we examine the associations between patterns of mother-infant inter-brain synchrony and the two well-studied maternal behavioral orientations-sensitivity and intrusiveness-which have repeatedly been shown to predict positive and negative socio-emotional outcomes, respectively. Using dual-electroencephalogram (EEG) recordings, we measure inter-brain connectivity between 60 mothers and their 5- to 12-month-old infants during face-to-face interaction. Thirty inter-brain connections show significantly higher correlations during the real mother-infant face-to-face interaction compared to surrogate data. Brain-behavior correlations indicate that higher maternal sensitivity linked with greater mother-infant neural synchrony, whereas higher maternal intrusiveness is associated with lower inter-brain coordination. Post hoc analysis reveals that the mother-right-frontal-infant-left-temporal connection is particularly sensitive to the mother's sensitive style, while the mother-left-frontal-infant-right-temporal connection indexes the intrusive style. Our results support the perspective that inter-brain synchrony is a mechanism by which mature brains externally regulate immature brains to social living and suggest that one pathway by which sensitivity and intrusiveness exert their long-term effect may relate to the provision of coordinated inputs to the social brain during its sensitive period of maturation.

Keywords: hyperscanning; inter-brain synchrony; intrusiveness; maternal sensitivity; social brain; social neuroscience.

Figure 1

Difference in connectivity values for all electrode combinations between the real face-to-face data and the surrogate data. (A) Infant–mother paradigm. Infant and mother were fitted with EEG electrodes and participated in a face-to-face (F2F) free interaction paradigm. (B) Illustration of infant–mother inter-brain neural synchrony. Electrodes recorded and analyzed are marked in bold dots; inter-brain neural synchrony values were calculated for theta frequency band (4 to 7 Hz) using weighted phase lag index (wPLI). Connectivity scores were computed for all inter-subject electrode combinations, resulting in 64 wPLI values per dyad. The lines between mother’s (left) and infant’s (right) electrodes reflect the significant inter-brain connections compared with surrogate data. The width of the lines reflects the number of significant connections each electrode is involved with. (C) The x axis represents the infant electrodes, and the y axis the mother electrodes. The color legend represents the difference between the real and the surrogate connectivity scores, such that dark red–colored squares represent comparisons with higher connectivity in the real F2F condition compared with the surrogate data. Nonparametric Mann–Whitney test followed by FDR correction for multiple comparisons revealed real significant neural connectivity during infant–mother face-to-face interaction. The significant comparisons following correction are marked with asterisks.

Figure 2

Visualization of brain–behavior correlations. Visualization of the CIB codes of maternal sensitivity and maternal intrusiveness correlations with wPLI values of frontal–temporal inter-brain neural synchrony and frontal–right temporal inter-brain neural synchrony. Mother-frontal–infant-temporal neural synchrony scores correlated with both (A) maternal sensitivity scores (N = 53, r = 0.31, p = 0.023) and (B) maternal intrusiveness scores (N = 53, r = −0.28, p = 0.041). (C) Mother-frontal–infant-right-temporal neural synchrony scores correlation with maternal sensitivity scores (N = 53, r = 0.34, p = 0.013), and (D) mother-left-frontal–infant-right-temporal neural synchrony scores correlation with maternal intrusiveness scores (N = 53, r = −0.39, p = 0.004).