The brain basis of social synchrony

Abstract

As a social species, humans evolved to detect information from the social behavior of others. Yet, the mechanisms used to evaluate social interactions, the brain networks implicated in such recognition, and whether individual differences in own social behavior determine response to similar behavior in others remain unknown. Here we examined social synchrony as a potentially important mechanism in the evaluation of social behavior and utilized the parenting context, an evolutionarily salient setting of significant consequences for infant survival, to test this issue. The brain response of healthy postpartum mothers to three mother-infant interaction vignettes was assessed. Videos included a typical synchronous interaction and two pathological interactions of mothers diagnosed with postpartum depression and anxiety that showed marked deviations from social synchrony. Mothers' own interactions with their 4- to 6-month-old infants were videotaped and micro-coded for synchrony. Results indicated that the recognition of social synchrony involved activations in the dorsal anterior cingulate cortex (dACC), fusiform, cuneus, inferior parietal lobule, supplementary motor area and NAcc. Mother's own synchrony with her infant correlated with her dACC response to synchrony in others. Findings are consistent with models suggesting that social action underpins social recognition and highlight social synchrony and the mother-infant bond as one prototypical context for studying the brain basis of social understanding.

Keywords: maternal anxiety; maternal depression; mothering; social brain; social synchrony.

Fig. 1

Experimental paradigm. Subjects were presented with three films each containing a 2-min mother–infant interaction as follows. (i) Interaction between a mother diagnosed with postpartum depression and her infant containing minimal maternal behavior and no social synchrony. (ii) Interaction between a healthy mother and her infant containing adequate amount of maternal behavior and social synchrony. (iii) Interaction between a mother diagnosed with generalized anxiety disorder and her infant containing minimal social synchrony. Clips were previewed by rest with fixation period of 1 min. A rest with fixation periods of 15–18 s was presented between films.

Fig. 2

Behavioral analysis of the three films presented to mothers as fMRI stimuli. (A) Parent gaze. The total proportion of time mother gazed at the infant’s face. (B) Infant’s social engagement. The total proportion of time infant gazed at mother’s face. (C) Synchrony. The total proportion of time mothers coordinated social gaze, positive vocalizations and affective touch with the infant’s social gaze and positive affect.

Fig. 3

Brain areas showing greater response to the synchronous compared to the depressed interaction. Fusiform (A), dACC (B) and NACC (C) showed greater activations when mothers observed the synchronous interaction (orange) compared to the depression interaction (green).

Fig. 4

Brain response in the overlap between the two contrasts of synchrony > depression and synchrony > anxiety. (A) dACC in the overlay of maps synchrony > depression and synchrony > anxiety. (B) Dorsal cingulate percentage signal change respond more during the synchrony interaction (in orange, levels of synchrony are demonstrated in (C). (D) Fusiform activation in the overlay of maps synchrony > depression and synchrony > anxiety. (E) Fusiform percentage signal change. The more maternal behavior is presented in the film (F), the stronger the percentage signal change, regardless of synchrony.

Fig. 5

dACC activation in the contrast synchronous interaction vs depression interaction is predicted by mothers’ behavioral synchrony scores. Pearson correlation between percentage signal change of the dACC in the contrast synchrony > depression interaction and the mothers’ synchrony scores (R_(Pearson) = −0.608, P = 0.001).