Affect-biased attention may play a fundamental role in early socioemotional development, but factors influencing its emergence and associations with typical versus pathological outcomes remain unclear. Here, we adopted a nonhuman primate model of early social adversity (ESA) to: (1) establish whether juvenile, pre-adolescent macaques demonstrate attention biases to both threatening and reward-related dynamic facial gestures; (2) examine the effects of early social experience on such biases; and (3) investigate how this relation may be linked to socioemotional behaviour. Two groups of juvenile macaques (ESA exposed and non-ESA exposed) were presented with pairs of dynamic facial gestures comprising two conditions: neutral-threat and neutral-lipsmacking. Attention biases to threat and lipsmacking were calculated as the proportion of gaze to the affective versus neutral gesture. Measures of anxiety and social engagement were also acquired from videos of the subjects in their everyday social environment. Results revealed that while both groups demonstrated an attention bias towards threatening facial gestures, a greater bias linked to anxiety was demonstrated by the ESA group only. Only the non-ESA group demonstrated a significant attention bias towards lipsmacking, and the degree of this positive bias was related to duration and frequency of social engagement in this group. These findings offer important insights into the effects of early social experience on affect-biased attention and related socioemotional behaviour in nonhuman primates, and demonstrate the utility of this model for future investigations into the neural and learning mechanisms underlying this relationship across development.

Processing facial expressions is an essential component of social interaction, especially for preverbal infants. In human adults and monkeys, this process involves the motor system, with a neural matching mechanism believed to couple self- and other-generated facial gestures. Here, we used electroencephalography to demonstrate recruitment of the human motor system during observation and execution of facial expressions in nine-month-old infants, implicating this system in facial expression processing from a very young age. Notably, examination of early video-recorded mother-infant interactions supported the common, but as yet untested, hypothesis that maternal mirroring of infant facial gestures is central to the development of a neural matching mechanism for these gestures. Specifically, the extent to which mothers mirrored infant facial expressions at two months postpartum predicted infant motor system activity during observation of the same expressions at nine months. This suggests that maternal mirroring strengthens mappings between visual and motor representations of facial gestures, which increases infant neural sensitivity to particularly relevant cues in the early social environment.

Simulation theories propose that observing another’s facial expression activates sensorimotor representations involved in the execution of that expression, facilitating recognition processes. The mirror neuron system (MNS) is a potential mechanism underlying simulation of facial expressions, with like neural processes activated both during observation and performance. Research with monkeys and adult humans supports this proposal, but so far there have been no investigations of facial MNS activity early in human development. The current study used electroencephalography (EEG) to explore mu rhythm desynchronization, an index of MNS activity, in 30-month-old children as they observed videos of dynamic emotional and non-emotional facial expressions, as well as scrambled versions of the same videos. We found significant mu desynchronization in central regions during observation and execution of both emotional and non-emotional facial expressions, which was right-lateralized for emotional and bilateral for non-emotional expressions during observation. These findings support previous research suggesting movement simulation during observation of facial expressions, and are the first to provide evidence for sensorimotor activation during observation of facial expressions, consistent with a functioning facial MNS at an early stage of human development.