Distinct EEG amplitude suppression to facial gestures as evidence for a mirror mechanism in newborn monkeys

At birth, human infants and newborns of other primate species demonstrate the capacity to attend and to respond to facial stimuli provided by a caregiver. Newborn infants are also capable of exhibiting a range of facial expressions. Identification of the neural underpinnings of these capacities represents a formidable challenge in understanding social development. One possible neuronal substrate is the mirror-neuron system assumed to activate shared motor cortical representations for both observation and production of actions. We tested this hypothesis by recording scalp electroencephalogram (EEG) from 1–7 days old newborn rhesus macaques who were observing and producing facial gestures. We found that 5–6 Hz EEG activity was suppressed both when the infants produced facial gestures and while they were observing facial gestures of a human experimenter, but not when they were observing non-biological stimuli. These findings demonstrate the presence of neural reactivity for biological, communicatively-relevant stimuli which may be a likely signature of neuronal mirroring. The basic elements of the mirror-neuron system appear to operate from the very first days of life and contribute to the encoding of socially relevant stimuli

Early social experience affects neural activity to affiliative facial gestures in newborn nonhuman primates

A fundamental issue in cognitive neuroscience is how the brain encodes the actions and intentions of others. The discovery of an action-production-perception mechanism underpinning such a capacity advanced our knowledge of how these processes occur; however, no study has examined how the early postnatal environment may shape action-production-perception. Here, we examined the effects of social experience on action-production-perception in 3-day-old rhesus macaques that were raised either with or without their biological mothers. We measured the neonatal imitation skills and brain electrical activity responses, while infants produced and observed facial gestures. We hypothesized that early social experiences may shape brain activity, as assessed via electroencephalogram suppression in the α band (5-7 Hz in infants, known as the mu rhythm) during action observation, and lead to more proficient imitation skills. Consistent with this hypothesis, the infants reared by their mothers were more likely to imitate lipsmacking (LS) - a natural, affiliative gesture - and exhibited greater mu rhythm desynchronization while viewing LS gestures than the nursery-reared infants. These effects were not found in response to tongue protrusion, a meaningless gesture, or a nonsocial control. These data suggest that socially enriched early experiences in the first days after birth increase brain sensitivity to socially relevant actions

The functional architecture of mother-infant communication, and the development of infant social expressiveness in the first two months

By two-three months, infants show active social expressions during face-to-face interactions. These interactions are important, as they provide the foundation for later emotional regulation and cognition, but little is known about how infant social expressiveness develops. We considered two different accounts. One emphasizes the contingency of parental responsiveness, regardless of its form; the other, the functional architecture account, emphasizes the preparedness of both infants and parents to respond in specific ways to particular forms of behaviour in their partner. We videotaped mother-infant interactions from one to nine weeks, and analysed them with a micro-analytic coding scheme. Infant social expressiveness increased through the nine-week period, particularly after 3 weeks. This development was unrelated to the extent of maternal contingent responsiveness, even to infant social expressions. By contrast, specific forms of response that mothers used preferentially for infant social expressions - mirroring, marking with a smile- predicted the increase in these infant behaviours over time. These results support a functional architecture account of the perceptual and behavioural predispositions of infants and parents that allows young infants to capitalize on relatively limited exposure to specific parental behaviours, in order to develop important social capacities

Early maternal mirroring predicts infant motor system activation during facial expression observation.

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