Delayed Imitation of Lipsmacking Gestures by Infant Rhesus Macaques (Macaca mulatta)

Human infants are capable of accurately matching facial gestures of an experimenter within a few hours after birth, a phenomenon called neonatal imitation. Recent studies have suggested that rather than being a simple reflexive-like behavior, infants exert active control over imitative responses and ‘provoke’ previously imitated gestures even after a delay of up to 24 h. Delayed imitation is regarded as the hallmark of a sophisticated capacity to control and flexibly engage in affective communication and has been described as an indicator of innate protoconversational readiness. However, we are not the only primates to exhibit neonatal imitation, and delayed imitation abilities may not be uniquely human. Here we report that 1-week-old infant rhesus macaques (Macaca mulatta) who show immediate imitation of a lipsmacking gesture also show delayed imitation of lipsmacking, facilitated by a tendency to refrain from lipsmacking toward a still face during baseline measurements. Individual differences in delayed imitation suggest that differentially matured cortical mechanisms may be involved, allowing some newborns macaques to actively participate in communicative exchanges from birth. Macaque infants are endowed with basic social competencies of intersubjective communication that indicate cognitive and emotional commonality between humans and macaques, which may have evolved to nurture an affective mother-infant relationship in primates

Neonatal imitation and its sensorimotor mechanism

In the present chapter, we propose that aspects of early social development—sensorimotor matching skills, social motivation, and temperament—may explain variability in neonatal imitation. We suggest that the presence of an action-perception mechanism at birth can be better understood by taking into account the complex interactions occurring during development between infants' social competences, in part a cause and consequence of their sensorimotor skills, and the effects of different experiences and environmental inputs on individual differences already present from birth (e.g., social interest temperament). We also present some findings and propose future directions aimed at testing these possibilities by examining individual differences related to imitative skill

Neonatal imitation predicts how infants engage with faces

In human infants, neonatal imitation and preferences for eyes are both associated with later social and communicative skills, yet the relationship between these abilities remains unexplored. Here we investigated whether neonatal imitation predicts facial viewing patterns in infant rhesus macaques. We first assessed infant macaques for lipsmacking (a core affiliative gesture) and tongue protrusion imitation in the first week of life. When infants were 10–28 days old, we presented them with an animated macaque avatar displaying a still face followed by lipsmacking or tongue protrusion movements. Using eye tracking technology, we found that macaque infants generally looked equally at the eyes and mouth during gesture presentation, but only lipsmacking-imitators showed significantly more looking at the eyes of the neutral still face. These results suggest that neonatal imitation performance may be an early measure of social attention biases and might potentially facilitate the identification of infants at risk for atypical social development

A modified mark test for own-body recognition in pig-tailed macaques (Macaca nemestrina)

Classic mirror self-recognition mark tests involve familiarizing the subject with its mirror image, surreptitiously applying a mark on the subject’s eyebrow, nose, or ear, and measuring self-directed behaviors towards the mark. For many non-human primate species, however, direct gaze at the face constitutes an aggressive and threatening signal. It is therefore possible that monkeys fail the mark test because they do not closely inspect their faces in a mirror and hence they have no expectations about their physical appearance. In the current study we prevented 2 pig-tailed macaques (Macaca nemestrina) from seeing their own faces in a mirror and we adopted a modified version of the classic mark test in which monkeys were marked on the chest, a body region to which they normally have direct visual access but that in the current study was visible only via a mirror. Neither monkey tried to touch the mark on its chest, possibly due to a failure to understand the mirror as a reflective surface. To further the monkeys’ understanding of the mirror image, we trained them to reach for food using the mirror as the only source of information. After both monkeys had learned mirror-mediated reaching, we replicated the mark test. In this latter phase of the study, only 1 monkey scratched the red dye on the chest once. The results are consistent with other findings suggesting that monkeys are not capable of passing a mark test, and imply that face and body recognition rely on the same cognitive abilities

Visual preferences for direct-gaze faces in infant macaques (Macaca mulatta ) with limited face exposure

From birth, human and nonhuman primates attend more to faces with direct gaze compared with averted gaze, and previous studies report that attention to the eyes is linked to the emergence of later social skills. Here, we explored whether early experiences influence attraction to eye contact in infant macaques by examining their attention to face pairs varying in their gaze direction across the first 13 weeks of life. Infants raised by human caretakers had limited conspecific interactions (nursery‐reared; N = 16) and were compared to infants raised in rich social environments (mother‐reared; N = 20). Both groups looked longer to faces and the eyes of direct compared to averted‐gaze faces. Looking to all faces and eyes also increased with age. Nursery‐reared infants did not display age‐associated increases in attention to direct‐gaze faces specifically, suggesting that, while there may be an initial preference for direct‐gaze faces from birth, social experiences may support its early development

Lipsmacking imitation skill in newborn macaques is predictive of social partner discrimination

Newborn rhesus macaques imitate facial gestures even after a delay, revealing the flexible nature of their early communicative exchanges. In the present study we examined whether newborn macaques are also sensitive to the identities of the social partners with whom they are interacting. We measured infant monkeys’ (n = 90) lipsmacking and tongue protrusion gestures in a face-to-face interaction task with a human experimenter in the first week of life. After a one minute delay, the same person who previously presented gestures or a different person returned and presented a still face to infants. We had two primary predictions: (1) infants would demonstrate higher rates of overall gesturing, and especially lipsmacking—an affiliative gesture—to a familiar person, compared to a novel person, and (2) infants’ imitative skills would positively correlate with gestures to familiar, but not unfamiliar, social partners, as both abilities may reflect a strong general social interest. We found that overall infants did not produce more gestures or more lipsmacking when approached by a familiar person compared to a novel person; however, we did find individual differences in infants’ social responsiveness: lipsmacking imitation was positively correlated with lipsmacking during the return period when the person was the same (p = .025), but not when the person was novel (p = .44). These findings are consistent with the notion that imitative skill is reflective of infants’ more general interest in social interactions

Neonatal imitation and early social experience predict gaze following abilities in infant monkeys

Individuals vary in their social skills and motivation, the causes of which remain largely unknown. Here we investigated whether an individual’s propensity to interact with others measured within days after birth, and differences in infants’ early social environment, may predict a later social skill. Specifically, we tested whether neonatal imitation—newborns’ capacity to match modelled actions—and social experience in the first months of life predict gaze following (directing attention to locations where others look), in infant macaques (Macaca mulatta; n = 119). Facial gesture imitation in the first week of life predicted gaze following at 7 months of age. Imitators were better at gaze following than non-imitators, suggesting neonatal imitation may be an early marker predicting socio-cognitive functioning. In addition, infants with rich social environments outperformed infants with less socialization, suggesting early social experiences also support the development of infants’ gaze following competence. The present study offers compelling evidence that an individual difference present from birth predicts a functional social cognitive skill in later infancy. In addition, this foundational skill—gaze following—is plastic, and can be improved through social interactions, providing infants with a strong foundation for later social interaction and learning

Recognizing Speech in a Novel Accent: The Motor Theory of Speech Perception Reframed

The motor theory of speech perception holds that we perceive the speech of another in terms of a motor representation of that speech. However, when we have learned to recognize a foreign accent, it seems plausible that recognition of a word rarely involves reconstruction of the speech gestures of the speaker rather than the listener. To better assess the motor theory and this observation, we proceed in three stages. Part 1 places the motor theory of speech perception in a larger framework based on our earlier models of the adaptive formation of mirror neurons for grasping, and for viewing extensions of that mirror system as part of a larger system for neuro-linguistic processing, augmented by the present consideration of recognizing speech in a novel accent. Part 2 then offers a novel computational model of how a listener comes to understand the speech of someone speaking the listener's native language with a foreign accent. The core tenet of the model is that the listener uses hypotheses about the word the speaker is currently uttering to update probabilities linking the sound produced by the speaker to phonemes in the native language repertoire of the listener. This, on average, improves the recognition of later words. This model is neutral regarding the nature of the representations it uses (motor vs. auditory). It serve as a reference point for the discussion in Part 3, which proposes a dual-stream neuro-linguistic architecture to revisits claims for and against the motor theory of speech perception and the relevance of mirror neurons, and extracts some implications for the reframing of the motor theory

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