Elizabeth A. Simpson

Inhaled oxytocin increases positive social behaviors in newborn macaques

Significance Oxytocin promotes positive social behaviors in several species and therefore may be a therapeutic tool for neurodevelopmental disorders. It remains untested, however, whether oxytocin may affect infants, and whether effects may vary depending on infants’ social skills or interest. To test these predictions, we administered nebulized oxytocin to rhesus macaque newborns. Macaques, like humans, engage in complex face-to-face mother–infant interactions. Oxytocin increased infants’ affiliative communicative gestures and decreased salivary cortisol, and higher oxytocin levels were associated with greater social interest. Infants with stronger imitative skills were most positively influenced by oxytocin, suggesting that oxytocin sensitivity may underlie early social motivation. These results suggest that oxytocin may be a promising early intervention for infants at risk for abnormal social functions. Early caregiver–infant interactions are critical for infants’ socioemotional and cognitive development. Several hormones and neuromodulators, including oxytocin, affect these interactions. Exogenous oxytocin promotes social behaviors in several species, including human and nonhuman primates. Although exogenous oxytocin increases social function in adults—including expression recognition and affiliation—it is unknown whether oxytocin can increase social interactions in infants. We hypothesized that nebulized oxytocin would increase affiliative social behaviors and such effects would be modulated by infants’ social skills, measured earlier in development. We also hypothesized that oxytocin’s effects on social behaviors may be due to its anxiolytic effects. We tested these hypotheses in a blind study by nebulizing 7- to 14-d-old macaques (n = 28) with oxytocin or saline. Following oxytocin administration, infants’ facial gesturing at a human caregiver increased, and infants’ salivary oxytocin was positively correlated with the time spent in close proximity to a caregiver. Infants’ imitative skill (measured earlier in development: 1–7 d of age) predicted oxytocin-associated increases in affiliative behaviors—lip smacking, visual attention to a caregiver, and time in close proximity to a caregiver—suggesting that infants with higher propensities for positive social interactions are more sensitive to exogenous oxytocin. Oxytocin also decreased salivary cortisol, but not stress-related behaviors (e.g., scratching), suggesting the possibility of some anxiolytic effects. To our knowledge, this study provides the first evidence that oxytocin increases positive social behaviors in newborns. This information is of critical importance for potential interventions aimed at ameliorating inadequate social behaviors in infants with higher likelihood of developing neurodevelopmental disorder.

Mirror neurons through the lens of epigenetics

The consensus view in mirror neuron research is that mirror neurons comprise a uniform, stable execution-observation matching system. In this opinion article, we argue that, in light of recent evidence, this is at best an incomplete and oversimplified view of mirror neurons, where activity is actually variable and more plastic than previously theorized. We propose an epigenetic account for understanding developmental changes in sensorimotor systems, including variations in mirror neuron activity. Although associative and genetic accounts fail to consider the complexity of genetic and nongenetic interactions, we propose a new evolutionary developmental biology (evo-devo) perspective, which predicts that environmental differences early in development should produce variations in mirror neuron response patterns, tuning them to the social environment.

Listen up! Processing of intensity change differs for vocal and nonvocal sounds

Changes in the intensity of both vocal and nonvocal sounds can be emotionally relevant. However, as only vocal sounds directly reflect communicative intent, intensity change of vocal but not nonvocal sounds is socially relevant. Here we investigated whether a change in sound intensity is processed differently depending on its social relevance. To this end, participants listened passively to a sequence of vocal or nonvocal sounds that contained rare deviants which differed from standards in sound intensity. Concurrently recorded event-related potentials (ERPs) revealed a mismatch negativity (MMN) and P300 effect for intensity change. Direction of intensity change was of little importance for vocal stimulus sequences, which recruited enhanced sensory and attentional resources for both loud and soft deviants. In contrast, intensity change in nonvocal sequences recruited more sensory and attentional resources for loud as compared to soft deviants. This was reflected in markedly larger MMN/P300 amplitudes and shorter P300 latencies for the loud as compared to soft nonvocal deviants. Furthermore, while the processing pattern observed for nonvocal sounds was largely comparable between men and women, sex differences for vocal sounds suggest that women were more sensitive to their social relevance. These findings extend previous evidence of sex differences in vocal processing and add to reports of voice specific processing mechanisms by demonstrating that simple acoustic change recruits more processing resources if it is socially relevant.

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.

Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys

In primates, including humans, mothers engage in face-to-face interactions with their infants, with frequencies varying both within and across species. However, the impact of this variation in face-to-face interactions on infant social development is unclear. Here we report that infant monkeys (Macaca mulatta) who engaged in more neonatal face-to-face interactions with mothers have increased social interactions at 2 and 5 months. In a controlled experiment, we show that this effect is not due to physical contact alone: monkeys randomly assigned to receive additional neonatal face-to-face interactions (mutual gaze and intermittent lip-smacking) with human caregivers display increased social interest at 2 months, compared with monkeys who received only additional handling. These studies suggest that face-to-face interactions from birth promote young primate social interest and competency.

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.

Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques

RationaleExogenous oxytocin administration is widely reported to improve social cognition in human and nonhuman primate adults. Risk factors of impaired social cognition, however, emerge in infancy. Early interventions—when plasticity is greatest—are critical to reverse negative outcomes.ObjectiveWe tested the hypothesis that oxytocin may exert similar positive effects on infant social cognition, as in adults. To test this idea, we assessed the effectiveness of acute, aerosolized oxytocin on two foundational social cognitive skills: working memory (i.e., ability to briefly hold and process information) and social gaze (i.e., tracking the direction of others’ gaze) in 1-month-old nursery-reared macaque monkeys (Macaca mulatta). We did not predict sex differences, but we included sex as a factor in our analyses to test whether our effects would be generalizable across both males and females.ResultsIn a double-blind, placebo-controlled design, we found that females were more socially skilled at baseline compared to males, and that oxytocin improved working memory and gaze following, but only in males.ConclusionsThese sex differences, while unexpected, may be due to interactions with gonadal steroids and may be relevant to sexually dimorphic disorders of social cognition, such as male-biased autism spectrum disorder, for which oxytocin has been proposed as a potential treatment. In sum, we report the first evidence that oxytocin may influence primate infant cognitive abilities. Moreover, these behavioral effects appear sexually dimorphic, highlighting the importance of considering sex differences. Oxytocin effects observed in one sex may not be generalizable to the other sex.

Experience-independent sex differences in newborn macaques: Females are more social than males.

Human females exhibit greater social interest and skills relative to males, appearing in infancy, suggesting biological roots; however, male and female infants may be treated differently, potentially causing or amplifying sex differences. Here, we tested whether sex differences in social motivation emerge in infant monkeys (n = 48) reared in a controlled postnatal environment. Compared to males, females at 2–3 weeks looked more at conspecifics’ faces (d = 0.65), especially the eyes (d = 1.09), and at 4–5 weeks exhibited more affiliative behaviors (d = 0.64), including gesturing, looking, and proximity to familiar and unfamiliar human caretakers. In sum, converging evidence from humans and monkeys suggests that female infants are more social than males in the first weeks of life, and that such differences may arise independent of postnatal experience. Individual differences in social interest have wide-ranging developmental consequences, impacting infants’ social interaction quality and opportunities for learning. Understanding the evolution of sex differences and their developmental emergence is necessary to best support infants with varying levels of sociality.

Look Here! The Development of Attentional Orienting to Symbolic Cues

Although much research has examined the development of orienting to social directional cues (e.g., eye gaze), little is known about the development of orienting to nonsocial directional cues, such as arrows. Arrow cues have been used in numerous studies as a means to study attentional orienting, but the development of childrens understanding of such cues has not previously been examined. It remains unclear to what extent the social nature of a cue is important for directing attention; further, it is unknown whether symbolic understanding is necessary for young children to be cued by symbols such as arrows. The present investigation explored when and how arrows cue childrens attention. Our results suggest that children younger than 5 years of age orient their attention using the perceptual properties of arrows, and it is not until sometime after 5 years of age that children use the conceptual meaning of arrows to orient their attention. Understanding of the directional meaning of arrows may develop through both exogenous and endogenous orienting; we discuss possible contributions of the compression-based and selection-based learning systems.

Neonatal imitation predicts infant rhesus macaque ( Macaca mulatta ) social and anxiety-related behaviours at one year

The identification of early markers that predict the development of specific social trajectories is critical to understand the developmental and neurobiological underpinnings of healthy social development. We investigated, in infant rhesus macaques (Macaca mulatta), whether newborns’ capacity to imitate facial gestures is a valid predictive marker for the emergence of social competencies later in development, at one year of age. Here we first assessed whether infant macaques (N = 126) imitate lipsmacking gestures (a macaque affiliative expression) performed by a human experimenter in their first week of life. We then collected data on infants’ social interactions (aggression, grooming, and play) and self-scratching (a proxy indicator of anxiety) at 11–14 months when infants were transferred into a new enclosure with a large social group. Our results show that neonatal imitators exhibit more dominant behaviours, are less anxious, and, for males only, spend more time in play at one year old. These findings suggest that neonatal imitation may be an early predictor of infant sociality and may help identify infants at risk of neurodevelopmental social deficits.