Social Perception in the Infant Brain and Its Link to Social Behavior.

The current longitudinal study (n = 98) utilized a developmental cognitive neuroscience approach to examine whether and how variability in social perception is linked to social behavior in early human development. Cortical responses to processing dynamic faces were investigated using functional near-infrared spectroscopy at 7 months. Individual differences in sociability were measured using the Early Childhood Behavior Questionnaire at 18 months. Confirming previous work with infants and adults, functional near-infrared spectroscopy results show that viewing changing faces recruited superior temporal cortices in 7-month-old infants, adding to the view that this brain system is specialized in social perception from early in ontogeny. Our longitudinal results show that greater engagement of the right superior temporal cortex at 7 months predicts higher levels of sociability at 18 months. This suggests that early variability in social perception is linked to later differences in overtly displayed social behavior, providing novel longitudinal evidence for a social brain-behavior association.

Love on the developing brain: Maternal sensitivity and infants' neural responses to emotion in the dorsolateral prefrontal cortex.

Infancy is a sensitive period of development, during which experiences of parental care are particularly important for shaping the developing brain. In a longitudinal study of N = 95 mothers and infants, we examined links between caregiving behavior (maternal sensitivity observed during a mother-infant free-play) and infants' neural response to emotion (happy, angry, and fearful faces) at 5 and 7 months of age. Neural activity was assessed using functional Near-Infrared Spectroscopy (fNIRS) in the dorsolateral prefrontal cortex (dlPFC), a region involved in cognitive control and emotion regulation. Maternal sensitivity was positively correlated with infants' neural responses to happy faces in the bilateral dlPFC and was associated with relative increases in such responses from 5 to 7 months. Multilevel analyses revealed caregiving-related individual differences in infants' neural responses to happy compared to fearful faces in the bilateral dlPFC, as well as other brain regions. We suggest that variability in dlPFC responses to emotion in the developing brain may be one correlate of early experiences of caregiving, with implications for social-emotional functioning and self-regulation.

The brain origins of early social cognition.

This commentary challenges Spelke's view on the early development of social cognition from a neuroscience perspective by presenting an overlooked body of evidence from neuroimaging research on joint attention with human infants. Indeed, evidence demonstrating adult-like, neural sensitivity to joint attention in young infants, supports alternative theoretical views concerning the origins of uniquely human forms of social cognition.

Extending and refining the fearful ape hypothesis.

The fearful ape hypothesis (FAH) presents an evolutionary-developmental framework stipulating that in the context of cooperative caregiving, unique to human great ape group life, heightened fearfulness was adaptive. This is because from early in human ontogeny fearfulness expressed and perceived enhanced care-based responding and cooperation with mothers and others. This response extends and refines the FAH by incorporating the commentaries' suggestions and additional lines of empirical work, providing a more comprehensive and nuanced version of the FAH. Specifically, it encourages and hopes to inspire cross-species and cross-cultural, longitudinal work elucidating evolutionary and developmental functions of fear in context. Beyond fear, it can be seen as a call for an evolutionary-developmental approach to affective science.

Becoming uniquely human? Comparing chimpanzee to human infancy.

Does comparing behavioral development between chimpanzees and humans during infancy hold the key to understanding what is uniquely human? Recent work shows that while many behaviors emerge at similar ages in chimpanzees, human infants develop behavioral traits underpinning our prosocial and ultra-cooperative nature at a much accelerated rate.

Fairness takes time: Development of cooperative decision making in fairness context.

The current study examined the development of fairness behavior and tested whether children's fair choices are fast and intuitive or slow and deliberate. Reaction times were measured while 4- to 9-year-olds (N = 94, 49 girls, 84.6% White) completed a novel social decision-making task contrasting fair choices with selfish choices. Fairness behavior increased during childhood, shifting from predominantly selfish choices among young children to fair choices by 7 years of age. Moreover, young children's fair choices were slow and deliberate, whereas reaction times did not predict older children's choices. These findings contrast with adults' intuitive cooperation and point to protracted development and learning of cooperative decision making in fairness contexts.

The human fear paradox: Affective origins of cooperative care.

Already as infants humans are more fearful than our closest living primate relatives, the chimpanzees. Yet heightened fearfulness is mostly considered maladaptive, as it is thought to increase the risk of developing anxiety and depression. How can this human fear paradox be explained? The fearful ape hypothesis presented herein stipulates that, in the context of cooperative caregiving and provisioning unique to human great ape group life, heightened fearfulness was adaptive. This is because from early in ontogeny fearfulness expressed and perceived enhanced care-based responding and provisioning from, while concurrently increasing cooperation with, mothers and others. This explanation is based on a synthesis of existing research with human infants and children, demonstrating a link between fearfulness, greater sensitivity to and accuracy in detecting fear in others, and enhanced levels of cooperative behaviors. These insights critically advance current evolutionary theories of human cooperation by adding an early-developing affective component to the human cooperative makeup. Moreover, the current proposal has important cultural, societal, and health implications, as it challenges the predominant view in Western, educated, industrialized, rich, and democratic (WEIRD) societies that commonly construe fearfulness as a maladaptive trait, potentially ignoring its evolutionary adaptive functions.

Gut microbiota composition is associated with newborn functional brain connectivity and behavioral temperament.

The gut microbiome appears to play an important role in human health and disease. However, only little is known about how variability in the gut microbiome contributes to individual differences during early and sensitive stages of brain and behavioral development. The current study examined the link between gut microbiome, brain, and behavior in newborn infants (N = 63; M [age] = 25 days). Infant gut microbiome diversity was measured from stool samples using metagenomic sequencing, infant functional brain network connectivity was assessed using a resting state functional near infrared spectroscopy (rs-fNIRS) procedure, and infant behavioral temperament was assessed using parental report. Our results show that gut microbiota composition is linked to individual variability in brain network connectivity, which in turn mediated individual differences in behavioral temperament, specifically negative emotionality, among infants. Furthermore, virulence factors, possibly indexing pathogenic activity, were associated with differences in brain network connectivity linked to negative emotionality. These findings provide novel insights into the early developmental origins of the gut microbiome-brain axis and its association with variability in important behavioral traits. This suggests that the gut microbiome is an important biological factor to consider when studying human development and health.

The neurodevelopmental precursors of altruistic behavior in infancy.

Altruistic behavior is considered a key feature of the human cooperative makeup, with deep ontogenetic roots. The tendency to engage in altruistic behavior varies between individuals and has been linked to differences in responding to fearful faces. The current study tests the hypothesis that this link exists from early in human ontogeny. Using eye tracking, we examined whether attentional responses to fear in others at 7 months of age predict altruistic behavior at 14 months of age. Our analysis revealed that altruistic behavior in toddlerhood was predicted by infants' attention to fearful faces but not happy or angry faces. Specifically, infants who showed heightened initial attention to (i.e., prolonged first look) followed by greater disengagement (i.e., reduced attentional bias over 15 seconds) from fearful faces at 7 months displayed greater prosocial behavior at 14 months of age. Our data further show that infants' attentional bias to fearful faces and their altruistic behavior was predicted by brain responses in the dorsolateral prefrontal cortex (dlPFC), measured through functional near-infrared spectroscopy (fNIRS). This suggests that, from early in ontogeny, variability in altruistic helping behavior is linked to our responsiveness to seeing others in distress and brain processes implicated in attentional control. These findings critically advance our understanding of the emergence of altruism in humans by identifying responsiveness to fear in others as an early precursor contributing to variability in prosocial behavior.

Mother's engagement with infant linked to infant's responding to threat.

The early development of threat perception in infancy might be dependent on caregiver context, but this link has not yet been studied in human infants. This study examined the emergence of the young infant's response to threat in the context of variations in caregiving behavior. Eighty infant-caregiver dyads (39 female infants, all of western European descent) visited the laboratory when the infant was 5 months old. Each dyad completed a free-play task, from which we coded for the mother's level of engagement: the amount of talking, close proximity, positive affect, and attention directed toward the infant. When the infant was 7 months old, they came back to the laboratory and we used functional near infrared spectroscopy and eye tracking to measure infants' neural and attentional responses to threatening angry faces. In response to threat, infants of more-engaged mothers showed increased brain responses in the left dorsolateral prefrontal cortex-a brain region associated with emotion regulation and cognitive control among adults-and reduced attentional avoidance. These results point to a role for caregiver behavioral context in the early development of brain systems involved in human threat responding.

Probing infants' sensitivity to pupil size when viewing eyes.

Sensitive responding to eye cues plays a key role in human social interactions. Pupil size provides subtle cues regarding a social interaction partner's arousal states. The current study assessed infants' sensitivity to and preference for differences in pupil size. Specifically, we examined White 14-month-old infants' pupillary responses when viewing own-race and other-race (Asian) eyes with dilating, constricting, and static medium-sized pupils. Our results show that, independent of race, infants' pupils dilated more when viewing eyes with dynamically changing (dilating and constricting) pupils than when viewing eyes with non-changing, static, and medium-sized pupils. We also measured infants' looking preferences, showing that, independent of race, infants preferentially attended to eyes with dilated pupils. Moreover, our results show that infants orient more quickly to pupillary changes in own-race eyes than in other-race eyes. These findings demonstrate that infants detect, but do not mimic, changes in pupil size in others and show a preference for eyes with dilated pupils.

Insights into the uniquely human origins of understanding other minds.

We summarize research and theory to show that, from early in human ontogeny, much information about other minds can be gleaned from reading the eyes. This analysis suggests that eyes serve as uniquely human windows into other minds, which critically extends the target article by drawing attention to what might be considered the neurodevelopmental origins of knowledge attribution in humans.

Correction to: Epigenetic tuning of brain signal entropy in emergent human social behavior.

An amendment to this paper has been published and can be accessed via the original article.

Epigenetic tuning of brain signal entropy in emergent human social behavior.

BACKGROUND: How the brain develops accurate models of the external world and generates appropriate behavioral responses is a vital question of widespread multidisciplinary interest. It is increasingly understood that brain signal variability-posited to enhance perception, facilitate flexible cognitive representations, and improve behavioral outcomes-plays an important role in neural and cognitive development. The ability to perceive, interpret, and respond to complex and dynamic social information is particularly critical for the development of adaptive learning and behavior. Social perception relies on oxytocin-regulated neural networks that emerge early in development. METHODS: We tested the hypothesis that individual differences in the endogenous oxytocinergic system early in life may influence social behavioral outcomes by regulating variability in brain signaling during social perception. In study 1, 55 infants provided a saliva sample at 5 months of age for analysis of individual differences in the oxytocinergic system and underwent electroencephalography (EEG) while listening to human vocalizations at 8 months of age for the assessment of brain signal variability. Infant behavior was assessed via parental report. In study 2, 60 infants provided a saliva sample and underwent EEG while viewing faces and objects and listening to human speech and water sounds at 4 months of age. Infant behavior was assessed via parental report and eye tracking. RESULTS: We show in two independent infant samples that increased brain signal entropy during social perception is in part explained by an epigenetic modification to the oxytocin receptor gene (OXTR) and accounts for significant individual differences in social behavior in the first year of life. These results are measure-, context-, and modality-specific: entropy, not standard deviation, links OXTR methylation and infant behavior; entropy evoked during social perception specifically explains social behavior only; and only entropy evoked during social auditory perception predicts infant vocalization behavior. CONCLUSIONS: Demonstrating these associations in infancy is critical for elucidating the neurobiological mechanisms accounting for individual differences in cognition and behavior relevant to neurodevelopmental disorders. Our results suggest that an epigenetic modification to the oxytocin receptor gene and brain signal entropy are useful indicators of social development and may hold potential diagnostic, therapeutic, and prognostic value.

A primer on investigating the role of the microbiome in brain and cognitive development.

Incorporating information regarding the gut microbiota into psychobiological research promises to shed new light on how individual differences in brain and cognitive development emerge. However, the investigation of the gut-brain axis in development is still in its infancy and poses several challenges, including data analysis. Considering that the gut microbiome is an eco-system containing millions of bacteria, one needs to utilize a breadth of methodologies and data analytic techniques. The present review serves two purposes. First, this review will inform developmental psychobiology researchers about the emerging study of the gut-brain axis in development and second, this review will propose methodologies and data analytic strategies for integrating microbiome data in developmental research.

Genetic variation in CD38 and breastfeeding experience interact to impact infants' attention to social eye cues.

Attending to emotional information conveyed by the eyes is an important social skill in humans. The current study examined this skill in early development by measuring attention to eyes while viewing emotional faces in 7-mo-old infants. In particular, we investigated individual differences in infant attention to eyes in the context of genetic variation (CD38 rs3796863 polymorphism) and experiential variation (exclusive breastfeeding duration) related to the oxytocin system. Our results revealed that, whereas infants at this age show a robust fear bias (increased attention to fearful eyes), their attention to angry and happy eyes varies as a function of exclusive breastfeeding experience and genetic variation in CD38. Specifically, extended exclusive breastfeeding duration selectively enhanced looking preference to happy eyes and decreased looking to angry eyes. Importantly, however, this interaction was impacted by CD38 variation, such that only the looking preferences of infants homozygous for the C allele of rs3796863 were affected by breastfeeding experience. This genotype has been associated with reduced release of oxytocin and higher rates of autism. In contrast, infants with the CA/AA genotype showed similar looking preferences regardless of breastfeeding exposure. Thus, differences in the sensitivity to emotional eyes may be linked to an interaction between the endogenous (CD38) and exogenous (breastfeeding) availability of oxytocin. These findings underline the importance of maternal care and the oxytocin system in contributing to the early development of responding to social eye cues.

Psychological effects of breastfeeding on children and mothers.

While the nutritional and physical health benefits of breastfeeding are well established, accumulating research demonstrates the far-reaching psychological effects of breastfeeding on children and their mothers. Here, we provide a non-exhaustive review of the empirical evidence, showing that breastfeeding impacts children's brain, cognitive, and socio-emotional development. In mothers, research is presented indicating that breastfeeding influences mood, affect, stress, and maternal care. The current review aims to provide a broad overview of existing findings on the psychological effects of breastfeeding, highlighting the important role that breastfeeding plays across several dimensions of psychological functioning. We also discuss the potential mechanisms that may underpin the observed effects, provide a constructive commentary on the limitations of the existing work, and put forth some considerations when evaluating this line of research.

Brain responses reveal that infants' face discrimination is guided by statistical learning from distributional information.

Infants' perception of faces becomes attuned to the environment during the first year of life. However, the mechanisms that underpin perceptual narrowing for faces are only poorly understood. Considering the developmental similarities seen in perceptual narrowing for faces and speech and the role that statistical learning has been shown to play for speech, the current study examined whether and how learning from distributional information impacts face identity discrimination. We familiarized 6.5-month-old infants with exemplars of female faces taken from a morphed continuum going from one identity to another. Using event-related brain potentials (ERPs), we show that only infants who were familiarized with a bimodal frequency distribution, but not infants familiarized with a unimodal frequency distribution, discriminated between identities. These results are the first to demonstrate the influence of probabilistic information on infants' face identity discrimination, suggesting that statistical learning contributes to perceptual attunement for both faces and language.

When in infancy does the "fear bias" develop?

Much research has focused on how infants respond to emotional facial expressions. One of the key findings in this area of research is that by 7months of age, but not younger, infants show a bias in processing fearful faces even when compared with other negative and novel facial expressions. A recent study by Heck and colleagues (Journal of Experimental Child Psychology, 2016, Vol. 147, pp. 100-110) challenges this idea by showing that 5-month-olds looked longer at fearful faces than at happy and at neutral faces when dynamic displays (videos) are used. Given that previous work failed to find enhanced attention to fearful faces in 5-month-olds using static displays (photographs), this was taken as evidence that biased attention to fear can be observed earlier when dynamic information is presented. However, we computed an analysis indicating that the overall amount of motion displayed in the videos in Heck and colleagues' study is confounded with emotion such that the greatest amount of motion is evident in the fearful face videos and may have driven infants' looking patterns. We discuss these findings and their limitations in the context of other research using dynamic emotion stimuli. Although these findings do not rule out the possibility that 5-month-olds are sensitive to fear, we stress the need to control for physical differences such as motion before any conclusions regarding the emergence of the fear bias during infancy can be drawn and in order to improve research practice in the field.

Unconscious discrimination of social cues from eye whites in infants.

Human eyes serve two key functions in face-to-face social interactions: they provide cues about a person's emotional state and attentional focus (gaze direction). Both functions critically rely on the morphologically unique human sclera and have been shown to operate even in the absence of conscious awareness in adults. However, it is not known whether the ability to respond to social cues from scleral information without conscious awareness exists early in human ontogeny and can therefore be considered a foundational feature of human social functioning. In the current study, we used event-related brain potentials (ERPs) to show that 7-mo-old infants discriminate between fearful and nonfearful eyes (experiment 1) and between direct and averted gaze (experiment 2), even when presented below the perceptual threshold. These effects were specific to the human sclera and not seen in response to polarity-inverted eyes. Our results suggest that early in ontogeny the human brain detects social cues from scleral information even in the absence of conscious awareness. The current findings support the view that the human eye with its prominent sclera serves critical communicative functions during human social interactions.