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.

Genetic variability in the oxytocin system is linked to individual differences in cuddliness among human infants.

Pleasant touch facilitates social interactions, affiliative behavior and emotional bonding, contributing to positive infant and child development. Oxytocin is presumed to play an important role in mediating these effects of pleasant touch on brain, body and behavior. However, little is known about the role the oxytocin system plays in pleasant touch during infancy. This study examined the hypothesis that genetic variability in the oxytocin system is linked to individual differences in infants' cuddliness operationalized as parent-reported behaviors indexing an infant's motivation to seek out and enjoy caregiver touch. Our results (N = 82) show that a polymorphism in CD38 (rs3796863), previously linked with increased release of oxytocin in adults, was associated with higher reported rates of cuddliness. In contrast, infants with CD38 genotype previously linked to autism spectrum disorder (ASD) and reduced release of oxytocin in adults, was associated with lower rates of cuddliness. These findings support the hypothesis that, from early in human ontogeny, genetic variation in the oxytocin system is systematically linked to individual differences in the reported motivation to seek out, and the enjoyment of receiving, pleasant caregiver touch. This provides novel insights into the neurohormonal processes involved in pleasant touch.

Variability in the expression and perception of positive affect in human infancy.

Positive emotions play a critical role in guiding human behavior and social interactions. This study examined whether and how genetic variability in the oxytocin system is linked to individual differences in expressing positive affect in human infants. Our results show that genetic variation in CD38 (rs3796863), previously linked to increased release of oxytocin, was associated with higher rates of positive affective displays among a sample of 7-month-old infants, using established parent-report measures. Moreover, infants displaying increased levels of positive affect (smiling and laughter) also showed enhanced brain responses in the right inferior frontal cortex, a brain region previously linked to perception-action coupling, when viewing others smile at them. These findings suggest that, from early in development, genetic variation in the oxytocin system is associated with individual differences in expressed positive affect, which in turn are linked to differences in perceiving positive affect. This helps uncover the neurobiological processes accounting for variability in the expression and perception of positive affect in infancy.

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.

Infant and maternal responses to emotional facial expressions: A longitudinal study.

The current longitudinal study (N = 107) examined mothers' facial emotion recognition using reaction time and their infants' affect-based attention at 5, 7, and 14 months of age using eyetracking. Our results, examining maternal and infant responses to angry, fearful and happy facial expressions, show that only maternal responses to angry facial expressions were robustly and positively linked across time points, indexing a consistent trait-like response to social threat among mothers. However, neither maternal responses to happy or fearful facial expressions nor infant responses to all three facial emotions show such consistency, pointing to the changeable nature of facial emotion processing, especially among infants. In general, infants' attention toward negative emotions (i.e., angry and fear) at earlier timepoints was linked to their affect-biased attention for these emotions at 14 months but showed greater dynamic change across time. Moreover, our results provide limited evidence for developmental continuity in processing negative emotions and for the bidirectional interplay of infant affect-biased attention and maternal facial emotion recognition. This pattern of findings suggests that infants' affect-biased attention to facial expressions of emotion are characterized by dynamic changes.

Maternal recognition of positive emotion predicts sensitive parenting in infancy.

Research on parent-child relationships demonstrates the importance of maternal sensitivity for the development of children's emotion regulation, social competence, and health; thus, it is important to understand the emotional-cognitive capacities underlying maternal sensitivity. We followed 120 mothers and their full-term infants from the newborn period to 5 months postpartum. Mothers' emotion recognition during the newborn period was measured using a validated facial emotion recognition task assessing discrimination (d') of six facial expressions of emotion: happiness, fear, anger, sadness, disgust, and neutrality. Maternal behavior at 5 months postpartum was coded from a mother-infant free-play session using Ainsworth's Sensitivity Scales. Preregistered analyses revealed that mothers' ability to detect happiness specifically (but not other emotions such as fear or sadness) in the neonatal period predicted greater observed sensitivity 4 months later, ß = .30, p = .002, ΔR² = .08. Results suggest that maternal recognition of positive emotion may be uniquely predictive of sensitive behavior in low-stress parent-infant interaction contexts. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Examining the Role of Socioeconomic Status and Maternal Sensitivity in Predicting Functional Brain Network Connectivity in 5-Month-Old Infants.

Infancy is a sensitive period of human brain development that is plastically shaped by environmental factors. Both proximal factors, such as sensitive parenting, and distal factors, such as socioeconomic status (SES), are known predictors of individual differences in structural and functional brain systems across the lifespan, yet it is unclear how these familial and contextual factors work together to shape functional brain development during infancy, particularly during the first months of life. In the current study, we examined pre-registered hypotheses regarding the interplay between these factors to assess how maternal sensitivity, within the broader context of socioeconomic variation, relates to the development of functional connectivity in long-range cortical brain networks. Specifically, we measured resting-state functional connectivity in three cortical brain networks (fronto-parietal network, default mode network, homologous-interhemispheric connectivity) using functional near-infrared spectroscopy (fNIRS), and examined the associations between maternal sensitivity, SES, and functional connectivity in a sample of 5-month-old infants and their mothers (N = 50 dyads). Results showed that all three networks were detectable during a passive viewing task, and that maternal sensitivity was positively associated with functional connectivity in the default mode network, such that infants with more sensitive mothers exhibited enhanced functional connectivity in this network. Contrary to hypotheses, we did not observe any associations of SES with functional connectivity in the brain networks assessed in this study. This suggests that at 5 months of age, maternal sensitivity is an important proximal environmental factor associated with individual differences in functional connectivity in a long-range cortical brain network implicated in a host of emotional and social-cognitive brain processes.

Processing third-party social interactions in the human infant brain.

The understanding of developing social brain functions during infancy relies on research that has focused on studying how infants engage in first-person social interactions or view individual agents and their actions. Behavioral research suggests that observing and learning from third-party social interactions plays a foundational role in early social and moral development. However, the brain systems involved in observing third-party social interactions during infancy are unknown. The current study tested the hypothesis that brain systems in prefrontal and temporal cortex, previously identified in adults and children, begin to specialize in third-party social interaction processing during infancy. Infants (N = 62), ranging from 6 to 13 months in age, had their brain responses measured using functional near-infrared spectroscopy (fNIRS) while viewing third-party social interactions and two control conditions, infants viewing two individual actions and infants viewing inverted social interactions. The results show that infants preferentially engage brain regions localized within the dorsomedial prefrontal cortex when viewing third-party social interactions. These findings suggest that brain systems processing third-party social interaction begin to develop early in human ontogeny and may thus play a foundational role in supporting the interpretation of and learning from social interactions.

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.

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.

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.

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.

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.

Variability in Infants' Functional Brain Network Connectivity Is Associated With Differences in Affect and Behavior.

Variability in functional brain network connectivity has been linked to individual differences in cognitive, affective, and behavioral traits in adults. However, little is known about the developmental origins of such brain-behavior correlations. The current study examined functional brain network connectivity and its link to behavioral temperament in typically developing newborn and 1-month-old infants (M [age] = 25 days; N = 75) using functional near-infrared spectroscopy (fNIRS). Specifically, we measured long-range connectivity between cortical regions approximating fronto-parietal, default mode, and homologous-interhemispheric networks. Our results show that connectivity in these functional brain networks varies across infants and maps onto individual differences in behavioral temperament. Specifically, connectivity in the fronto-parietal network was positively associated with regulation and orienting behaviors, whereas connectivity in the default mode network showed the opposite effect on these behaviors. Our analysis also revealed a significant positive association between the homologous-interhemispheric network and infants' negative affect. The current results suggest that variability in long-range intra-hemispheric and cross-hemispheric functional connectivity between frontal, parietal, and temporal cortex is associated with individual differences in affect and behavior. These findings shed new light on the brain origins of individual differences in early-emerging behavioral traits and thus represent a viable novel approach for investigating developmental trajectories in typical and atypical neurodevelopment.

Genetic variation in the oxytocin system and its link to social motivation in human infants.

Frontal brain asymmetry has been linked to motivational processes in infants and adults, with left lateralization reflecting motivation to approach and right lateralization reflecting motivation to withdraw. We examined the hypothesis that variability in infants' social motivation may be linked to genetic variation in the oxytocin system. Eleven-month-old infants' brain responses and looking preferences to smiling and frowning individuals were assessed in conjunction with a polymorphism in CD38 (rs3796863) linked to autism spectrum disorder (ASD) and reduced oxytocin. Frontal brain asymmetry and looking preferences differed as a function of CD38 genotype. While non-risk A-allele carriers displayed left lateralization to smiling faces (approach) and a heightened looking preference for the individual who smiled, infants with the CC (ASD risk) genotype displayed withdrawal from smiling faces and a preference for the individual who frowned. Findings demonstrate that the oxytocin system is linked to brain and behavioral markers of social motivation in infancy.