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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.

 

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 ofN = 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 tohappyfaces 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.

 

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. 

Abstract Forming an impression of another person is an essential aspect of human social cognition linked to medial prefrontal cortex (mPFC) function in adults. The current study examined the neurodevelopmental origins of impression formation by testing the hypothesis that infants rely on processes localized in mPFC when forming impressions about individuals who appear friendly or threatening. Infants’ brain responses were measured using functional near-infrared spectroscopy while watching 4 different face identities displaying either smiles or frowns directed toward or away from them (N = 77). This was followed by a looking preference test for these face identities (now displaying a neutral expression) using eyetracking. Our results show that infants’ mPFC responses distinguish between smiling and frowning faces when directed at them and that these responses predicted their subsequent person preferences. This suggests that the mPFC is involved in impression formation in human infants, attesting to the early ontogenetic emergence of brain systems supporting person perception and adaptive behavior. 

Abstract 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. 

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.

 

The contribution of nature versus nurture to the development of human behavior has been debated for centuries. Here, we offer a piece to this complex puzzle by identifying the human endogenous oxytocin system—known for its critical role in mammalian sociality—as a system sensitive to its early environment and subject to epigenetic change. Recent animal work suggests that early parental care is associated with changes in DNA methylation of conserved regulatory sites within the oxytocin receptor gene ( OXTR m). Through dyadic modeling of behavior and OXTR m status across the first year and a half of life, we translated these findings to 101 human mother-infant dyads. We show that OXTR m is dynamic in infancy and its change is predicted by maternal engagement and reflective of behavioral temperament. We provide evidence for an early window of environmental epigenetic regulation of the oxytocin system, facilitating the emergence of individual differences in human behavior.