Oxytocin is a neuropeptide positively associated with prosociality in adults. Here, we studied whether infants' salivary oxytocin can be reliably measured, is developmentally stable, and is linked to social behavior. We longitudinally collected saliva from 62 U.S. infants (44 % female, 56 % Hispanic/Latino, 24 % Black, 18 % non-Hispanic White, 11 % multiracial) at 4, 8, and 14 months of age and offline-video-coded the valence of their facial affect in response to a video of a smiling woman. We also captured infants' affective reactions in terms of excitement/joyfulness during a live, structured interaction with a singing woman in the Early Social Communication Scales at 14 months. We detected stable individual differences in infants' oxytocin levels over time (over minutes and months) and in infants' positive affect over months and across contexts (video-based and in live interactions). We detected no statistically significant changes in oxytocin levels between 4 and 8 months but found an increase from 8 to 14 months. Infants with higher oxytocin levels showed more positive facial affect to a smiling person video at 4 months; however, this association disappeared at 8 months, and reversed at 14 months (i.e., higher oxytocin was associated with less positive facial affect). Infant salivary oxytocin may be a reliable physiological measure of individual differences related to socio-emotional development.
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Epigenetic tuning of brain signal entropy in emergent human social 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.
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- Award ID(s):
- 1729289
- PAR ID:
- 10300540
- Date Published:
- Journal Name:
- BMC Medicine
- Volume:
- 18
- Issue:
- 1
- ISSN:
- 1741-7015
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Oxytocin (OXT) is a peptide hormone and a neuropeptide that regulates various peripheral physiological processes and modulates behavioral responses in the central nervous system. While the humoral release occurs from the axons arriving at the median eminence, the neuropeptide is also released from oxytocinergic cell axons in various brain structures that contain its receptor, and from their dendrites in hypothalamic nuclei and potentially into the cerebrospinal fluid (CSF). Understanding oxytocin’s complex functions requires the knowledge on patterns of oxytocinergic projections in relationship to its receptor (OXTR). This study provides the first comprehensive examination of the oxytocinergic system in the prairie vole (
Microtus ochrogaster ), an animal exhibiting social behaviors that mirror human social behaviors linked to oxytocinergic functioning. Using light and electron microscopy, we characterized the neuroanatomy of the oxytocinergic system in this species. OXT+ cell bodies were found primarily in the hypothalamus, and axons were densest in subcortical regions. Examination of the OXT+ fibers and their relationship to oxytocin receptor transcripts (Oxtr ) revealed that except for some subcortical structures, the presence of axons was not correlated with the amount ofOxtr across the brain. Of particular interest, the cerebral cortex that had high expression ofOxtr transcripts contained little to no fibers. Electron microscopy is used to quantify dense cored vesicles (DCV) in OXT+ axons and to identify potential axonal release sites. The ependymal cells that line the ventricles were frequently permissive of DCV-containing OXT+ dendrites reaching the third ventricle. Our results highlight a mechanism in which oxytocin is released directly into the ventricles and circulates throughout the ventricular system, may serve as the primary source for oxytocin that binds to OXTR in the cerebral cortex. -
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Abstract 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.
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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.more » « less
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Abstract 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.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1186/s12916-020-01683-x
