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

   https://doi.org/10.1186/s12916-020-01683-x  

   Puglia, Meghan H. ; Krol, Kathleen M. ; Missana, Manuela ; Williams, Cabell L. ; Lillard, Travis S. ; Morris, James P. ; Connelly, Jessica J. ; Grossmann, Tobias ( December 2020 , BMC Medicine)

   null (Ed.)

   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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2. Infants' salivary oxytocin and positive affective reactions to people

   https://doi.org/10.1016/j.yhbeh.2024.105579  

   Zeng, Guangyu ; Leung, Tiffany S ; Maylott, Sarah E ; Malik, Arushi ; Adornato, Alexis A ; Lebowitz, Mendel ; Messinger, Daniel S ; Szeto, Angela ; Feldman, Ruth ; Simpson, Elizabeth A ( August 2024 , Hormones and Behavior)

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

   https://doi.org/10.1162/jocn_a_02165  

   Grossmann, Tobias ( January 2024 , Journal of Cognitive Neuroscience)

   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.

    

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

   https://doi.org/10.3389/fpsyt.2021.685754  

   Kelsey, Caroline M. ; Farris, Katrina ; Grossmann, Tobias ( June 2021 , Frontiers in Psychiatry)

   null (Ed.)

   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. 

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5. Paleogenomic insights into cooperation in the ancient Andes from positive selection on oxytocin pathway genes

   https://doi.org/10.1111/gbb.12877  

   Joseph, Sophie K. ; Wagman, Elizabeth ; Diab, Nabeel ; Ryu, Nicholas ; Lee, Minwoo ; Haas, Randall ; Rilling, James K. ; Aldenderfer, Mark S. ; Lindo, John ( February 2024 , Genes, Brain and Behavior)

   Human societies are characterized by norms that restrict selfish behavior and promote cooperation. The oxytocin system is an important modulator of social behavior that may be involved in the evolution of cooperation. Oxytocin acts in both the nucleus accumbens and the anterior cingulate cortex to promote social bonding and social cohesion. Expression of theCD38andOXTRgenes is known to affect oxytocin secretion and binding, respectively, in these brain areas. The Andean highlands provide an excellent opportunity to evaluate the role of oxytocin in the evolution of cooperation. The rich archeological record spans 13,000 years of population growth and cooperative challenges through periods of highland exploration, hunting economies, agro‐pastoralism, and urbanization. Through allele trajectory modeling using both ancient and contemporary whole genomes, we find evidence for strong positive selection on theOXTRandCD38alleles linked with increased oxytocin signaling. These selection events commenced around 2.5 and 1.25 thousand years ago, placing them in the region's Upper Formative and Tiwanaku periods—a time of population growth, urbanization, and relatively low rates of violence. Along with remarkable and enduring cultural developments, increased oxytocin secretion and receptor binding in these brain areas may have facilitated large‐scale cooperation that promoted early urbanization in the Titicaca Basin of the Andean highlands.

    

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