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  Epigenetic tuning of brain signal entropy in emergent human social behavior

Puglia, M. H., Krol, K. M., Missana, M., Williams, C. L., Lillard, T. S., Morris, J. P., et al. (2020). Epigenetic tuning of brain signal entropy in emergent human social behavior. BMC Medicine, 18(1): 244. doi:10.1186/s12916-020-01683-x.

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Item Permalink: http://hdl.handle.net/21.11116/0000-0007-1776-B Version Permalink: http://hdl.handle.net/21.11116/0000-0007-1777-A
Genre: Journal Article

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 Creators:
Puglia, Meghan H.1, 2, Author
Krol, K. M.1, 3, Author              
Missana, Manuela3, 4, Author              
Williams, Cabell L.1, Author
Lillard, Travis S.1, Author
Morris, James P.1, Author
Connelly, Jessica J.1, Author
Grossmann, Tobias1, 3, Author              
Affiliations:
1Department of Psychology, University of Virginia, Charlottesville, VA, USA, ou_persistent22              
2Department of Neurology, University of Virginia, Charlottesville, VA, USA, ou_persistent22              
3Max Planck Research Group Early Social Development, MPI for Human Cognitive and Brain Sciences, Max Planck Society, ou_1356545              
4Department of Early Child Development and Culture, University of Leipzig, Germany, ou_persistent22              

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Free keywords: EEG; Infant development; Multiscale entropy; OXTR epigenetics; Social perception
 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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Language(s): eng - English
 Dates: 2019-10-012020-06-262020-08-17
 Publication Status: Published online
 Pages: -
 Publishing info: -
 Table of Contents: -
 Rev. Type: -
 Identifiers: DOI: 10.1186/s12916-020-01683-x
PMID: 32799881
PMC: PMC7429788
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Project name : -
Grant ID : 1729289
Funding program : -
Funding organization : Max Planck Society
Project name : -
Grant ID : F31HD090865
Funding program : -
Funding organization : National Institute of Child Health and Development

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Title: BMC Medicine
Source Genre: Journal
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Publ. Info: BioMed Central
Pages: - Volume / Issue: 18 (1) Sequence Number: 244 Start / End Page: - Identifier: ISSN: 1741-7015
CoNE: https://pure.mpg.de/cone/journals/resource/111071069889002