Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development

Although positive effects of oxytocin (OT) on social functioning are well-demonstrated, little is known about the mechanisms through which OT may drive early social development, or its therapeutic efficacy in infancy. To address these critical issues, we investigated the effects of exogenous OT on n...

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Main Authors: Fabrizia Festante, Holly Rayson, Annika Paukner, Stefano S.K. Kaburu, Giulia Toschi, Nathan A. Fox, Pier Francesco Ferrari
Format: Article
Language:English
Published: Elsevier 2021-04-01
Series:Developmental Cognitive Neuroscience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1878929321000414
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spelling doaj-7e14c37eb1a6428ebf425de2cee255682021-04-16T04:53:11ZengElsevierDevelopmental Cognitive Neuroscience1878-92932021-04-0148100950Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social developmentFabrizia Festante0Holly Rayson1Annika Paukner2Stefano S.K. Kaburu3Giulia Toschi4Nathan A. Fox5Pier Francesco Ferrari6Department of Developmental Neuroscience, IRCCS Fondazione Stella Maris, 56128, Pisa, Italy; Department of Clinical and Experimental Medicine, University of Pisa, 56126, Pisa, ItalyInstitut des Sciences Cognitives Marc Jeannerod, CNRS/Université Claude Bernard Lyon, Bron, Cedex, 69675, FrancePsychology Department, Nottingham Trent University, Nottingham, NG1 4FQ, UKDepartment of Biomedical Science & Physiology, University of Wolverhampton, Wolverhampton, WV1 1LY, UKDepartment of Medicine and Surgery, University of Parma, 43125, Parma, ItalyDepartment of Human Development and Quantitative Methodology, University of Maryland, College Park, MD, 20740, USAInstitut des Sciences Cognitives Marc Jeannerod, CNRS/Université Claude Bernard Lyon, Bron, Cedex, 69675, France; Department of Medicine and Surgery, University of Parma, 43125, Parma, Italy; Corresponding author at: Institut des Sciences Cognitives Marc Jeannerod, Unit 5229, CNRS / Université Claude Bernard Lyon, 67 Bd Pinel, 69675, Bron Cedex, France.Although positive effects of oxytocin (OT) on social functioning are well-demonstrated, little is known about the mechanisms through which OT may drive early social development, or its therapeutic efficacy in infancy. To address these critical issues, we investigated the effects of exogenous OT on neural (EEG) and behavioral responses during observation of live facial gestures in infant macaques with limited social exposure (i.e. nursery-reared). Three key findings were revealed. First, OT increased alpha suppression over posterior scalp regions during observation of facial gestures but not non-biological movement, suggesting that OT targets self-other matching and attentional cortical networks involved in social perception from very early infancy. Second, OT increased infant production of matching facial gestures and attention towards the most socially-relevant facial stimuli, both behaviors typically silenced by early social deprivation. Third, infants with higher cortisol levels appeared to benefit the most from OT, displaying greater improvements in prosocial behaviors after OT administration. Altogether, these findings suggest that OT promotes prosocial behaviors and associated neural responses likely impacted by early social adversity, and demonstrate the potential of OT administration to ameliorate social difficulties in the context of neurodevelopmental and early-emerging psychiatric disorders, at a developmental stage when brain plasticity is greatest.http://www.sciencedirect.com/science/article/pii/S1878929321000414InfancyEEG mu/alpha suppressionSelf-other matchingSocial attunementOxytocin
collection DOAJ
language English
format Article
sources DOAJ
author Fabrizia Festante
Holly Rayson
Annika Paukner
Stefano S.K. Kaburu
Giulia Toschi
Nathan A. Fox
Pier Francesco Ferrari
spellingShingle Fabrizia Festante
Holly Rayson
Annika Paukner
Stefano S.K. Kaburu
Giulia Toschi
Nathan A. Fox
Pier Francesco Ferrari
Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development
Developmental Cognitive Neuroscience
Infancy
EEG mu/alpha suppression
Self-other matching
Social attunement
Oxytocin
author_facet Fabrizia Festante
Holly Rayson
Annika Paukner
Stefano S.K. Kaburu
Giulia Toschi
Nathan A. Fox
Pier Francesco Ferrari
author_sort Fabrizia Festante
title Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development
title_short Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development
title_full Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development
title_fullStr Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development
title_full_unstemmed Oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development
title_sort oxytocin promotes prosocial behavior and related neural responses in infant macaques at-risk for compromised social development
publisher Elsevier
series Developmental Cognitive Neuroscience
issn 1878-9293
publishDate 2021-04-01
description Although positive effects of oxytocin (OT) on social functioning are well-demonstrated, little is known about the mechanisms through which OT may drive early social development, or its therapeutic efficacy in infancy. To address these critical issues, we investigated the effects of exogenous OT on neural (EEG) and behavioral responses during observation of live facial gestures in infant macaques with limited social exposure (i.e. nursery-reared). Three key findings were revealed. First, OT increased alpha suppression over posterior scalp regions during observation of facial gestures but not non-biological movement, suggesting that OT targets self-other matching and attentional cortical networks involved in social perception from very early infancy. Second, OT increased infant production of matching facial gestures and attention towards the most socially-relevant facial stimuli, both behaviors typically silenced by early social deprivation. Third, infants with higher cortisol levels appeared to benefit the most from OT, displaying greater improvements in prosocial behaviors after OT administration. Altogether, these findings suggest that OT promotes prosocial behaviors and associated neural responses likely impacted by early social adversity, and demonstrate the potential of OT administration to ameliorate social difficulties in the context of neurodevelopmental and early-emerging psychiatric disorders, at a developmental stage when brain plasticity is greatest.
topic Infancy
EEG mu/alpha suppression
Self-other matching
Social attunement
Oxytocin
url http://www.sciencedirect.com/science/article/pii/S1878929321000414
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