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Human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context

Both oxytocin (OT) and touch are key mediators of social attachment. In rodents, tactile stimulation elicits the endogenous release of OT, potentially facilitating attachment and other forms of prosocial behavior, yet the relationship between endogenous OT and neural modulation remains unexplored in...

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Autores principales: Handlin, Linda, Novembre, Giovanni, Lindholm, Helene, Kämpe, Robin, Paul, Elisabeth, Morrison, India
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10168694/
https://www.ncbi.nlm.nih.gov/pubmed/37157840
http://dx.doi.org/10.7554/eLife.81197
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author Handlin, Linda
Novembre, Giovanni
Lindholm, Helene
Kämpe, Robin
Paul, Elisabeth
Morrison, India
author_facet Handlin, Linda
Novembre, Giovanni
Lindholm, Helene
Kämpe, Robin
Paul, Elisabeth
Morrison, India
author_sort Handlin, Linda
collection PubMed
description Both oxytocin (OT) and touch are key mediators of social attachment. In rodents, tactile stimulation elicits the endogenous release of OT, potentially facilitating attachment and other forms of prosocial behavior, yet the relationship between endogenous OT and neural modulation remains unexplored in humans. Using a serial sampling of plasma hormone levels during functional neuroimaging across two successive social interactions, we show that contextual circumstances of social touch influence not only current hormonal and brain responses but also later responses. Namely, touch from a male to his female romantic partner enhanced her subsequent OT release for touch from an unfamiliar stranger, yet females’ OT responses to partner touch were dampened following stranger touch. Hypothalamus and dorsal raphe activation reflected plasma OT changes during the initial social interaction. In the subsequent interaction, precuneus and parietal-temporal cortex pathways tracked time- and context-dependent variables in an OT-dependent manner. This OT-dependent cortical modulation included a region of the medial prefrontal cortex that also covaried with plasma cortisol, suggesting an influence on stress responses. These findings demonstrate that modulation between hormones and the brain during human social interactions can flexibly adapt to features of social context over time.
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spelling pubmed-101686942023-05-10 Human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context Handlin, Linda Novembre, Giovanni Lindholm, Helene Kämpe, Robin Paul, Elisabeth Morrison, India eLife Neuroscience Both oxytocin (OT) and touch are key mediators of social attachment. In rodents, tactile stimulation elicits the endogenous release of OT, potentially facilitating attachment and other forms of prosocial behavior, yet the relationship between endogenous OT and neural modulation remains unexplored in humans. Using a serial sampling of plasma hormone levels during functional neuroimaging across two successive social interactions, we show that contextual circumstances of social touch influence not only current hormonal and brain responses but also later responses. Namely, touch from a male to his female romantic partner enhanced her subsequent OT release for touch from an unfamiliar stranger, yet females’ OT responses to partner touch were dampened following stranger touch. Hypothalamus and dorsal raphe activation reflected plasma OT changes during the initial social interaction. In the subsequent interaction, precuneus and parietal-temporal cortex pathways tracked time- and context-dependent variables in an OT-dependent manner. This OT-dependent cortical modulation included a region of the medial prefrontal cortex that also covaried with plasma cortisol, suggesting an influence on stress responses. These findings demonstrate that modulation between hormones and the brain during human social interactions can flexibly adapt to features of social context over time. eLife Sciences Publications, Ltd 2023-05-09 /pmc/articles/PMC10168694/ /pubmed/37157840 http://dx.doi.org/10.7554/eLife.81197 Text en © 2023, Handlin, Novembre et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Handlin, Linda
Novembre, Giovanni
Lindholm, Helene
Kämpe, Robin
Paul, Elisabeth
Morrison, India
Human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context
title Human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context
title_full Human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context
title_fullStr Human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context
title_full_unstemmed Human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context
title_short Human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context
title_sort human endogenous oxytocin and its neural correlates show adaptive responses to social touch based on recent social context
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10168694/
https://www.ncbi.nlm.nih.gov/pubmed/37157840
http://dx.doi.org/10.7554/eLife.81197
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