Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations
- University of Electronic Science and Technology of China, China
- Chongqing Normal University, China
- Sichuan University, China
Abstract
Background: Social touch constitutes a key component of human social relationships although in some conditions with social dysfunction, such as autism, it can be perceived as unpleasant. We have previously shown that intranasal administration of oxytocin facilitates the pleasantness of social touch and activation of brain reward and social processing regions, although it is unclear if it influences responses to gentle stroking touch mediated by cutaneous C-touch fibers or pressure touch mediated by other types of fibers. Additionally, it is unclear whether endogenous oxytocin acts via direct entry into the brain or by increased peripheral blood concentrations.
Methods: In a randomized controlled design, we compared effects of intranasal (direct entry into the brain and increased peripheral concentrations) and oral (only peripheral increases) oxytocin on behavioral and neural responses to social touch targeting C-touch (gentle-stroking) or other (medium pressure without stroking) cutaneous receptors.
Results: Although both types of touch were perceived as pleasant, intranasal and oral oxytocin equivalently enhanced pleasantness ratings and responses of reward, orbitofrontal cortex, and social processing, superior temporal sulcus, regions only to gentle-stroking not medium pressure touch. Furthermore, increased blood oxytocin concentrations predicted the pleasantness of gentle stroking touch. The specificity of neural effects of oxytocin on C-touch targeted gentle stroking touch were confirmed by time-course extraction and classification analysis.
Conclusions: Increased peripheral concentrations of oxytocin primarily modulate its behavioral and neural responses to gentle social touch mediated by C-touch fibers. Findings have potential implications for using oxytocin therapeutically in conditions where social touch is unpleasant.
Funding: Key Technological Projects of Guangdong Province grant 2018B030335001.
Clinical trial number: NCT05265806.
Data availability
Individual data is plotted in Figure 2, 4 and 5. The group-level statistics are plotted in Figure 2, 3 and 6. The source data for Figure 2-6 of this study is available on Open Science Framework (https://osf.io/cykru/). The code for the condition decoding analysis (Figure 5 and Figure 5-figure supplement 1) was initially from Emberson et al (2017) (https://teammcpa.github.io/EmbersonZinszerMCPA/) and revised for group classification analysis.
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Effects of oxytocin on social touchOpen Science Framework, doi:10.17605/OSF.IO/CYKRU.
Article and author information
Author details
Funding
Key Technological Projects of Guangdong Province (2018B030335001)
- Keith M Kendrick
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Margaret M McCarthy, University of Maryland School of Medicine, United States
Ethics
Human subjects: All subjects gave written informed consent prior to any study procedures. All experimental procedures were in accordance with the latest revision of the declaration of Helsinki and approved by the local ethics committee of the University of Electronic Science and Technology of China.
Version history
- Received: December 28, 2022
- Preprint posted: January 5, 2023 (view preprint)
- Accepted: May 11, 2023
- Accepted Manuscript published: May 12, 2023 (version 1)
- Version of Record published: May 30, 2023 (version 2)
Copyright
© 2023, Chen et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations
eLife 12:e85847.
https://doi.org/10.7554/eLife.85847
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