Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations

  1. Yuanshu Chen
  2. Haochen Zou
  3. Xin Hou
  4. Chuimei Lan
  5. Jing Wang
  6. Yanan Qing
  7. Wangjun Chen
  8. Shuxia Yao  Is a corresponding author
  9. Keith M Kendrick  Is a corresponding author
  1. University of Electronic Science and Technology of China, China
  2. Chongqing Normal University, China
  3. 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.

The following data sets were generated
    1. Yuanshu Chen
    2. Keith Kendrick
    (2023) Effects of oxytocin on social touch
    Open Science Framework, doi:10.17605/OSF.IO/CYKRU.

Article and author information

Author details

  1. Yuanshu Chen

    Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8500-7647
  2. Haochen Zou

    Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Xin Hou

    School of Educational Sciences, Chongqing Normal University, Chongqing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Chuimei Lan

    Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Jing Wang

    West China School of Pharmacy, Sichuan University, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Yanan Qing

    Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Wangjun Chen

    Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Shuxia Yao

    Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, China
    For correspondence
    yaoshuxia@uestc.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  9. Keith M Kendrick

    Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, China
    For correspondence
    k.kendrick.uestc@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0371-5904

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.

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.

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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  1. Yuanshu Chen
  2. Haochen Zou
  3. Xin Hou
  4. Chuimei Lan
  5. Jing Wang
  6. Yanan Qing
  7. Wangjun Chen
  8. Shuxia Yao
  9. Keith M Kendrick
(2023)
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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https://doi.org/10.7554/eLife.85847

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