Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations
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...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2023-05-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/85847 |
| _version_ | 1797816525268189184 |
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| author | Yuanshu Chen Haochen Zou Xin Hou Chuimei Lan Jing Wang Yanan Qing Wangjun Chen Shuxia Yao Keith M Kendrick |
| author_facet | Yuanshu Chen Haochen Zou Xin Hou Chuimei Lan Jing Wang Yanan Qing Wangjun Chen Shuxia Yao Keith M Kendrick |
| author_sort | Yuanshu Chen |
| collection | DOAJ |
| description | 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 |
| first_indexed | 2024-03-13T08:39:58Z |
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| id | doaj.art-524fb9c9ab67441b9b8aec8c738efa84 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-13T08:39:58Z |
| publishDate | 2023-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-524fb9c9ab67441b9b8aec8c738efa842023-05-30T15:12:30ZengeLife Sciences Publications LtdeLife2050-084X2023-05-011210.7554/eLife.85847Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrationsYuanshu Chen0https://orcid.org/0000-0001-8500-7647Haochen Zou1Xin Hou2Chuimei Lan3Jing Wang4Yanan Qing5Wangjun Chen6Shuxia Yao7Keith M Kendrick8https://orcid.org/0000-0002-0371-5904The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for NeuroInformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for NeuroInformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaSchool of Educational Sciences, Chongqing Normal University, Chongqing, ChinaThe Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for NeuroInformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaWest China School of Pharmacy, Sichuan University, Chengdu, ChinaThe Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for NeuroInformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for NeuroInformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for NeuroInformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for NeuroInformation, Center for Information in Medicine, University of Electronic Science and Technology of China, Chengdu, ChinaBackground: 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: NCT05265806https://elifesciences.org/articles/85847intranasal oxytocinoral oxytocinsocial touchCT fibersorbitofrontal cortexsuperior temporal sulcus |
| spellingShingle | Yuanshu Chen Haochen Zou Xin Hou Chuimei Lan Jing Wang Yanan Qing Wangjun Chen Shuxia Yao Keith M Kendrick Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations eLife intranasal oxytocin oral oxytocin social touch CT fibers orbitofrontal cortex superior temporal sulcus |
| title | Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations |
| title_full | Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations |
| title_fullStr | Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations |
| title_full_unstemmed | Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations |
| title_short | Oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations |
| title_sort | oxytocin administration enhances pleasantness and neural responses to gentle stroking but not moderate pressure social touch by increasing peripheral concentrations |
| topic | intranasal oxytocin oral oxytocin social touch CT fibers orbitofrontal cortex superior temporal sulcus |
| url | https://elifesciences.org/articles/85847 |
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