Oxytocin Enhancement of Emotional Empathy: Generalization Across Cultures and Effects on Amygdala Activity

Accumulating evidence suggests that the neuropeptide oxytocin (OXT) can enhance empathy although it is unclear which specific behavioral and neural aspects are influenced, and whether the effects are modulated by culture, sex, and trait autism. Based on previous findings in Caucasian men, we hypothe...

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Main Authors: Yayuan Geng, Weihua Zhao, Feng Zhou, Xiaole Ma, Shuxia Yao, Rene Hurlemann, Benjamin Becker, Keith M. Kendrick
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-07-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2018.00512/full
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author Yayuan Geng
Weihua Zhao
Feng Zhou
Xiaole Ma
Shuxia Yao
Rene Hurlemann
Rene Hurlemann
Benjamin Becker
Keith M. Kendrick
author_facet Yayuan Geng
Weihua Zhao
Feng Zhou
Xiaole Ma
Shuxia Yao
Rene Hurlemann
Rene Hurlemann
Benjamin Becker
Keith M. Kendrick
author_sort Yayuan Geng
collection DOAJ
description Accumulating evidence suggests that the neuropeptide oxytocin (OXT) can enhance empathy although it is unclear which specific behavioral and neural aspects are influenced, and whether the effects are modulated by culture, sex, and trait autism. Based on previous findings in Caucasian men, we hypothesized that a single intranasal dose of OXT would specifically enhance emotional empathy (EE) via modulatory effects on the amygdala in an Asian (Chinese) population and explored the modulatory role of sex and trait autism on the effects. We first conducted a double-blind, randomized between-subject design experiment using a modified version of the multifaceted empathy task to determine whether OXT’s facilitation of EE can be replicated in Chinese men (n = 60). To further explore neural mechanisms behind and potential sex differences, functional MRI and skin conductance measures were acquired in an independent experiment incorporating men and women (n = 72). OXT enhanced EE across experiments and sex, an effect that was accompanied by reduced amygdala activity and increased skin conductance responses. On the network level OXT enhanced functional coupling of the right amygdala with the insula and posterior cingulate cortex for positive valence stimuli but attenuated coupling for negative valence stimuli. The effect of OXT on amygdala functional connectivity with the insula was modulated by trait autism. Overall, our findings provide further support for the role of OXT in facilitating EE and demonstrate that effects are independent of culture and sex and involve modulatory effects on the amygdala and its interactions with other key empathy regions.
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spelling doaj.art-81e8349005fe447e9f39174aa1b7e0872022-12-21T17:48:29ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2018-07-011210.3389/fnins.2018.00512390349Oxytocin Enhancement of Emotional Empathy: Generalization Across Cultures and Effects on Amygdala ActivityYayuan Geng0Weihua Zhao1Feng Zhou2Xiaole Ma3Shuxia Yao4Rene Hurlemann5Rene Hurlemann6Benjamin Becker7Keith M. Kendrick8The Clinical Hospital of the Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of the Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of the Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of the Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of the Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation, University of Electronic Science and Technology of China, Chengdu, ChinaDepartment of Psychiatry, University of Bonn, Bonn, GermanyDivision of Medical Psychology, University of Bonn, Bonn, GermanyThe Clinical Hospital of the Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation, University of Electronic Science and Technology of China, Chengdu, ChinaThe Clinical Hospital of the Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation, University of Electronic Science and Technology of China, Chengdu, ChinaAccumulating evidence suggests that the neuropeptide oxytocin (OXT) can enhance empathy although it is unclear which specific behavioral and neural aspects are influenced, and whether the effects are modulated by culture, sex, and trait autism. Based on previous findings in Caucasian men, we hypothesized that a single intranasal dose of OXT would specifically enhance emotional empathy (EE) via modulatory effects on the amygdala in an Asian (Chinese) population and explored the modulatory role of sex and trait autism on the effects. We first conducted a double-blind, randomized between-subject design experiment using a modified version of the multifaceted empathy task to determine whether OXT’s facilitation of EE can be replicated in Chinese men (n = 60). To further explore neural mechanisms behind and potential sex differences, functional MRI and skin conductance measures were acquired in an independent experiment incorporating men and women (n = 72). OXT enhanced EE across experiments and sex, an effect that was accompanied by reduced amygdala activity and increased skin conductance responses. On the network level OXT enhanced functional coupling of the right amygdala with the insula and posterior cingulate cortex for positive valence stimuli but attenuated coupling for negative valence stimuli. The effect of OXT on amygdala functional connectivity with the insula was modulated by trait autism. Overall, our findings provide further support for the role of OXT in facilitating EE and demonstrate that effects are independent of culture and sex and involve modulatory effects on the amygdala and its interactions with other key empathy regions.https://www.frontiersin.org/article/10.3389/fnins.2018.00512/fullamygdalaautismcognitive empathycultureemotional empathyoxytocin
spellingShingle Yayuan Geng
Weihua Zhao
Feng Zhou
Xiaole Ma
Shuxia Yao
Rene Hurlemann
Rene Hurlemann
Benjamin Becker
Keith M. Kendrick
Oxytocin Enhancement of Emotional Empathy: Generalization Across Cultures and Effects on Amygdala Activity
Frontiers in Neuroscience
amygdala
autism
cognitive empathy
culture
emotional empathy
oxytocin
title Oxytocin Enhancement of Emotional Empathy: Generalization Across Cultures and Effects on Amygdala Activity
title_full Oxytocin Enhancement of Emotional Empathy: Generalization Across Cultures and Effects on Amygdala Activity
title_fullStr Oxytocin Enhancement of Emotional Empathy: Generalization Across Cultures and Effects on Amygdala Activity
title_full_unstemmed Oxytocin Enhancement of Emotional Empathy: Generalization Across Cultures and Effects on Amygdala Activity
title_short Oxytocin Enhancement of Emotional Empathy: Generalization Across Cultures and Effects on Amygdala Activity
title_sort oxytocin enhancement of emotional empathy generalization across cultures and effects on amygdala activity
topic amygdala
autism
cognitive empathy
culture
emotional empathy
oxytocin
url https://www.frontiersin.org/article/10.3389/fnins.2018.00512/full
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