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Research Article

Testosterone reduces generosity through cortical and subcortical mechanisms

View ORCID ProfileJianxin Ou, View ORCID ProfileYin Wu, Yang Hu, View ORCID ProfileXiaoxue Gao, Hong Li, and View ORCID ProfilePhilippe N. Tobler
  1. aSchool of Psychology, Shenzhen University, 518060 Shenzhen, China;
  2. bSchool of Psychology, Shanghai University of Sport, Shanghai 200438, China;
  3. cSchool of Psychological and Cognitive Sciences, Peking University, 100871 Beijing, China;
  4. dSchool of Business and Management, Shanghai International Studies University, Shanghai 201620, China;
  5. eSchool of Psychology, South China Normal University, 510631 Guangzhou, China;
  6. fInstitute for Brain and Psychological Sciences, Sichuan Normal University, 610066 Chengdu, China;
  7. gZurich Center for Neuroeconomics, Department of Economics, University of Zurich, 8006 Zürich, Switzerland

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PNAS March 23, 2021 118 (12) e2021745118; https://doi.org/10.1073/pnas.2021745118
Jianxin Ou
aSchool of Psychology, Shenzhen University, 518060 Shenzhen, China;
bSchool of Psychology, Shanghai University of Sport, Shanghai 200438, China;
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  • ORCID record for Jianxin Ou
Yin Wu
aSchool of Psychology, Shenzhen University, 518060 Shenzhen, China;
bSchool of Psychology, Shanghai University of Sport, Shanghai 200438, China;
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  • ORCID record for Yin Wu
  • For correspondence: yinwu0407@gmail.com lihongwrm@vip.sina.com
Yang Hu
cSchool of Psychological and Cognitive Sciences, Peking University, 100871 Beijing, China;
dSchool of Business and Management, Shanghai International Studies University, Shanghai 201620, China;
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Xiaoxue Gao
cSchool of Psychological and Cognitive Sciences, Peking University, 100871 Beijing, China;
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Hong Li
eSchool of Psychology, South China Normal University, 510631 Guangzhou, China;
fInstitute for Brain and Psychological Sciences, Sichuan Normal University, 610066 Chengdu, China;
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  • For correspondence: yinwu0407@gmail.com lihongwrm@vip.sina.com
Philippe N. Tobler
gZurich Center for Neuroeconomics, Department of Economics, University of Zurich, 8006 Zürich, Switzerland
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  1. Edited by Ernst Fehr, University of Zurich, Zurich, Switzerland, and accepted by Editorial Board Member Michael S. Gazzaniga February 4, 2021 (received for review October 17, 2020)

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Significance

Testosterone is associated with aggressive behavior in both animals and humans. Here, we establish a link between increased testosterone and selfishness in economic decision making and identify the neural mechanisms through which testosterone reduces generosity in a double-blind, placebo-controlled, between-participant study. We find that testosterone induces more selfish choices, particularly when distant others are concerned. Moreover, it disrupts the representation of other-regarding value in local activity and functional connectivity involving the temporoparietal junction and subcortical regions involved in reward processing. Our study provides causal evidence for a testosterone-mediated neurohormonal link between generosity and the valuation system.

Abstract

Recent evidence has linked testosterone, a major sex hormone, to selfishness in economic decision-making. Here, we aimed to investigate the neural mechanisms through which testosterone reduces generosity by combining functional MRI with pharmacological manipulation among healthy young males in a double-blind, placebo-controlled, between-subject design. After testosterone or placebo gel administration, participants performed a social discounting task in which they chose between selfish options (benefiting only the participant) and generous options (providing also some benefit to another person at a particular social distance). At the behavioral level, testosterone reduced generosity compared to the placebo. At the neural level (n = 60), the temporoparietal junction (TPJ) encoded the other-regarding value of the generous option during generous choices, and this effect was attenuated by testosterone, suggesting that testosterone reduced the consideration of other’s welfare as underpinned by TPJ activity. Moreover, TPJ activity more strongly reflected individual differences in generosity in the placebo than the testosterone group. Furthermore, testosterone weakened the relation between the other-regarding value of generous decisions and connectivity between the TPJ and a region extending from the insula into the striatum. Together, these findings suggest that a network encompassing both cortical and subcortical components underpins the effects of testosterone on social preferences.

  • altruistic preferences
  • androgen
  • temporoparietal junction
  • prosocial behavior
  • social cognition

Footnotes

  • ↵1J.O. and Y.W. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: yinwu0407{at}gmail.com or lihongwrm{at}vip.sina.com.
  • Author contributions: J.O., Y.W., and P.N.T. designed research; J.O. and Y.W. performed research; J.O., Y.W., Y.H., X.G., H.L., and P.N.T. contributed new reagents/analytic tools; J.O., Y.W., and Y.H. analyzed data; and J.O., Y.W., Y.H., X.G., H.L., and P.N.T. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission. E.F. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2021745118/-/DCSupplemental.

Data Availability

Behavioral data with the analyzed code are available on the Open Science Framework at https://osf.io/mw3tj/.

Published under the PNAS license.

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Testosterone reduces generosity through cortical and subcortical mechanisms
Jianxin Ou, Yin Wu, Yang Hu, Xiaoxue Gao, Hong Li, Philippe N. Tobler
Proceedings of the National Academy of Sciences Mar 2021, 118 (12) e2021745118; DOI: 10.1073/pnas.2021745118

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Testosterone reduces generosity through cortical and subcortical mechanisms
Jianxin Ou, Yin Wu, Yang Hu, Xiaoxue Gao, Hong Li, Philippe N. Tobler
Proceedings of the National Academy of Sciences Mar 2021, 118 (12) e2021745118; DOI: 10.1073/pnas.2021745118
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