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Brain Imaging and Behavior

, Volume 9, Issue 4, pp 754–764 | Cite as

Oxytocin and vasopressin effects on the neural response to social cooperation are modulated by sex in humans

  • Chunliang Feng
  • Patrick D. Hackett
  • Ashley C. DeMarco
  • Xu Chen
  • Sabrina Stair
  • Ebrahim Haroon
  • Beate Ditzen
  • Giuseppe Pagnoni
  • James K. Rilling
Original Research

Abstract

Recent research has examined the effects of oxytocin (OT) and vasopressin (AVP) on human social behavior and brain function. However, most participants have been male, while previous research in our lab demonstrated sexually differentiated effects of OT and AVP on the neural response to reciprocated cooperation. Here we extend our previous work by significantly increasing the number of participants to enable the use of more stringent statistical thresholds that permit more precise localization of OT and AVP effects in the brain. In a double-blind, placebo-controlled study, 153 men and 151 women were randomized to receive 24 IU intranasal OT, 20 IU intranasal AVP or placebo. Afterwards, they were imaged with fMRI while playing an iterated Prisoner’s Dilemma Game with same-sex partners. Sex differences were observed for effects of OT on the neural response to reciprocated cooperation, such that OT increased the caduate/putamen response among males, whereas it decreased this response among females. Thus, 24 IU OT may increase the reward or salience of positive social interactions among men, while decreasing their reward or salience among women. Similar sex differences were also observed for AVP effects within bilateral insula and right supramarginal gyrus when a more liberal statistical threshold was employed. While our findings support previous suggestions that exogenous nonapeptides may be effective treatments for disorders such as depression and autism spectrum disorder, they caution against uniformly extending such treatments to men and women alike.

Keywords

Oxytocin Vasopressin fMRI Cooperation Sex differences 

Notes

Acknowledgments

We thank Susan Rogers, Jianguo Xu and Larry Young for assistance with various aspects of this study. This study was supported by National Institute of Mental Health [grant number R01 MH084068-01A1] and the National Center for Advancing Translational Sciences of the National Institutes of Health under Award Number UL1TR000454. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Conflict of interest

Chunliang Feng, Patrick D. Hackett, Ashley C. DeMarco, Xu Chen, Sabrina Stair, Ebrahim Haroon, Beate Ditzen, Giuseppe Pagnoni and James K. Rilling declare that they have no conflict of interest.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from all subjects for being included in the study.

Supplementary material

11682_2014_9333_MOESM1_ESM.doc (1.4 mb)
ESM 1 (DOC 1.38 mb)

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Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Chunliang Feng
    • 1
  • Patrick D. Hackett
    • 1
  • Ashley C. DeMarco
    • 6
  • Xu Chen
    • 1
    • 2
  • Sabrina Stair
    • 2
  • Ebrahim Haroon
    • 2
  • Beate Ditzen
    • 2
    • 3
    • 7
  • Giuseppe Pagnoni
    • 8
  • James K. Rilling
    • 1
    • 2
    • 3
    • 4
    • 5
    • 9
  1. 1.Department of AnthropologyEmory UniversityAtlantaUSA
  2. 2.Department of Psychiatry and Behavioral SciencesEmory UniversityAtlantaUSA
  3. 3.Center for Behavioral NeuroscienceEmory UniversityAtlantaUSA
  4. 4.Yerkes National Primate Research CenterEmory UniversityAtlantaUSA
  5. 5.Center for Translational Social NeuroscienceEmory UniversityAtlantaUSA
  6. 6.Department of PsychologyUniversity of KansasLawrenceUSA
  7. 7.Department of PsychologyUniversity of ZurichZurichSwitzerland
  8. 8.Department of Neural, Biomedical, and Metabolic SciencesUniversity of Modena and Reggio EmiliaModenaItaly
  9. 9.Department of Anthropology, Department of Psychiatry and Behavioral SciencesEmory UniversityAtlantaUSA

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