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Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles

View ORCID ProfileAmélie M. Borie, Sena Agezo, Parker Lunsford, Arjen J. Boender, Ji-Dong Guo, Hong Zhu, Gordon J. Berman, Larry J. Young, Robert C. Liu
doi: https://doi.org/10.1101/2021.07.06.451323
Amélie M. Borie
1Center for Translational Social Neuroscience
2Silvio O. Conte Center for Oxytocin and Social Cognition
3Yerkes National Primate Research Center
4Department of Biology, Emory University
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  • ORCID record for Amélie M. Borie
Sena Agezo
1Center for Translational Social Neuroscience
2Silvio O. Conte Center for Oxytocin and Social Cognition
3Yerkes National Primate Research Center
4Department of Biology, Emory University
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Parker Lunsford
1Center for Translational Social Neuroscience
2Silvio O. Conte Center for Oxytocin and Social Cognition
3Yerkes National Primate Research Center
4Department of Biology, Emory University
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Arjen J. Boender
1Center for Translational Social Neuroscience
2Silvio O. Conte Center for Oxytocin and Social Cognition
3Yerkes National Primate Research Center
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Ji-Dong Guo
1Center for Translational Social Neuroscience
2Silvio O. Conte Center for Oxytocin and Social Cognition
3Yerkes National Primate Research Center
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Hong Zhu
1Center for Translational Social Neuroscience
2Silvio O. Conte Center for Oxytocin and Social Cognition
3Yerkes National Primate Research Center
4Department of Biology, Emory University
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Gordon J. Berman
1Center for Translational Social Neuroscience
3Yerkes National Primate Research Center
4Department of Biology, Emory University
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Larry J. Young
1Center for Translational Social Neuroscience
2Silvio O. Conte Center for Oxytocin and Social Cognition
3Yerkes National Primate Research Center
5Department of Psychiatry and Behavioral Science, Emory University School of Medicine
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  • For correspondence: lyoung03@emory.edu robert.liu@emory.edu
Robert C. Liu
1Center for Translational Social Neuroscience
2Silvio O. Conte Center for Oxytocin and Social Cognition
3Yerkes National Primate Research Center
4Department of Biology, Emory University
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  • For correspondence: lyoung03@emory.edu robert.liu@emory.edu
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Abstract

Social relationships are dynamic and evolve with shared and personal experiences. Whether the functional role of social neuromodulators also evolves with experience to shape the trajectory of relationships is unknown. We utilized pair bonding in the socially monogamous prairie voles as an example of socio-sexual experience that dramatically alters behaviors displayed toward other individuals. We investigated oxytocin-dependent modulation of excitatory synaptic transmission in the nucleus accumbens as a function of pair bonding status. We found that an oxytocin receptor agonist decreases the amplitude of spontaneous Excitatory Postsynaptic Currents (EPSCs) in sexually naive virgin, but not pair-bonded, female voles, while it increases the amplitude of electrically evoked EPSCs in paired voles, but not in virgins. This oxytocin-dependent potentiation of synaptic transmission relies on the de novo coupling between oxytocin receptor signaling and endocannabinoid CB1 receptor signaling in pair bonded voles. Blocking CB1 receptors after pair bond formation increases the occurrence of a specific form of social rejection – defensive upright response – that is displayed towards the partner but not towards a novel individual. Altogether, our results demonstrate that oxytocin’s action in the nucleus accumbens is changed through social experience in a way that regulates the trajectory of social interactions as the relationship with the partner unfolds, potentially promoting the maintenance of a pair bond by inhibiting aggressive responses. These results provide a mechanism by which social experience and context shift oxytocinergic signaling to impact neural and behavioral responses to social cues.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Lead author: Robert C. Liu

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 06, 2021.
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Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles
Amélie M. Borie, Sena Agezo, Parker Lunsford, Arjen J. Boender, Ji-Dong Guo, Hong Zhu, Gordon J. Berman, Larry J. Young, Robert C. Liu
bioRxiv 2021.07.06.451323; doi: https://doi.org/10.1101/2021.07.06.451323
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Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles
Amélie M. Borie, Sena Agezo, Parker Lunsford, Arjen J. Boender, Ji-Dong Guo, Hong Zhu, Gordon J. Berman, Larry J. Young, Robert C. Liu
bioRxiv 2021.07.06.451323; doi: https://doi.org/10.1101/2021.07.06.451323

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