Letter | Published:

Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles

Nature volume 546, pages 297301 (08 June 2017) | Download Citation

Abstract

Adult pair bonding involves dramatic changes in the perception and valuation of another individual1. One key change is that partners come to reliably activate the brain’s reward system2,3,4,5,6, although the precise neural mechanisms by which partners become rewarding during sociosexual interactions leading to a bond remain unclear. Here we show, using a prairie vole (Microtus ochrogaster) model of social bonding7, how a functional circuit from the medial prefrontal cortex to nucleus accumbens is dynamically modulated to enhance females’ affiliative behaviour towards a partner. Individual variation in the strength of this functional connectivity, particularly after the first mating encounter, predicts how quickly animals begin affiliative huddling with their partner. Rhythmically activating this circuit in a social context without mating biases later preference towards a partner, indicating that this circuit’s activity is not just correlated with how quickly animals become affiliative but causally accelerates it. These results provide the first dynamic view of corticostriatal activity during bond formation, revealing how social interactions can recruit brain reward systems to drive changes in affiliative behaviour.

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Acknowledgements

We thank H.-P. Lipp for Neurologgers; F. Lin for initial testing of Neurologgers; J. Manns, G. Berman, and T. Madsen for methodological feedback and discussions on the manuscript; G. Wong for behavioural scoring; M. Zhang, R. Tangutoori, and R. Stanford for assistance with implant design and construction; the members of the Liu, Young and Rainnie laboratories for training, manuscript feedback, and discussions; L. Matthews and the Yerkes animal care and veterinary staff for vole husbandry and care; G. Feldpausch for custom cage design and machining; and J. LaPrairie and L.-L. Shen for assistance. This work was funded by an Emory Neuroscience Initiative grant (R.C.L., L.J.Y.), National Institute of Mental Health (NIMH) R21MH97187 (R.C.L.), NIMH P50MH100023 (L.J.Y., R.C.L.), National Institute of Neurological Disorders and Stroke R90 DA033462 (V.S.), Emory University Biology Graduate Student Award (E.A.A.), and Office of Research Infrastructure Programs’ Primate centers P51OD11132 (YNPRC).

Author information

Author notes

    • Elizabeth A. Amadei
    •  & Zachary V. Johnson

    These authors contributed equally to this work.

Affiliations

  1. Silvio O. Conte Center for Oxytocin and Social Cognition, Center for Translational Social Neuroscience, Emory University, Atlanta, Georgia 30322, USA

    • Elizabeth A. Amadei
    • , Zachary V. Johnson
    • , Yong Jun Kwon
    • , Wittney D. Mays
    • , Steven J. Ryan
    • , Hasse Walum
    • , Donald G. Rainnie
    • , Larry J. Young
    •  & Robert C. Liu
  2. Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, Georgia 30332, USA

    • Elizabeth A. Amadei
  3. Department of Biology, Emory University, Atlanta, Georgia 30322, USA

    • Elizabeth A. Amadei
    • , Yong Jun Kwon
    • , Aaron C. Shpiner
    • , Varun Saravanan
    • , Wittney D. Mays
    •  & Robert C. Liu
  4. Graduate Program in Neuroscience, Emory University, Atlanta, Georgia 30322, USA

    • Zachary V. Johnson
    • , Yong Jun Kwon
    • , Varun Saravanan
    • , Larry J. Young
    •  & Robert C. Liu
  5. Yerkes National Primate Research Center (YNPRC), Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, Georgia 30322, USA

    • Zachary V. Johnson
    • , Steven J. Ryan
    • , Hasse Walum
    • , Donald G. Rainnie
    •  & Larry J. Young
  6. Undergraduate Program in Neuroscience and Behavioral Biology, Emory University, Atlanta, Georgia 30322, USA

    • Aaron C. Shpiner

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Contributions

E.A.A. adapted the Neurologger to a vole preparation and designed and performed in vivo electrophysiology experiments, which motivated an optogenetics approach; optogenetics experiments were designed and performed by E.A.A. and Z.V.J., assisted by Y.J.K.; Z.V.J. validated viral techniques and performed optogenetics surgeries and histology; S.J.R. and E.A.A. designed slice electrophysiology experiments; Z.V.J. performed all surgeries and histology for slice electrophysiology experiments; S.J.R. performed slice electrophysiology experiments, assisted and supervised by E.A.A. and D.G.R., respectively. E.A.A., Z.V.J., Y.J.K., S.J.R., H.W., A.C.S., V.S., and W.D.M. analysed data; E.A.A. drafted the manuscript; Z.V.J., A.C.S., Y.J.K., S.J.R., H.W., and V.S. contributed to the writing; R.C.L. and L.J.Y. edited the manuscript and supervised all aspects of the study.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Robert C. Liu.

Reviewer Information Nature thanks R. Fernald and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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DOI

https://doi.org/10.1038/nature22381

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