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Corresponding author: Robert Liu (robert.liu@emory.edu), Rollins Research Building, Rm. 2006, 1510 Clifton Rd. NE, Atlanta, GA 30322

Elizabeth A. Amadei and Zachary V. Johnson contributed equally to this work.

Author 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.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.K., S.J.R., H.W., A.C.S., V.S. and W.D.M. analyzed data; E.A.A. drafted the manuscript; Z.V.J., A.C.S., Y.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.

We thank Dr. Hans-Peter Lipp for Neurologgers; Dr. Frank Lin for initial testing of Neurologgers; Dr. Joseph Manns, Dr. Gordon Berman and Dr. Teresa Madsen for methodological feedback and fruitful discussions on the manuscript; Gerald Wong for behavioral scoring; Mengqi Zhang, Rasika Tangutoori and Rachel Stanford for assistance with implant design and construction; the Liu, Young and Rainnie laboratories for training, manuscript feedback and helpful discussions; Lorra Matthews and the Yerkes animal care and veterinary staff for vole husbandry and care; Garrett Feldpausch for custom cage design and machining; and Dr. Jamie LaPrairie and Li-Ling Shen for their assistance.

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

The authors declare no competing financial interests.

Subjects:

Research Funding:

This work was funded by an Emory Neuroscience Initiative grant (R.C.L., L.J.Y.), NIMH R21MH97187 (R.C.L.), NIMH P50MH100023 (L.J.Y., R.C.L.), NINDS R90DA033462 (V.S.), Emory University Biology Graduate Student Award (E.A.A.) and Office of Research Infrastructure Programs' Primate centers P51OD11132 (YNPRC).

Keywords:

  • Science & Technology
  • Multidisciplinary Sciences
  • Science & Technology - Other Topics
  • NUCLEUS-ACCUMBENS
  • PARTNER PREFERENCE
  • GAMMA OSCILLATIONS
  • MEMORY FORMATION
  • ROMANTIC LOVE
  • RAT
  • HIPPOCAMPUS
  • FREQUENCY
  • CORTEX
  • PROJECTIONS
  • Motivation
  • Neural circuits
  • Reward
  • Social behaviour
  • Social neuroscience

Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles

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Journal Title:

Nature

Volume:

Volume 546, Number 7657

Publisher:

, Pages 297-301

Type of Work:

Article | Post-print: After Peer Review

Abstract:

Adult pair bonding involves dramatic changes in the perception and valuation of another individual. One key change is that partners come to reliably activate the brain's reward system, 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 bonding, 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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© 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.

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