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Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds

Nature Neuroscience volume 9, pages 133–139 (2006)Cite this article

Abstract

The involvement of dopamine within the nucleus accumbens in the formation and maintenance of pair bonds was assessed in a series of experiments using the monogamous prairie vole. We show that dopamine transmission that promotes pair bond formation occurs within the rostral shell of the nucleus accumbens, but not in its core or caudal shell. Within this specific brain region, D1- and D2-like receptor activation produced opposite effects: D1-like activation prevented pair bond formation, whereas D2-like activation facilitated it. After extended cohabitation with a female, male voles showed behavior indicative of pair bond maintenance—namely, selective aggression towards unfamiliar females. These voles also showed a significant upregulation in nucleus accumbens D1-like receptors, and blockade of these receptors abolished selective aggression. Thus, neuroplastic reorganization of the nucleus accumbens dopamine system is responsible for the enduring nature of monogamous pair bonding. Finally, we show that this system may also contribute to species-specific social organization.

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Figure 1: Activation of D2-like receptors within the rostral NAcc shell, but not core, is critical for partner preferences.
Figure 2: Histological verification of injection sites for experiment 1.
Figure 3: D1- and D2-like receptors within rostral NAcc shell have opposing effects on partner-preference formation.
Figure 4: Pair bonded males have significantly more D1-like receptors within the NAcc than do non–pair bonded males.
Figure 5: Blockade of D1-like receptors within the NAcc abolishes monogamous selective aggression.
Figure 6: Species differences in D1-like receptor binding within the NAcc are consistent with species differences in social behavior.

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Acknowledgements

The authors would like to thank F.K. Stephan, M.E. Freeman, K.J. Berkley, R.J. Contreras, C.D. Fowler and M.D. Smeltzer for critical reading of the manuscript and J. Bredesen for technical assistance. This work was supported by US National Institutes of Health grants MH-67396 to B.J.A, HD-40722 to J.T.C, and MH-58616, MH-66734 and DA-19627 to Z.W.

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  1. Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, 32306-1270, Florida, USA

    Brandon J Aragona, Yan Liu, Y Joy Yu, J Thomas Curtis, Jacqueline M Detwiler & Zuoxin Wang

  2. National Institute of Mental Heath, 6001 Executive Boulevard, MSC 9669, Bethesda, 20892-9669, Maryland, USA

    Thomas R Insel

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Correspondence to Brandon J Aragona.

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Aragona, B., Liu, Y., Yu, Y. et al. Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nat Neurosci 9, 133–139 (2006). https://doi.org/10.1038/nn1613

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