Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A role for central vasopressin in pair bonding in monogamous prairie voles

Abstract

MONOGAMOUS social organization is characterized by selective affiliation with a partner, high levels of paternal behaviour and, in many species, intense aggression towards strangers for defence of territory, nest and mate1,2. Although much has been written about the evolutionary causes of monogamy, little is known about the proximate mechanisms for pair bonding in monogamous mammals2,3. The prairie vole, Microtus ochrogaster, is a monogamous, biparental rodent which exhibits long-term pair bonds characterized by selective affiliation (partner preference) and aggression4,5. Here we describe the rapid development of both selective aggression and partner preferences following mating in the male of this species. We hypothesized that either argininevasopressin (AVP) or oxytocin (OT), two nine-amino-acid neuropeptides with diverse forebrain projections, could mediate the development of selective aggression and affiliation. This hypothesis was based on the following observations: (1) monogamous and polygamous voles differ specifically in the distribution of forebrain AVP and OT receptors6,7; (2) AVP innervation in the prairie vole brain is sexually dimorphic and important for paternal behaviour8; (3) central AVP pathways have been previously implicated in territorial displays and social memory9,10; and (4) central OT pathways have been previously implicated in affiliative behaviours11. We now demonstrate that central AVP is both necessary and sufficient for selective aggression and partner preference formation, two critical features of pair bonding in the monogamous prairie vole.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Kleiman, D. G. Q. Rev. Biol. 52, 39–69 (1977).

    CAS  Article  Google Scholar 

  2. 2

    Cutton-Brock, T. H. Proc. R. Soc. Lond. 236, 339–372 (1989).

    ADS  Article  Google Scholar 

  3. 3

    Dewsbury, D. A. in American Zoology Nebraska Symposium on Motivation (ed. Leger, D. W.) 1–50 (Univ. Nebraska Press, Lincoln, 1988).

    Google Scholar 

  4. 4

    Getz, L. L., Carter, C. S. & Gavish, L. Behav. Ecol. Sociobiol. 8, 189–194 (1981).

    Article  Google Scholar 

  5. 5

    Carter, C. S., Getz, L. L. & Cohen-Parsons, M. in Advances in the Study of Behavior (eds Rosenblatt, J. S., Beer, C., Busnel, M. C. & Slater, P. J. B.) 109–145 (Academic, New York, 1986).

    Book  Google Scholar 

  6. 6

    Insel, T. & Shapiro, L. Proc. natn. Acad. Sci. U.S.A. 89, 5981–5985 (1992).

    ADS  CAS  Article  Google Scholar 

  7. 7

    Insel, T. R. et al. Regul. Peptides 45, 127–131 (1993).

    CAS  Article  Google Scholar 

  8. 8

    Bamshad, M., Novak, M. & deVries, G. J. Neuroendocr. 5, 247–256 (1993).

    CAS  Article  Google Scholar 

  9. 9

    Ferris, C. F., Albers, H. E., Wesolowski, S. M. & Goldman, B. D. Science 224, 521–523 (1984).

    ADS  CAS  Article  Google Scholar 

  10. 10

    Dantzer, R., Bluthe, R.-M., Koob, G. F. & Le Moal, M. Psychopharmacology 91, 363–368 (1987).

    CAS  Article  Google Scholar 

  11. 11

    Insel, T. R. Psychoneuroendocrinology 17, 3–33 (1992).

    CAS  Article  Google Scholar 

  12. 12

    Miczek, K. A. & Winslow, J. T. in Experimental Psychopharmacology (eds Greenshaw, A. J. & Dourish, C. T.) 27–113 (Humana, Clifton, New Jersey, 1987).

    Google Scholar 

  13. 13

    Williams, J. R., Catania, K. C. & Carter, C. S. Horm. Behav. 26, 339 (1992).

    CAS  Article  Google Scholar 

  14. 14

    Jannett, F. J. Biologist 62, 3–19 (1980).

    Google Scholar 

  15. 15

    Jones, P. M. & Robinson, I. C. A. F. Neuroendocrinology 34, 297–302 (1982).

    CAS  Article  Google Scholar 

  16. 16

    Roche, K. E. & Lesnner, A. I. Science 204, 1343–1344 (1979).

    ADS  CAS  Article  Google Scholar 

  17. 17

    Compaan, J. C., Buijs, R. M., Pool, C. W., de Ruiter, A. J. H. & Koolhaas, J. M. Br. Res. Bull. 30, 1–6 (1993).

    CAS  Article  Google Scholar 

  18. 18

    De Wied, D., Elands, J. & Kovaks, G. Proc. natn. Acad. Sci. U.S.A. 88, 1494–1498 (1991).

    ADS  CAS  Article  Google Scholar 

  19. 19

    Hughes, A. M., Everitt, B. J., Lightman, S. L. & Todd, K. Br. Res. 414, 133–137 (1987).

    CAS  Article  Google Scholar 

  20. 20

    Bamshad, M., Novak, M. & deVries, G. Soc. Neurosci. Abstr. 18, 152.10 (Soc. for Neuroscience, Anaheim, California, 1992).

    Google Scholar 

  21. 21

    Murphy, M. R., Seckl, J. R., Burton, S., Checkley, S. A. & Lightman, S. L. J. clin. Endocr. Metab. 65, 738–741 (1987).

    CAS  Article  Google Scholar 

  22. 22

    Pierce, J. D. J., Pellis, V. C., Dewsbury, D. A. & Pellis, S. M. Aggressive Behav. 17, 337–349 (1991).

    Article  Google Scholar 

  23. 23

    Elands, J. et al. Eur. J. Pharmac. 147, 197–207 (1987).

    Article  Google Scholar 

  24. 24

    Kruszynski, M. et al. J. med. Chem. 23, 364 (1980).

    CAS  Article  Google Scholar 

  25. 25

    Ferris, C. F., Singer, E. A., Meenan, D. M. & Albers, H. E. Eur. J. Pharmac. 154, 153–159 (1988).

    CAS  Article  Google Scholar 

  26. 26

    Witt, D. M. & Insel, T. R. Endocrinology 128, 3269–3276 (1991).

    CAS  Article  Google Scholar 

  27. 27

    Popick, F. R. Life Sci. 18, 197–204 (1975).

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Winslow, J., Hastings, N., Carter, C. et al. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365, 545–548 (1993). https://doi.org/10.1038/365545a0

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing