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.

  • Letter
  • Published:

Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole

Abstract

Arginine vasopressin influences male reproductive and social behaviours in several vertebrate taxa1 through its actions at the V1a receptor in the brain. The neuroanatomical distribution of vasopressin V1a receptors varies greatly between species with different forms of social organization2,3. Here we show that centrally administered arginine vasopressin increases affiliative behaviour in the highly social, monogamous prairie vole, but not in the relatively asocial, promiscuous montane vole. Molecular analyses indicate that gene duplication and/or changes in promoter structure of the prairie vole receptor gene may contribute to the species differences in vasopressin-receptor expression. We further show that mice that are transgenic for the prairie vole receptor gene have a neuroanatomical pattern of receptor binding that is similar to that of the prairie vole, and exhibit increased affiliative behaviour after injection with arginine vasopressin. These data indicate that the pattern of V1a-receptor gene expression in the brain may be functionally associated with species-typical social behaviours in male vertebrates.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Montane and prairie voles differ both in V1a-receptor binding pattern and behavioural response to arginine vasopressin.
Figure 2: Structure of the V1a-receptor gene in voles V1a-receptor genes from montane vole (M. mon) and prairie vole (M. och) were isolated from genomic DNA libraries.
Figure 3: The pattern of V1a-receptor binding of mice that are transgenic for the V1a-receptor gene from the prairie vole is similar to that of the prairie vole.
Figure 4: Behavioural response to AVD in transgenic mice.

Similar content being viewed by others

References

  1. Young, L. J., Wang, Z. & Insel, T. R. Neuroendocrine bases of monogamy. Trends Neurosci. 21, 71–75 (1998).

    Article  CAS  PubMed  Google Scholar 

  2. Bester-Meredith, J. K., Young, L. J. & Marler, C. A. Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm. Behav.(in the press).

  3. Insel, T. R., Wang, Z. & Ferris, C. F. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 14, 5381–5392 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ritters, L. V. & Panksepp, J. Effects of vastotocin on aggressive behavior in male Japanese quail. Ann. NY Acad. Sci. 807, 478–480 (1997).

    Article  ADS  Google Scholar 

  5. Ferris, C. F. et al. Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in gold hamsters. J. Neurosci. 17, 4331–4340 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Young, L. J., Winslow, J. T., Nilsen, R. & Insel, T. R. Species differences in V1areceptor gene expression in monogamous and non-monogamous voles: behavioral consequences. Behav. Neurosci. 111, 599–605 (1997).

    Article  CAS  PubMed  Google Scholar 

  7. Moore, F. L. & Miller, L. J. Arginine vasotocin induces sexual behavior of newts by acting on cells in the brain. Peptides 4, 97–102 (1983).

    Article  CAS  PubMed  Google Scholar 

  8. Winslow, J., Hastings, N., Carter, C. S., Harbaugh, C. & Insel, T. Arole for central vasopressin in pair bonding in monogamous prairie voles. Nature 365, 545–548 (1993).

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Ferris, C. F. & Potegal, M. Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters. Physiol. Behav. 44, 235–239 (1988).

    Article  CAS  PubMed  Google Scholar 

  10. Barberis, C. & Tribollet, E. Vasopressin and oxytocin receptors in the central nervous system. Crit. Rev. Neurobiol. 10, 119–154 (1996).

    Article  CAS  PubMed  Google Scholar 

  11. Shapiro, L. E. & Dewsbury, D. A. Differences in affiliative behavior, pair bonding, and vaginal cytology in two species of vole (Microtus ochrogaster and M. montanus). J. Comp. Psychol. 104, 268–274 (1990).

    Article  PubMed  Google Scholar 

  12. Bamshad, M., Novak, M. & DeVries, G. J. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles. Physiol. Behav. 56, 751–758 (1994).

    Article  CAS  PubMed  Google Scholar 

  13. Wang, Z., Smith, W., Major, D. E. & De Vries, G. J. Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus and stria terminalis in prairie voles (Microtus orchogaster) and meadow voles (Microtus pennsylvanicus). Brain Res. 650, 212–218 (1994).

    Article  CAS  PubMed  Google Scholar 

  14. Wang, Z., Ferris, C. F. & De Vries, G. J. Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc. Natl Acad. Sci. USA 91, 400–404 (1994).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  15. Choong, C. S., Kemppainen, J. A., Zhou, Z. & Wilson, E. M. Reduced androgen receptor gene expression with first exon CAG repeat expansion. Mol. Endrocrinol. 10, 1527–1535 (1997).

    Google Scholar 

  16. Klesert, T. R., Otten, A. D., Bird, T. D. & Tapscott, S. J. Trinucleotide repeat expansion at the myotonin dystrophy locus reduces expression of DMAHP. Nature Genet. 16, 402–406 (1997).

    Article  CAS  PubMed  Google Scholar 

  17. Meloni, R., Albanése, V., Ravassard, P., Treilhou, F. & Mallet, J. Atetranucleotide polymoric microsatellite, located in the first intron of the tyrosine hydroxylase gene, acts as a transcription regulatory element in vitro. Hum. Mol. Gen. 7, 423–428 (1998).

    Article  CAS  PubMed  Google Scholar 

  18. Barberis, C. et al. Characterization of a novel, linear radioiodinated vasopressin antagonist: an excellent radioligand for vasopressin V1areceptors. Neuroendocrinol. 62, 135–146 (1995).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the NIMH and NCRR to L.J.Y. and T.R.I.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roger Nilsen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Young, L., Nilsen, R., Waymire, K. et al. Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400, 766–768 (1999). https://doi.org/10.1038/23475

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/23475

This article is cited by

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