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.
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Young, L. J., Wang, Z. & Insel, T. R. Neuroendocrine bases of monogamy. Trends Neurosci. 21, 71–75 (1998).
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).
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).
Ritters, L. V. & Panksepp, J. Effects of vastotocin on aggressive behavior in male Japanese quail. Ann. NY Acad. Sci. 807, 478–480 (1997).
Ferris, C. F. et al. Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in gold hamsters. J. Neurosci. 17, 4331–4340 (1997).
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).
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).
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).
Ferris, C. F. & Potegal, M. Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters. Physiol. Behav. 44, 235–239 (1988).
Barberis, C. & Tribollet, E. Vasopressin and oxytocin receptors in the central nervous system. Crit. Rev. Neurobiol. 10, 119–154 (1996).
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).
Bamshad, M., Novak, M. & DeVries, G. J. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles. Physiol. Behav. 56, 751–758 (1994).
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).
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).
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).
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).
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).
Barberis, C. et al. Characterization of a novel, linear radioiodinated vasopressin antagonist: an excellent radioligand for vasopressin V1areceptors. Neuroendocrinol. 62, 135–146 (1995).
This work was supported by grants from the NIMH and NCRR to L.J.Y. and T.R.I.
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