Skip to main content

Oxytocin, Vasopressin, and the Neuroendocrine Basis of Pair Bond Formation

  • Chapter
Vasopressin and Oxytocin

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 449))

Abstract

Several lines of evidence support a role for oxytocin and vasopressin in complex social behaviors, including parental care, sex behavior, and aggression. Recent studies in a monogamous mammal, the prairie vole, suggest an additional role for both peptides in the formation of pair bonds. Central administration of oxytocin facilitates and administration of an oxytocin antagonist inhibits partner preference formation in female prairie voles. Conversely, vasopressin facilitates and a V1a receptor antagonist inhibits pair bonding in males. A potential cellular basis for these effects is the species-specific pattern of expression of oxytocin and V1a receptors in reward pathways of the prairie vole brain. At a molecular level, comparative sequencing of the oxytocin and V1a receptors reveals species differences in the promoter sequences that may guide regional expression in the brain. Transgenic mice created with the 5’ flanking region of the prairie vole oxytocin receptor gene demonstrate that sequences in this region influence the pattern of expression within the brain. The unique promoter sequences of the prairie vole OTR and V1a receptor genes and the resulting species-specific pattern of regional expression provide a potential molecular mechanism for the evolution of pair bonding behaviors and a cellular basis for monogamy.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

eBook
USD 9.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  1. du Vigneaud, V., C. Ressler, and S. Trippett 1953 The sequence of amino acids in oxytocin, with a proposal for the structure of oxytocin. J Biol Chem 205:949–957.

    CAS  Google Scholar 

  2. Barberis, C. and E. Tribollet 1996 Vasopressin and oxytocin receptors in the central nervous system. Crit. Rev. Neurobio. 10:119–154.

    Article  CAS  Google Scholar 

  3. Archer, R. 1974 Chemistry of the neurohypophyseal hormones: an example of molecular evolution. In: E. Knobil and W. Sawyer (eds) Handbook of Physiology. American Physiological Society, Washington, D.C., p. 119–130.

    Google Scholar 

  4. Gautvik, K.M., et al. 1996 Overview of the most prevalent hypothalamus-specific mRNAs, as identified by directional tag PCR subtration. Proc. Natl. Acad. Sci. 93:8733–8738.

    Article  PubMed  CAS  Google Scholar 

  5. Insel, T.R., Z. Wang, and C.F. Ferris 1994 Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. Journal of Neuroscience 14:5381–5392.

    PubMed  CAS  Google Scholar 

  6. Insel, T. and L. Shapiro 1992 Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl. Acad. Sci. USA 89:5981–5985.

    Article  PubMed  CAS  Google Scholar 

  7. Insel, T., et al. 1993 Gonadal steroids have paradoxical effects on brain oxytocin receptors. J Neuroendo 5:619–628.

    Article  CAS  Google Scholar 

  8. Argiolas, A. and G.L. Gessa 1991 Central functions of oxytocin. Neurosci Biobeh Rev 15:217–231.

    Article  CAS  Google Scholar 

  9. de Wied, D., M. Diamant, and M. Fodor 1993 Central nervous system effects of the neurohypophyseal hormones and related peptides. Frontiers in Neuroendo. 14:251–302.

    Article  Google Scholar 

  10. Manning, M., et al. 1995 Advances in the design of selective antagonists, potential tocolytics, and radioiodinated ligands for oxytocin receptors. In: R. Nell and J.A. Russell (eds) Oxytocin: Cellular and Molecular Approaches in Medicine and Research. Plenum Press, New York, p. 559–583.

    Google Scholar 

  11. Insel, T. 1992 Oxytocin: a neuropeptide for affiliation-evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendo. 17:3–33.

    Article  CAS  Google Scholar 

  12. Carter, C. 1992 Oxytocin and sexual behavior. Neurosci. Biobehay. Rev. 16:131–144.

    CAS  Google Scholar 

  13. Witt, D. 1995 Oxytocin and dent sociosexual responses: frm behavio to gene expression. Neurosci. Biobeh. Rev. 19:315–324.

    Article  CAS  Google Scholar 

  14. Witt, D.M. and T.R. Insel 1991 A selective oxytocin antagonist attenuates progesterone facilitation of female sexual behavior. Endocrin. 128:3269–3276.

    Article  CAS  Google Scholar 

  15. Wang, Z.X., C.F. Ferris, and G.J. De Vries 1993 The role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc Natl Acad Sci, USA 91:400–404.

    Article  Google Scholar 

  16. Ferris, C. 1992 Role of vasopressin in aggressive and dominant/subordinant behaviors. In: C. Pedersen, et al. (eds) Oxytocin in Maternal, Sexual, and Social Behaviors. New Pork Academy of Sciences Press, New York, p. 212–227.

    Google Scholar 

  17. De Vries, G.J., R.M. Buijs, and A.A. Sluiter 1984 Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain. Br Res 298:141–145.

    Article  Google Scholar 

  18. De Vries, G.J., et al. 1986 Effects of androgens and estrogens on the vasopressin and oxytocin innervation of the adult rat brain. Br Res 399:296–302.

    Article  Google Scholar 

  19. Compaan, J.C., et al. 1993 Differential lateral septal vasopressin in aggressive and nonaggressive mice. Br. Res. Bull. 30:1–6.

    Article  CAS  Google Scholar 

  20. Ferris, C., et al. 1984 Vasopressin injected into the hypothalamus triggers a stereotypic behavior in Golden hamsters. Science 224:521–523.

    Article  PubMed  CAS  Google Scholar 

  21. Argiolas, A., et al. 1989 Penile erection and yawning induced by oxytocin and related peptides: Structure-activity relationship. Peptides 10:559–563.

    Article  PubMed  CAS  Google Scholar 

  22. Pedersen, C.A. and A.J. Prange, Jr 1979 Induction of maternal behaviour in virgin rats after inracerebroventricular administration of oxytocin. Proc Natl Acad Sci USA 76:6661–6665.

    Article  PubMed  CAS  Google Scholar 

  23. Nishimori, K., et al. 1996 Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc. Natl. Acad. Sci. (USA) 93:777–783.

    Article  Google Scholar 

  24. Kleiman, D.G. 1977 Monogamy in mammals. Q. Rev. Biol. 52:39–69.

    Article  PubMed  CAS  Google Scholar 

  25. Dewsbury, D.A. 1988 The comparative psychology of monogamy. In: D.W. Leger (eds) American Zoology Nebraska symposium on motivation. University of Nebraska Press, Lincoln, NE, p. 1–50.

    Google Scholar 

  26. Getz, L.L. and J.E. Hofman 1986 Social organization in free living prairie voles, Microtus ochrogaster. Behay. Ecol. Sociobiol. 18:275–282.

    Article  Google Scholar 

  27. Getz, L.L., C.S. Carter, and L. Gavish 1981 The mating system of the prairie vole Microtus ochrogaster: Field and laboratory evidence for pair bonding. Behay. Ecol. Sociobiol. 8:189–194.

    Article  Google Scholar 

  28. Getz, L., et al. 1993 Social organization of the prairie vole (Microtus ochrogaster). J Mammal. 74:44–58.

    Article  Google Scholar 

  29. Carter, C.S., et al. 1987 Male stimuli are necessary for female sexual behavior and uterine growth in prairie voles (Microtus ochrogaster). Horm Behav 21:74–82.

    Article  PubMed  CAS  Google Scholar 

  30. Carter, C., A. DeVries, and L. Getz 1995 Physiological substrates of mammalian monogamy: The prairie vole model. Neurosci and Biobeh Rev 19:303–314.

    Article  CAS  Google Scholar 

  31. Shapiro, L.E. and D.A. Dewsbury 1990 Differences in affiliative behavior, pair bonding, and vaginal cytology in two species of vole. J. Comp. Psychol. 104:268–274.

    Article  PubMed  CAS  Google Scholar 

  32. Oliveras, D. and M. Novak 1986 A comparison of paternal behavior in the meadow vole, the pine vole, and the prairie vole. Anim. Behay. 34:519–526.

    Article  Google Scholar 

  33. McGuire, B. and M. Novak 1984 A comparison of maternal behavior in the meadow vole, prairie vole, and pine vole. Anim. Behay. 32:1132–1141.

    Article  Google Scholar 

  34. Shapiro, L.E. and T.R. Insel 1990 Infant’s response to social separation reflects adult differences in affiliative behavior: A comparative developmental study in prairie and montane voles. Dev Psychobiol 23:375–394.

    Article  PubMed  CAS  Google Scholar 

  35. McGuire, B. 1986 Parental care and its relationship to social organization in the montane vole (Microtus montanus). J. Mammology 67:305–311.

    Article  Google Scholar 

  36. Jannett, F.J. 1980 Social dynamics in the montane vole Microtus montanus as a paradigm. The Biologist 62:3–19.

    Google Scholar 

  37. Jannett, F. 1982 The nesting patterns of adult voles (Microtus montanus) in field populations. J. Mammology 63:495–498.

    Article  Google Scholar 

  38. Williams, J., K. Catania, and C. Carter 1992 Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Homi. Beh. 26:339–349.

    Article  CAS  Google Scholar 

  39. Murphy, M.R., et al. 1987 Changes in oxytocin and vasopressin secretion during sexual activity in men. J Clin Endocrinol Metab 65:738–741.

    Article  PubMed  CAS  Google Scholar 

  40. Kendrick, K.M., et al. 1988 Microdialysis measurement of oxytocin, aspartate, GABA and glutamate release from the olfactory bulb of sheep during vaginocervical stimulation. Br Res 442:171–177.

    Article  CAS  Google Scholar 

  41. Hughes, A.M., et al. 1987 Oxytocin in the central nervous system and sexual behavior in male rats. Br Res 414:133–137.

    Article  CAS  Google Scholar 

  42. Insel, T.R., S..Preston, and J.T. Winslow 1995 Mating in the monogamous male: Behavioral consequences. Physio and Beh. 57:615–627.

    Article  CAS  Google Scholar 

  43. Insel, T.R. and T.J. Hulihan 1995 A gender specific mechanism for pair bonding: oxytocin and partner preference formation in monogamous voles. Behavioral Neuroscience 109:782–789.

    Article  PubMed  CAS  Google Scholar 

  44. Winslow, J., et al. 1993 A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365:545–548.

    Article  PubMed  CAS  Google Scholar 

  45. Williams, J., et al. 1994 Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J Neuroendo 6:247–250.

    Article  CAS  Google Scholar 

  46. Winslow, J., et al. 1993 Oxytocin and complex social behaviors: species comparisons. Psychopharm. Bull. 29:409–414.

    CAS  Google Scholar 

  47. Young, L.J., et al. 1997 Species differences in Via receptor gene expression in monogamous and non-monogamous voles: Behavioral consequences. Behavioral Neuroscience 111:599–605.

    Article  PubMed  CAS  Google Scholar 

  48. Wang, Z.X., et al. 1996 Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: A quantitative comparative study. J Comp Neurol 366:726–737.

    Article  PubMed  CAS  Google Scholar 

  49. Young, L.J., et al. 1996 Species differences in central oxytocin receptor gene expression: Comparative analysis of promoter sequences. Journal of Neuroendocrinology 8:777–783.

    Article  PubMed  CAS  Google Scholar 

  50. Young, L.J., et al. 1997 Gene targeting approaches to neuroendocrinology: Oxytocin, maternal behavior, and affiliation. Hormones and Behavior 31:221–231.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1998 Springer Science+Business Media New York

About this chapter

Cite this chapter

Insel, T.R., Winslow, J.T., Wang, Z., Young, L.J. (1998). Oxytocin, Vasopressin, and the Neuroendocrine Basis of Pair Bond Formation. In: Zingg, H.H., Bourque, C.W., Bichet, D.G. (eds) Vasopressin and Oxytocin. Advances in Experimental Medicine and Biology, vol 449. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-4871-3_28

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-4871-3_28

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-7210-3

  • Online ISBN: 978-1-4615-4871-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics