Review Article | Published:

The neurobiology of pair bonding

Nature Neuroscience volume 7, pages 10481054 (2004) | Download Citation

Subjects

Abstract

A neurobiological model for pair-bond formation has emerged from studies in monogamous rodents. The neuropeptides oxytocin and vasopressin contribute to the processing of social cues necessary for individual recognition. Mesolimbic dopamine is involved in reinforcement and reward learning. Concurrent activation of neuropeptide and dopamine receptors in the reward centers of the brain during mating results in a conditioned partner preference, observed as a pair bond. Differential regulation of neuropeptide receptor expression may explain species differences in the ability to form pair bonds. These and other studies discussed here have intriguing implications for the neurobiology of social attachment in our own species.

Access optionsAccess 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.

    , , & Multi-male mating by paired and unpaired female prairie voles (Microtus ochrogaster). Behaviour 139, 1147–1160 (2002).

  2. 2.

    Monogamy in mammals. Q. Rev. Biol. 52, 39–69 (1977).

  3. 3.

    & The neurobiology of attachment. Nat. Rev. Neurosci. 2, 129–136 (2001).

  4. 4.

    , & Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci. Biobehav. Rev. 19, 303–314 (1995).

  5. 5.

    , & Mating in the monogamous male: behavioral consequences. Physiol. Behav. 57, 615–627 (1995).

  6. 6.

    et al. Enhanced partner preference in promiscuous species by manipulating the expression of a single gene. Nature 429, 754–757 (2004).

  7. 7.

    & Parental behavior in voles. Adv. Study Behav. 25, 361–384 (1996).

  8. 8.

    & Prairie-vole partnerships. Am. Sci. 84, 56–62 (1996).

  9. 9.

    , & Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm. Behav. 26, 339–349 (1992).

  10. 10.

    et al. Neural control of maternal behavior and olfactory recognition of offspring. Brain Res. Bull. 44, 383–395 (1997).

  11. 11.

    & Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res. Rev. 35, 246–265 (2001).

  12. 12.

    , , , & Vasopressin injected into the hypothalamus triggers a stereotypic behavior in golden hamsters. Science 224, 521–523 (1984).

  13. 13.

    , , & Oxytocin administered centrally facilitates formation of a partner preference in prairie voles (Microtus ochrogaster). J. Neuroendocrinol. 6, 247–250 (1994).

  14. 14.

    , , & & A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365, 545–548 (1993).

  15. 15.

    & A gender-specific mechanism for pair bonding: Oxytocin and partner preference formation in monogamous voles. Behav. Neurosci. 109, 782–789 (1995).

  16. 16.

    , , & The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav. Neurosci. 113, 1071–1079 (1999).

  17. 17.

    & Peripheral pulses of oxytocin increase partner preferences in female, but not male, prairie voles. Horm. Behav. 37, 49–56 (2000).

  18. 18.

    & Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster). Behav. Neurosci. 117, 854–859 (2003).

  19. 19.

    , , & Stress has sexually dimorphic effects on pair bonding in prairie voles. Proc. Natl. Acad. Sci. USA 93, 11980–11984 (1996).

  20. 20.

    , , & Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone. Proc. Natl. Acad. Sci. USA 92, 7744–7748 (1995).

  21. 21.

    , , , & Corticotropin-releasing factor induces social preferences in male prairie voles. Psychoneuroendocrinology 27, 705–714 (2002).

  22. 22.

    & Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl. Acad. Sci. USA 89, 5981–5985 (1992).

  23. 23.

    , & Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 14, 5381–5392 (1994).

  24. 24.

    , , & Cellular mechanisms of social attachment. Horm. Behav. 40, 133–148 (2001).

  25. 25.

    & Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience 125, 35–45 (2004).

  26. 26.

    , & Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behav. Neurosci. 115, 910–919 (2001).

  27. 27.

    Brain reward circuitry: insights from unsensed incentives. Neuron 36, 229–240 (2002).

  28. 28.

    , , , & Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41, 89–125 (1991).

  29. 29.

    , , & Topography and functional role of dopaminergic projection from the ventral messencephallic tegmentum to the ventral pallidum. Neuroscience 50, 371–386 (1992).

  30. 30.

    & The functional output of the mesolimbic dopamine system. Ann. N.Y. Acad. Sci. 537, 216–227 (1988).

  31. 31.

    , & The circuitry mediating the translation of motivational stimuli into adaptive motor responses. in Limbic Motor Circuits and Neuropsychiatry (eds. Kalivas, P.W. & Barnes, C.D.) 237–288 (CRC Press, Boca Raton, Florida, USA, 1993).

  32. 32.

    Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav. Brain Res. 137, 75–114 (2002).

  33. 33.

    & The neurobiology of drug addiction. J. Neuropsychiatry Clin. Neurosci. 9, 482–497 (1997).

  34. 34.

    & The neuroscience of natural rewards: relevance to addictive drugs. J. Neurosci. 22, 3306–3311 (2002).

  35. 35.

    , & The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat. J. Neurosci. 21, 3236–3241 (2001).

  36. 36.

    et al. Sexual behavior enhances central dopamine transmission in the male rat. Brain Res. 530, 345–348 (1990).

  37. 37.

    Is social attachment an addictive disorder. Physiol. Behav. 79, 351–357 (2003).

  38. 38.

    & Sexual behavior regulated (paced) by the female induces conditioned place preference. Behav. Neurosci. 111, 123–128 (1997).

  39. 39.

    Sexual motivation: a neural and behavioral analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci. Biobehav. Rev. 14, 217–232 (1990).

  40. 40.

    & Role of dopamine in anticipitory and consummatory measures of sexual behavior in the male rat. Behav. Neurosci. 105, 727–743 (1991).

  41. 41.

    , , , & Opposite modulation of social attachment by D1- and D2-type dopamine receptor activation in nucleus accumbens shell. Horm. Behav. 44, 37 (2003).

  42. 42.

    , , , & A critical role for nucleus accumbens dopamine in partner preference formation of male prairie voles. J. Neurosci. 23, 3483–3490 (2003).

  43. 43.

    , , , & Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster). Behav. Neurosci. 114, 173–183 (2000).

  44. 44.

    & Nucleus accumbens dopamine and oxytocin interact to regulate pair bond formation in female prairie voles. Neuroscience 121, 537–544 (2003).

  45. 45.

    et al. Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J. Neurosci. 21, 7392–7396 (2001).

  46. 46.

    , & Oxytocin and addiction: a review. Psychoneuroendocrinology 23, 945–962 (1998).

  47. 47.

    & Influence of exogenously administered oxytocin on central noradrenaline, dopamine and serotonin levels following psychological stress in nulliparous female rats (Rattus norvegicus). Int. J. Neurosci. 45, 221–229 (1989).

  48. 48.

    , & Apomorphine increases plasma oxytocin concentration in male rats. Neurosci. Lett. 98, 351–355 (1989).

  49. 49.

    , & The neuroendocrine basis of social recognition. Front. Neuroendocrinol. 23, 200–224 (2002).

  50. 50.

    , , , & Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 25, 284–288 (2000).

  51. 51.

    , , & Oxytocin in the medial amygdala is essential for social recognition in the mouse. J. Neurosci. 21, 8278–8285 (2001).

  52. 52.

    & Differential modulation of lateral septal vasopressin receptor blockade in spatial-learning, social recognition, and anxiety-related behaviors in rats. Behav. Brain Res. 99, 7–16 (1999).

  53. 53.

    et al. V1 vasopressin receptor antisense oligodeoxynucleotide into septum reduces vasopressin binding, social discrimination abilities and anxiety-related behavior in rats. J. Neurosci. 15, 4250–4258 (1995).

  54. 54.

    et al. Viral vector mediated gene transfer of the vole V1a vasopressin receptor in the rat septum: improved social discrimination and affiliative behavior. Eur. J. Neurosci. 18, 403–411 (2003).

  55. 55.

    , , , & Profound impairment in social recognition and reduction in anxiety in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29, 483–493 (2004).

  56. 56.

    & Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res. Bull. 44, 397–407 (1997).

  57. 57.

    & The origin of vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Res. 273, 307–317 (1983).

  58. 58.

    , , & Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: a quantitative comparative study. J. Comp. Neurol. 366, 726–737 (1996).

  59. 59.

    , , & Cerebrospinal fluid levels of acetylcholinesterase, monoamines and oxytocin during labor, parturition, vaginocervical stimulation, lamb separation and suckling in sheep. Neuroendocrinology 44, 149–156 (1986).

  60. 60.

    , & Conditioning and sexual behavior: a review. Horm. Behav. 40, 291–321 (2001).

  61. 61.

    , , , & Increased affiliative response to vasopressin in mice expressing the vasopressin receptor from a monogamous vole. Nature 400, 766–768 (1999).

  62. 62.

    , , & Microsatellites within genes: structure, function, and evolution. Mol. Biol. Evol. 21, 991–1007 (2004).

  63. 63.

    et al. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527–1531 (1996).

  64. 64.

    , , , & The dopamine transporter gene (SLC6A3) variable number of tandem repeats domain enhances transcription in dopamine neurons. J. Neurochem. 79, 1033–1038 (2001).

  65. 65.

    & Functional microsatellite polymorphisms associated with divergent social structure in vole species. Mol. Biol. Evol. 21, 1057–1063 (2004).

  66. 66.

    et al. Examination of AVPR1a as an autism susceptibility gene. Mol. Psychiatry published online (2004).

  67. 67.

    et al. Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol. Psychiatry 7, 503–507 (2002).

  68. 68.

    et al. Plasma oxytocin increases in the human sexual response. J. Clin. Endocrinol. Metab. 64, 27–31 (1987).

  69. 69.

    , , , & Changes in oxytocin and vasopressin secretion during sexual activity in men. J. Clin. Endocrinol. Metab. 65, 738–741 (1987).

  70. 70.

    , , , & Effect of nipple stimulation on uterine activity and on plasma levels of oxytocin in full term, healthy, pregnant women. Acta Obstet. Gynaecol. Scand. 68, 205–210 (1989).

  71. 71.

    & The neural basis for romantic love. Neuroreport 11, 3829–3834 (2000).

  72. 72.

    , , & Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res. 555, 220–232 (1991).

  73. 73.

    , , , & Vasopressin, oxytocin and neurophysins in the human brain and spinal cord. Brain Res. 291, 111–117 (1984).

  74. 74.

    & The neural correlates of maternal and romantic love. Neuroimage 21, 1155–1166 (2004).

  75. 75.

    et al. Brain activation during human male ejaculation. J. Neurosci. 23, 9185–9193 (2003).

  76. 76.

    et al. Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles: a mechanism for pair bonding. Behav. Neurosci. 113, 602–611 (1999).

Download references

Acknowledgements

The authors acknowledge A.Z. Murphy, E.A.D. Hammock, M.M. Lim, B. Aragona and T. Curtis for discussion and comments during the writing of this manuscript. The authors especially thank C.S. Carter and T.R. Insel for their pioneering work, which laid the foundation for neurobiological studies of social bonding. Much of this work was supported by National Institute of Mental Health grants to L.J.Y. and Z.X.W.

Author information

Affiliations

  1. Center for Behavioral Neuroscience, Department of Psychiatry and Behavioral Sciences, and Yerkes National Primate Research Center, Emory University, Atlanta, Georgia 30322, USA.

    • Larry J Young
  2. Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, Florida 32306, USA.

    • Zuoxin Wang

Authors

  1. Search for Larry J Young in:

  2. Search for Zuoxin Wang in:

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Larry J Young.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nn1327

Further reading