Advertisement

Olfactory Control of Sex-Recognition and Sexual Behavior in Mice

  • Matthieu Keller
  • Michael J. Baum
  • Julie Bakker
Conference paper

Abstract

In this chapter, we review recent data about the involvement of both the main and the accessory olfactory system in mate recognition and the control of sexual behavior in mice. Whereas the main olfactory system seems to play a central role in mate recognition in both male and female mice, clear sex differences emerge with regard to which olfactory system plays a more important role in the control of sexual behavior. Indeed, the main but not the accessory olfactory system seems to be more important in regulating sexual behavior in male mice, whereas in female mice, the accessory olfactory system seems to play a critical role in the control of mating.

Olfaction is of primary importance for social recognition in mammals, including mice. Thus mice use odors to distinguish sex, social or reproductive status of conspecifics (Brennan and Zufall 2006; Brown 1979). In addition, odors have been shown to facilitate the display of sexual behavior (e.g. Thompson and Edwards 1972) and to induce neuroendocrine responses (e.g. pregnancy block in female mice; Brennan and Keverne 1997).

Keywords

Sexual Behavior Olfactory System Zinc Sulfate Mate Recognition Main Olfactory Bulb 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Reference

  1. Bakker, J., Honda, S., Harada, N. and Balthazart, J. (2002) The aromatase knock-out mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood. J. Neurosci. 22, 9104–9112.PubMedGoogle Scholar
  2. Brennan, P.A. and Keverne, E.B. (1997) Neural mechanisms of mammalian olfactory learning. Prog. Neurobiol. 51, 457–481.PubMedCrossRefGoogle Scholar
  3. Brennan, P.A. and Zufall, F. (2006) Pheromonal communication in vertebrates. Nature 444, 308–315.PubMedCrossRefGoogle Scholar
  4. Brown, R.E. (1979) Mammalian social odors. Adv. Stud. Behav. 10, 107–161.Google Scholar
  5. Curtis, J. T., Liu, Y. and Wang, Z. (2001) Lesions of the vomeronasal organ disrupt mating-induced pair bonding in female prairie voles (Microtus ochrogaster). Brain Res. 18, 167–174.CrossRefGoogle Scholar
  6. Del Punta, K., Leinders-Zufall, T., Rodriguez, I., Jukam, D., Wysocki, C. J., Ogawa, S., Zufall, F. and Mombaerts, P. (2002) Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419, 70–74.PubMedCrossRefGoogle Scholar
  7. Edwards, D.A. and Burge, K.G. (1973) Olfactory control of sexual behavior of female and male mice. Physiol. Behav. 11, 867–872.PubMedCrossRefGoogle Scholar
  8. Firestein, S. (2001) How the olfactory system makes sense of scents. Nature 413, 211–218.PubMedCrossRefGoogle Scholar
  9. Hurst, J.L. and Beynon, R. (2004) Scent wars: the chemobiology of competitive signalling in mice. Bioessays 26, 1288–1298.PubMedCrossRefGoogle Scholar
  10. Keller, M., Douhard, Q., Baum, M.J. and Bakker, J. (2006a) Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chem. Senses 31, 4, 315–323.CrossRefGoogle Scholar
  11. Keller, M., Douhard, Q., Baum, M.J. and Bakker, J. (2006b) Sexual experience does not modulate the detrimental effects of zinc sulfate–lesioning of the main olfactory epithelium on sexual behavior in male mice. Chem. Senses 31, 8, 753–762.CrossRefGoogle Scholar
  12. Keller, M., Pierman, S., Douhard, Q., Baum, M.J. and Bakker, J. (2006c) The vomeronasal organ is required for the expression of lordosis behahavior, but not sex discrimination in female mice. Eur. J. Neurosci. 23, 521–530.CrossRefGoogle Scholar
  13. Kelliher, K.R., Spehr, M., Li, X.H., Zufall, F. and Leinders-Zufall, T. (2006) Pheromonal recognition memory induced by TRPC2-independent vomeronasal sensing. Eur. J. Neurosci. 23, 3385–3390.PubMedCrossRefGoogle Scholar
  14. Keverne, E.B. (1999) The vomeronasal organ. Science 286, 716–720.PubMedCrossRefGoogle Scholar
  15. Leinders-Zufall, T., Brennan, P.A., Widmayer, Prasanth Chandramani, C., Maul-Pavicic, A., Jager, M., Li, X.H., Breer, H., Zufall, F. and Boehm, T. (2004) MHC class I peptides as chemosignals in the vomeronasal organ. Science 306, 1033–1037.Google Scholar
  16. Leinders-Zufall, T., Lane, A.P., Puche, A.C., Ma, W., Novotny, M.V., Shipley, M.T. and Zufall, F. (2000) Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 405, 470–477.CrossRefGoogle Scholar
  17. Leypold, B.G., Yu, C.R., Leinders-Zufall, T., Kim, M.M., Zufall, F. and Axel, R. (2002) Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl. Acad. Sci. USA 99, 6376–6381.PubMedCrossRefGoogle Scholar
  18. Lin, D.Y., Zhang, S.Z., Block, E. and Katz, L.C. (2005) Encoding social signals in the mouse main olfactory bulb. Nature 434, 470–477.PubMedCrossRefGoogle Scholar
  19. Lloyd-Thomas, A. and Keverne, E.B. (1982) Role of the brain and accessory olfactory system in the block of pregnancy in mice. Neuroscience 7, 907–913.PubMedCrossRefGoogle Scholar
  20. Luo, M., Fee, M.S. and Katz, L.C. (2003) Encoding pheromonal signal in the accessory olfactory bulb of behaving mice. Science 299, 1196–1201.PubMedCrossRefGoogle Scholar
  21. Ma, D., Allen, N.D., Van Bergen, Y.C., Jones, C.M., Baum, M.J., Keverne, E.B. and Brennan, P.A. (2002) Selective ablation of olfactory receptor neurons without functional impairement of vomeronasal receptor neurons in OMP-ntr transgenic mice. Eur. J. Neurosci. 16, 2317–2323.PubMedCrossRefGoogle Scholar
  22. Mackay-Sim, A. and Rose, J.D. (1986) Removal of vomeronasal organ impairs lordosis in female hamsters: effect is reversed by luteinising hormone-releasing hormone. Neuroendocrinology 42, 489–493.PubMedGoogle Scholar
  23. Mandiyan, V.S., Coats, J.K. and Shah, N.M. (2005) Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat. Neurosci. 8, 1660–1662.PubMedCrossRefGoogle Scholar
  24. Meredith, M. (1986) Vomeronasal organ removal before sexual experience impairs male hamster mating behavior. Physiol. Behav. 36, 737–743.PubMedCrossRefGoogle Scholar
  25. Meredith, M. and O’Connell (1979) Efferents control of stimulus access to the hamster vomeronasal organ. J. Physiol. 286, 301–316.PubMedGoogle Scholar
  26. Moncho-Bogani, J., Lanuza, E., Hernandez, A., Novejarque, A. and Martinez-Garcia, F. (2002) Attractive properties of sexual pheromones in mice: innate or learned? Physiol. Behav. 77, 167–176.Google Scholar
  27. Moncho-Bogani, J., Lanuza, E., Lorente, M.J. and Martinez-Garcia F. (2004) Attraction to male pheromones and sexual behavior show different regulatory mechanisms in female mice. Physiol. Behav. 81, 427–434.PubMedCrossRefGoogle Scholar
  28. O’Connell, R.J. and Meredith, M. (1984) Effects of volatile and nonvolatile chemical signals on male sexual behaviors mediated by the main and accessory olfactory systems. Behav. Neurosci. 98, 1083–1093.PubMedCrossRefGoogle Scholar
  29. Pankevich, D.E., Baum, M.J. and Cherry, J.A. (2004) Olfactory sex-discrimination persists, whereas the preference for urinary odorants from estrous females disappears in male mice after vomeronasal organ removal. J. Neurosci. 24, 9451–9457.PubMedCrossRefGoogle Scholar
  30. Petrulis, A., Peng, M. and Johnston, R.E. (1999) Effects of vomeronasal organ removal on individual odor discrimination, sex-odor preference, and scent marking by female hamsters. Physiol. Behav. 66, 73–83.PubMedCrossRefGoogle Scholar
  31. Powers, J.B. and Winans, S.S. (1975) Vomeronasal organ: critical role in mediating sexual behavior of the male hamster. Science 187, 961–963.PubMedCrossRefGoogle Scholar
  32. Powers, J. B., Fields, R. B. and Winans, S. S. (1979) Olfactory and vomeronasal system articipation in male hamsters’ attraction to female vaginal secretions. Physiol. Behav. 22, 77–84.PubMedCrossRefGoogle Scholar
  33. Rajendren, J.B., Dudley, C.A., and Moss, R.L. (1990) Role of the vomeronasal organ in the male-induced enhancement of sexual receptivity in female rats. Neuroendocrinology 52, 368–372.PubMedGoogle Scholar
  34. Restrepo, D., Lin, W., Salcedo, E., Yamazaki, K. and Beauchamp, G. (2006) Odortypes and MHC peptides: complementary chemosignals of MHC haplotype? Trends Neurosci. 29, 604–609.PubMedCrossRefGoogle Scholar
  35. Scalia, F. and Winans, S.S. (1975) The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161, 31–35.PubMedCrossRefGoogle Scholar
  36. Spehr, M., Kelliher, K.R., Li, X.H., Boehm, T., Leinders-Zufall, T. and Zufall, F. (2006) Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J. Neurosci. 26, 1961–1970.PubMedCrossRefGoogle Scholar
  37. Stowers, L., Holy, T. E., Meister, M., Dulac, C. and Koentges, G. (2002). Loss of sex-discrimination and male-male aggression in mice deficient for TRP2. Science 295, 1493–1500.PubMedCrossRefGoogle Scholar
  38. Thompson, M.L. and Edwards, D.A. (1972) Olfactory bulb removal impairs the hormonal induction of sexual receptivity in spayed female mice. Physiol. Behav. 8, 1141–1146.PubMedCrossRefGoogle Scholar
  39. Winans, S. S. and Powers, J. B. (1977) Olfactory and vomeronasal deafferantation of male hamsters: Histological and behavioral analyses. Brain Res. 126, 325–344.PubMedCrossRefGoogle Scholar
  40. Woodley, S.K., Cloe, A.L., Waters, P. and Baum, M.J. (2004) Effects of vomeronasal organ removal on olfactory sex discrimination and odor preferences of female ferrets. Chem. Senses 29, 659–669.PubMedCrossRefGoogle Scholar
  41. Wysocki, C.J. and Wysocki, L.M. (1995) Surgical removal of the vomeronasal organ and its verification. In: Speilman, A.I. and Brands, J.G. (Eds.), Experimental Cell Biology of Taste and Olfaction. CRC Press, New York, pp. 49–57.Google Scholar
  42. Yoon, H., Enquist, L.W. and Dulac, C. (2005) Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 123, 669–682.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media,LLC 2008

Authors and Affiliations

  • Matthieu Keller
    • 1
    • 2
  • Michael J. Baum
  • Julie Bakker
  1. 1.Centre for Cellular and Molecular NeurobiologyUniversity of LiègeLiege B-4000Belgium
  2. 2.Laboratory of Behavioral and Reproductive PhysiologyCNRS/INRA/University of ToursFrance

Personalised recommendations