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Journal of Chemical Ecology

, Volume 11, Issue 9, pp 1147–1159 | Cite as

Access of large and nonvolatile molecules to the vomeronasal organ of mammals during social and feeding behaviors

  • Charles J. Wysocki
  • Gary K. Beauchamp
  • Russell R. Reidinger
  • Judith L. Wellington
Article

Abstract

The vomeronasal organ, a chemosensory structure in the nasal cavity, is important in the detection of mammalian chemosignals, many of which are thought to be large molecules having low volatility. We conducted a series of experiments to determine whether nonvolatile molecules enter the vomeronasal organ during a variety of behavioral contexts in five species. We found that a nonvolatile dye entered the vomeronasal organ during investigation of urine from conspecific donors (experiment 1), during investigation of urine from heterospecific donors (experiment 2), during self-grooming (experiment 3), and during social grooming (experiment 4). In other experiments, we determined that nonvolatile molecules entered the vomeronasal organ during consumatory behaviors. Animals that ate a dye-adulterated familiar food had the nonvolatile marker in their vomeronasal organs (experiment 5). Animals that drank either familiar or novel dye-adulterated solutions also had the nonvolatile marker in their vomeronasal organs (experiment 6). In Experiment 7, large (66,000-dalton) fluorescent molecules were mixed with female urine which was then presented to male animals. We observed that the large molecules were transported to the vomeronasal organ. In the final experiment, we determined that mere contact between the snout of a dead animal and the stimulus resulted in transport of nonvolatile substances to the vomeronasal organ. We conclude that the vomeronasal organ, like the olfactory epithelium, is in continuous contact with the environment, but unlike the olfactory epithelium, the sensory receptors of the vomeronasal organ interact with molecules of low volatility, in addition to more volatile odorants.

Key words

Vomeronasal organ Jacobson's organ olfaction feeding grooming urine chemicals volatility high molecular weight 

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References

  1. Bean, N.J. 1982a. Olfactory and vomeronasal mediation of ultrasonic vocalizations in male mice.Physiol Behav. 28:31–37.Google Scholar
  2. Bean, N.J. 1982b. Modulation of agonistic behavior by the dual olfactory system in male mice.Physiol. Behav. 29:433–437.Google Scholar
  3. Beauchamp, G.K., Martin, I.G., Wysocki, C.J., andWellington, J.L. 1982. Chemoinvestigatory and sexual behavior of male guinea pigs following vomeronasal organ removal.Physiol. Behav. 29:329–336.Google Scholar
  4. Bellringer, J.F., Pratt, H.P.M., andKeverne, E.B. 1980. Involvement of the vomeronasal organ and prolactin in pheromonal induction of delayed implantation in mice.J. Reprod. Fertil. 59:223–228.Google Scholar
  5. Beruter, J., Beauchamp, G.K., andMuetterties, E.L. 1973. Complexity of chemical communication in mammals: Urinary components mediating sex discrimination by male guinea pigs.Biochem. Biophys. Res. Comm. 53, 264–271.Google Scholar
  6. Breipohl, W. (ed.). 1982. Olfaction and Endocrine Regulation. IRL Press Ltd., London.Google Scholar
  7. Chen, R.F. 1969. Fluorescent protein-dye conjugates II. Gamma globulin conjugated with various dyes.Arch. Biochem. Biophys. 133:263–276.Google Scholar
  8. Clancy, A.N., Coquelin, A., Macrides, F., Gorski, R.A., andNoble, E.P. 1984a. Sexual behavior and aggression in male mice: Involvment of the vomeronasal system.J. Neurosci. 4:2222–2229.Google Scholar
  9. Clancy, A.N., Macrides, F., Singer, A.G., andAgosta, W.C. 1984b. Male hamster copulatory responses to a high molecular weight fraction of vaginal discharge: Effects of vomeronasal organ removal.Physiol. Behav. 33:653–660.Google Scholar
  10. Coquelin, A., Clancy, A.N., Macrides, F., Noble, E.P., andGorski, R. 1984. Pheromonally induced release of luteinizing hormone in male mice: Involvment of the vomeronasal system.J. Neurosci. 4:2230–2236.Google Scholar
  11. Fleming, A., Vaccarino, F., Tambosso, L., andChee, P. 1979. Vomeronasal and olfactory system modulation of maternal behavior in rats.Science 203:372–373.Google Scholar
  12. Johns, M.A., Feder, H.H., Komisaruk, B.R., andMayer, A.D. 1978. Urine-induced reflex ovulation in anovulatory rats may be a vomeronasal effect.Nature 272:446–448.Google Scholar
  13. Kaneko, N., Debski, E.A., Wilson, M.C., andWhitten, W.K. 1980. Puberty acceleration in mice. II. Evidence that the vomeronasal organ is a receptor for the primer pheromone in male mouse urine.Biol. Reprod. 22:873–878.Google Scholar
  14. Keverne, E.B., 1979. Dual olfactory projections and their significance for behavior, pp. 75–83,in F. J. Ritter (ed.). Chemical Ecology: Odour Communication in Animals. Elsevier, Amsterdam.Google Scholar
  15. Kevetter, G.A. andWinans, S.S. 1981a. Connections of the corticomedial amygdala in the golden hamster. I. Efferents of the “vomeronasal amygdala.”J. Comp. Neurol. 197:81–98.Google Scholar
  16. Kevetter, G.A. andWinans, S.S. 1981b. Connections of the corticomedial amygdala in the golden hamster. II. Efferents of the “olfactory amygdala.”J. Comp. Neurol. 197:99–111.Google Scholar
  17. Krettek, J.E. andPrice, J.L. 1978. A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections.J. Comp. Neurol. 178:255–279.Google Scholar
  18. Kubie, J.L. andHalpern, M. 1976. Chemical senses involved in garter snake prey trailing.J. Comp. Physiol. Psychol. 93:648–667.Google Scholar
  19. Ladewig, J. andHart, B.L. 1980. Flehmen and vomeronasal organ function in male goats.Physiol. Behav. 24:1067–1071.Google Scholar
  20. Lehman, M.N., andWinans, S.S. 1982. Vomeronasal and olfactory pathways to the amygdala controlling male hamster sexual behavior: Autoradiographic and behavioral analyses.Brain Res. 240:27–41.Google Scholar
  21. Lehman, M.N., Winans, S.S., andPowers, J.B. 1980. Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior.Science 210:557–560.Google Scholar
  22. Meredith, M. andO'Connell, R.J. 1979. Efferent control of stimulus access to the hamster vomeronasal organ.J. Physiol. 286:301–316.Google Scholar
  23. Meredith, M., Marques, D.M., O'Connell, R.J., andStern, F.L. 1980. Vomeronasal pump: Significance for hamster sexual behavior.Science 207:1224–1225.Google Scholar
  24. Müller-Schwarze, D. andSilverstein, R.M. (eds.). 1980. Chemical Signals: Vertebrates and Aquatic Invertebrates. Plenum Press, New York.Google Scholar
  25. Müller-Schwarze, D. andSilverstein, R.M. (eds.). 1983. Chemical Signals in Vertebrates, Vol. 3. Plenum Press, New York.Google Scholar
  26. Nyby, J. andWhitney, G. 1980. Experience affects behavioral responses to sex odors, pp. 173–192,in D. Müller-Schwarze and R.M. Silverstein (eds.). Chemical Signals: Vertebrates and Aquatic Invertebrates. Plenum Press, New York.Google Scholar
  27. Nyby, J., Wysocki, C.J., Whitney, G., Dizinno, G., andSchenider, J. 1979. Elicitation of male mouseMus musculus ultrasonic vocalizations: I. Urinary cues.J. Comp. Physiol. Psychol. 93:957–975.Google Scholar
  28. Powers, J.B., andWinans, S.S. 1975. Vomeronasal organ: Critical role in mediating sexual behavior of the male hamster.Science 187:961–963.Google Scholar
  29. Reynolds, J. andKerverne, E.B. 1979. The accessory olfactory system and its role in the pheromonally mediated suppression of oestrus in grouped mice.J. Reprod. Fertil. 57:31–35.Google Scholar
  30. Sanchez-Criado, J.E. 1982. Involvment of the vomeronasal system in the reproductive physiology of the rat, pp. 209–221,in W. Breipohl (ed.). Olfaction and Endocrine Regulation. IRL Press Ltd., London.Google Scholar
  31. Scalia, F. andWinans, S.S. 1975. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals.J. Comp. Neurol. 61:31–56.Google Scholar
  32. Schilling, A. 1980. The possible role of urine in territoriality of some nocturnal prosimians.Symp. Zool. Soc. London, 45:165–193.Google Scholar
  33. Singer, A.G., Clancy, A.N., Macrides, F., andAgosta, W.C. 1984. Chemical studies of hamster vaginal discharge: Male behavioral responses to a high-molecular-weight fraction require physical contact.Physiol. Behav. 33:645–651.Google Scholar
  34. Winans, S.S. andPowers., J.B. 1977. Olfactory and vomeronasal deafferentation of male hamsters: Histological and behavioral analyses.Brain Res. 126:325–344.Google Scholar
  35. Winans, S.S. andScalia, F. 1970. Amygdaloid nucleus: New afferent input from the vomeronasal organ.Science 170:330–332.Google Scholar
  36. Wysocki, C.J. 1979. Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction.Neurosci. Biobehav. Rev. 3:301–341.Google Scholar
  37. Wysocki, C.J., Wellington, J.L., andBeauchamp, G.K. 1980a. Access of urinary nonvolatiles to the mammalian vomeronasal organ.Science 207:781–783.Google Scholar
  38. Wysocki, C.J., Beauchamp, G.K., Wellington, J.L., andErisman, S. 1980b. Access of low volitile stimuli to the rodent vomeronasal organ during social and feeding behaviors.Soc. Neurosci. Abstr. 6:305.Google Scholar
  39. Wysocki, C.J., Nyby, J., Whitney, G., Beauchamp, G.K., andKatz, Y. 1982. The vomeronasal organ: Primary role in mouse chemosensory gender recognition.Physiol. Behav. 29:315–327.Google Scholar
  40. Wysocki, C.J., Katz, Y., andBernhard, R. 1983. The male vomeronasal organ mediates female-induced testosterone surges in mice.Biol. Reprod. 28:917–922.Google Scholar

Copyright information

© Plenum Publishing Corporation 1985

Authors and Affiliations

  • Charles J. Wysocki
    • 1
  • Gary K. Beauchamp
    • 1
  • Russell R. Reidinger
    • 1
  • Judith L. Wellington
    • 1
  1. 1.Monell Chemical Senses CenterPhiladelphia

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