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Olfactory exposure to males, including men, causes stress and related analgesia in rodents

Abstract

We found that exposure of mice and rats to male but not female experimenters produces pain inhibition. Male-related stimuli induced a robust physiological stress response that results in stress-induced analgesia. This effect could be replicated with T-shirts worn by men, bedding material from gonadally intact and unfamiliar male mammals, and presentation of compounds secreted from the human axilla. Experimenter sex can thus affect apparent baseline responses in behavioral testing.

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Figure 1: Male-associated olfactory stimuli produce decreased pain behavior in mice.
Figure 2: Observed decreases in pain behavior are due to stress-induced analgesia.
Figure 3: Mice tested by male experimenters display lower apparent baseline pain sensitivity than those tested by female experimenters.

References

  1. Davis, H., Taylor, A.A. & Norris, C. Psychon. Bull. Rev. 4, 118–120 (1997).

    Article  Google Scholar 

  2. van Driel, K.S. & Talling, J.C. Behav. Brain Res. 159, 243–245 (2005).

    Article  Google Scholar 

  3. Langford, D.J. et al. Nat. Methods 7, 447–449 (2010).

    Article  CAS  Google Scholar 

  4. Sergeant, M.J.T. Vitam. Horm. 83, 25–45 (2010).

    Article  Google Scholar 

  5. Zeng, X.-N., Leyden, J.J., Spielman, A.I. & Preti, G. J. Chem. Ecol. 22, 237–257 (1996).

    Article  CAS  Google Scholar 

  6. Butler, R.K. & Finn, D.P. Prog. Neurobiol. 88, 184–202 (2009).

    Article  CAS  Google Scholar 

  7. Lester, L.S. & Fanselow, M.S. Behav. Neurosci. 99, 756–759 (1985).

    Article  CAS  Google Scholar 

  8. Kavaliers, M. & Innes, D.G.L. Physiol. Behav. 42, 131–135 (1988).

    Article  CAS  Google Scholar 

  9. Akil, H., Madden, J., Patrick, R.L. & Barchas, J.D. in Opiates and Endogenous Opioid Peptides (ed. Kosterlitz, H.W.) 63–70 (Elsevier, 1976).

  10. Hohmann, A.G. et al. Nature 435, 1108–1112 (2005).

    Article  CAS  Google Scholar 

  11. Mogil, J.S., Sternberg, W.F., Balian, H., Liebeskind, J.C. & Sadowski, B. Physiol. Behav. 59, 123–132 (1996).

    Article  CAS  Google Scholar 

  12. Gower, D.B., Holland, K.T., Mallet, A.I., Rennie, P.J. & Watkins, W.J. J. Steroid Biochem. Mol. Biol. 48, 409–418 (1994).

    Article  CAS  Google Scholar 

  13. Wyart, C. et al. J. Neurosci. 27, 1261–1265 (2007).

    Article  CAS  Google Scholar 

  14. Savic, I., Berglund, H., Gulyas, B. & Roland, P. Neuron 31, 661–668 (2001).

    Article  CAS  Google Scholar 

  15. Frasnelli, J., Lundström, J.N., Boyle, J.A., Katsarkas, A. & Jones-Gotman, M. Hum. Brain Mapp. 32, 450–460 (2011).

    Article  Google Scholar 

  16. Kobayakawa, K. et al. Nature 450, 503–508 (2007).

    Article  CAS  Google Scholar 

  17. Callahan, B.L., Gil, A.S.C., Levesque, A. & Mogil, J.S. J. Pain 9, 174–184 (2008).

    Article  Google Scholar 

  18. Sotocinal, S.G. et al. Mol. Pain 7, 55 (2011).

    PubMed  PubMed Central  Google Scholar 

  19. Mogil, J.S. et al. Pain 126, 24–34 (2006).

    Article  Google Scholar 

  20. Lamprea, M.R., Cardenas, F.P., Setem, J. & Morato, S. Braz. J. Med. Biol. Res. 41, 135–140 (2008).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the following individuals for serving as observers and/or T-shirt donators: N.M. Agalave, A. Brookins, A.J. Chabot-Dore, L.S. Dewberry, G. Hathaway, J. Feingold, T. Gao, M. Hatzopoulou, J.M.C. Mogil, J. Rinz, K. Sandor, A. Scholl, S. Stephenson, J. Su, S. Totsch and L. Topham. Thanks to L.S. Stone for use of her laboratory. This work was supported by an unrestricted grant from the Louise and Alan Edwards Foundation (J.S.M.), a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant (J.S.M.) and a Research in Undergraduate Institutions grant from the US National Science Foundation (W.F.S.).

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R.E.S., S.G.S. and J.S.M. conceived of the study. R.E.S., L.J.M. and J.S.M. designed most experiments. R.E.S., L.J.M., K.A.I., S.G.S., S.R., A.H.T., J.S.W., E.L.A., A. Delaney, B.K., P.L., J.C.S.M., M.M., A. Dokova, G.W., A.P.S., T.Q. and W.F.S. collected and analyzed data. J.F. and C.I.S. designed certain experiments. R.E.S., L.J.M. and J.S.M. wrote the paper.

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Correspondence to Jeffrey S Mogil.

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The authors declare no competing financial interests.

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Sorge, R., Martin, L., Isbester, K. et al. Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nat Methods 11, 629–632 (2014). https://doi.org/10.1038/nmeth.2935

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