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A preliminary study for identifying olfactory markers of fear in the rat

Abstract

In stressful situations, many animals release alarm pheromones to warn conspecifics of impending danger. The authors sought to establish experimental conditions for a larger study aimed at identifying alarm pheromones emitted by the rat. They placed rats in a specially designed chamber and exposed them to aversive tactile, visual and acoustic stimuli over the course of a few days. The researchers observed rats' behavior and analyzed air samples taken from their immediate environment under the following conditions: (i) when rats were unstressed; (ii) immediately after rats were exposed to aversive stimuli; and (iii) when rats were left alone in the chamber after being conditioned to fear imminent aversive stimuli. Stressed rats emitted several substances that are known to function as alarm pheromones in insects. When previously unstressed control rats were exposed to these same substances, they had a distinct behavioral fear response.

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Figure 1: A construction diagram of the exposure device.

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References

  1. Wheeler, J.W. Insect and mammalian pheromones. Lloydia 39, 53–59 (1976).

    CAS  PubMed  Google Scholar 

  2. McClintock, M.K. On the nature of mammalian and human pheromones. Ann. N. Y. Acad. Sci. 855, 390–392 (1998).

    Article  CAS  Google Scholar 

  3. Silvotti, L., Montani, G. & Tirindelli, R. How mammals detect pheromones. J. Endocrinol. Invest. 26, 49–53 (2003).

    Article  CAS  Google Scholar 

  4. Brennan, P.A. & Keverne, E.B. Something in the air? New insights into mammalian pheromones. Curr. Biol. 14, 81–89 (2004).

    Article  Google Scholar 

  5. Konopski, L. & Koberda, M. Human Pheromones [Polish] (Scholar, Warszawa, 2003).

    Google Scholar 

  6. El-Sayed, A.M. The Pherobase: Extensive Database of Insect Pheromones and Semiochemicals. (2005) http://pherobase.net/

  7. Pauling, L., Robinson, A.B., Teranishi, R. & Cary, P. Quantitative analysis of urine vapor and breath by gas chromatography. Proc. Natl. Acad. Sci. USA 68, 2374–2376 (1971).

    Article  CAS  Google Scholar 

  8. Stevens, D.A. & Saplikoski, N.J. Rats′ reactions to conspecific muscle and blood: evidence for an alarm substance. Behav. Biol. 8, 75–82 (1973).

    Article  CAS  Google Scholar 

  9. Stevens, D.A. & Gerzog-Thomas, D.A. Fright reaction in rats to conspecifics tissue. Physiol. Behav. 18, 47–51 (1977).

    Article  CAS  Google Scholar 

  10. Kiyokawa, Y., Kikusui, T., Takeuchi, Y. & Mori, Y. Alarm pheromones with different functions are released from different regions of the body surface of male rats. Chem. Senses 29, 35–40 (2004).

    Article  Google Scholar 

  11. Hauser, R., Wiergowski, M., Gos, T., Marczak, M., Karaszewski, B. & Wodniak–Ochocińska, Ł . Alarm pheromones as an exponent of emotional state shortly before death—science fiction or a new challenge? Forensic Sci. Int. 155, 226–230 (2005).

    Article  CAS  Google Scholar 

  12. Kiyokawa, Y., Shimozuru, M., Kikusui, T., Takeuchi, Y. & Mori, Y. Alarm pheromone increases defensive and risk assessment behaviors in male rats. Physiol. Behav. 87, 383–387 (2006).

    Article  CAS  Google Scholar 

  13. Takefumi, K., Shu, T., Yukari, T. & Yuji, M. Alarm pheromone enhances stress-induced hyperthermia in rats. Physiol. Behav. 72, 45–50 (2001).

    Article  Google Scholar 

  14. Millar, J.G. in Sampling and Sample Preparation in Field and Laboratory (ed. Pawliszyn, J.) 669–697 (Elsevier, Amsterdam, 2002).

    Book  Google Scholar 

  15. Barbier, M. Les pheromones, aspects biochimiques et biologiques (Masson, Paris, 1982).

    Google Scholar 

  16. Wood, W.F., Fisher, C.O. & Graham, G.A. Volatile components in defensive spray of the hog–nosed skunk (Conepatus mesoleucus). J. Chem. Ecol. 19, 837–841 (1993).

    Article  CAS  Google Scholar 

  17. Wheeler, J.W., Nyalley, L., Davis, D.M. & Weldon, P.J. Additional sulfur compounds from anal glands of striped polecat. Z. Naturforsch. [C] 52, 283–285 (1997).

    Article  CAS  Google Scholar 

  18. Regnier, F.E. & Law, J.H. Insect pheromones. J. Lipid Res. 9, 541–551 (1968).

    CAS  PubMed  Google Scholar 

  19. Howe, N.R. & Sheikh, Y.M. Anthopleurine: a sea anemone alarm pheromone. Science 189, 386–388 (1975).

    Article  CAS  Google Scholar 

  20. Pfeiffer, W., Riegelbauer, G., Meier, G. & Scheibler, B. Effect of hypoxantine-3(N)-oxide and hypoxantine-1(N)-oxide on central nervous excitation of the black tetra Gymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light response. J. Chem. Ecol. 11, 507–523 (1985).

    Article  CAS  Google Scholar 

  21. Brown, G.E., Adrian, J.C., Naderi, N.T., Harvey, M.C. & Kelly, J.M. Nitrogen oxides elicit antipredator responses in juvenile channel catfish, but not in convict cichlids or rainbow trout: conservation of the ostariophysan alarm pheromone. J. Chem. Ecol. 29, 1782–1796 (2003).

    Article  Google Scholar 

  22. Ono, M., Terabe, H., Hori, H. & Sasaki, M. Insect signaling: components of giant hornet alarm pheromone. Nature 424, 637–638 (2003).

    Article  CAS  Google Scholar 

  23. Hauser, R., Marczak, M., Karaszewski, B. & Namieśnik, J. A chamber for the testing the release of volatile substances secreted by animals, especially mammals, as exemplified by substances released by rats in response to stress. Instr. Sci. Technol. 33, 541–550 (2005).

    Article  CAS  Google Scholar 

  24. Hauser, R., Gos, T., Krzyżanowski, M. & Goyke, E. The concentration of glutamate in cerebral tissue as a factor for the assessment of the emotional state before death. A preliminary report. Int. J. Legal Med. 112, 184–187 (1999).

    Article  CAS  Google Scholar 

  25. Hauser, R., Gos, T., Hartwich, J. & Dębińska-Kieć, A. The activity of constitutive nitric oxide synthase in prefrontal cortex of rats as an exponent of emotional state before death. A preliminary report. Neural Plast. 7, 205–211 (2000).

    Article  CAS  Google Scholar 

  26. Gos, T., Hauser, R. & Krzyżanowski, M. The post-mortem concentration of glutamate in the structures of rat brain as an exponent of short aversive sensory stimulation preceding death. Forensic Sci. Int. 123, 130–134 (2001).

    Article  CAS  Google Scholar 

  27. Gos, T., Hauser, R. & Krzyżanowski, M. Regional distribution of glutamate in the central nervous system of rat terminated by carbon dioxide euthanasia. Lab. Anim. 36, 127–133 (2002).

    Article  CAS  Google Scholar 

  28. Laska, M. & Seibt, A. Olfactory sensitivity for aliphatic alcohols in squirrel monkeys and pigtail macaques. J. Exp. Biol. 205, 1633–1643 (2002).

    CAS  PubMed  Google Scholar 

  29. Hernandez-Salazar, L.T., Laska, M. & Rodriguez-Luna, E. Olfactory sensitivity for aliphatic esters in spider monkeys (Ateles geoffroyi). Behav. Neurosci. 117, 1142–1149 (2003).

    Article  Google Scholar 

  30. Laska, M., Wieser, A., Rivas-Bautista, R.M. & Hernandez-Salazar, L.T. Olfactory sensitivity for carboxylic acids in spider monkeys and pigtail macaques. Chem. Senses 29, 101–109 (2004).

    Article  Google Scholar 

  31. Laska, M., Miethe, V., Rieck, C. & Weindl, K. Olfactory sensitivity for aliphatic ketones in squirrel monkeys and pigtail macaques. Exp. Brain Res. 160, 302–311 (2005).

    Article  CAS  Google Scholar 

  32. McFarlane, J.E., Steeves, E. & Alli, I. Aggregation of larvae of the house cricket, Acheta domesticus (L), by propionic acid present in the excreta. J. Chem. Ecol. 9, 1307–1315 (1983).

    Article  CAS  Google Scholar 

  33. Blatt, S.E., Borden, J.H., Pierce, H.D., Gries, R. & Gries G. Alarm pheromone system of the western conifer seed bug, Leptoglossus occidentalis. J. Chem. Ecol. 24, 1013–1031 (1998).

    Article  CAS  Google Scholar 

  34. Wager, B.R. & Breed, M.D. Does honey bee sting alarm pheromone give orientation information to defensive bees? Ann. Entomol. Soc. Am. 93, 1329–1332 (2000).

    Article  CAS  Google Scholar 

  35. Hughes, W.O., Howse, P.E. & Goulson, D. Mandibular gland chemistry of grass–cutting ants: species, caste, and colony variation. J. Chem. Ecol. 27, 109–124 (2001).

    Article  CAS  Google Scholar 

  36. Comfort, A. Likelihood of human pheromones. Nature 230, 432–433 (1971).

    Article  CAS  Google Scholar 

  37. Smith, B.H. & Roubik, D.W. Mandibular glands of stingless bees (Hymenoptera: Aphidae): chemical analysis of their contents and biological function in two species of Melipona. J. Chem. Ecol. 9, 1465–1472 (1983).

    Article  CAS  Google Scholar 

  38. Rasmussen, L.E.L., Lee, T.D., Roelofs, W.L., Zhang, A. & Daves Jr., G.D. Insect pheromone in elephants. Nature 379, 684 (1996).

    Article  CAS  Google Scholar 

  39. Rasmussen, L.E.L., Lee, T.D., Zhang, A., Roelofs, W.L. & Daves Jr., G.D. Purification, identification, concentration and bioactivity of (Z)-7-dodecen-1-yl acetate: sex pheromone of the female Asian elephant (Elephas maximus). Chem. Senses 22, 417–437 (1997).

    Article  CAS  Google Scholar 

  40. Gutierrez-Garcia, A.G. et al. A single session of emotional stress produces anxiety in Wistar rats. Behav. Brain. Res. 167, 30–35 (2006).

    Article  CAS  Google Scholar 

  41. Wang, Z., Balet-Sindreu, C., Li, V., Nudelman, A., Chan, G.C. & Storm, D.R. Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J. Neurosci. 26, 7375–7379 (2006).

    Article  CAS  Google Scholar 

  42. Singer, A.G. A chemistry of mammalian pheromones. J. Steroid. Mol. Biol. 39, 627–632 (1991).

    Article  CAS  Google Scholar 

  43. Abel, E.L. Alarm substance emitted by rats in the forced-swim test is a low volatile pheromone. Physiol. Behav. 50, 723–727 (1991).

    Article  CAS  Google Scholar 

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Correspondence to Roman Hauser.

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Hauser, R., Marczak, M., Karaszewski, B. et al. A preliminary study for identifying olfactory markers of fear in the rat. Lab Anim 37, 76–80 (2008). https://doi.org/10.1038/laban0208-76

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