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Responses to Domestic Cat Chemical Signals in the House Mouse Are Modulated by Early Olfactory Experience

  • Vera V. VoznessenskayaEmail author
  • Ilya G. Kvasha
  • Artyom B. Klinov
  • Tatiana K. Laktionova

Abstract

Many studies suggest that prey can distinguish predator species by detecting a carnivore signal or odor. The domestic cat is the most specialized predator to the house mouse. We examined the influence of the species-specific compound from the cat urine l-felinine on the investigatory behavior and neuroendocrine response of mice, and how those responses can be modulated by a mouse’s early olfactory experience with that compound. Patterns of investigatory and avoidance behavior were analyzed using an open field paradigm. Plasma corticosterone was monitored using an ELISA technique. We found that mice exposed to chemical cues of cats during their critical period for odor sensitization (14–28 days after birth) significantly elevated investigatory activity and suppressed patterns of avoidance behavior to cat odors during the open field test. At the same time corticosterone response of the mouse did not change, suggesting an innate corticosterone response to cat odors.

Keywords

House Mouse Predator Odor Neonatal Exposure Investigatory Activity Corticosterone Response 
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.

Notes

Acknowledgments

Research was supported by Russian Foundation for Basic Research # 14-04-05011 to V.V.V.

References

  1. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144CrossRefPubMedGoogle Scholar
  2. Blanchard RJ, Nikulina JN, Sakai RR, McKittrick C, McEwen B, Blanchard DC (1998) Behavioral and endocrine change following chronic predatory stress. Physiol Behav 63:561–569CrossRefPubMedGoogle Scholar
  3. Brown GR, Nemes C (2008) The exploratory behaviour of rats in the hole-board apparatus: is head-dipping a valid measure of neophilia? Behav Proc 78:442–448CrossRefGoogle Scholar
  4. Blanchard DC, Griebel G, Blanchard RJ (2001a) Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic. Neurosci Biobehav Rev 25:205–218CrossRefPubMedGoogle Scholar
  5. Blanchard RJ, McKittrick CR, Blanchard DC (2001b) Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol Behav 73:261–271CrossRefPubMedGoogle Scholar
  6. Cohen H, Benjamin J, Kaplan Z, Kotler M (2000) Administration of high-dose ketoconazole, an inhibitor of steroid synthesis, prevents posttraumatic anxiety in an animal model. Eur Neuropsychopharmacol 10:429–435CrossRefPubMedGoogle Scholar
  7. Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R (1997) Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology 132:107–124CrossRefPubMedGoogle Scholar
  8. Figueiredo HF, Bodie BL, Tauchi M, Dolgas CM, Herman JP (2003) Stress integration after acute and chronic predator stress: differential activation of central stress circuitry and sensitization of the hypothalamo–pituitary–adrenocortical axis. Endocrinology 144:5249–5258CrossRefPubMedGoogle Scholar
  9. File SE, Zangrossi H Jr, Sanders FL, Mabbutt PS (1993) Dissociation between behavioral and corticosterone responses on repeated exposures to cat odor. Physiol Behav 54:1109–1111CrossRefPubMedGoogle Scholar
  10. Greenberg R (2003) The role of neophobia and neophilia in the development of innovative behaviour of birds. In: Reader SM, Laland KN (eds) Animal innovation. Cambridge University Press, Cambridge, pp 175–196CrossRefGoogle Scholar
  11. Harvell CD (1990) The ecology and evolution of inducible defenses. Q Rev Biol 65:323–340CrossRefPubMedGoogle Scholar
  12. Hayes RA (2008) Seasonal responses to predator fecal odours in Australian native rodents vary between species. In: Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (eds) Chemical signals in vertebrates 11. Springer, New York, pp 379–387CrossRefGoogle Scholar
  13. Hayes RA, Nahrung HF, Wilson JC (2006) The response of native Australian rodents to predator odours varies seasonally: a by-product of life-history variations? Anim Behav 71:1307–1314CrossRefGoogle Scholar
  14. Hendriks WH, Moughan PJ, Tarttelin MF, Woolhouse AD (1995) Felinine: a urinary amino acid of Felidae. Comp Biochem Physiol B Biochem Mol Biol 112:581–588CrossRefPubMedGoogle Scholar
  15. Hughes RN (2007) Neotic preferences in laboratory rodents: issues, assessment and substrates. Neurosci Biobehav Rev 31:441–464CrossRefPubMedGoogle Scholar
  16. Hurst JL, West RS (2010) Taming anxiety in laboratory mice. Nat Methods 7:825–826CrossRefPubMedGoogle Scholar
  17. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  18. Miyazaki M, Yamashita T, Hosokawa M, Taira H, Suzuki A (2006a) Species-, sex-, and age-dependent urinary excretion of cauxin, a mammalian carboxylesterase family. Comp Biochem Physiol B Biochem Mol Biol 145:270–277CrossRefPubMedGoogle Scholar
  19. Miyazaki M, Yamashita T, Suzuki Y, Soeta S, Taira H, Suzuki A (2006b) A major urinary protein of the domestic cat regulates the production of felinine, a putative pheromone precursor. Chem Biol 13:1071–1079CrossRefPubMedGoogle Scholar
  20. Miyazaki M, Yamashita T, Taira H, Suzuki A (2008) The biological function of cauxin, a major urinary protein of the domestic cat (Felis catus). In: Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (eds) Chemical signals in vertebrates 11. Springer, New York, pp 51–60CrossRefGoogle Scholar
  21. Montgomery KC (1955) The relation between fear induced by novel stimulation and exploratory behavior. J Comp Physiol Psychol 48:254–260CrossRefPubMedGoogle Scholar
  22. Montgomery KC, Monkman JA (1955) The relation between fear and exploratory behavior. J Comp Physiol Psychol 48:132–136CrossRefPubMedGoogle Scholar
  23. Müller-Schwarze D (2006) Chemical ecology of vertebrates. Cambridge University Press, New YorkCrossRefGoogle Scholar
  24. Papes F, Logan DW, Stowers L (2010) The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 141:692–703PubMedCentralCrossRefPubMedGoogle Scholar
  25. Rutherfurd KJ, Rutherfurd SM, Moughan PJ, Hendriks WH (2002) Isolation and characterization of a felinine-containing peptide from the blood of the domestic cat (Felis catus) J Biol Chem 277:114–119 catus) J Biol Chem 277:114–119Google Scholar
  26. Stanford SC (2007) The open field test: reinventing the wheel. J Psychopharm 21:134–135CrossRefGoogle Scholar
  27. Stoddart M (1980) The ecology of vertebrate olfaction. Chapman & Hall, LondonCrossRefGoogle Scholar
  28. Stone A, Manavalan S, Zhang Y, Quartermain D (1995) Beta-adrenoceptor blockade mimics effects of stress on motor activity in mice. Neuropsychopharmacology 12:65–71CrossRefPubMedGoogle Scholar
  29. Sullivan RM, Gratton A (1998) Relationships between stress-induced increases in medial prefrontal cortical dopamine and plasma corticosterone levels in rats: role of cerebral laterality. Neuroscience 83:81–91CrossRefPubMedGoogle Scholar
  30. Walsh RN, Cummins RA (1976) The open-field test: a critical review. Psychol Bull 83:482–504CrossRefPubMedGoogle Scholar
  31. Voznessenskaya VV (2014) Influence of cat odor on reproductive behavior and physiology in the house mouse: (Mus musculus). In: Mucignat-Caretta C (ed) Neurobiology of chemical communication. CRC Press, Boca Raton, pp 389–405CrossRefGoogle Scholar
  32. Voznessenskaya VV, Feoktistova NY, Wysocki CJ (1999) Is there a period during neonatal development for maximal imprinting an odor? In: Johnston RE, Müller-Schwarze D, Sorensen PW (eds) Advances in chemical signals in vertebrates 8. Kluwer, New York, pp 617–621CrossRefGoogle Scholar
  33. Voznesenskaya VV, Poletaeva II (1983) The effect of ACTH4–10 on the diurnal cycle of locomotor activity in mice. Zh Vyssh Nerv Deiat Im I P Pavlova 33:960–961Google Scholar
  34. Voznessenskaya VV, Poletaeva II (1987) Orienting-investigatory reaction of mice with different genotypes under injection of ACTH 4–10. Zh Vyssh Nervn Deiat im I P Pavlova 37:174–176Google Scholar
  35. Voznessenskaya VV, Naidenko SV, Feoktistova NY, Krivomazov GJ, Miller LA, Clark L (2003) Predator odors as reproductive inhibitors for Norway rats. In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM (eds) Rats, mice and people: rodent biology and management, vol 96, ACIAR monograph. ACIAR, Canberra, pp 131–136Google Scholar
  36. Voznessenskaya VV, Parfyonova VM, Wysocki CJ (1995) Induced olfactory sensitivity in rodents: a general phenomenon. Adv Biosci 93:399–406Google Scholar
  37. Zangrossi JH, File SE (1994) Habituation and generalization of phobic responses to cat odor. Brain Res Bull 33:189–194CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Vera V. Voznessenskaya
    • 1
    Email author
  • Ilya G. Kvasha
    • 1
  • Artyom B. Klinov
    • 1
  • Tatiana K. Laktionova
    • 1
  1. 1.A. N. Severtsov Institute of Ecology and Evolution Russian Academy of SciencesMoscowRussia

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