The influence of the smell of men and women on the behavior of laboratory rats

Authors

DOI:

https://doi.org/10.33910/2687-1270-2021-2-2-189-195

Keywords:

human odor, sex differences, pheromones, anxiety, aggression, rats’ behavior

Abstract

The results of behavioral tests of laboratory animals are highly variable. Even within the same laboratory the results of the same test can differ significantly. We tested the effect of the experimenter’s smell — male and female — on the behavior of male Wistar rats. The smell donors were clinically healthy non-smoking, low-alcohol-consuming volunteers aged 20–21: four men, and four women in the luteal phase of the menstrual cycle. They wore cotton socks and T-shirts at night, which, in the morning, were sealed in plastic bags. The animals were tested on the same day. In the first experiment (n = 20), smell samples were placed in the center of the elevated zero maze. First, we tested naive animals, after 20 days in the presence of a male smell, and after another 20 days in the presence of a female smell. The presence of human body smells during testing increased the rats’ anxiety. A male smell had a greater effect than a female smell. In the second experiment (n = 29), the delayed effect of exposure to human smells was studied. The home cages were equipped with perforated plastic containers with fabric inside. They remained in the cages for one hour. During exposure to the smell, the animals were aroused, which was manifested in an intensive examination of containers and multiple agonistic contacts. Four hours later, increased anxiety was noted only after exposure to a female smell. The obtained data show that the results of behavioral tests on laboratory rats may depend, inter alia, on the sex of the experimenter.

References

Banner, A., Shamay-Tsoory, S. (2018) Effects of androstadienone on dominance perception in males with low and high social anxiety. Psychoneuroendocrinology, vol. 95, pp. 138–144. https://www.doi.org/10.1016/j.psyneuen.2018.05.032 (In English)

Bogale, B. A., Aoyama, M., Sugita, S. (2011) Categorical learning between ‘male’ and ‘female’ photographic human faces in jungle crows (Corvus macrorhynchos). Behavioral Processes, vol. 86, no. 1, pp. 109–118. https://www.doi.org/10.1016/j.beproc.2010.10.002 (In English)

Burwash, M. D., Tobin, M. E., Woolhouse, A. D., Sullivan, T. P. (1998) Laboratory evaluation of predator odors for eliciting an avoidance response in roof rats (Rattus rattus). Journal of Chemical Ecology, vol. 24, no. 1, pp. 49–66. https://www.doi.org/10.1023/A:1022384728170 (In English)

Carballo, F., Freidin, E., Putrino, N. et al. (2015) Dog’s discrimination of human selfish and generous attitudes: The role of individual recognition, experience, and experimenters’ gender. PLoS ONE, vol. 10, no. 2, article e0116314. https://www.doi.org/10.1371/journal.pone.0116314 (In English)

Davis, H., Taylor, A. A., Norris, C. (1997) Preference for familiar humans by rats. Psychonomic Bulletin & Review, vol. 4, no. 1, pp. 118–120. https://doi.org/10.3758/BF03210783 (In English)

De Groot, J. H. B., Smeets, M. A. M. (2017) Human fear chemosignaling: Evidence from a meta-analysis. Chemical Senses, vol. 42, no. 8, pp. 663–673. https://www.doi.org/10.1093/chemse/bjx049 (In English)

Dewsbury, D. A. (1978) Comparative animal behavior. New York: McGraw-Hill Publ., 452 p. (In English)

Dobrakovova, M., Jurcovicova, J. (1984) Corticosterone and prolactin responses to repeated handling and transfer of male rats. Experimental and Clinical Endocrinology & Diabetes, vol. 83, no. 1, pp. 21–27. https://www.doi.org/10.1055/s-0029-1210308 (In English)

Garcia, M. J., Williams, J., Sinderman, B., Earley, R. L. (2015) Ready for a fight? The physiological effects of detecting an opponent’s pheromone cues prior to a contest. Physiology and Behavior, vol. 149, pp. 1–7. https://www.doi.org/10.1016/j.physbeh.2015.05.014 (In English)

European Convention for the Protection of Vertebrate Animals Used for Experimental and other Scientific Purposes. (1986) European Treaty Series, no. 123, pp. 1–11. [Online]. Available at: https://rm.coe.int/168007a67b (accessed 20.05.2021). (In English)

Hennessy, M. B., Davis, H. N., Williams, M. T. et al. (1997) Plasma cortisol levels of dogs at a county animal shelter. Physiology & Behavior, vol. 62, no. 3, pp. 485–490. https://www.doi.org/10.1016/s0031-9384(97)80328-9 (In English)

Karlson, P., Lüscher, M. (1959) ‘Pheromones’: A new term for a class of biologically active substances. Nature, vol. 183, no. 4653, pp. 55–56. https://www.doi.org/10.1038/183055a0 (In English)

Lecorps, B., Rödel, H. G., Féron, C. (2016) Assessment of anxiety in open field and elevated plus maze using infrared thermography. Physiology & Behavior, vol. 157, pp. 209–216. https://www.doi.org/10.1016/j.physbeh.2016.02.014 (In English)

Nolte, D. L., Mason, J. R., Epple, G. et al. (1994) Why are predator urines aversive to prey? Journal of Chemical Ecology, vol. 20, no. 7, pp. 1505–1516. https://www.doi.org/10.1007/BF02059876 (In English)

Novikov, S. N. (1988) Feromony i razmnozhenie mlekopitayuschshikh: Fiziologicheskie aspekty [Pheromones and mammalian reproduction: Physiological aspects]. Leningrad: Nauka Publ., 167 p. (In Russian)

Pellow, S., Chopin, P., File, S. E., Briley, M. (1985) Validation of open: Closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. Journal of Neuroscience Methods, vol. 14, no. 3, pp. 149–167. https://www.doi.org/10.1016/0165-0270(85)90031-7 (In English)

Piccinni, A., Veltri, A., Marazziti, D. et al. (2018) Human Appeasing Pheromone (HAP) influence on behavior and psychopathological residual symptoms of patients with complex psychiatric disorders. Clinical Case Reports, vol. 6, no. 4, pp. 664–668. https://www.doi.org/10.1002/ccr3.1348 (In English)

Shepherd, J. K., Grewal, S. S., Fletcher, A. et al. (1994) Behavioural and pharmacological characterisation of the elevated “zero-maze” as an animal model of anxiety. Psychopharmacology, vol. 116, no. 1, pp. 56–64. https://www.doi.org/10.1007/BF02244871 (In English)

Sorge, R. E., Martin, L. J., Isbester, K. A. et al. (2014) Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nature Methods, vol. 11, no. 6, pp. 629–632. https://www.doi.org/10.1038/nmeth.2935 (In English)

Takahashi, L. K., Nakashima, B. R., Hong, H., Watanabe, K. (2005) The smell of danger: A behavioral and neural analysis of predator odor-induced fear. Neuroscience and Biobehavioral Reviews, vol. 29, no. 8, pp. 1157–1167. https://www.doi.org/10.1016/j.neubiorev.2005.04.008 (In English)

Tsapygina, R. I., Daev, E. V., Novikov, S. N. (1981) Dejstvie ekzogennykh metabolitov samtsov domovoj myshi na protsess kletochnogo deleniya v generativnoj tkani molodykh zhivotnykh pri odnokratnykh i mnogokratnykh vozdejstviyakh [The effect of exogenic metabolites of male domestic mice on the process of cell division in the generative tissue of young animals under single and repeated exposure]. Issledovaniya po genetike, no. 9, pp. 17–23. (In Russian)

Tucker, L. B., McCabe, J. T. (2017) Behavior of male and female C57BL/6J mice is more consistent with repeated trials in the elevated zero maze than in the elevated plus maze. Frontiers in Behavioral Neuroscience, vol. 11, article 13. https://www.doi.org/10.3389/fnbeh.2017.00013 (In English)

van Driel, K. S., Talling, J. C. (2005) Familiarity increases consistency in animal tests. Behavioral Brain Research, vol. 159, no. 2, pp. 243–245. https://www.doi.org/10.1016/j.bbr.2004.11.005 (In English)

Vinogradova, E. P., Nemetz, V. V., Zhukov, D. A. (2013) Aktivnaya strategiya povedeniya kak factor riska depressivnopodobnykh narushenij posle khronicheskogo umerennogo stressa [Active coping style as a risk factor of depressive-like disorders after chronic mild stress]. Zhurnal vysshej nervnoj deyatelnosti im. I. P. Pavlova — I. P. Pavlov Journal of Higher Nervous Activity, vol. 63, no. 5, pp. 589–596. https://www.doi.org/10.7868/s0044467713050109 (In Russian)

Vinogradova, E. P., Zhukov, D. A. (2018) The effects of intranasal administration of oxytocin on the behavior of rats with different behavioral strategies subjected to chronic mild stress. Neuroscience and Behavioral Physiology, vol. 48, no. 3, pp. 333–336. https://www.doi.org/10.1007/s11055-018-0566-8 (In English)

Wah, D. T. O., Ossenkopp, K.-P., Bishnoi, I., Kavaliers, M. (2019) Predator odor exposure in early adolescence influences the effects of the bacterial product, propionic acid, on anxiety, sensorimotor gating, and acoustic startle response in male rats in later adolescence and adulthood. Physiology & Behavior, vol. 199, pp. 35–46. https://www.doi.org/10.1016/j.physbeh.2018.11.003 (In English)

Wells, D. L., Hepper, P. G. (1999) Male and female dogs respond differently to men and women. Applied Animal Behaviour Science, vol. 61, no. 4, pp. 341–349. https://www.doi.org/10.1016/S0168-1591(98)00202-0 (In English)

Zhang, J.-X., Cao, C., Gao, H. et al. (2003) Effects of weasel odor on behavior and physiology of two hamster species. Physiology & Behavior, vol. 79, no. 4–5, pp. 549–552. https://www.doi.org/10.1016/s0031-9384(03)00123-9 (In English)

Zhang, J.-X., Sun, L., Bruce, K. E., Novotny, M. V. (2008) Chronic exposure of cat odor enhances aggression, urinary attractiveness and sex pheromones of mice. Journal of Ethology, vol. 26, no. 2, pp. 279–286. https://www.doi.org/10.1007/s10164-007-0060-1 (In English)

Zhukov, D. A. (1996) Reaktsiya osobi na nekontroliruemoe vozdejstviye zavisit ot strategii povedeniya [The individual’s response to uncontrolled exposure depends on the coping style]. Fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 82, no. 4, pp. 21–29. (In Russian)

Published

2021-06-28

Issue

Section

Experimental articles