Skip to main content
SpringerLink
Log in

Features of the Social Behavior of Mice after Prolonged Exposure to Psychoemotional and Infective Factors

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

We report here studies of the behavior of male mice of the inbred strain C57BL/6 after prolonged exposure to two factors – social stress and infections with Opisthorchis, a combination which is often seen in humans. Mice of four groups were compared: 1) mice with prolonged experience of defeat in intermale confrontations (30 days) (SS); 2) those infected with O. felineus helminths (six months) (OF); 3) animals subjected to both factors (SS + OF); and 4) mice experiencing neither factor (CON). The behavior of all animals was evaluated in an open field test including a box, which was empty for the first 3 min of the test and contained an unfamiliar male of the inbred strain BALB/c during the second 3 min. Social stress had a stronger influence on the behavioral parameters evaluated in this test than infection. SS mice were more active than all others in exploring the box containing an unfamiliar male: they climbed onto it much more frequently and had longer mean durations of time spent close to the box. In addition, during the first 3 min of the test, these animals displayed elevated exploratory activity (number of rearings by the wall), and greater numbers and durations of grooming episodes. Infected mice of the OF group showed no difference in behavior from the CON group in either the first 3 min or the second 3 min of the test. In mice with the combination of factors (SS + OF), nonsocial forms of behavior were also no different from those in controls and reactions to the unfamiliar male were weaker than in SS mice. These data lead to the conclusions that prolonged experience of defeats in intermale confrontations had a stronger influence on social and nonsocial behavior in mice than chronic infection of the animals with O. felineus helminths and that the combination of these factors reduces social interest in mice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. D. F. Avgustinovich, O. V. Alekseenko, I. V. Bakshtanovskaya, et al., “Dynamic changes in brain serotonergic and dopaminergic activities during the development of anxious depression: an experimental study,” Usp. Fiziol. Nauk., 35, No. 4, 19–40 (2004).

    CAS  PubMed  Google Scholar 

  2. M. D. Weber, J. P. Godbout, and J. F. Sheridan, “Repeated social defeat, neuroinflammation, and behavior: monocytes carry the signal,” Neuropsychopharmacology, 42, No. 1, 46–61 (2017).

    Article  PubMed  Google Scholar 

  3. A. Niraula, Y. Wang, J. P. Godbout, and J. F. Sheridan, “Corticosterone production during repeated social defeat causes monocyte mobilization from the bone marrow, glucocorticoid resistance, and neurovascular adhesion molecule expression,” J. Neurosci., 38, No. 9, 2328–2340 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. B. F. Reader, B. L. Jarrett, D. B. McKim, et al., “Peripheral and central effects of repeated social defeat stress: monocyte trafficking, microglial activation, and anxiety,” Neuroscience, 289, 429–442 (2015).

    Article  CAS  PubMed  Google Scholar 

  5. C. D’Mello and M. G. Swain, “Liver-brain inflammation axis,” Am. J. Physiol. Gastrointest. Liver Physiol., 301, No. 5, G749–G761 (2011).

    Article  PubMed  Google Scholar 

  6. M. A. Laine, E. Sokolowska, M. Dudek, et al., “Brain activation induced by chronic psychosocial stress in mice,” Sci. Rep., 7, No. 1, 15061: 1–11 (2017).

  7. C. Montoliu, M. Llansola, and V. Felipo, “Neuroinflammation and neurological alterations in chronic liver diseases,” Neuroimmunol. Neuroinflammat., 2, No. 3, 138–144 (2015).

    Article  CAS  Google Scholar 

  8. C. D’Mello and M. G. Swain, “Liver-brain interactions in inflammatory liver diseases: implications for fatigue and mood disorders,” Brain Behav. Immun., 35, 9–20 (2014).

    Article  PubMed  Google Scholar 

  9. V. Hernandez-Rabaza, A. Agusti, A. Cabrera-Pastor, et al., “Sildenafil reduces neuroinflammation and restores spatial learning in rats with hepatic encephalopathy: underlying mechanisms,” J. Neuroinflammation, 12, No. 195, 1–12 (2015).

    Google Scholar 

  10. V. Felipo, J. F. Ordono, A. Urios, et al., “Patients with minimal hepatic encephalopathy show impaired mismatch negativity correlating with reduced performance in attention tests,” Hepatology, 55, No. 2, 530–539 (2012).

    Article  PubMed  Google Scholar 

  11. V. Felipo, “Hepatic encephalopathy: effects of liver failure on brain function,” Nat. Rev. Neurosci., 14, 851–858 (2013).

    Article  CAS  PubMed  Google Scholar 

  12. Food and Agriculture Organization of the United Nations and World Health Organization, “Multicriteria-based ranking for risk management of food-borne parasites,” Microbiological Risk Assessment Series (MRA), No. 23 (2014), www.fao.org/publications/card/en/c/ee07c6ae-b86c-4d5f-915c-94c93ded7d9e/.

  13. N. I. Yurlova, E. N. Yadrenkina, N. M. Rastyazhenko, et al., “Opisthorchiasis in Western Siberia: Epidemiology and distribution in human, fish, snail, and animal populations,” Parasitol. Int., 66, No. 4, 355–364 (2017).

    Article  PubMed  Google Scholar 

  14. A. M. Bronshtein and V. I. Luchshev, “Liver trematodes: opisthorchiasis and clonorchiasis,” Ross. Med. Zh., 6, No. 3, 140–148 (1998).

    Google Scholar 

  15. N. A. Brazhnikova and M. V. Tolkaeva, “Characteristics of the clinical features, diagnosis, and treatment of opisthorchiasis liver abscesses,” Ann. Khirurg. Gepatol., 5, No. 1, 37–42 (2000).

    Google Scholar 

  16. N. A. Brazhnikova and M. V. Tolkaeva, “Cancer of the liver, biliary tract, and pancreas in chronic opisthorchiasis,” Byull. Sibirsk. Med., 2, 71–76 (2002).

    Article  Google Scholar 

  17. I. V. Bakshtanovskaya and T. F. Stepanova, “Analysis of a set of biochemical indicators of liver function in chronic opisthorchiasis,” Med. Parazitol. Parazitarn. Bol., 4, 18–21 (2005).

    Google Scholar 

  18. B. Sripa, S. Kaewkes, P. Sithithaworn, et al., “Liver fluke induces cholangiocarcinoma,” PLoS Med., 4, No. 7, e201: 1148–1155 (2007).

  19. B. Sripa, E. Mairiang, B. Thinkhamrop, et al., “Advanced periductal fibrosis from infection with the carcinogenic human liver fluke Opisthorchis viverrini correlates with elevated levels of interleukin-6,” Hepatology, 50, 1273–1281 (2009).

  20. K. Milewski and M. Oria, “What we know: the inflammatory basis of hepatic encephalopathy,” Metab. Brain. Dis., 31, No. 6, 1239–1247 (2016).

    Article  CAS  PubMed  Google Scholar 

  21. T. F. Stepanova, I. V. Bakshtanovskaya, and S. I. Skichko, “Parameters of thyroid status in patients with acute and superinvasion opisthorchiasis,” Fundament. Issled., 6, 103–104 (2004).

    Google Scholar 

  22. V. A. Akhmedov and M. A. Kritevich, “Chronic opisthorchiasis is a multiorgan pathology,” Vestn. NGU Ser. Biol. Klin. Med., 7, No. 1, 118–121 (2009).

    Google Scholar 

  23. D. F. Avgustinovich, M. K. Marenina, S. Y. Zhanaeva, et al., “Combined effects of social stress and liver fluke infection in a mouse model,” Brain Behav. Immun., 53, 262–272 (2016).

    Article  PubMed  Google Scholar 

  24. E. S. Wohleb, D. B. McKim, J. F. Sheridan, and J. P. Godbout, “Monocyte trafficking to the brain with stress and inflammation: a novel axis of immune-to-brain communication that influences mood and behavior,” Front. Neurosci., 8, Art. 447, 1–17 (2015), https://doi.org/10.3389/fnins.2014.00447.

  25. D. F. Avgustinovich, I. L. Kovalenko, and N. P. Bondar, “Selection of ‘controls;’ in experimental studies of social interactions in mice,” Ros. Fiziol. Zh., 91, No. 12, 1454–1468 (2005).

    CAS  Google Scholar 

  26. N. N. Kudryavtseva, “The sensory contact model for the study of aggressive and submissive behaviors in male mice,” Aggress. Behav., 17, No. 5, 285–291 (1991).

    Article  Google Scholar 

  27. J. Hartmann, K. V. Wagner, N. Dedic, et al., “Fkbp52 heterozygosity alters behavioral, endocrine and neurogenetic parameters under basal and chronic stress conditions in mice,” Psychoneuroendocrinology, 37, No. 12, 2009–2021 (2012).

    Article  CAS  PubMed  Google Scholar 

  28. A. D. Benson, J. A. Burket, and S. I. Deutsch, “Balb/c mice treated with D-cycloserine arouse increased social interest in conspecifics,” Brain Res. Bull., 99, 95–99 (2013).

    Article  CAS  PubMed  Google Scholar 

  29. M. Masana, Y. A. Su, C. Liebl, et al., “The stress-inducible actininteracting protein DRR1 shapes social behavior,” Psychoneuroendocrinology, 48, 98–110 (2014).

    Article  CAS  PubMed  Google Scholar 

  30. H. Arakawa, “Analysis of social process in two inbred strains of male mice: A predominance of contact-based investigation in BALB/c mice,” Neuroscience, 369, 124–138 (2018).

    Article  CAS  PubMed  Google Scholar 

  31. C. S. Hall, “Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality,” J. Comp. Psychol., 18, No. 3, 385–403 (1934).

    Article  Google Scholar 

  32. E. Choleris, A. W. Thomas, M. Kavaliers, and F. S. Prato, “A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field,” Neurosci. Biobehav. Rev., 25, 235–260 (2001).

    Article  CAS  PubMed  Google Scholar 

  33. S. D. Iniguez, A. Aubry, L. M. Riggs, et al., “Social defeat stress induces depression-like behavior and alters spine morphology in the hippocampus of adolescent male C57BL/6 mice,” Neurobiol. Stress, 5, 54–64 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  34. N. Bondar, L. Bryzgalov, N. Ershov, et al., “Molecular adaptations to social defeat stress and induced depression in mice,” Mol. Neurobiol., 55, No. 4, 3394–3407 (2018).

    Article  CAS  PubMed  Google Scholar 

  35. M. L. Lehmann, T. Mustafa, A. M. Eiden, et al., “PACAP-deficient mice show attenuated corticosterone secretion and fail to develop depressive behavior during chronic social defeat stress,” Psychoneuroendocrinology, 38, No. 5, 702–715 (2013).

    Article  CAS  PubMed  Google Scholar 

  36. C. Hamelink, O. Tjurmina, R. Damadzic, et al., “Pituitary adenylate cyclase-activating polypeptide is a sympathoadrenal neurotransmitter involved in catecholamine regulation and glucohomeostasis,” Proc. Natl. Acad. Sci. USA, 99, No. 1, 461–466 (2002).

    Article  CAS  PubMed  Google Scholar 

  37. R. J. Fishkin and J. T. Winslow, “Endotoxin-induced reduction of social investigation by mice: interaction with amphetamine and anti-inflammatory drugs,” Psychopharmacology (Berlin), 132, No. 4, 335–341 (1997).

    Article  CAS  Google Scholar 

  38. H. Arakawa, S. Cruz, and T. Deak, “From models to mechanisms: odorant communication as a key determinant of social behavior in rodents during illness-associated states,” Neurosci. Biobehav. Rev., 35, No. 9, 1916–1928 (2011).

    Article  PubMed  Google Scholar 

  39. A. V. Kalueff and P. Tuohimaa, “Grooming analysis algorithm for neurobehavioural stress research,” Brain Res. Brain Res. Protoc., 13, No. 3, 151–158 (2004).

    Article  PubMed  Google Scholar 

  40. N. N. Kudryavtseva and D. F. Avgustinovich, “Behavioral and physiological markers of experimental depression induced by social conflicts (DISC),” Aggress. Behav., 24, 271–286 (1998).

    Article  Google Scholar 

  41. A. Mouri, M. Ukai, M. Uchida, et al., “Juvenile social defeat stress exposure persistently impairs social behaviors and neurogenesis,” Neuropharmacology, 133, 23–37 (2018).

    Article  CAS  PubMed  Google Scholar 

  42. M. G. Frank, R. M. Barrientos, L. R. Watkins, and S. F. Maier, “Aging sensitizes rapidly isolated hippocampal microglia to LPS ex vivo,” J. Neuroimmunol., 226, No. 1–2, 181–184 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. R. M. Barrientos, V. M. Thompson, V. V. Kitt, et al., “Greater glucocorticoid receptor activation in hippocampus of aged rats sensitizes microglia,” Neurobiol. Aging, 36, No. 3, 1483–1495 (2015).

    Article  CAS  PubMed  Google Scholar 

  44. R. J. Tynan, S. Naicker, M. Hinwood, et al., “Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions,” Brain Behav. Immun., 24, No. 7, 1058–1068 (2010).

    Article  CAS  PubMed  Google Scholar 

  45. F. Boulle, R. Massart, E. Stragier, et al., “Hippocampal and behavioral dysfunctions in a mouse model of environmental stress: normalization by agomelatine,” Transl. Psychiatry, 4, No. 11, e485 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. E. S. Wohleb, A. M. Fenn, A. M. Pacenta, et al., “Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice,” Psychoneuroendocrinology, 37, No. 9, 1491–1505 (2012).

  47. R. R. Johnson, T. W. Prentice, P. Bridegam, et al., “Social stress alters the severity and onset of the chronic phase of Theiler’s virus infection,” J. Neuroimmunol., 175, No. 1–2, 39–51 (2006).

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia

    D. F. Avgustinovich & N. P. Bondar

  2. Institute of Solid State Chemistry and Mechanochemistry, Siberian Branch, Russian Academy of Sciences, Novosibirsk, Russia

    D. F. Avgustinovich

  3. Novosibirsk State University, Novosibirsk, Russia

    N. P. Bondar

Authors
  1. D. F. Avgustinovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. P. Bondar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. F. Avgustinovich.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 107, No. 1, pp. 28–42, January, 2021.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Avgustinovich, D.F., Bondar, N.P. Features of the Social Behavior of Mice after Prolonged Exposure to Psychoemotional and Infective Factors. Neurosci Behav Physi 51, 960–968 (2021). https://doi.org/10.1007/s11055-021-01153-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-021-01153-8

Keywords

Search

Navigation