Advertisement

Experimental Brain Research

, Volume 235, Issue 9, pp 2893–2899 | Cite as

Effect of post-weaning isolation on anxiety- and depressive-like behaviors of C57BL/6J mice

  • Qian Huang
  • Ying Zhou
  • Lin-Yun LiuEmail author
Research Article

Abstract

Effects of post-weaning isolation on depressive- and anxiety-like behaviors in rodents have been well studied in the past. However, few studies included both sexes in a single experiment to study the sex difference in this animal model. The present study investigated the effect of post-weaning isolation on anxiety- and depressive-like behaviors in both male and female C57BL/6 J mice. Mice were individually or grouped housed from postnatal day 21 for 5 weeks until behavioral tests began. The results showed that social isolation resulted in increased anxiety in the open field. Isolated-reared female, but not male mice showed an increased transition between two compartments in the light–dark box and a decreased immobile time in the forced swim test. We conclude that post-weaning isolation has a sex-specific effect on emotional behaviors.

Keywords

Social isolation Anxiety Depression Sex difference Mice 

Notes

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31200827) and Shanghai Municipal Commission of Health and Family Planning (20134Y134).

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

References

  1. Ago Y, Takahashi K, Nakamura S, Hashimoto H, Baba A, Matsuda T (2007) Anxiety-like and exploratory behaviors of isolation-reared mice in the staircase test. J Pharmacol Sci 104:153–158CrossRefPubMedGoogle Scholar
  2. Aleman A, Kahn RS, Selten JP (2003) Sex differences in the risk of schizophrenia: evidence from meta-analysis. Arch Gen Psychiatry 60:565–571. doi: 10.1001/archpsyc.60.6.565 CrossRefPubMedGoogle Scholar
  3. Altemus M (2006) Sex differences in depression and anxiety disorders: potential biological determinants. Horm Behav 50:534–538. doi: 10.1016/j.yhbeh.2006.06.031 CrossRefPubMedGoogle Scholar
  4. Bledsoe AC, Oliver KM, Scholl JL, Forster GL (2011) Anxiety states induced by post-weaning social isolation are mediated by CRF receptors in the dorsal raphe nucleus. Brain Res Bull 85:117–122. doi: 10.1016/j.brainresbull.2011.03.003 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bourin M, Hascoet M (2003) The mouse light/dark box test. Eur J Pharmacol 463:55–65CrossRefPubMedGoogle Scholar
  6. Carola V, D’Olimpio F, Brunamonti E, Mangia F, Renzi P (2002) Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav Brain Res 134:49–57. doi: 10.1016/S0166-4328(01)00452-1 CrossRefPubMedGoogle Scholar
  7. Espejo EP, Hammen CL, Connolly NP, Brennan PA, Najman JM, Bor W (2007) Stress sensitization and adolescent depressive severity as a function of childhood adversity: a link to anxiety disorders. J Abnorm Child Psychol 35:287–299. doi: 10.1007/s10802-006-9090-3 CrossRefPubMedGoogle Scholar
  8. Fone KC, Porkess MV (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32:1087–1102. doi: 10.1016/j.neubiorev.2008.03.003 CrossRefPubMedGoogle Scholar
  9. Frye CA, Petralia SM, Rhodes ME (2000) Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3alpha,5alpha-THP. Pharmacol Biochem Behav 67:587–596CrossRefPubMedGoogle Scholar
  10. Goldstein JM, Cherkerzian S, Tsuang MT, Petryshen TL (2013) Sex differences in the genetic risk for schizophrenia: history of the evidence for sex-specific and sex-dependent effects. Am J Med Genet B Neuropsychiatr Genet 162B:698–710. doi: 10.1002/ajmg.b.32159 CrossRefPubMedGoogle Scholar
  11. Guo M, Wu CF, Liu W, Yang JY, Chen D (2004) Sex difference in psychological behavior changes induced by long-term social isolation in mice. Prog Neuropsychopharmacol Biol Psychiatry 28:115–121. doi: 10.1016/j.pnpbp.2003.09.027 CrossRefPubMedGoogle Scholar
  12. Gutman DA, Nemeroff CB (2003) Persistent central nervous system effects of an adverse early environment: clinical and preclinical studies. Physiol Behav 79:471–478CrossRefPubMedGoogle Scholar
  13. Heim C, Plotsky PM, Nemeroff CB (2004) Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 29:641–648. doi: 10.1038/sj.npp.1300397 CrossRefPubMedGoogle Scholar
  14. Hiroi R, Neumaier JF (2006) Differential effects of ovarian steroids on anxiety versus fear as measured by open field test and fear-potentiated startle. Behav Brain Res 166:93–100. doi: 10.1016/j.bbr.2005.07.021 CrossRefPubMedGoogle Scholar
  15. Hong S, Flashner B, Chiu M, ver Hoeve E, Luz S, Bhatnagar S (2012) Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats. Physiol Behav 105:269–275. doi: 10.1016/j.physbeh.2011.08.036 CrossRefPubMedGoogle Scholar
  16. Koonce CJ, Walf AA, Frye CA (2012) Type 1 5alpha-reductase may be required for estrous cycle changes in affective behaviors of female mice. Behav Brain Res 226:376–380. doi: 10.1016/j.bbr.2011.09.028 CrossRefPubMedGoogle Scholar
  17. Kulesskaya N, Rauvala H, Voikar V (2011) Evaluation of social and physical enrichment in modulation of behavioural phenotype in C57BL/6J female mice. PLoS One 6:e24755. doi: 10.1371/journal.pone.0024755 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Lalonde R, Strazielle C (2008) Relations between open-field, elevated plus-maze, and emergence tests as displayed by C57/BL6 J and BALB/c mice. J Neurosci Meth 171:48–52. doi: 10.1016/j.jneumeth.2008.02.003 CrossRefGoogle Scholar
  19. Lukkes JL, Mokin MV, Scholl JL, Forster GL (2009a) Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm Behav 55:248–256. doi: 10.1016/j.yhbeh.2008.10.014 CrossRefPubMedGoogle Scholar
  20. Lukkes JL, Watt MJ, Lowry CA, Forster GL (2009b) Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents. Front Behav Neurosci 3:18. doi: 10.3389/neuro.08.018.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Lukkes JL, Engelman GH, Zelin NS, Hale MW, Lowry CA (2012) Post-weaning social isolation of female rats, anxiety-related behavior, and serotonergic systems. Brain Res 1443:1–17. doi: 10.1016/j.brainres.2012.01.005 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Marcondes FK, Miguel KJ, Melo LL, Spadari-Bratfisch RC (2001) Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 74:435–440CrossRefPubMedGoogle Scholar
  23. Martin AL, Brown RE (2010) The lonely mouse: verification of a separation-induced model of depression in female mice. Behav Brain Res 207:196–207. doi: 10.1016/j.bbr.2009.10.006 CrossRefPubMedGoogle Scholar
  24. Meziane H, Ouagazzal AM, Aubert L, Wietrzych M, Krezel W (2007) Estrous cycle effects on behavior of C57BL/6 J and BALB/cByJ female mice: implications for phenotyping strategies. Genes Brain Behav 6:192–200. doi: 10.1111/j.1601-183X.2006.00249.x CrossRefPubMedGoogle Scholar
  25. Moreau JL (2002) Simulating the anhedonia symptom of depression in animals. Dialogues Clin Neurosci 4:351–360PubMedPubMedCentralGoogle Scholar
  26. Pietropaolo S, Singer P, Feldon J, Yee BK (2008) The postweaning social isolation in C57BL/6 mice: preferential vulnerability in the male sex. Psychopharmacology 197:613–628. doi: 10.1007/s00213-008-1081-3 CrossRefPubMedGoogle Scholar
  27. Pisu MG et al (2016) Sex differences in the outcome of juvenile social isolation on HPA axis function in rats. Neuroscience 320:172–182. doi: 10.1016/j.neuroscience.2016.02.009 CrossRefPubMedGoogle Scholar
  28. Voikar V, Koks S, Vasar E, Rauvala H (2001) Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol Behav 72:271–281CrossRefPubMedGoogle Scholar
  29. Võikar V, Polus A, Vasar E, Rauvala H (2005) Long-term individual housing in C57BL/6 J and DBA/2 mice: assessment of behavioral consequences. Genes Brain Behav 4:240–252. doi: 10.1111/j.1601-183X.2004.00106.x CrossRefPubMedGoogle Scholar
  30. Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2:322–328CrossRefPubMedPubMedCentralGoogle Scholar
  31. Walf AA, Koonce CJ, Frye CA (2009) Adult female wild type, but not oestrogen receptor beta knockout, mice have decreased depression-like behaviour during pro-oestrus and following administration of oestradiol or diarylpropionitrile. J Psychopharmacol 23:442–450. doi: 10.1177/0269881108089598 CrossRefPubMedGoogle Scholar
  32. Weintraub A, Singaravelu J, Bhatnagar S (2010) Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity. Brain Res 1343:83–92. doi: 10.1016/j.brainres.2010.04.068 CrossRefPubMedGoogle Scholar
  33. Weiss IC, Feldon J (2001) Environmental animal models for sensorimotor gating deficiencies in schizophrenia: a review. Psychopharmacology 156:305–326CrossRefPubMedGoogle Scholar
  34. Weiss IC, Pryce CR, Jongen-Relo AL, Nanz-Bahr NI, Feldon J (2004) Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 152:279–295. doi: 10.1016/j.bbr.2003.10.015 CrossRefPubMedGoogle Scholar
  35. Zhang Y, Zu X, Luo W, Yang H, Luo G, Zhang M, Tang S (2012) Social isolation produces anxiety-like behaviors and changes PSD-95 levels in the forebrain. Neurosci Lett 514:27–30. doi: 10.1016/j.neulet.2012.02.043 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Institutes of Brain Science, State Key Laboratory of Medical Neurobiology, Collaborative Innovation Center for Brain ScienceFudan UniversityShanghaiChina

Personalised recommendations