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Exploring test batteries for depression- and anxiety-like behaviours in female and male ICR and black Swiss mice

Published online by Cambridge University Press:  07 May 2020

Lydmila Kazavchinsky ,
Sofi Dahan  and
Haim Einat Open the ORCID record for Haim Einat [Opens in a new window]
Lydmila Kazavchinsky
Affiliation:
School of Zoology, Tel-Aviv University, Tel-Aviv, Israel School of Behavioural Sciences, Tel Aviv-Yaffo Academic College, Tel-Aviv, Israel
Sofi Dahan
Affiliation:
School of Behavioural Sciences, Tel Aviv-Yaffo Academic College, Tel-Aviv, Israel
Haim Einat*
Affiliation:
School of Behavioural Sciences, Tel Aviv-Yaffo Academic College, Tel-Aviv, Israel
*
Author for correspondence: Haim Einat, Email: haimh@mta.ac.il
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Abstract

Objective and rationale: Animal models are critical for the study of mental disorders and their treatments but are repeatedly criticized for problems with validity and reproducibility. One approach to enhance validity and reproducibility of models is to use test batteries rather than single tests. Yet, a question regarding batteries is whether one can expect a consistent individual behavioural phenotype in mice across tests that can be presumed to be part of the same construct. This study was designed to explore the relationship between the behaviours of mice across tests in some variations of test batteries for depression- and anxiety-like behaviours. Methods: Female and male healthy, intact, and untreated mice from the ICR and black Swiss strains were used in four separate experiments. With some variations, mice were exposed to a battery of behavioural tests representing affective- and anxiety-like behaviours. Data were analysed for differences between sexes and for correlations between behaviours within and across the tests in the battery. Results: No differences were found between the sexes. With very few exceptions, we found correlations within tests (when one test has more than one measure or is repeated) but not across different tests within the battery. Conclusions: The results cast some doubt on the utility of behavioural test batteries to represent different facets of emotional behaviour in healthy intact outbred mice, without any interventions or treatments. Additional studies are designed to explore whether stronger relationship between the tests will appear after manipulations or drug treatments.

Keywords

depressionaffective disordersanimal modelsvalidityreproducibility
Type
Original Article
Information
Acta Neuropsychiatrica , Volume 32 , Issue 6 , December 2020 , pp. 293 - 302
Copyright
© Scandinavian College of Neuropsychopharmacology 2020

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Footnotes

a

These authors had equal contribution to the study.

References

Bailey, KR, Rustay, NR and Crawley, JN (2006) Behavioral phenotyping of transgenic and knockout mice: practical concerns and potential pitfalls. ILAR Journal 47, 124–131.CrossRefGoogle ScholarPubMed
Belzung, C and Lemoine, M (2011) Criteria of validity for animal models of psychiatric disorders: focus on anxiety disorders and depression. Biology of Mood & Anxiety Disorders 1, 9. doi:10.1186/2045-5380-1-9 CrossRefGoogle ScholarPubMed
Bilu, C, Einat, H, Tal-Krivisky, K, Mizrahi, J, Vishnevskia-Dai, V, Agam, G and Kronfeld-Schor, N (2019) Red white and blue – bright light effects in a diurnal rodent model for seasonal affective disorder. Chronobiology International 15, 1–8.Google Scholar
Castro, JE, Diessler, S, Varea, E, Marquez, C, Larsen, MH, Cordero, MI and Sandi, C (2012) Personality traits in rats predict vulnerability and resilience to developing stress-induced depression-like behaviors, HPA axis hyper-reactivity and brain changes in perk1/2 activity. Psychoneuroendocrinology 37, 1209–1223. doi:10.1016/j.psyneuen.2011.12.014 CrossRefGoogle ScholarPubMed
Crabbe, JC, Wahlsten, D and Dudek, BC (1999) Genetics of mouse behavior: interactions with laboratory environment. Science 284, 1670–1672.CrossRefGoogle ScholarPubMed
Crawley, JN (2000) What’s Wrong with My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice. New York: Wiley-Liss.Google Scholar
Crawley, JN and Paylor, R. (1997) A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Hormones and Behavior 31, 197–211.CrossRefGoogle ScholarPubMed
Cryan, JF and Holmes, A (2005) The ascent of mouse: advances in modelling human depression and anxiety. Nature Reviews Drug Discovery 4, 775–790.CrossRefGoogle ScholarPubMed
Deacon, RM (2011) Hyponeophagia: a measure of anxiety in the mouse. Journal of Visualized Experiments 51(51), 2613. doi:10.3791/2613.Google Scholar
Einat, H (2006) Modelling facets of mania – new directions related to the notion of endophenotypes. Journal of Psychopharmacology 20, 714–722.CrossRefGoogle ScholarPubMed
Einat, H (2014) New ways of modeling bipolar disorder. Harvard Review of Psychiatry 22, 348–352. doi:10.1097/HRP.0000000000000059 CrossRefGoogle ScholarPubMed
Einat, H, Ezer, I, Kara, NZ and Belzung, C. (2018) Individual responses of rodents in modelling of affective disorders and in their treatment: prospective review. Acta Neuropsychiatrica 18, 1–6.Google Scholar
Einat, H, Shaldubina, A, Bersudskey, Y and Belmaker, RH (2007) Prospects for the development of animal models for the study of bipolar disorder. In: Soares, JC and Young, A (eds.) Bipolar Disorders: Basic Mechanisms And Therapeutic Implications, 2nd Edn. New York: Taylor & Francis.Google Scholar
Ene, HM, Kara, NZ, Barak, N, Reshef Ben-Mordechai, T and Einat, H (2016) Effects of repeated asenapine in a battery of tests for anxiety-like behaviours in mice. Acta Neuropsychiatrica 28, 85–91. doi:10.1017/neu.2015.53 CrossRefGoogle Scholar
Ene, HM, Kara, NZ and Einat, H (2015) Introducing female black swiss mice: minimal effects of sex in a strain-specific battery of tests for mania-like behavior and response to lithium. Pharmacology 95, 224–228.CrossRefGoogle Scholar
Flaisher-Grinberg, S and Einat, H (2009) Mice models for the manic pole of bipolar disorder. In: Gould, TD (ed.) Mice Models For Mood And Anxiety Disorders. Berlin: Springer Press.Google Scholar
Flaisher-Grinberg, S and Einat, H (2010) Strain specific battery of tests for separate behavioral domains of mania. Frontiers in Psychiatry 1, 1–10.Google Scholar
Flaisher-Grinberg, S, Overgaard, S and Einat, H (2009) Attenuation of high sweet solution preference by mood stabilizers: a possible mouse model for the increased reward-seeking domain of mania. Journal of Neuroscience Methods 177, 44–50.CrossRefGoogle ScholarPubMed
Hannah-Poquette, C, Anderson, GW, Flaisher-Grinberg, S, Wang, J, Meinerding, TM and Einat, H (2011) Modeling mania: further validation for black swiss mice as model animals. Behavioural Brain Research 223, 222–226.CrossRefGoogle ScholarPubMed
Kafkafi, N, Agassi, J, Chesler, EJ, Crabbe, JC, Crusio, WE, Eilam, D, Gerlai, R, Golani, I, Gomez-Marin, A, Heller, R, Iraqi, F, Jaljuli, I, Karp, NA, Morgan, H, Nicholson, G, Pfaff, DW, Richter, SH, Stark, PB, Stiedl, O, Stodden, V, Tarantino, LM, Tucci, V, Valdar, W, Williams, R W, Wurbel, H and Benjamini, Y (2018) Reproducibility and replicability of rodent phenotyping in preclinical studies. Neuroscience & Biobehavioral Reviews 18, 30657-1.Google Scholar
Kara, NZ and Einat, H (2013) Rodent models for mania: practical approaches. Cell and Tissue Research 354, 191–201. doi:10.1007/s00441-013-1594-x CrossRefGoogle ScholarPubMed
Kara, NZ, Flaisher-Grinberg, S, Anderson, GW, Agam, G and Einat, H (2018a). Mood-stabilizing effects of rapamycin and its analog temsirolimus: relevance to autophagy. Behavioural Pharmacology 29, 379–384. doi:10.1097/FBP.0000000000000334 CrossRefGoogle Scholar
Kara, NZ, Karpel, O, Toker, L, Agam, G, Belmaker, RH and Einat, H (2014) Chronic oral carbamazepine treatment elicits mood-stabilising effects in mice. Acta Neuropsychiatrica 26, 29–34. doi:10.1017/neu.2013.23 CrossRefGoogle ScholarPubMed
Kara, NZ, Stukalin, Y and Einat, H (2018b). Revisiting the validity of the mouse forced swim test: systematic review and meta-analysis of the effects of prototypic antidepressants. Neuroscience & Biobehavioral Reviews 84, 1–11. doi:10.1016/j.neubiorev.2017.11.003 CrossRefGoogle ScholarPubMed
Kazavchinsky, L, Dafna, A and Einat, H (2019) Individual variability in female and male mice in a test-retest protocol of the forced swim test. Journal of Pharmacological and Toxicological Methods 95, 12–15. doi:10.1016/j.vascn.2018.11.007 CrossRefGoogle Scholar
Lan, A and Einat, H (2019) Questioning the predictive validity of the amphetamine-induced hyperactivity model for screening mood stabilizing drugs. Behavioural Brain Research 362, 109–113. doi:10.1016/j.bbr.2019.01.006 CrossRefGoogle ScholarPubMed
Lister, RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berl). 92, 180–185.CrossRefGoogle ScholarPubMed
Messiha, FS, Martin, WJ and Bucher, KD (1990) Behavioral and genetic interrelationships between locomotor activity and brain biogenic amines. General Pharmacology 21, 459–464.CrossRefGoogle ScholarPubMed
Nestler, EJ and Hyman, SE (2010) Animal models of neuropsychiatric disorders. Nature Neuroscience 13, 1161–1169.CrossRefGoogle ScholarPubMed
Nicolas, LB, Kolb, Y and Prinssen, EP (2006) A combined marble burying-locomotor activity test in mice: a practical screening test with sensitivity to different classes of anxiolytics and antidepressants. European Journal of Pharmacology 547, 106–115.CrossRefGoogle ScholarPubMed
Pollock, V, Cho, DW, Reker, D and Volavka, J (1979) Profile of mood states: the factors and their physiological correlates. Journal of Nervous and Mental Disease 167, 612–614. doi:10.1097/00005053-197910000-00004 CrossRefGoogle ScholarPubMed
Porsolt, RD, Bertin, A and Jalfre, M (1977) Behavioral despair in mice: a primary screening test for antidepressants. Archives Internationales de Pharmacodynamie et de Therapie 229, 327–336.Google ScholarPubMed
Porsolt, RD, Bertin, A and Jalfre, M (1978) “Behavioural despair” in rats and mice: strain differences and the effects of imipramine. European Journal of Pharmacology 51, 291–294.CrossRefGoogle ScholarPubMed
Sade, Y, Kara, NZ, Toker, L, Bersudsky, Y, Einat, H and Agam, G (2014) Beware of your mouse strain; differential effects of lithium on behavioral and neurochemical phenotypes in Harlan ICR mice bred in Israel or the USA. Pharmacology, Biochemistry and Behavior 124C 36–39. doi:10.1016/j.pbb.2014.05.007 CrossRefGoogle Scholar
Sadock, JB, Sadock, VA and Ruiz, P (2015) Kaplan and Sadock’s Synopsis of Psychiatry. Philadelphia: Lippincott & Williams.Google Scholar
Shemesh, G, Kara, N and Einat, H (2018) Chronic stress may not be a factor in the behavioral response to chronic lithium in ICR mice. Pharmacology 102, 281–286. doi:10.1159/000492717 CrossRefGoogle Scholar
Steru, L, Chermat, R, Thierry, B and Simon, P (1985) The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 85, 367–370.CrossRefGoogle ScholarPubMed
Stukalin, Y and Einat, H (2019) Analyzing test batteries in animal models of psychopathology with multivariate analysis of variance (MANOVA): one possible approach to increase external validity. Pharmacology, Biochemistry and Behavior 178, 51–55. doi:10.1016/j.pbb.2017.11.003 CrossRefGoogle ScholarPubMed
Stukalin, Y, Lan, A and Einat, H (2020) Revisiting the validity of the mouse tail suspension test: systematic review and meta-analysis of the effects of prototypic antidepressants. Neuroscience & Biobehavioral Reviews 29, 30544–30545.Google Scholar
Sugimoto, Y, Kajiwara, Y, Hirano, K, Yamada, S, Tagawa, N, Kobayashi, Y, Hotta, Y and Yamada, J (2008) Mouse strain differences in immobility and sensitivity to fluvoxamine and desipramine in the forced swimming test: analysis of serotonin and noradrenaline transporter binding. European Journal of Pharmacology 592, 116–122. doi:10.1016/j.ejphar.2008.07.005 CrossRefGoogle ScholarPubMed
Tuttle, AH, Philip, VM, Chesler, EJ and Mogil, JS (2018) Comparing phenotypic variation between inbred and outbred mice. Nature Methods 15, 994–996. doi:10.1038/s41592-018-0224-7 CrossRefGoogle ScholarPubMed
Van Der Staay, FJ, Arndt, SS and Nordquist, RE (2009) Evaluation of animal models of neurobehavioral disorders. Behavioral and Brain Functions 5, 11.CrossRefGoogle ScholarPubMed
Wang, YP and Gorenstein, C (2013) Assessment of depression in medical patients: a systematic review of the utility of the Beck Depression Inventory-II. Clinics (Sao Paulo) 68, 1274–1287. doi:10.6061/clinics/2013(09)15 CrossRefGoogle ScholarPubMed
Watson, D, Clark, LA and Tellegen, A (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. Journal of Personality and Social Psychology 54, 1063–1070. doi:10.1037//0022-3514.54.6.1063 CrossRefGoogle ScholarPubMed
Williams, JB (2001) Standardizing the Hamilton Depression Rating Scale: past, present, and future. E European Archives of Psychiatry and Clinical Neuroscience 251, II6–12.CrossRefGoogle ScholarPubMed
Willner, P (1997) Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl), 134, 319–29.CrossRefGoogle ScholarPubMed
Willner, P, Moreau, JL, Nielsen, CK, Papp, M and Sluzewska, A (1996) Decreased hedonic responsiveness following chronic mild stress is not secondary to loss of body weight. Physiology & Behavior 60, 129–34.CrossRefGoogle Scholar
Young, JW and Einat, H (2019) The importance and depth of reproducibility in rodent models of psychiatric diseases. Pharmacology, Biochemistry and Behavior 178, 1–2. doi:10.1016/j.pbb.2019.01.009 CrossRefGoogle ScholarPubMed
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