Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-27T17:17:34.929Z Has data issue: false hasContentIssue false

Decreased sensitivity to antidepressant drugs in Wistar Hannover rats submitted to two animal models of depression

Published online by Cambridge University Press:  14 September 2022

Kennia M. Silveira
Affiliation:
Department of Biomolecular Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil Translational Neuropsychiatry Unit, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
Ariandra G. Sartim
Affiliation:
Department of Biomolecular Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
Letícia Vieira
Affiliation:
Department of Biomolecular Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
Sabrina F. Lisboa
Affiliation:
Department of Biomolecular Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil
Gregers Wegener
Affiliation:
Translational Neuropsychiatry Unit, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
Sâmia R. L. Joca*
Affiliation:
Department of Biomolecular Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil Department of Biomedicine, Aarhus University, Aarhus, Denmark
*
Author for correspondence: Sâmia R. L. Joca, Email: sjoca@biomed.au.dk

Abstract

The Wistar Hannover rat (WHR) is a strain commonly used for toxicity studies but rarely used in studies investigating depression neurobiology. In this study, we aimed to characterise the behavioural responses of WHR to acute and repeated antidepressant treatments upon exposure to the forced swim test (FST) or learned helplessness (LH) test. WHR were subjected to forced swimming pre-test and test with antidepressant administration (imipramine, fluoxetine, or escitalopram) at 0, 5 h and 23 h after pre-test. WHR displayed high immobility in the test compared to unstressed controls (no pre-swim) and failed to respond to the antidepressants tested. The effect of acute and repeated treatment (imipramine, fluoxetine, escitalopram or s-ketamine) was then tested in animals not previously exposed to pre-test. Only imipramine (20 mg/kg, 7 days) and s-ketamine (acute) reduced the immobility time in the test. To further investigate the possibility that the WHR were less responsive to selective serotonin reuptake inhibitors, the effect of repeated treatment with fluoxetine (20 mg/kg, 7 days) was investigated in the LH model. The results demonstrated that fluoxetine failed to reduce the number of escape failures in two different protocols. These data suggest that the WHR do not respond to the conventional antidepressant treatment in the FST or the LH. Only s-ketamine and repeated imipramine were effective in WHR in a modified FST protocol. Altogether, these results indicate that WHR may be an interesting tool to investigate the mechanisms associated with the resistance to antidepressant drugs and identify more effective treatments.

Type
Original Article
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of Scandinavian College of Neuropsychopharmacology

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abelaira, HM, Réus, GZ and Quevedo, J (2013) Animal models as tools to study the pathophysiology of depression. Revista Brasileira De Psiquiatria 35(Suppl 2), S112S120.CrossRefGoogle ScholarPubMed
Aleksandrova, LR, Wang, YT and Phillips, AG (2019) Evaluation of the Wistar-Kyoto rat model of depression and the role of synaptic plasticity in depression and antidepressant response. Neuroscience & Biobehavioral Reviews 105, 123.CrossRefGoogle ScholarPubMed
Anisman, H and Sklar, LS (1979) Catecholamine depletion in mice upon reexposure to stress: mediation of the escape deficits produced by inescapable shock. Journal of Comparative and Physiological Psychology 93(4), 610625.CrossRefGoogle ScholarPubMed
Avey, MT, Moher, D, Sullivan, KJ, Fergusson, D, Griffin, G, Grimshaw, JM, Hutton, B, Lalu, MM, Macleod, M, Marshall, J, Mei, SHJ, Rudnicki, M, Stewart, DJ, Turgeon, AF, McIntyre, L and Canadian Critical Care Translational Biology Group, The devil is in the details: Incomplete reporting in preclinical animal research. PLoS One 11(11), 113.Google Scholar
Begley, CG and Ioannidis, JPA (2015) Reproducibility in science: improving the standard for basic and preclinical research. Circulation Research 116(1), 116126.CrossRefGoogle ScholarPubMed
Bennabi, D, Charpeaud, T, Yrondi, A, Genty, JB, Destouches, S, Lancrenon, S, Alaïli, N, Bellivier, F, Bougerol, T, Camus, V, Dorey, JM, Doumy, O, Haesebaert, F, Holtzmann, J, Lançon, C, Lefebvre, M, Moliere, F, Nieto, I, Rabu, C, Richieri, R, Schmitt, L, Stephan, F, Vaiva, G, Walter, M, Leboyer, M, El-Hage, W, Llorca, P-M, Courtet, P and Aouizer, B (2019) Clinical guidelines for the management of treatment-resistant depression: French recommendations from experts, the French Association for Biological Psychiatry and Neuropsychopharmacology and the fondation FondaMental. BMC Psychiatry 19(1), 112.Google ScholarPubMed
Berman, RM, Cappiello, A, Anand, A, Oren, DA, Heninger, GR, Charney, DS and Krystal, JH (2000) Antidepressant effects of ketamine in depressed patients. Biological Psychiatry 47(4):351354.CrossRefGoogle ScholarPubMed
Bogdanovaa, OV, Kanekara, S, D’Ancid, KE and Renshawa, PF (2013) Factors influencing behavior in the forced swim test. Physiology & Behavior 118(4–5), 227239.CrossRefGoogle Scholar
Borsini, F, Lecci, A, Sessarego, A, Frassine, R and Meli, A (1989) Discovery of antidepressant activity by forced swimming test may depend on pre-exposure of rats to a stressful situation. Psychopharmacology 97(2), 183188.CrossRefGoogle ScholarPubMed
Brand, SJ and Harvey, BH (2017) Exploring a post-traumatic stress disorder paradigm in Flinders sensitive line rats to model treatment-resistant depression I: bio-behavioural validation and response to imipramine. Acta Neuropsychiatrica 29(4), 193206.CrossRefGoogle ScholarPubMed
Brekke, TD, Steele, KA and Mulley, JF (2018) Inbred or outbred? Genetic diversity in laboratory rodent colonies. G3: Genes, Genomes, Genetics 8(2), 679686.CrossRefGoogle ScholarPubMed
Browne, CA, van, Nest D and Lucki, I (2015) Antidepressant-like effects of buprenorphine in rats are strain dependent. Behavioural Brain Research 176(1), 139148.Google Scholar
Calil, CM and Marcondes, FK (2006) The comparison of immobility time in experimental rat swimming models. Life Sciences 79(18), 17121719.CrossRefGoogle ScholarPubMed
Charles River Laboratories International I (2011) Wistar Han IGS Rats. https://www.criver.com/sites/default/files/resources/rm_d_Wistar_Han_IGS_Rat.pdf (accessed 27 October 2022).Google Scholar
Charles River Laboratories International I (2015) Outbred rats Outbred rats. https://www.criver.com/products-services/find-model/wistar-han-igs-rat?region=3621 (accessed 27 October 2022).Google Scholar
Chesler, EJ, Wilson, SG, Lariviere, WR, Rodriguez-Zas, SL and Mogil, JS (2002) Influences of laboratory environment on behavior. Nature Neuroscience 5(11), 11011102.CrossRefGoogle ScholarPubMed
Chia, R, Achilli, F, Festing, MFW and Fisher, EMC (2005) The origins and uses of mouse outbred stocks. Nature Genetics 37(11), 11811186.CrossRefGoogle ScholarPubMed
CLEA Japan, Inc. (2020) https://www.clea-japan.com/en/products/outbred/item_a0370 (accessed 10 November 2020).Google Scholar
Cryan, JF and Lucki, I (2000) Antidepressant-like behavioral effects mediated by 5-Hydroxytryptamine(2C) receptors. Journal of Pharmacology and Experimental Therapeutics 295(3), 11201126.Google ScholarPubMed
Cryan, JF, Markou, A and Lucki, I (2002) Assessing antidepressant activity in rodents: recent developments and future needs. Trends in Pharmacological Sciences 23(5), 238245.CrossRefGoogle ScholarPubMed
Cryan, JF, Valentino, RJ and Lucki, I (2005) Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neuroscience & Biobehavioral Reviews 29(4-5), 547569.CrossRefGoogle ScholarPubMed
Detke, MJ, Rickels, M and Lucki, I (1995) Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 121(1), 6672.CrossRefGoogle ScholarPubMed
Diniz, CRAF, Casarotto, PC, Fred, SM, Biojone, C, Castrén, E and Joca, SRL (2018) Antidepressant-like effect of losartan involves TRKB transactivation from angiotensin receptor type 2 (AGTR2) and recruitment of FYN. Neuropharmacology 135(10), 163171.CrossRefGoogle ScholarPubMed
Drugan, RC, Christianson, JP, Warner, TA and Kent, S (2013) Resilience in shock and swim stress models of depression. Frontiers in Behavioral Neuroscience 7, 18.CrossRefGoogle ScholarPubMed
Durand, M, Berton, O, Aguerre, S, Edno, L, Combourieu, I, Mormède, P and Chaouloff, F (1999) Effects of repeated fluoxetine on anxiety-related behaviours, central serotonergic systems, and the corticotropic axis in SHR and WKY rats. Neuropharmacology 38(6), 893907.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 30(6), 323333.CrossRefGoogle ScholarPubMed
Fanelli, D (2018) Is science really facing a reproducibility crisis, and do we need it to? Proceedings of the National Academy of Sciences USA 115(11), 26282631.CrossRefGoogle ScholarPubMed
Febbraro, F, Svenningsen, K, Tran, TP and Wiborg, O (2017) Neuronal substrates underlying stress resilience and susceptibility in rats. PLoS One 12(6), 119.CrossRefGoogle ScholarPubMed
Fernández-guasti, A, Olivares-nazario, M, Reyes, R and Martínez-mota, L (2017) Pharmacology, biochemistry and behavior sex and age differences in the antidepressant-like effect of fluoxetine in the forced swim test. Pharmacology Biochemistry and Behavior 152, 8189.CrossRefGoogle ScholarPubMed
France, C, Li, J-X, Owens, W, Koek, W, Toney, G and Daws, L (2009) Reduced effectiveness of escitalopram in the forced swimming test is associated with increased serotonin clearance rate in food restricted rats. The International Journal of Neuropsychopharmacology 12(6), 731736.CrossRefGoogle ScholarPubMed
Gauvin, DV, Dalton, JA, Harter, ML, Holdsworth, D, May, J, Tapp, R, Zimmermann, ZJ, Kilgus, Q and Baird, TJ (2019) Relative equivalence of CNS safety (FOB) assessment outcomes in male and female Wistar-Han and Sprague-Dawley rats. Journal of Pharmacological and Toxicological Methods 95, 211.CrossRefGoogle ScholarPubMed
Geoffroy, M and Christensen, AV (1993) Psychomotor stimulants versus antidepressants in the learned helplessness model of depression. Drug Development Research 29(1), 4855.CrossRefGoogle Scholar
Giknis, ML and Clifford, C (2009) Reproductive parameters and fetal data from reproductive toxicity studies in the Charles River Wistar Hannover [Crl:WI(Han)] rat. Charles River Laboratories technical data 130.Google Scholar
Goepfrich, AA, Gluch, C, Friemel, CM and Schneider, M (2013) Behavioral differences in three Wistar Han rat lines for emotional reactivity, cognitive processing and ethanol intake. Physiology & Behavior 10-1111, 102108.CrossRefGoogle Scholar
Hayakawa, K, Mimura, Y, Tachibana, S, Furuya, M, Kodama, T, Aoki, T, Hosokawa, S, Fukui, M, Shibata, S, Yoshida, M, Masuyama, T, Narita, T, Kuwagata, M, Hisada, S, Maki, E (2013) Study for collecting background data on Wistar Hannover [Crl: Wi(Han)] rats in general toxicity studies - comparative data to Sprague Dawley rats. Journal of Toxicological Sciences 38(6), 855873.CrossRefGoogle ScholarPubMed
Honndorf, S, Lindemann, C, Töllner, K and Gernert, M (2011) Female Wistar rats obtained from different breeders vary in anxiety-like behavior and epileptogenesis ଝ. Epilepsy Research 94(1-2), 2638.CrossRefGoogle ScholarPubMed
Hunter, P (2017) The reproducibility “crisis”. Embo Reports 18(9), 14931496.CrossRefGoogle ScholarPubMed
Du Jardin, KG, Liebenberg, N, Cajina, M, Müller, HK, Elfving, B, Sanchez, C and Wegener, G (2018) S-ketamine mediates its acute and sustained antidepressant-like activity through a 5-HT1B receptor dependent mechanism in a genetic rat model of depression. Frontiers in Pharmacology 8, 111.CrossRefGoogle Scholar
Jin, ZL, Chen, XF, Ran, YH, Li, XR, Xiong, J, Zheng, YY, Gao, NN and Li, YF (2017) Mouse strain differences in SSRI sensitivity correlate with serotonin transporter binding and function. Scientific Reports 7(1), 110.Google ScholarPubMed
Joca, SRL, Padovan, CM and Guimarães, FS (2003) Activation of post-synaptic 5-HT1A receptors in the dorsal hippocampus prevents learned helplessness development. Brain Research 978(1-2), 177184.CrossRefGoogle Scholar
Joca, SRL, Zanelati, T and Guimarães, FS (2006) Post-stress facilitation of serotonergic, but not noradrenergic, neurotransmission in the dorsal hippocampus prevents learned helplessness development in rats. Brain Research 1087(2006), 6774.CrossRefGoogle Scholar
Kara, NZ, Stukalin, Y and Einat, H (2018) Revisiting the validity of the mouse forced swim test: systematic review and meta-analysis of the effects of prototypic antidepressants. Neuroscience & Biobehavioral Reviews 84, 111.CrossRefGoogle ScholarPubMed
Kawai, H, Kodaira, N, Tanaka, C, Ishibashi, T, Kudo, N, Kawashima, Y and Mitsumoto, A (2018) Time of administration of acute or chronic doses of imipramine affects its antidepressant action in rats. Journal of Circadian Rhythms 16(1), 19.CrossRefGoogle ScholarPubMed
Kin, K, Yasuhara, T, Kameda, M, Agari, T, Sasaki, T, Morimoto, J, Okazaki, M, Umakoshi, M, Kuwahara, K, Kin, I, Tajiri, N, Date, I (2017) Hippocampal neurogenesis of Wistar Kyoto rats is congenitally impaired and correlated with stress resistance. Behavioural Brain Research 329, 148156.CrossRefGoogle ScholarPubMed
La Garza, RDe and Mahoney, JJ (2004) A distinct neurochemical profile in WKY rats at baseline and in response to acute stress: implications for animal models of anxiety and depression. Brain Research 1021(2), 209218.CrossRefGoogle Scholar
Lahmame, A, Del, Arco C, Pazos, A, Yritia, M and Armario, A (1997) Are Wistar-Kyoto rats a genetic animal model of depression resistant to antidepressants? European Journal of Pharmacology 337(2-3), 115123.CrossRefGoogle ScholarPubMed
Lahmanme, A and Armario, A (1996) Differential responsiveness of inbred strains of rats to antidepressants in the forced swimming test: are Wistar Kyoto rats an animal model of subsensitivity to antidepressants? Psychopharmacology 123(2), 191198.CrossRefGoogle Scholar
Lohmiller, JJ and Swing, SP (2006) Reproduction and Breeding. Amsterdam: Elsevier.CrossRefGoogle Scholar
López-Rubalcava, C and Lucki, I (2000) Strain differences in the behavioral effects of antidepressant drugs in the rat forced swimming test. Neuropsychopharmacology 22(2), 191199.CrossRefGoogle ScholarPubMed
Lucki, I (1997) The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behavioural pharmacology 8, 523532.CrossRefGoogle Scholar
Lucki, I, Dalvi, A and Mayorga, AJ (2001) Sensitivity to the effects of pharmacologically selective antidepressants in different strains of mice. Psychopharmacology 155(3), 315322.CrossRefGoogle Scholar
Macedo, GVF, Cladouchos, ML, Sifonios, L, Cassaneli, PM and Wikinski, S (2013) Effects of fluoxetine on CRF and CRF1 expression in rats exposed to the learned helplessness paradigm. Psychopharmacology 225(3), 647659.CrossRefGoogle Scholar
Maier, SF and Seligman, MEP (2016) Learned helplessness at fifty: insights from neuroscience. Psychological Review 123(4), 119.CrossRefGoogle ScholarPubMed
Marti, J and Armario, A (1996) Forced swimming behavior is not related to the corticosterone levels achieved in the test: a study with four inbred rat strains. Physiology & Behavior 59(2), 369373.CrossRefGoogle ScholarPubMed
McCormick, DL (2017) Preclinical evaluation of carcinogenicity using standard-bred and genetically engineered rodent models. In A Comprehensive Guide to Toxicology in Nonclinical Drug Development. New York: Elsevier.Google Scholar
Momeni, S, Segerström, L and Roman, E (2015) Supplier-dependent differences in intermittent voluntary alcohol intake and response to naltrexone in Wistar rats. Frontiers in Neuroscience 9, 113.CrossRefGoogle ScholarPubMed
Morilak, DA, Barrera, G, Echevarria, DJ, Garcia, AS, Hernandez, A, Ma, S and Petre, CO (2005) Role of brain norepinephrine in the behavioral response to stress. Progress in Neuro-Psychopharmacology and Biological Psychiatry 29(8), 12141224.CrossRefGoogle ScholarPubMed
Murrough, JW, Iosifescu, DV, Chang, LC, Al Jurdi, RK, Green, CE, Perez, AM, Pillemer, S, Foulkes, A and Mathew, SJ (2013) Antidepressant efficacy of ketamine in treatment-resistant major depression: a two-site randomized controlled trial. The American Journal of Psychiatry 170(10), 11341142.CrossRefGoogle ScholarPubMed
Noritake, K, Ikeda, T, Ito, K, Miwa, Y and Senuma, M (2013) Study for collecting background data on Wistar Hannover [Crl:WI(Han)] rats in embryo-fetal development studies - comparative data to Sprague Dawley rats. The Journal of Toxicological Sciences 38(6), 847854.CrossRefGoogle ScholarPubMed
Olorisade, BK, Brereton, P and Andras, P (2017) Reproducibility of studies on text mining for citation screening in systematic reviews: evaluation and checklist. Journal of Biomedical Informatics 73(1), 113.CrossRefGoogle ScholarPubMed
Oswald, BIAN, Brezinova, V and Dunleavy, DLF (1972) On the slowness of action of tricycic antidepressant drugs. British Journal of Psychiatry 120(559), 673677.CrossRefGoogle Scholar
Overstreet, DH, Friedman, E, Mathé, AA and Yadid, G (2005) The Flinders Sensitive Line rat: a selectively bred putative animal model of depression. Neuroscience & Biobehavioral Reviews 29(4-5), 739759.CrossRefGoogle Scholar
Overstreet, DH and Wegener, G (2013) The flinders sensitive line rat model of depression-25 years and still producing. Pharmacological Reviews 65(1), 143155.CrossRefGoogle ScholarPubMed
Overstreet, DI (1986) Selective breeding for increased cholinergic function: development of a new animal model of depression. Biological Psychiatry 21(1), 4958.CrossRefGoogle ScholarPubMed
Palm, S, Hävermark, Å., Meyerson, BJ, Nylander, I and Roman, E (2011) When is a Wistar a Wistar ? Behavioral profiling of outbred Wistar rats from five different suppliers using the MCSF test. Applied Animal Behaviour Science 135(1-2), 128137.CrossRefGoogle Scholar
Pardon, MC, Gould, GG, Garcia, A, Phillips, L, Cook, MC, Miller, SA, Mason, PA and Morilak, DA (2002) Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 115(1), 229242.CrossRefGoogle ScholarPubMed
Paré, WP (1994) Open field, learned helplessness, conditioned defensive burying, and forced-swim tests in WKY rats. Physiology & Behavior 55(3), 433439.CrossRefGoogle ScholarPubMed
Paré, WP and Kluczynski, J (1997) Differences in the stress response of Wistar-Kyoto (WKY) rats from different vendors. Physiology & Behavior 62(3), 643648.CrossRefGoogle ScholarPubMed
Pecoraro, N, Ginsberg, AB, Warne, JP, Gomez, F, la, Fleur SE and Dallman, MF (2006) Diverse basal and stress-related phenotypes of Sprague Dawley rats from three vendors. Physiology & Behavior 89(4), 598610.CrossRefGoogle ScholarPubMed
Petty, F, Kramer, G and Wilson, LeAnn (1992) Prevention of learned helplessness: in vivo correlation with cortical serotonin. Pharmacology Biochemistry and Behavior 43(2), 361367.CrossRefGoogle ScholarPubMed
Pollier, F, Sarre, S, Aguerre, S, Ebinger, G, Mormède, P, Michotte, Y and Chaouloff, F (2000) Serotonin reuptake inhibition by citalopram in rat strains differing for their emotionality. Neuropsychopharmacology 22(1), 6476.CrossRefGoogle ScholarPubMed
Porsolt, RD, Anton, G, Blavet, N and Jalfre, M (1978a) Behavioural despair in rats: a new model sensitive to antidepressant treatments. European Journal of Pharmacology 47(4), 379391.CrossRefGoogle ScholarPubMed
Porsolt, RD, Bertin, A and Jalfre, M (1978b) Behavioural despair, in rats and mice: strain differences and the effects of imipramine. European Journal of Pharmacology 51(3), 291294.CrossRefGoogle ScholarPubMed
Porsolt, RD, Le, Pichon M and Jalfre, M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266(5604), 730732.CrossRefGoogle ScholarPubMed
Posternak, MA and Zimmerman, M (2005) Is there a delay in the antidepressant effect? A meta-analysis. The Journal of Clinical Psychiatry 66(2), 148158.CrossRefGoogle Scholar
Pound, P and Ritskes-Hoitinga, M (2018) Is it possible to overcome issues of external validity in preclinical animal research? Why most animal models are bound to fail. Journal of Translational Medicine 16(1), 18.CrossRefGoogle ScholarPubMed
Pryce, CR, Azzinnari, D, Spinelli, S, Seifritz, E, Tegethoff, M and Meinlschmidt, G (2011) Helplessness: a systematic translational review of theory and evidence for its relevance to understanding and treating depression. Pharmacology & Therapeutics 132(3), 242267.CrossRefGoogle ScholarPubMed
Pucilowski, O and Overstreet, DH (1993) Effect of chronic antidepressant treatment on responses to apomorphine in selectively bred rat strains. Brain Research Bulletin 32(5), 471475.CrossRefGoogle ScholarPubMed
Reinés, A, Cereseto, M, Ferrero, A, Bonavita, C and Wikinski, S (2004) Neuronal cytoskeletal alterations in an experimental model of depression. Neuroscience 129(3), 529538.CrossRefGoogle Scholar
Reinés, A, Cereseto, M, Ferrero, A, Sifonios, L, Podestá, MF and Wikinski, S (2008) Maintenance treatment with fluoxetine is necessary to sustain normal levels of synaptic markers in an experimental model of depression: correlation with behavioral response. Neuropharmacology 33, 18961908.Google Scholar
Ribeiro, A, Ferraz-de-Paula, V, Pinheiro, ML and Palermo-Neto, J (2009) Dose-response effects of systemic anandamide administration in mice sequentially submitted to the open field and elevated plus-maze tests. Brazilian Journal of Medical and Biological Research 42(6), 556560.CrossRefGoogle Scholar
Ribeiro, DE, Casarotto, PC, Staquini, L, Silva, Pinto E, Biojone, MA, Wegener, C, Joca, G and S (2019) Reduced P2X receptor levels are associated with antidepressant effect in the learned helplessness model. PeerJ 2019(10), 117.Google Scholar
Rittenhouse, PA, López-Rubalcava, C, Stanwood, GD and Lucki, I (2002) Amplified behavioral and endocrine responses to forced swim stress in the Wistar-Kyoto rat. Psychoneuroendocrinology 27(3), 303318.CrossRefGoogle ScholarPubMed
Rockett, JC, Narotsky, MG, Thompson, KE, Thillainadarajah, I, Blystone, CR, Goetz, AK, Ren, H, Best, DS, Murrell, RN, Nichols, HP, Schmid, JE, Wolf, DC, Dix, DJ (2006) Effect of conazole fungicides on reproductive development in the female rat. Reproductive Toxicology 22(4), 647658.CrossRefGoogle ScholarPubMed
Russel, WMS and Burch, RL (1959) The Principles of Humane Experimental Technique. London: Methuen & Co. Ltd.Google Scholar
Russo, SJ, Murrough, JW, Han, MH, Charney, DS and Nestler, EJ (2012) Neurobiology of resilience. Nature Neuroscience 15(11), 14751484.CrossRefGoogle ScholarPubMed
Sales, AJ, Fogaça, MV, Sartim, AG, Pereira, VS, Wegener, G, Guimarães, FS and Joca, SRL (2018) Cannabidiol induces rapid and sustained antidepressant-like effects through increased BDNF signaling and synaptogenesis in the prefrontal cortex. Molecular Neurobiology 56(2), 10701081.CrossRefGoogle ScholarPubMed
Sales, AJ, Maciel, IS, Suavinha, ACDR and Joca, SRL (2021) Modulation of DNA methylation and gene expression in rodent cortical neuroplasticity pathways exerts rapid antidepressant-like effects. Molecular Neurobiology 58(2), 777794.CrossRefGoogle ScholarPubMed
Sartim, AG, Moreira, FA and Joca, SRL (2017) Involvement of CB1 and TRPV1 receptors located in the ventral medial prefrontal cortex in the modulation of stress coping behavior. Neuroscience 340, 126134.CrossRefGoogle ScholarPubMed
Schiller, GD, Pucilowski, O, Wienicke, C and Overstreet, DH (1992a) Immobility-reducing effects of antidepressants in a genetic animal model of depression. Brain Research Bulletin 28(5), 821823.CrossRefGoogle Scholar
Schiller, GD, Pucilowski, O, Wienicke, C and Overstreet, DH (1992b) Immobility-reducing effects of antidepressants in a genetic animal model of depression. Brain Research Bulletin 28(5), 821823.CrossRefGoogle Scholar
Sherman, AD and Petty, F (1980) Neurochemical basis of the action of antidepressants on learned helplessness. Behavioral and Neural Biology 30(2), 119134.CrossRefGoogle ScholarPubMed
Sherman, AD, Sacquitne, JL and Petty, F (1982) Specificity of the learned helplessness model of depression. Pharmacology Biochemistry and Behavior 16(3), 449454.CrossRefGoogle ScholarPubMed
Slattery, DA and Cryan, JF (2014) The ups and downs of modelling mood disorders in rodents. ILAR Journal 55(2), 297309.CrossRefGoogle ScholarPubMed
Slattery, DA, Desrayaud, S and Cryan, JF (2005) GABAB receptor antagonist-mediated antidepressant-like behavior is serotonin-dependent. Journal of Pharmacology and Experimental Therapeutics 312(1), 290296.CrossRefGoogle ScholarPubMed
Soares-Cunha, C, Coimbra, B, Borges, S, Domingues, AV, Silva, D, Sousa, N and Rodrigues, AJ (2018) Mild prenatal stress causes emotional and brain structural modifications in rats of both sexes. Frontiers in Behavioral Neuroscience 12, 115.CrossRefGoogle ScholarPubMed
Stanquini, LA, Biojone, C, Guimarães, FS and Joca, SR (2017) Repeated treatment with nitric oxide synthase inhibitor attenuates learned helplessness development in rats and increases hippocampal BDNF expression. Acta Neuropsychiatrica 30(3), 127136.CrossRefGoogle ScholarPubMed
Tejani-Butt, SM, Paré, WP and Yang, J (1994) Effect of repeated novel stressors on depressive behavior and brain norepinephrine receptor system in Sprague-Dawley and Wistar Kyoto (WKY) rats. Brain Research 649(1-2), 2735.CrossRefGoogle ScholarPubMed
Theilmann, W, Kleimann, A, Rhein, M, Bleich, S, Frieling, H, Löscher, W and Brandt, C (2016) Behavioral differences of male Wistar rats from different vendors in vulnerability and resilience to chronic mild stress are reflected in epigenetic regulation and expression of p11. Brain Research 1642, 505515.CrossRefGoogle ScholarPubMed
Tillmann, S (2017) Mind the gap – towards complete and transparent reporting of animal research. Medical Writing 26(4), 2427.Google Scholar
Tizabi, Y, Bhatti, BH, Manaye, KF, Das, JR and Akinfiresoye, L (2012) Antidepressant-like effects of low ketamine dose is associated with increased hippocampal AMPA/NMDA receptor density ratio in female Wistar-Kyoto rats. Neuroscience 213, 7280.CrossRefGoogle ScholarPubMed
Tizabi, Y, Hauser, SR, Tyler, KY, Getachew, B, Madani, R, Sharma, Y and Manaye, KF (2010) Effects of nicotine on depressive-like behavior and hippocampal volume of female WKY rats. Progress in Neuro-Psychopharmacology and Biological Psychiatry 34(1), 6269.CrossRefGoogle ScholarPubMed
Vollmayr, B and Gass, P (2013) Learned helplessness: unique features and translational value of a cognitive depression model. Cell and Tissue Research 354(1), 171178.CrossRefGoogle ScholarPubMed
Wang, Q, Timberlake, MA, Prall, K and Dwivedi, Y (2017) The recent progress in animal models of depression. Progress in Neuro-Psychopharmacology and Biological Psychiatry 77(3), 99109.CrossRefGoogle ScholarPubMed
Wieland, S, Boren, JL, Consroe, PF and Martin, A (1986) Stock differences in the susceptibility of rats to learned helplessness training. Life Sciences 39(10), 937944.CrossRefGoogle ScholarPubMed
Will, CC, Aird, F and Redei, EE (2003) Selectively bred Wistar-Kyoto rats: an animal model of depression and hyper-responsiveness to antidepressants. Molecular Psychiatry 8(11), 925932.CrossRefGoogle ScholarPubMed
Willner, P, Gruca, P, Lason, M, Tota-Glowczyk, K, Litwa, E, Niemczyk, M and Papp, M (2019) Validation of chronic mild stress in the Wistar-Kyoto rat as an animal model of treatment-resistant depression. Behavioural Pharmacology 30(2 and 3), 239250.CrossRefGoogle ScholarPubMed
Wood, CM, Nicolas, CS, Choi, SL, Roman, E, Nylander, I, Fernandez-Teruel, A, Kiianmaa, K, Bienkowski, P, de Jong, TR, Colombo, G, Chastagnier, D, Wafford, KA, Collingridge, GL, Wildt, SJ, Conway-Campbell, BL, Robinson, ESJ, Lodge, D (2017) Prevalence and influence of cys407* Grm2 mutation in Hannover-derived Wistar rats: mGlu2 receptor loss links to alcohol intake, risk taking and emotional behaviour. Neuropharmacology 115(3), 128138.CrossRefGoogle ScholarPubMed
Wood, SK and Bhatnagar, S (2015) Resilience to the effects of social stress: evidence from clinical and preclinical studies on the role of coping strategies. Neurobiology of Stress 1(1), 164173.CrossRefGoogle Scholar
Zazpe, A, Artaiz, I, Labeaga, L, Lucero, ML and Orjales, A (2007) Reversal of learned helplessness by selective serotonin reuptake inhibitors in rats is not dependent on 5-HT availability. Neuropharmacology 52(3), 975984.CrossRefGoogle Scholar