The chronic mild stress (CMS) model of depression: History, evaluation and usage

Neurobiology of Stress

Volumn 6, Issue , 2017, Pages 78-93

  Willner, Paul ^a  

^a SWANSEA UNIVERSITY   (United Kingdom)

Author keywords

Antidepressant; Chronic mild stress; Depression; Hippocampus; Neurobiology of stress; Prefrontal cortex; Reliability; Validity

Indexed keywords

ANTIDEPRESSANT AGENT;

ANHEDONIA; ANTIDEPRESSANT ACTIVITY; BEHAVIOR CHANGE; CHRONIC MILD STRESS MODEL; CHRONIC STRESS; DEPRESSION; DISEASE MODEL; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; HOST SUSCEPTIBILITY; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; NEUROBIOLOGY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; RELIABILITY; REVIEW; TRANSLATIONAL RESEARCH; VALIDITY;

EID: 84994079393     PISSN: None     EISSN: 23522895     Source Type: Journal    
DOI: 10.1016/j.ynstr.2016.08.002     Document Type: Review

References (245)

1. Adachi, M., Barrot, M., Autry, A.E., Theobald, D., Monteggia, L.M., Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol. Psychiatr. 63 (2008), 642–649.
2. American Psychiatric Association, DSM-5: Diagnostic and Statistical Manual of Mental Disorders. 2013, American Psychiatric Association, Washington DC.
3. Amr, M., El-Mogy, A., Shams, T., Vieira, K., Lakhan, S.E., Efficacy of vitamin C as an adjunct to fluoxetine therapy in pediatric major depressive disorder: a randomized, double-blind, placebo-controlled pilot study. Nutr. J., 12, 2013, 31.
4. Atanasova, B., El-Hage, W., Chabanet, C., Gaillard, P., Belzung, C., Camus, V., Olfactory anhedonia and negative olfactory alliesthesia in depressed patients. Psychiatry Res. 176 (2010), 190–196.
5. Banasr, M., Duman, R.S., Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol. Psychiatry 64 (2008), 863–870.
6. Banasr, M., Valentine, G.W., Li, X.Y., Gourley, S.L., Taylor, J.R., Duman, R.S., Chronic unpredictable stress decreases cell proliferation in the cerebral cortex of the adult rat. Biol. Psychiatry 62 (2007), 496–504.
7. Banasr, M., Chowdhury, G.M., Terwilliger, R., Newton, S.S., Duman, R.S., Behar, K.L., Sanacora, G., Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Mol. Psychiatry 15 (2010), 501–511.
8. Belzung, C., Billette de Villemeur, E., The design of new antidepressants: can formal models help? A first attempt using a model of the hippocampal control over the HPA-axis based on a review from the literature. Behav. Pharmacol. 21 (2010), 677–689.
9. Bergström, A., Jayatissa, M.N., Mørk, A., Wiborg, O., Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study. Brain Res. 1196 (2008), 41–52.
10. Bérubé, P., Poulin, J.F., Laforest, S., Drolet, G., Enkephalin knockdown in the basolateral amygdala reproduces vulnerable anxiety-like responses to chronic unpredictable stress. Neuropsychopharmacology 39 (2014), 1159–1168.
11. Bessa, J.M., Ferreira, D., Melo, I., Marques, F., Cerqueira, J.J., Palha, J.A., Almeida, O.F., Sousa, N., The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol. Psychiatry 14 (2009), 764–773.
12. Benelli, A., Filaferro, M., Bertolini, A., Genedani, S., Influence of S-adenosyl-L-methionine on chronic mild stress-induced anhedonia in castrated rats. Br. J. Pharmacol. 127 (1999), 645–654.
13. Berman, R.M., Cappiello, A., Anand, A., Oren, D.A., Heninger, G.R., Charney, D.S., Krystal, J.H., Antidepressant effects of ketamine in depressed patients. Biol. Psychiatry 47 (2000), 351–354.
14. Bersani, G., Meco, G., Denaro, A., Liberati, D., Colletti, C., Nicolai, R., Bersani, F.S., Koverech, A., L-Acetylcarnitine in dysthymic disorder in elderly patients: a double-blind, multicenter, controlled randomized study vs. fluoxetine. Eur. Neuropsychopharmacol. 23 (2013), 1219–1225.
15. Bewernick, B.H., Kayser, S., Sturm, V., Schlaepfer, T.E., Long-term effects of nucleus accumbens deep brain stimulation in treatment-resistant depression: evidence for sustained efficacy. Neuropsychopharmacology 37 (2012), 1975–1985.
16. Bisgaard, C.F., Jayatissa, M.N., Enghild, J.J., Sanchéz, C., Artemychyn, R., Wiborg, O., Proteomic investigation of the ventral rat hippocampus links DRP-2 to escitalopram treatment resistance and SNAP to stress resilience in the chronic mild stress model of depression. J. Mol. Neurosci. 32 (2007), 132–144.
17. Bondi, C.O., Jett, J.D., Morilak, D.A., Beneficial effects of desipramine on cognitive function of chronically stressed rats are mediated by alpha1-adrenergic receptors in medial prefrontal cortex. Prog. Neuropsychopharmacol. Biol. Psychiatry 34 (2010), 913–923.
18. Boulle, F., Massart, R., Stragier, E., Païzanis, E., Zaidan, L., Marday, S., Gabriel, C., Mocaer, E., Mongeau, R., Lanfumey, L., Hippocampal and behavioral dysfunctions in a mouse model of environmental stress: normalization by agomelatine. Transl. Psychiatry, 4, 2014, e485.
19. Burgdorf, J., Kroes, R.A., Zhang, X.L., Gross, A.L., Schmidt, M., Weiss, C., Disterhoft, J.F., Burch, R.M., Stanton, P.K., Moskal, J.R., Rapastinel (GLYX-13) has therapeutic potential for the treatment of post-traumatic stress disorder: characterization of a NMDA receptor-mediated metaplasticity process in the medial prefrontal cortex of rats. Behav. Brain Res. 294 (2015), 177–185.
20. Caldecott-Hazard, S., Mazziotta, J., Phelps, M., Cerebral correlates of depressed behavior in rats, visualized using 14C-2-deoxyglucose autoradiography. J. Neurosci. 8 (1988), 1951–1961.
21. Campbell, S., Marriott, M., Nahmias, C., MacQueen, G.M., Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am. J. Psychiatry 161 (2004), 598–607.
22. Castro, J.E., Diessler, S., Varea, E., Márquez, C., Larsen, M.H., Cordero, M.I., Sandi, C., 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 (2012), 1209–1223.
23. Chang, C.H., Grace, A.A., Amygdala-ventral pallidum pathway decreases dopamine activity after chronic mild stress in rats. Biol. Psychiatry 76 (2014), 223–230.
24. Cheeta, S., Broekkamp, C., Willner, P., Stereospecific reversal of stress-induced anhedonia by mianserin and its (+)-enantiomer. Psychopharmacology 116 (1994), 523–528.
25. Cheeta, S., Ruigt, G., van Proosdij, J., Willner, P., Changes in sleep architecture following chronic mild stress. Biol. Psychiatry 41 (1997), 419–427.
26. Chen, J., Wang, Z.Z., Zuo, W., Zhang, S., Chu, S.F., Chen, N.H., Effects of chronic mild stress on behavioral and neurobiological parameters - role of glucocorticoid. Horm. Behav. 78 (2016), 150–159.
27. Christensen, T., Bisgaard, C.F., Wiborg, O., Biomarkers of anehdonic-like behaviour, antidepressant drug refraction, and stress resilience in a rat model of depression. Neuroscience 196 (2011), 66–79.
28. Couch, Y., Anthony, D.C., Dolgov, O., Revischin, A., Festoff, B., Santos, A.I., Steinbusch, H.W., Strekalova, T., Microglial activation, increased TNF and SERT expression in the prefrontal cortex define stress-altered behaviour in mice susceptible to anhedonia. Brain Behav. Immun. 29 (2013), 136–146.
29. Couroussé, T., Bacq, A., Belzung, C., Guiard, B., Balasse, L., Louis, F., Le Guisquet, A.M., Gardier, A.M., Schinkel, A.H., Giros, B., Gautron, S., Brain organic cation transporter 2 controls response and vulnerability to stress and GSK3β signaling. Mol. Psychiatry, 2014, 10.1038/mp.2014.86 Aug 5.
30. Coyle, C.M., Laws, K.R., The use of ketamine as an antidepressant: a systematic review and meta-analysis. Hum. Psychopharmacol. 30 (2015), 152–163.
31. Cuadrado-Tejedor, M., Ricobaraza, A., Del Río, J., Frechilla, D., Franco, R., Pérez-Mediavilla, A., Garcia-Osta, A., Chronic mild stress in mice promotes cognitive impairment and CDK5-dependent tau hyperphosphorylation. Behav. Brain Res. 220 (2011), 338–343.
32. Cubelos, B., Gimenez, C., Zafra, F., Localization of the GLYT1 glycine transporter at glutamatergic synapses in the rat brain. Cereb. Cortex 15 (2005), 448–459.
33. D'Aquila, P., Brain, P.F., Willner, P., Effects of chronic mild stress in behavioural tests relevant to anxiety and depression. Physiol. Behav. 56 (1994), 861–867.
34. de Kloet, E.R., Otte, C., Kumsta, R., Kok, L., Hillegers, M.H., Hasselmann, H., Kliegel, D., Joëls, M., Stress and depression a crucial role of the mineralocorticoid receptor. J. Neuroendocrinol., 2016, 10.1111/jne.12379 2016 Mar 11.
35. Delgado, P.L., Charney, D.S., Price, L.H., Aghajanian, G.K., Landis, H., Heninger, G.R., Serotonin function and the mechanism of antidepressant action: reversal of antidepressant induced remission by rapid depletion of plasma tryptophan. Arch. Gen. Psychiatry 47 (1990), 411–418.
36. Delgado, P.L., Miller, H.M., Salomon, R.M., Licinio, J., Gelenberg, A.J., Charney, D.S., Monoamines and the mechanism of antidepressant action: effects of catecholamine depletion on mood in patients treated with antidepressants. Psychopharmacol. Bull. 29 (1993), 389–396.
37. Delgado, P.L., Miller, H.L., Salomon, R.M., Licinio, J., Krystal, J.H., Moreno, F.A., Heninger, G.R., Charney, D.S., Tryptophan-depletion challenge in depressed patients treated with desipramine or fluoxetine: implications for the role of serotonin in the mechanism of antidepressant action. Biol. Psychiatry 46 (1999), 212–220.
38. Delgado y Palacios, R., Campo, A., Henningsen, K., Verhoye, M., Poot, D., Dijkstra, J., Van Audekerke, J., Benveniste, H., Sijbers, J., Wiborg, O., Van der Linden, A., Magnetic resonance imaging and spectroscopy reveal differential hippocampal changes in anhedonic and resilient subtypes of the chronic mild stress rat model. Biol. Psychiatry 70 (2011), 449–457.
39. Delgado y Palacios, R., Verhoye, M., Henningsen, K., Wiborg, O., Van der Linden, A., Diffusion kurtosis imaging and high-resolution MRI demonstrate structural aberrations of caudate putamen and amygdala after chronic mild stress. PLoS One, 9(4), 2014, e95077.
40. Depoortère, R., Dargazanli, G., Estenne-Bouhtou, G., Coste, A., Lanneau, C., Desvignes, C., Poncelet, M., Heaulme, M., Santucci, V., Decobert, M., Cudennec, A., Voltz, C., Boulay, D., Terranova, J.P., Stemmelin, J., Roger, P., Marabout, B., Sevrin, M., Vigé, X., Biton, B., Steinberg, R., Françon, D., Alonso, R., Avenet, P., Oury-Donat, F., Perrault, G., Griebel, G., George, P., Soubrié, P., Scatton, B., Neurochemical, electrophysiological and pharmacological profiles of the selective inhibitor of the glycine transporter-1 SSR504734, a potential new type of antipsychotic. Neuropsychopharmacology 30 (2005), 1963–1985.
41. Dias-Ferreira, E., Sousa, J.C., Melo, I., Morgado, P., Mesquita, A.R., Cerqueira, J.J., Costa, R.M., Sousa, N., Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325 (2009), 621–625.
42. Diazgranados, N., Ibrahim, L., Brutsche, N.E., Newberg, A., Kronstein, P., Khalife, S., Kammerer, W.A., Quezado, Z., Luckenbaugh, D.A., Salvadore, G., Machado-Vieira, R., Manji, H.K., Zarate, C.A. Jr., A randomized add-on trial of an N-methyl-D-aspartate antagonist in treatment-resistant bipolar depression. Arch. Gen. Psychiatry 67 (2010), 793–802.
43. Dichter, G.S., Smoski, M.J., Kampov-Polevoy, A.B., Gallop, R., Garbutt, J.C., Unipolar depression does not moderate responses to the Sweet Taste Test. Depress. Anxiety 27 (2010), 859–863.
44. Di Chiara, G., Loddo, P., Tanda, G., Reciprocal changes in prefrontal and limbic dopamine responsiveness to aversive and rewarding stimuli after chronic mild stress: implications for the psychobiology of depression. Biol. Psychiatry 46 (1999), 1624–1633.
45. Disner, S.G., Beevers, C.G., Haigh, E.A., Beck, A.T., Neural mechanisms of the cognitive model of depression. Nat. Rev. Neurosci. 12 (2011), 467–477.
46. Dournes, C., Beeské, S., Belzung, C., Griebel, G., Deep brain stimulation in treatment-resistant depression in mice: comparison with the CRF1 antagonist, SSR125543. Prog. Neuropsychopharmacol. Biol. Psychiatry 40 (2013), 213–220.
47. Ducottet, C., Belzung, C., Behaviour in the elevated plus-maze predicts coping after subchronic mild stress in mice. Physiol. Behav. 81 (2004), 417–426.
48. Ducottet, C., Belzung, C., Correlations between behaviours in the elevated plus-maze and sensitivity to unpredictable subchronic mild stress: evidence from inbred strains of mice. Behav. Brain Res. 156 (2005), 153–162.
49. Ducottet, C., Aubert, A., Belzung, C., Susceptibility to subchronic unpredictable stress is related to individual reactivity to threat stimuli in mice. Behav. Brain Res. 155 (2004), 291–299.
50. Ducottet, C., Griebel, G., Belzung, C., Effects of the selective nonpeptide corticotropin-releasing factor receptor 1 antagonistantalarmin in the chronic mild stress model of depression in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 27 (2003), 625–631.
51. Duman, R.S., Monteggia, L.M., A neurotrophic model for stress-related mood disorders. Biol. Psych. 59 (2006), 1116–1127.
52. Duman, R.S., Li, N., Liu, R.J., Duric, V., Aghajanian, G., Signaling pathways underlying the rapid antidepressant actions of ketamine. Neuropharmacology 62 (2012), 35–41.
53. Dziedzicka-Wasylewska, M., Willner, P., Papp, M., Changes in dopamine receptor mRNA expression following chronic mild stress and chronic antidepressant treatment. Behav. Pharmacol. 8 (1997), 607–618.
54. Elizalde, N., Gil-Bea, F.J., Ramírez, M.J., Aisa, B., Lasheras, B., Del Rio, J., Tordera, R.M., Long-lasting behavioral effects and recognition memory deficit induced by chronic mild stress in mice: effect of antidepressant treatment. Psychopharmacol. Berl. 199 (2008), 1–14.
55. Elsayed, M., Banasr, M., Duric, V., Fournier, N.M., Licznerski, P., Duman, R.S., Antidepressant effects of fibroblast growth factor-2 in behavioral and cellular models of depression. Biol. Psychiatry 72 (2012), 258–265.
56. Farhang, S., Barar, J., Fakhari, A., Mesgariabbasi, M., Khani, S., Omidi, Y., Farnam, A., Asymmetrical expression of BDNF and NTRK3 genes in frontoparietal cortex of stress-resilient rats in an animal model of depression. Synapse, 68, 2014 387–293.
57. Farley, S., Dumas, S., El Mestikawy, S., Giros, B., Increased expression of the Vesicular Glutamate Transporter-1 (VGLUT1) in the prefrontal cortex correlates with differential vulnerability to chronic stress in various mouse strains: effects of fluoxetine and MK-801. Neuropharmacology 62 (2012), 503–517.
58. Fava, M., Targum, S.D., Nierenberg, A.A., Bleicher, L.S., Carter, T.A., Wedel, P.C., Hen, R., Gage, F.H., Barlow, C., An exploratory study of combination buspirone and melatonin SR in major depressive disorder (MDD): a possible role for neurogenesis in drug discovery. J. Psychiatr. Res. 46 (2012), 1553–1563.
59. Feng, S.F., Shi, T.Y., Fan-Yang, Wang WN., Chen, Y.C., Tan, Q.R., Long-lasting effects of chronic rTMS to treat chronic rodent model of depression. Behav. Brain Res. 232 (2012), 245–251.
60. Filho, C.B., Jesse, C.R., Donato, F., Giacomeli, R., Del Fabbro, L., da Silva Antunes, M., de Gomes, M.G., Goes, A.T., Boeira, S.P., Prigol, M., Souza, L.C., Chronic unpredictable mild stress decreases BDNF and NGF levels and Na(+),K(+)-ATPase activity in the hippocampus and prefrontal cortex of mice: antidepressant effect of chrysin. Neuroscience 289 (2015), 367–380.
61. Forbes, N.F., Stewart, C.A., Matthews, K., Reid, I.C., Chronic mild stress and sucrose consumption: validity as a model of depression. Physiol. Behav. 60 (1996), 1481–1484.
62. Forster, G.L., Novick, A.M., Scholl, J.L., Watt, M.J., The role of the amygdala in anxiety disorders. Ferry, B., (eds.) The Amygdala: a Discrete Multitasking Manager, 2012, InTech, Rijeka, Croatia.
63. French, S.J., Totterdell, S., Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus accumbens. J. Comp. Neurol. 446 (2002), 151–165.
64. French, S.J., Totterdell, S., Individual nucleus accumbens-projection neutons receive both basolateral amygdala and ventral subicular afferences in rats. Neuroscience 119 (2003), 19–31.
65. Furlanetti, L.L., Coenen, V.A., Aranda, I.A., Döbrössy, M.D., Chronic deep brain stimulation of the medial forebrain bundle reverses depressive-like behavior in a hemiparkinsonian rodent model. Exp. Brain Res. 233 (2015), 3073–3085.
66. Furr, A., Lapiz-Bluhm, M.D., Morilak, D.A., 5-HT2A receptors in the orbitofrontal cortex facilitate reversal learning and contribute to the beneficial cognitive effects of chronic citalopram treatment in rats. Int. J. Neuropsychopharmacol. 15 (2011), 1295–1305.
67. Gallagher, P., Malik, N., Newham, J., Young, A.H., Ferrier, I.N., Mackin, P., Antiglucocorticoid treatments for mood disorders. Cochrane Database Syst. Rev., 2008 CD005168.
68. Gálvez, J.F., Keser, Z., Mwangi, B., Ghouse, A.A., Fenoy, A.J., Schulz, P.E., Sanches, M., Quevedo, J., Selvaraj, S., Gajwani, P., Zunta-Soares, G., Hasan, K.M., Soares, J.C., The medial forebrain bundle as a deep brain stimulation target for treatment resistant depression: a review of published data. Prog. Neuropsychopharmacol. Biol. Psychiatry 58 (2015), 59–70.
69. Garcia, L.S., Comim, C.M., Valvassori, S.S., Réus, G.Z., Stertz, L., Kapczinski, F., Gavioli, E.C., Quevedo, J., Ketamine treatment reverses behavioral and physiological alterations induced by chronic mild stress in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 33 (2009), 450–455.
70. Garcia-Garcia, A.L., Elizalde, N., Matrov, N., Harro, J., Wojcik, S.M., Venzala, E., Ramírez, M.J., Del Rio, J., Tordera, R.M., Increased vulnerability to depressive-like behavior of mice with decreased expression of VGLUT1. Biol. Psychiatr. 66 (2009), 275–282.
71. García-Gutiérrez, M.S., Pérez-Ortiz, J.M., Gutiérrez-Adán, A., Manzanares, J., Depression-resistant endophenotype in mice overexpressing cannabinoid CB(2) receptors. Brit. J. Pharmacol. 160 (2010), 1773–1784.
72. Gersner, R., Toth, E., Isserles, M., Zangen, A., Site-specific antidepressant effects of repeated subconvulsive electrical stimulation: potential role of brain-derived neurotrophic factor. Biol. Psychiatry 67 (2010), 125–132.
73. Gorzalka, B.B., Hill, M.N., Putative role of endocannabinoid signaling in the etiology of depression and actions of antidepressants. Prog. Neuropsychopharmacol. Biol. Psychiatry 35 (2011), 1575–1585.
74. Goshen, I., Kreisel, T., Ben-Menachem-Zidon, O., Licht, T., Weidenfeld, J., Ben-Hur, T., Yirmiya, R., Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiatry 13 (2008), 717–728.
75. Gourley, S.L., Taylor, J.R., Recapitulation and reversal of a persistent depression-like syndrome in rodents. Curr. Protoc. Neurosci., 2009 Chapter 9: Unit 9.32.
76. Greene, J., Banasr, M., Lee, B., Warner-Schmidt, J., Duman, R.S., Vascular endothelial growth factor signaling is required for the behavioral actions of antidepressant treatment: pharmacological and cellular characterization. Neuropsychopharmacology 34 (2009), 2459–2568.
77. Griffiths, J., Shanks, M., Anisman, H., Strain-specific alterations in consumption of a palatable diet following repeated stressor exposure. Pharmacol. Biochem. Behav. 42 (1992), 219–227.
78. Grønli, J., Bramham, C., Murison, R., Kanhema, T., Fiske, E., Bjorvatn, B., Ursin, R., Portas, C.M., Chronic mild stress inhibits BDNF protein expression and CREB activation in the dentate gyrus but not in the hippocampus proper. Pharmacol. Biochem. Behav. 85 (2006), 842–849.
79. Guo, F., Zhang, Q., Zhang, B., Fu, Z., Wu, B., Huang, C., Li, Y., Burst-firing patterns in the prefrontal cortex underlying the neuronal mechanisms of depression probed by antidepressants. Eur. J. Neurosci., 40, 2014 3538–3347.
80. Hamani, C., Mayberg, H., Stone, S., Laxton, A., Haber, S., Lozano, A.M., The subcallosal cingulate gyrus in the context of major depression. Biol. Psych. 69 (2011), 301–308.
81. Hamani, C., Machado, D.C., Hipólide, D.C., Dubiela, F.P., Suchecki, D., Macedo, C.E., Tescarollo, F., Martins, U., Covolan, L., Nobrega, J.N., Deep brain stimulation reverses anhedonic-like behavior in achronic model of depression: role of serotonin and brain derived neurotrophic factor. Biol. Psychiatry 71 (2012), 30–35.
82. Han, X., Shao, W., Liu, Z., Fan, S., Yu, J., Chen, J., Qiao, R., Zhou, J., Xie, P., iTRAQ-based quantitative analysis of hippocampal postsynaptic density-associated proteins in a rat chronic mild stress model of depression. Neuroscience 298 (2015), 220–292.
83. Hanson, N.D., Owens, M.J., Nemeroff, C.B., Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology 36 (2011), 2589–2602.
84. Haridas, S., Kumar, M., Manda, K., Melatonin ameliorates chronic mild stress induced behavioral dysfunctions in mice. Physiol. Behav. 119 (2013), 201–207.
85. Henningsen, K., Andreasen, J.T., Bouzinova, E.V., Jayatissa, M.N., Jensen, M.S., Redrobe, J.P., Wiborg, O., Cognitive deficits in the rat chronic mild stress model for depression: relation to anhedonic-like responses. Behav. Brain Res. 198 (2009), 136–141.
86. Henningsen, K., Palmfeldt, J., Christiansen, S., Baiges, I., Bak, S., Jensen, O.N., Gregersen, N., Wiborg, O., Candidate hippocampal biomarkers of susceptibility and resilience to stress in a rat model of depression. Mol. Cell Proteomics, 2012 2012 Jul;11(7):M111.016428.
87. Hinwood, M., Morandini, J., Day, T.A., Walker, F.R., Evidence that microglia mediate the neurobiological effects of chronic psychological stress on the medial prefrontal cortex. Cereb. Cortex 22 (2011), 1442–1454.
88. Herman, J.P., Prewitt, C.M.F., Cullinan, W.E., Neuronal circuit regulation of the hypothalamo-pituitary-adrenocortical stress axis. Crit. Rev. Neurobiol. 10 (1996), 371–394.
89. Herman, J.P., Ostrander, M.M., Mueller, N.K., Figueiredo, H., Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychiatry 29 (2005), 1201–1213.
90. Hikosaka, O., The habenula: from stress-evasion to value-based decision making. Nat. Rev. Neurosci. 11 (2010), 503–513.
91. Hill, M.N., Hellemans, K.G., Verma, P., Gorzalka, B.B., Weinberg, J., Neurobiology of chronic mild stress: parallels to major depression. Neurosci. Biobehav Rev. 36 (2012), 2085–2117.
92. Hoeffer, C.A., Klann, E., mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci. 33 (2010), 67–75.
93. Ibarguen-Vargas, Y., Surget, A., Vourc'h, P., Leman, S., Andres, C., Gardier, A., Belzung, C., Deficit in BDNF level does not increase vulnerability to stress but dampens antidepressant-like effects in the unpredictable chronic mild stress. Behav. Brain Res. 202 (2009), 245–251.
94. Ide, J.S., Li, C.S.R., Error-related functional connectivity of the habenula in humans. Front. Hum. Neurosci., 5, 2011, 25.
95. Iñiguez, S.D., Vialou, V., Warren, B.L., Cao, J.L., Alcantara, L.F., Davis, L.C., Manojlovic, Z., Neve, R.L., Russo, S.J., Han, M.H., Nestler, E.J., Bolaños-Guzmán, C.A., Extracellular signal-regulated kinase-2 within the ventral tegmental area regulates responses to stress. J. Neurosci. 30 (2010), 7652–7663.
96. Jacobson, L., Sapolsky, R., The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 12 (1991), 118–134.
97. Jankord, R., Herman, J.P., Limbic regulation of hypothalamo-pituitary-adrenocortical function during acute and chronic stress. Ann. N. Y. Acad. Sci. 1148 (2008), 64–73.
98. Jayatissa, M.N., Bisgaard, C.F., West, M.J., Wiborg, O., The number of granule cells in rat hippocampus is reduced after chronic mild stress and re-established after chronic escitalopram treatment. Neuropharmacology 54 (2008), 530–541.
99. Jayatissa, M.N., Henningsen, K., Nikolajsen, G., West, M.J., Wiborg, O., A reduced number of hippocampal granule cells does not associate with an anhedonia-like phenotype in a rat chronic mild stress model of depression. Stress 13 (2010), 95–105.
100. Jin, P., Yu, H.L., Tian-Lan, Zhang F., Quan, Z.S., Antidepressant-like effects of oleoylethanolamide in a mouse model of chronic unpredictable mild stress. Pharmacol. Biochem. Behav. 133 (2015), 146–154.
101. Kallarackal, A.J., Kvarta, M.D., Cammarata, E., Jaberi, L., Cai, X., Bailey, A.M., Thompson, S.M., Chronic stress induces a selective decrease in AMPA receptor-mediated synaptic excitation at hippocampal temporoammonic-CA1 synapses. J. Neurosci. 33 (2013), 15669–15674.
102. Kanatsou, S., Fearey, B.C., Kuil, L.E., Lucassen, P.J., Harris, A.P., Seckl, J.R., Krugers, H., Joels, M., Overexpression of mineralocorticoid receptors partially prevents chronic stress-induced reductions in hippocampal memory and structural plasticity. PLoS One, 10(11), 2015, e0142012.
103. Katz, R.J., Animal model of depression: pharmacological sensitivity of a hedonic deficit. Pharmacol. Biochem. Behav. 16 (1982), 965–968.
104. Katz, R., Baldrighi, G., A further parametric study of imipramine in an animal model of depression. Pharmacol. Biochem. Behav. 16 (1982), 969–972.
105. Katz, R., Hersch, S., Amitriptyline and scopolamine in an animal model of depression. Neurosci. Biobehav Rev. 5 (1981), 265–271.
106. Katz, R., Roth, K., Carroll, B., Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neurosci. Biobehav Rev. 5 (1981), 247–251.
107. Katz, R., Roth, K., Schmaltz, K., Amphetamine and tranylcypromine in an animal model of depression. Pharmacological specificity of the reversal effect. Neurosci. Biobehav Rev. 5 (1981), 259–264.
108. Keating, C., Tilbrook, A., Kulkarni, J., Oestrogen: an overlooked mediator in the neuropsychopharmacology of treatment response?. Int. J. Neuropsychopharmacol. 14 (2011), 553–566.
109. 1H-NMR spectroscopy study at 11.7T. Neurosci. Lett. 572 (2014), 32–37.
110. Klimek, V., Papp, M., The effect of MK-801 and imipramine on beta-adrenergic and 5-HT2 receptors in the chronic mild stress model of depression in rats. Pol. J. Pharmacol. 46 (1994), 67–69.
111. Kling, M.A., Coleman, V.H., Schulkin, J., Glucocorticoid inhibition in the treatment of depression: can we think outside the endocrine hypothalamus?. Depress Anxiety 26 (2009), 641–649.
112. Kong, H., Sha, L.L., Fan, Y., Xiao, M., Ding, J.H., Wu, J., Hu, G., Requirement of AQP4 for antidepressive efficiency of fluoxetine: implication in adult hippocampal neurogenesis. Neuropsychopharmacology 34 (2009), 1263–1276.
113. Kreisel, T., Frank, M.G., Licht, T., Reshef, R., Ben-Menachem-Zidon, O., Baratta, M.V., Maier, S.F., Yirmiya, R., Dynamic microglial alterations underlie stress-induced depressive-like behavior and suppressed neurogenesis. Mol. Psychiatry 19 (2014), 699–709.
114. Kriston, L., von Wolff, A., Westphal, A., Hölzel, L.P., Härter, M., Efficacy and acceptability of acute treatments for persistent depressive disorder: a network meta-analysis. Depress Anxiety 31 (2014), 621–630.
115. Kvarta, M.D., Bradbrook, K.E., Dantrassy, H.M., Bailey, A.M., Thompson, S.M., Corticosterone mediates the synaptic and behavioral effects of chronic stress at rat hippocampal temporoammonic synapses. J. Neurophysiol. 114 (2015), 1713–1724.
116. Lattanzi, L., Dell'Osso, L., Cassano, P., Pini, S., Rucci, P., Houck, P.R., Gemignani, A., Battistini, G., Bassi, A., Abelli, M., Cassano, G.B., Pramipexole in treatment-resistant depression: a 16-week naturalistic study. Bipolar Disord. 4 (2002), 307–314.
117. Li, N., Lee, B., Liu, R.J., Banasr, M., Dwyer, J.M., Iwata, M., Li, X.Y., Aghajanian, G., Duman, R.S., mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329 (2010), 959–964.
118. Li, N., He, X., Zhang, Y., Qi, X., Li, H., Zhu, X., He, S., Brain-derived neurotrophic factor signalling mediates antidepressant effects of lamotrigine. Int. J. Neuropsychopharmacol. 14 (2011), 1091–1098.
119. Li, N., Liu, R.J., Dwyer, J.M., Banasr, M., Lee, B., Son, H., Li, X.Y., Aghajanian, G., Duman, R.S., Glutamate N-methyl-D-aspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure. Biol. Psychiatry 69 (2011), 754–761.
120. Li, X.L., Yuan, Y.G., Xu, H., Wu, D., Gong, W.G., Geng, L.Y., Wu, F.F., Tang, H., Xu, L., Zhang, Z.J., Changed synaptic plasticity in neural circuits of depressive-like and escitalopram-treated rats. Int. J. Neuropsychopharmacol., 18(10), 2015, pyv046.
121. Li, Y., Wang, H., Wang, X., Liu, Z., Wan, Q., Wang, G., Differential expression of hippocampal EphA4 and ephrinA3 in anhedonic-like behavior, stress resilience, and antidepressant drug treatment after chronic unpredicted mild stress. Neurosci. Lett. 566 (2014), 292–297.
122. Licznerski, P., Duman, R.S., Remodeling of axo-spinous synapses in the pathophysiology and treatment of depression. Neuroscience 251 (2013), 33–50.
123. Lim, L.W., Prickaerts, J., Huguet, G., Kadar, E., Hartung, H., Sharp, T., Temel, Y., Electrical stimulation alleviates depressive-like behaviors of rats: investigation of brain targets and potential mechanisms. Transl. Psychiatry, 5, 2015, e535.
124. Liu, D., Wang, Z., Gao, Z., Xie, K., Zhang, Q., Jiang, H., Pang, Q., Effects of curcumin on learning and memory deficits, BDNF, and ERK protein expression in rats exposed to chronic unpredictable stress. Behav. Brain Res. 271 (2014), 116–121.
125. Liu, R.J., Aghajanian, G.K., Stress blunts serotonin- and hypocretin-evoked EPSCs in prefrontal cortex: role of corticosterone-mediated apical dendritic atrophy. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 359–364.
126. Luo, L., Tan, R.X., Fluoxetine inhibits dendrite atrophy of hippocampal neurons by decreasing nitric oxide synthase expression in rat depression model. Acta Pharmacol. Sin. 22 (2001), 865–870.
127. Luo, L., Liu, X.L., Mu, R.H., Wu, Y.J., Liu, B.B., Geng, D., Liu, Q., Yi, L.T., Hippocampal BDNF signaling restored with chronic asiaticoside treatment in depression-like mice. Brain Res. Bull. 114 (2015), 62–69.
128. Luo, Y., Cao, Z., Wang, D., Wu, L., Li, Y., Sun, W., Zhu, Y., Dynamic study of the hippocampal volume by structural MRI in a rat model of depression. Neurol. Sci. 35 (2014), 1777–1783.
129. Magarinos, A.M., McEwen, B.S., Flugge, G., Fuchs, E., Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J. Neurosci. 16 (1996), 3534–3540.
130. Ma, X.C., Dang, Y.H., Jia, M., Ma, R., Wang, F., Wu, J., Gao, C.G., Hashimoto, K., Long-lasting antidepressant action of ketamine, but not glycogen synthase kinase-3 inhibitor SB216763, in the chronic mild stress model of mice. PLoS One, 8(2), 2013, e56053.
131. Mao, Q.Q., Huang, Z., Zhong, X.M., Xian, Y.F., Ip, S.P., Brain-derived neurotrophic factor signalling mediates the antidepressant-like effect of piperine in chronically stressed mice. Behav. Brain Res. 261 (2014), 140–145.
132. Martinowich, K., Manji, H., Lu, B., New insights into BDNF function in depression and anxiety. Nat. Neurosci. 10 (2007), 1089–1093.
133. Mateus-Pinheiro, A., Pinto, L., Bessa, J.M., Morais, M., Alves, N.D., Monteiro, S., Patrício, P., Almeida, O.F., Sousa, N., Sustained remission from depressive-like behavior depends on hippocampal neurogenesis. Transl. Psychiatry, 3, 2013 Jan 15, e210.
134. Matthews, K., Forbes, N., Reid, I.C., Sucrose consumption as a hedonic measure following chronic unpredictable mild stress. Physiol. Behav. 57 (1995), 241–248.
135. Mayberg, H.S., Targeted electrode-based modulation of neural circuits for depression. J. Clin. Investig. 119 (2009), 717–725.
136. McEwen, B.S., Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling. Ann. N. Y. Acad. Sci. 1204:Suppl. l (2010), E38–E59.
137. Meng, H., Wang, Y., Huang, M., Lin, W., Wang, S., Zhang, B., Chronic deep brain stimulation of the lateral habenula nucleus in a rat model of depression. Brain Res. 1422 (2011), 32–38.
138. Millan, M.J., Dekeyne, A., Papp, M., La Rochelle, C.D., MacSweeny, C., Peglion, J.L., Brocco, M., S33005, a novel ligand at both serotonin and norepinephrine transporters: II. Behavioral profile in comparison with venlafaxine, reboxetine, citalopram, and clomipramine. J. Pharmacol. Exp. Ther. 298 (2001), 581–591.
139. Miller, H.L., Delgado, P.L., Salomon, R.M., Berman, R., Krystal, J.H., Heninger, G.R., Charney, D.S., Clinical and biochemical effects of catecholamine depletion on antidepressant-induced remission of depression. Arch. Gen. Psychiatry 53 (1996), 117–128.
140. Mineur, Y.S., Belzung, C., Crusio, W.E., Functional implications of decreases in neurogenesis following chronic mild stress in mice. Neuroscience 150 (2007), 251–259.
141. Monleon, S., D'Aquila, P., Parra, A., Simon, V.M., Brain, P.F., Willner, P., Attenuation of sucrose consumption in mice by chronic mild stress and its restoration by imipramine. Psychopharmacology 117 (1994), 453–457.
142. Monteggia, L.M., Barrot, M., Powell, C.M., Berton, O., Galanis, V., Gemelli, T., Meuth, S., Nagy, A., Greene, R.W., Nestler, E.J., Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 10827–10832.
143. Monteiro, S., Roque, S., de Sá-Calçada, D., Sousa, N., Correia-Neves, M., Cerqueira, J.J., An Efficient Chronic Unpredictable Stress Protocol to Induce Stress-related Responses in C57BL/6 Mice. 2015.
144. Montgomery, S.A., Loft, H., Sánchez, C., Reines, E.H., Papp, M., Escitalopram (S-enantiomer of citalopram): clinical efficacy and onset of action predicted from a rat model. Pharmacol. Toxicol. 88 (2001), 282–286.
145. Morais, M., Santos, P.A., Mateus-Pinheiro, A., Patrício, P., Pinto, L., Sousa, N., Pedroso, P., Almeida, S., Filipe, A., Bessa, J.M., The effects of chronic stress on hippocampal adult neurogenesis and dendritic plasticity are reversed by selective MAO-A inhibition. J. Psychopharmacol. 28 (2014), 1178–1183.
146. Moreau, J.-L., Jenck, F., Martin, J.R., Mortas, P., Haefely, W.E., Antidepressant treatment prevents chronic mild stress-induced anhedonia as assessed by ventral tegmentum self-stimulation behaviour in rats. Eur. Neuropsychopharmacol. 2 (1992), 43–49.
147. Moreau, J.-L., Jenck, F., Martin, J.R., Mortas, P., Haefely, W.E., Effects of moclobemide, a new generation reversible MAO-A inhibitor, in a novel animal model of depression. Pharmacopsychiatry 26 (1993), 30–33.
148. Moretti, M., Colla, A., de Oliveira Balen, G., dos Santos, D.B., Budni, J., de Freitas, A.E., Farina, M., Severo Rodrigues, A.L., Ascorbic acid treatment, similarly to fluoxetine, reverses depressive-like behavior and brain oxidative damage induced by chronic unpredictable stress. J. Psychiatr. Res. 46 (2012), 331–340.
149. Muscat, R., Willner, P., Suppression of sucrose drinking by chronic mild unpredictable stress: a methodological analysis. Neurosci. Biobehav Rev. 16 (1992), 507–517.
150. Muscat, R., Sampson, D., Willner, P., Dopaminergic mechanism of imipramine action in an animal model of depression. Biol. Psychiatry 28 (1990), 223–229.
151. Muscat, R., Papp, M., Willner, P., Reversal of stress-induced anhedonia by the atypical antidepressants, fluoxetine and maprotiline. Psychopharmacology 109 (1992), 433–438.
152. Myers, B., McKlveen, J.M., Herman, J.P., Neural regulation of the stress response: the many faces of feedback. Cell Mol. Neurobiol., 2012, 10.1007/s10571-012-9801-y.
153. Nasca, C., Xenos, D., Barone, Y., Caruso, A., Scaccianoce, S., Matrisciano, F., Battaglia, G., Mathé, A.A., Pittaluga, A., Lionetto, L., Simmaco, M., Nicoletti, F., L-acetylcarnitine causes rapid antidepressant effects through the epigenetic induction of mGlu2 receptors. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 4804–4809.
154. Naudin, M., El-Hage, W., Gomes, M., Gaillard, P., Belzung, C., Atanasova, B., State and trait olfactory markers of major depression. PLoS One, 7(10), 2012, e46938.
155. Naudin, M., Mondon, K., El-Hage, W., Desmidt, T., Jaafari, N., Belzung, C., Gaillard, P., Hommet, C., Atanasova, B., Long-term odor recognition memory in unipolar major depression and Alzheimer's disease. Psychiatry Res. 220 (2014), 861–866.
156. Nibuya, M., Morinobu, S., Duman, R.S., Regulation of BDNF and TrkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neuosci. 15 (1995), 7539–7547.
157. Nieto-Gonzalez, J.L., Holm, M.M., Vardya, I., Christensen, T., Wiborg, O., Jensen, K., Presynaptic plasticity as a hallmark of rat stress susceptibility and antidepressant response. PLoS One, 10(3), 2015, e0119993.
158. Oomen, C.A., Mayer, J.L., de Kloet, E.R., Joels, M., Lucassen, P.J., Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur. J. Neurosci. 26 (2007), 3395–3401.
159. Onaivi, E.S., Ishiguro, H., Gong, J.P., Patel, S., Meozzi, P.A., Myers, L., Perchuk, A., Mora, Z., Tagliaferro, P.A., Gardner, E., Brusco, A., Akinshola, B.E., Liu, Q.R., Chirwa, S.S., Hope, B., Lujilde, J., Inada, T., Iwasaki, S., Macharia, D., Teasenfitz, L., Arinami, T., Uhl, G.R., Functional expression of brain neuronal CB2 cannabinoid receptors are involved in the effects of drugs of abuse and in depression. Ann. N. Y. Acad. Sci. 1139 (2008), 434–449.
160. Orsetti, M., Colella, L., Dellarole, A., Canonico, P.L., Ghi, P., Modification of spatial recognition memory and object discrimination after chronic administration of haloperidol, amitriptyline, sodium valproate or olanzapine in normal and anhedonic rats. Int. J. Neuropsychopharmacol. 10 (2007), 345–357.
161. Palumbo, M.L., Canzobre, M.C., Pascuan, C.G., Ríos, H., Wald, M., Genaro, A.M., Stress induced cognitive deficit is differentially modulated in BALB/c and C57Bl/6 mice: correlation with Th1/Th2 balance after stress exposure. J. Neuroimmunol. 218 (2010), 12–20.
162. Papp, M., Moryl, E., Antidepressant activity of non-competitive and competitive NMDA receptor antagonists in a chronic mild stress model of depression. Eur. J. Pharmacol. 263 (1994), 1–7.
163. Papp, M., Wieronska, J., Antidepressant-like activity of amisulpride in two animal models of depression. J. Psychopharmacol. 14 (2000), 46–52.
164. Papp, M., Willner, P., Muscat, R., An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacol 104 (1991), 255–259.
165. Papp, M., Lappas, S., Muscat, R., Willner, P., Attenuation of place preference conditioning but not place aversion conditioning by chronic mild stress. J. Psychopharmacol. 6 (1992), 352–356.
166. Papp, M., Klimek, V., Willner, P., Parallel changes in dopamine D2 receptor binding in limbic forebrain associated with chronic mild stress-induced anhedonia and its reversal by imipramine. Psychopharmacology 115 (1994), 441–446.
167. Papp, M., Moryl, E., Willner, P., Pharmacological validation of the chronic mild stress model of depression. Eur. J. Pharmacol. 296 (1996), 129–136.
168. Papp, M., Gruca, P., Boyer, P.A., Mocaër, E., Effect of agomelatine in the chronic mild stress model of depression in the rat. Neuropsychopharmacology 28 (2003), 694–703.
169. Papp, M., Gruca, P., Lason-Tyburkiewicz, M., Willner, P., Antidepressant, anxiolytic and pro-cognitive effects of subacute and chronic ketamine in the chronic mild stress model of depression. Behav. Pharmacol., 2016 (in press).
170. Papp, M., Gruca, P., Lason-Tyburkiewicz, M., Willner, P., Antidepressant, anxiolytic and pro-cognitive effects of anti-dementia drugs in the chronic mild stress model in rats. Psychopharmacology, 2016, 10.1007/s00213-016-4206-0.
171. Petrik, D., Lagace, D.C., Eisch, A.J., The neurogenesis hypothesis of affective and anxiety disorders: are we mistaking the scaffolding for the building?. Neuropharmacology 62 (2012), 21–34.
172. Pothion, S., Bizot, J.C., Trovero, F., Belzung, C., Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav. Brain Res. 155 (2004), 135–146.
173. Preskorn, S., Macaluso, M., Mehra, D.O., Zammit, G., Moskal, J.R., Burch, R.M., GLYX-13 Clinical Study Group. Randomized proof of concept trial of GLYX-13, an N-methyl-D-aspartate receptor glycine site partial agonist, in major depressive disorder nonresponsive to a previous antidepressant agent. J. Psychiatr. Pract. 21 (2015), 140–149.
174. Proulx, C.D., Hikosaka, O., Malinow, R., Reward processing by the lateral habenula in normal and depressive behaviors. Nat. Neurosci. 17 (2014), 1146–1152.
175. Pucilowski, O., Overstreet, D.H., Revzani, A.H., Janowsky, D.S., Chronic mild stress-induced anhedonia: greater effect in a genetic rat model of depression. Physiol. Behav. 54 (1993), 1215–1220.
176. Qiao, H., Li, M.X., Xu, C., Chen, H.B., An, S.C., Ma, X.M., Dendritic spines in depression: what we learned from animal models. Neural Plast., 2016, 2016, 8056370.
177. Radley, J.J., Sawchenko, P.E., Evidence for involvement of a limbic paraventricular hypothalamic inhibitory network in hypothalamic-pituitary-adrenal axis adaptations to repeated stress. J. Comp. Neurol. 523 (2015), 2769–2787.
178. Raison, C.L., Rutherford, R.E., Woolwine, B.J., Shuo, C., Schettler, P., Drake, D.F., Haroon, E., Miller, A.H., A randomized controlled trial of the tumor necrosis factor antagonist infliximab for treatment-resistant depression: the role of baseline inflammatory biomarkers. JAMA Psychiatry 70 (2013), 31–41.
179. Remus, J.L., Stewart, L.T., Camp, R.M., Novak, C.M., Johnson, J.D., Interaction of metabolic stress with chronic mild stress in altering brain cytokines and sucrose preference. Behav. Neurosci., 129, 2015 321–230.
180. Romano-Torres, M., Fernández-Guasti, A., Estradiol valerate elicits antidepressant-like effects in middle-aged female rats under chronic mild stress. Behav. Pharmacol. 21 (2010), 104–111.
181. Rossetti, A.C., Papp, M., Gruca, P., Paladini, M.S., Racagni, G., Riva, M.A., Molteni, R., Stress-induced anhedonia is associated with the activation of the inflammatory system in the rat brain: restorative effect of pharmacological intervention. Pharmacol. Res. 103 (2016), 1–12.
182. Rossini, D., Lucca, A., Zanardi, R., Magri, L., Smeraldi, E., Transcranial magnetic stimulation in treatment-resistant depressed patients: a double-blind, placebo-controlled trial. Psychiatry Res. 137 (2005), 1–10.
183. Saarelainen, T., Hendolin, P., Lucas, G., Koponen, E., Sairanen, M., MacDonald, E., Agerman, K., et al. Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J. Neurosci. 23 (2003), 349–357.
184. Sampson, D., Muscat, R., Willner, P., Reversal of antidepressant action by dopamine antagonists in an animal model of depression. Psychopharmacology 104 (1991), 491–495.
185. Samuels, B.A., Hen, R., Neurogenesis and affective disorders. Eur. J. Neurosci. 33 (2011), 1152–1159.
186. Sanmukhani, J., Satodia, V., Trivedi, J., Patel, T., Tiwari, D., Panchal, B., Goel, A., Tripathi, C.B., Efficacy and safety of curcumin in major depressive disorder: a randomized controlled trial. Phytother. Res. 28 (2014), 579–585.
187. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C., Hen, R., Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301 (2003), 805–809.
188. Sapolsky, R.M., Krey, L.C., McEwen, B.S., Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc. Natl. Acad. Sci. U. S. A. 81 (1984), 6174–6177.
189. Sarris, J., Murphy, J., Mischoulon, D., Papakostas, G.I., Fava, M., Berk, M., Ng, C.H., Adjunctive nutraceuticals for depression: a systematic review and meta-analyses. Am. J. Psychiatry 173 (2016), 575–587.
190. Sartorius, A., Kiening, K.L., Kirsch, P., von Gall, C.C., Haberkorn, U., Unterberg, A.W., Henn, F.A., Meyer-Lindenberg, A., Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol. Psychiatry 67 (2010), e9–e11.
191. Sesack, S.R., Grace, A.A., Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology 35 (2010), 27–47.
192. Sharma, H.R., Thakur, M.K., Correlation of ERα/ERβ expression with dendritic and behavioural changes in CUMS mice. Physiol. Behav. 145 (2015), 71–83.
193. Song, L., Che, W., Min-Wei, W., Murakami, Y., Matsumoto, K., Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol. Biochem. Behav. 83 (2006), 186–193.
194. Sousa, N., Lukoyanov, N.V., Madeira, M.D., Almeida, O.F., Paula-Barbosa, M.M., Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97 (2000), 253–266.
195. Stamford, J.A., Muscat, R., O'Connor, J.J., Patel, J., Trout, S.J., Wieczorek, W.J., Zruk, Z.L., Willner, P., Subsensitivity to reward following chronic mild stress is associated with increased release of mesolimbic dopamine. Psychopharmacology 105 (1991), 275–282.
196. Stedenfeld, K.A., Clinton, S.M., Kerman, I.A., Akil, H., Watson, S.J., Sved, A.F., Novelty-seeking behavior predicts vulnerability in a rodent model of depression. Physiol. Behav. 103 (2011), 210–216.
197. Steiner, J.E., Lidar-Lifschitz, D., Perl, E., Taste and odor: reactivity in depressive disorders, a multidisciplinary approach. Percept. Mot. Ski. 77 (1993), 1331–1346.
198. Strekalova, T., Steinbusch, H.W., Measuring behavior in mice with chronic stress depression paradigm. Prog. Neuropsychopharmacol. Biol. Psychiatry 34 (2010), 348–361.
199. Strekalova, T., Spanagel, R., Bartsch, D., Henn, F.A., Gass, P., Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29 (2004), 2007–2017.
200. Strekalova, T., Couch, Y., Kholod, N., Boyks, M., Malin, D., Leprince, P., Steinbusch, H.M., Update in the methodology of the chronic stress paradigm: internal control matters. Behav. Brain Funct., 7, 2011, 9.
201. Surget, A., Saxe, M., Leman, S., Ibarguen-Vargas, Y., Chalon, S., Griebel, G., Hen, R., Belzung, C., Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol. Psychiatry 64 (2008), 293–301.
202. Surget, A., Tanti, A., Leonardo, E.D., Laugeray, A., Rainer, Q., Touma, C., Palme, R., Griebel, G., Ibarguen-Vargas, Y., Hen, R., Belzung, C., Antidepressants recruit new neurons to improve stress response regulation. Mol. Psychiatry 16 (2011), 1177–1188.
203. Taliaz, D., Stall, N., Dar, D.E., Zangen, A., Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol. Psychiatry 15 (2010), 80–92.
204. Taliaz, D., Loya, A., Gersner, R., Haramati, S., Chen, A., Zangen, A., Resilience to chronic stress is mediated by hippocampal brain-derived neurotrophic factor. J. Neurosci. 31 (2011), 4475–4483.
205. Tanda, G., Frau, R., Di Chiara, G., Chronic Desipramine and Fluoxetine Differentially Affect Extracellular Dopamine in the Rat Prefrontal Cortex. 1996.
206. Tang, M., Lei, J., Sun, X., Liu, G., Zhao, S., Stress-induced anhedonia correlates with lower hippocampal serotonin transporter protein expression. Brain Res. 1513 (2013), 127–134.
207. Tang, J., Xue, W., Xia, B., Ren, L., Tao, W., Chen, C., Zhang, H., Wu, R., Wang, Q., Wu, H., Duan, J., Chen, G., Involvement of normalized NMDA receptor and mTOR-related signaling in rapid antidepressant effects of Yueju and ketamine on chronically stressed mice. Sci. Rep., 5, 2015, 13573.
208. Tang, M., Jiang, P., Li, H., Cai, H., Liu, Y., Gong, H., Zhang, L., Antidepressant-like effect of n-3 PUFAs in CUMS rats: role of tPA/PAI-1 system. Physiol. Behav. 139 (2015), 210–215.
209. Taylor, D., Sparshatt, A., Varma, S., Olofinjana, O., Antidepressant efficacy of agomelatine: meta-analysis of published and unpublished studies. Brit. Med. J., 348, 2014, g1888.
210. Theilmann, W., Kleimann, A., Rhein, M., Bleich, S., Frieling, H., Löscher, W., Brandt, C., 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 Res. 1642 (2016), 505–515 Jul 1.
211. Tye, K.M., Mirzabekov, J.J., Warden, M.R., Ferenczi, E.A., Tsai, H.C., Finkelstein, J., Kim, S.Y., Adhikari, A., Thompson, K.R., Andalman, A.S., Gunaydin, L.A., Witten, I.B., Deisseroth, K., Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493 (2013), 537–541.
212. Tyszkiewicz, J.P., Gu, Z., Wang, X., Cai, X., Yan, Z., Group II metabotropic glutamate receptors enhance NMDA receptor currents via a protein kinase C-dependent mechanism in pyramidal neurones of rat prefrontal cortex. J. Physiol. 554 (2004), 765–777.
213. Ulrich-Lai, Y.M., Herman, J.P., Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 10 (2009), 397–409.
214. Valverde, O., Torrens, M., CB1 receptor-deficient mice as a model for depression. Neuroscience 204 (2012), 193–206.
215. Vancassel, S., Leman, S., Hanonick, L., Denis, S., Roger, J., Nollet, M., Bodard, S., Kousignian, I., Belzung, C., Chalon, S., n-3 polyunsaturated fatty acid supplementation reverses stress-induced modifications on brain monoamine levels in mice. J. Lipid Res. 49 (2008), 340–348.
216. Videbech, P., Ravnkilde, B., Hippocampal volume and depression: a meta-analysis of MRI studies. Am. J. Psychiatry 161 (2004), 1957–1966.
217. Walker, F.R., Nilsson, M., Jones, K., Acute and chronic stress-induced disturbances of microglial plasticity, phenotype and function. Curr. Drug Targets 14 (2013), 1262–1276.
218. Wang, H.N., Wang, L., Zhang, R.G., Chen, Y.C., Liu, L., Gao, F., Nie, H., Hou, W.G., Peng, Z.W., Tan, Q., Anti-depressive mechanism of repetitive transcranial magnetic stimulation in rat: the role of the endocannabinoid system. J. Psychiatr. Res. 51 (2014), 79–87.
219. Wang, S.S., Yan, X.B., Hofman, M.A., Swaab, D.F., Zhou, J.N., Increased expression level of corticotropin-releasing hormone in the amygdala and in the hypothalamus in rats exposed to chronic unpredictable mild stress. Neurosci. Bull. 26 (2010), 297–303.
220. Warner-Schmidt, J.L., Duman, R.S., VEGF is an essential mediator of the neurogenic and behavioral actions of antidepressants. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 4647–4652.
221. Wiborg, O., Chronic mild stress for modeling anhedonia. Cell Tissue Res. 354 (2013), 155–169.
222. Willner, P., Validity, reliability and utility of the chronic mild stress (CMS) model of depression: a ten-year review and evaluation. Psychopharmacology 134 (1997), 319–329.
223. Willner, P., The validity of animal models of depression. Psychopharmacology 83 (1984), 1–16.
224. Willner, P., Animal models for psychiatric states. Stolerman, I.P., (eds.) Encyclopedia of Psychopharmacology, 2009, Springer, Heidelberg.
225. Willner, P., Reliability of the chronic mild stress model of depression: a user survey. Neurobiol. Stress 6 (2017), 68–77.
226. Willner, P., Belzung, C., Treatment-resistant depression: are animal models of depression fit for purpose?. Psychopharmacology 232 (2015), 3473–3495.
227. Willner, P., Towell, A., Sampson, D., Muscat, R., Sophokleous, S., Reduction of sucrose preference by chronic mild stress and its restoration by a tricyclic antidepressant. Psychopharmacology 93 (1987), 358–364.
228. Willner, P., Muscat, R., Papp, M., Chronic mild stress-induced anhedonia: a realistic animal model of depression. Neurosci. Biobehav. Rev. 16 (1992), 525–534.
229. Willner, P., Lappas, S., Cheeta, S., Muscat, R., Reversal of stress-induced anhedonia by the dopamine receptor agonist, pramipexole. Psychopharmacology 115 (1994), 454–462.
230. Willner, P., Moreau, J.-M., Nielsen, C., Papp, M., Sluzewska, A., Decreased hedonic responsiveness following chronic mild stress is not secondary to loss of body weight. Physiol. Behav. 60 (1996), 129–134.
231. Willner, P., Hale, A.S., Argyropoulos, S., Dopaminergic mechanism of antidepressant action in depressed patients. J. Affect. Disord. 86 (2005), 37–45.
232. Willner, P., Scheel-Kruger, J., Belzung, C., The neuropharmacology of depression and antidepressant treatment. Neurosci. Biobehav. Rev. 37 (2013), 2331–2371.
233. Willner, P., Belzung, C., Scheel-Kruger, J., Resistance to antidepressant drugs: the case for a more predisposition-based and less hippocampocentric research paradigm. Behav. Pharmacol. 25 (2014), 352–371.
234. Wong, E.Y., Herbert, J., The corticoid environment: a determining factor for neural progenitors' survival in the adult hippocampus. Eur. J. Neurosci. 20 (2004), 2491–2498.
235. Wu, L.M., Han, H., Wang, Q.N., Hou, H.L., Tong, H., Yan, X.B., Zhou, J.N., Mifepristone repairs region-dependent alteration of synapsin I in hippocampus in rat model of depression. Neuropsychopharmacology 32 (2007), 2500–2510.
236. Yi, L.T., Liu, B.B., Li, J., Luo, L., Liu, Q., Geng, D., Tang, Y., Xia, Y., Wu, D., BDNF signaling is necessary for the antidepressant-like effect of naringenin. Prog. Neuropsychopharmacol. Biol. Psychiatry 48 (2014), 135–141.
237. Zacharko, R.M., Bowers, W.J., Kokkinidis, L., Anisman, H., Region specific reductions of intracranial self-stimulation after uncontrollable stress: possible effects on reward processes. Behav. Brain Res. 9 (1983), 129–141.
238. Zacharko, R.M., Bowers, W.J., Anisman, H., Responding for brain stimulation: stress and desmethylimipramine. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 8 (1984), 601–606.
239. Zarate, C.A. Jr., Payne, J.L., Quiroz, J., Sporn, J., Denicoff, K.K., Luckenbaugh, D., Charney, D.S., Manji, H.K., An open-label trial of riluzole in patients with treatment-resistant major depression. Am. J. Psychiatry 161 (2004), 171–174.
240. Zarate, C.A. Jr., Singh, J.B., Carlson, P.J., Brutsche, N.E., Ameli, R., Luckenbaugh, D.A., Charney, D.S., Manji, H.K., A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch. Gen. Psychiatry 63 (2006), 856–864.
241. Zhao, Y., Wang, Z., Dai, J., Chen, L., Huang, Y., Zhan, Z., Beneficial effects of benzodiazepine diazepam on on chronic stress-induced impairment of hippocampal structural plasticity and depression-like behavior in mice. Behav. Brain Res. 228 (2012), 339–350.
242. Zhu, S., Shi, R., Wang, J., Wang, J.F., Li, X.M., Unpredictable chronic mild stress not chronic restraint stress induces depressive behaviours in mice. Neuroreport 25 (2014), 1151–1155.
243. Zhu, W.L., Wang, S.J., Liu, M.M., Shi, H.S., Zhang, R.X., Liu, J.F., Ding, Z.B., Lu, L., Glycine site N-methyl-D-aspartate receptor antagonist 7-CTKA produces rapid antidepressant-like effects in male rats. J. Psychiatry Neurosci. 38 (2013), 306–316.
244. Zobel, A.W., Nickel, T., Künzel, H.E., Ackl, N., Sonntag, A., Ising, M., Holsboer, F., Effects of the high-affinity corticotropin-releasing hormone receptor 1 antagonist R121919 in major depression: the first 20 patients treated. J. Psychiatr. Res. 34 (2000), 171–181.
245. 2 receptor plasticity contributes to stress resilience in rats subjected to chronic mild stress. Psychopharmacology 227 (2013), 583–593.