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Cited by 370Neurotransmitter Receptor Influence on BehaviorTreatment of Major DepressionStress Responses and Cortisol

The recent progress in animal models of depression

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Wang, Qingzhong, Timberlake, Matthew A., Prall, Kevin, Dwivedi, Yogesh·2017·Progress in Neuro-Psychopharmacology and Biological Psychiatry
DOI 10.1016/j.pnpbp.2017.04.008PMC PMC5605906
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Abstract

Major depression disorder (MDD) is a debilitating mental illness with significant morbidity and mortality. Despite the growing number of studies that have emerged, the precise underlying mechanisms of MDD remain unknown. When studying MDD, tissue samples like peripheral blood or post-mortem brain samples are used to elucidate underlying mechanisms. Unfortunately, there are many uncontrollable factors with such samples such as medication history, age, time after death before post-mortem tissue was collected, age, sex, race, and living conditions. Although these factors are critical, they introduce confounding variables that can influence the outcome profoundly. In this regard, animal models provide a crucial approach to examine neural circuitry and molecular and cellular pathways in a controlled environment. Further, manipulations with pharmacological agents and gene editing are accepted methods of studying depression in animal models, which is impossible to employ in human patient studies. Here, we have reviewed the most widely used animal models of depression and delineated the salient features of each model in terms of behavioral and neurobiological outcomes. We have also illustrated the current challenges in using these models and have suggested strategies to delineate the underlying mechanism associated with vulnerability or resilience to developing depression.

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  1. Abdolmaleky HM Thiagalingam S Wilcox M 2005 Genetics and epigenetics in major psychiatric disorders Am J Pharmacogenomics 5 3 149 160 15952869
  2. Abrous DN Koehl M Le Moal M 2005 Adult neurogenesis: from precursors to network and physiology Physiol Rev 85 2 523 569 15788705
  3. Alvarez C Vitalis T Fon E Hanoun N Hamon M Seif I Edwards R Gaspar P Cases O 2002 Effects of genetic depletion of monoamines on somatosensory cortical development Neuroscience 115 3 753 764 12435414
  4. Amat J Baratta MV Paul E Bland ST Watkins LR Maier SF 2005 Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus Nat Neurosci 8 3 365 371 15696163
  5. Anisman H Matheson K 2005 Stress, depression, and anhedonia: caveats concerning animal models Neurosci Biobehav Rev 29 4 525 546 15925696
  6. Aznar S Klein AB Santini MA Knudsen GM Henn F Gass P Vollmayr B 2010 Aging and depression vulnerability interaction results in decreased serotonin innervation associated with reduced BDNF levels in hippocampus of rats bred for learned helplessness Synapse 64 7 561 20222154
  7. Bahi A Chandrasekar V Dreyer J-L 2014 Selective lentiviral-mediated suppression of microRNA124a in the hippocampus evokes antidepressants- like effects in rats Psychoneuroendocrinology 46 78 87 24882160
  8. Bai M Zhu X Zhang Y Zhang S Zhang L Xue L Yi J Yao S Zhang X 2012 Abnormal hippocampal BDNF and miR-16 expression is associated with depression-like behaviors induced by stress during early life PLoS One 7 10 e46921 23056528 PMC3466179
  9. Baudry A Mouillet-Richard S Schneider B Launay J-M Kellermann O 2010 miR-16 targets the serotonin transporter: a new facet for adaptive responses to antidepressants Science 329 5998 1537 1541 20847275
  10. Belzung C Lemoine M 2011 Criteria of validity for animal models of psychiatric disorders: focus on anxiety disorders and depression Biol Mood Anxiety Disord 1 1 1 22738250 PMC3384226
  11. Björkqvist K 2001 Social defeat as a stressor in humans Physiol Behav 73 3 435 442 11438372
  12. Bland ST Tamlyn JP Barrientos RM Greenwood BN Watkins LR Campeau S Day HE Maier SF 2007 Expression of fibroblast growth factor-2 and brain-derived neurotrophic factor mRNA in the medial prefrontal cortex and hippocampus after uncontrollable or controllable stress Neuroscience 144 4 1219 1228 17197100 PMC1904349
  13. Bohus B Koolhaas JM Heijneri C de Boer O 1993 Immunological responses to social stress: dependence on social environment and coping abilities Neuropsychobiology 28 1–2 95 99 8255418
  14. Brandão ML Zanoveli JM Ruiz-Martinez RC Oliveira LC Landeira-Fernandez J 2008 Different patterns of freezing behavior organized in the periaqueductal gray of rats: association with different types of anxiety Behav Brain Res 188 1 1 13 18054397
  15. Brunello N Mendlewicz J Kasper S Leonard B Montgomery S Nelson JC Paykel E Versiani M Racagni G 2002 The role of noradrenaline and selective noradrenaline reuptake inhibition in depression Eur Neuropsychopharmacol 12 5 461 475 12208564
  16. Bunney WE Bunney BG Vawter MP Tomita H Li J Evans SJ Choudary PV Myers RM Jones EG Watson SJ 2003 Microarray technology: a review of new strategies to discover candidate vulnerability genes in psychiatric disorders Am J Psychiatry 160 4 657 666 12668351
  17. Butler LD Layman NK Riedl PE Cain RL Shellhaas J Evans GF Zuckerman SH 1989 Neuroendocrine regulation of in vivo cytokine production and effects: I. In vivo regulatory networks involving the neuroendocrine system, interleukin-1 and tumor necrosis factor-α J Neuroimmunol 24 1–2 143 153 2681261
  18. Calvano SE Xiao W Richards DR Felciano RM Baker HV Cho RJ Chen RO Brownstein BH Cobb JP Tschoeke SK 2005 A network-based analysis of systemic inflammation in humans Nature 437 7061 1032 1037 16136080
  19. Cao M Chen D Zhang C Wu Z 2013 Screening of specific microRNA in hippocampus of depression model rats and intervention effect of Chaihu Shugan San Zhongguo Zhong Yao Za Zhi 38 10 1585 1589 23947143
  20. Carney RM Freedland KE Miller GE Jaffe AS 2002 Depression as a risk factor for cardiac mortality and morbidity: a review of potential mechanisms J Psychosom Res 53 4 897 902 12377300
  21. Caspi A Moffitt TE 2006 Gene–environment interactions in psychiatry: joining forces with neuroscience Nature Rev Neurosci 7 7 583 590 16791147
  22. Champagne F Diorio J Sharma S Meaney MJ 2001 Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors Proc Natl Acad Sci 98 22 12736 12741 11606726 PMC60123
  23. Chertkow-Deutsher Y Cohen H Klein E Ben-Shachar D 2010 DNA methylation in vulnerability to post-traumatic stress in rats: evidence for the role of the post-synaptic density protein Dlgap2 Int J Neuropsychopharmacol 13 3 347 359 19793403
  24. Chourbaji S Hörtnagl H Molteni R Riva M Gass P Hellweg R 2012 The impact of environmental enrichment on sex-specific neurochemical circuitries–effects on brain-derived neurotrophic factor and the serotonergic system Neuroscience 220 267 276 22710068
  25. Chourbaji S Zacher C Sanchis-Segura C Dormann C Vollmayr B Gass P 2005 Learned helplessness: validity and reliability of depressive-like states in mice Brain Res Prot 16 1 70 78 16338640
  26. Corum RC Thurmond JB 1977 Effects of acute exposure to stress on subsequent aggression and locomotion performance Psychosom Med 39 6 436 443 563607
  27. Crema L Schlabitz M Tagliari B Cunha A Simão F Krolow R Pettenuzzo L Salbego C Vendite D Wyse AT 2010 Na+, K+ ATPase activity is reduced in amygdala of rats with chronic stress-induced anxiety- like behavior Neurochem Res 35 11 1787 1795 20717721
  28. Cryan JF Bruijnzeel AW Skjei KL Markou A 2003 Bupropion enhances brain reward function and reverses the affective and somatic aspects of nicotine withdrawal in the rat Psychopharmacology 168 3 347 358 12698231
  29. Daniels W Pietersen C Carstens M Stein D 2004 Maternal separation in rats leads to anxiety- like behavior and a blunted ACTH response and altered neurotransmitter levels in response to a subsequent stressor Metab Brain Dis 19 1–2 3 14 15214501
  30. Delgado PL 2000 Depression: the case for a monoamine deficiency J Clin Psychiatry 61 suppl 6 7 11 10775018
  31. Denenberg VH 1969 Open-filed behavior in the rat: what does it mean ? Ann N Y Acad Sci 159 3 852 859 5260302
  32. Dibbets P van den Broek A Evers EA 2015 Fear conditioning and extinction in anxiety-and depression-prone persons Memory 23 3 350 364 24601711
  33. Dwivedi Y Mondal AC Shukla PK Rizavi HS Lyons J 2004 Altered protein kinase a in brain of learned helpless rats: effects of acute and repeated stress Biol Psychiatry 56 1 30 40 15219470
  34. Dwivedi Y Rizavi HS Conley RR Roberts RC Tamminga CA Pandey GN 2003 Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects Arch Gen Psychiatry 60 8 804 815 12912764
  35. Dwivedi Y Roy B Lugli G Rizavi H Zhang H Smalheiser N 2015 Chronic corticosterone-mediated dysregulation of microRNA network in prefrontal cortex of rats: relevance to depression pathophysiology Transl Psychiatry 5 11 e682 26575223 PMC5068767
  36. Elliott E Ezra-Nevo G Regev L Neufeld-Cohen A Chen A 2010 Resilience to social stress coincides with functional DNA methylation of the Crf gene in adult mice Nat Neurosci 13 11 1351 1353 20890295
  37. Enthoven L Oitzl M Koning N Van Der Mark M De Kloet E 2008 Hypothalamic-pituitary-adrenal axis activity of newborn mice rapidly desensitizes to repeated maternal absence but becomes highly responsive to novelty Endocrinology 149 12 6366 6377 18635659
  38. Etzersdorfer E Klein J Baus N Sonneck G Kapusta ND 2015 Epidemiology of suicide in Austria during 2000–2010: potential years of life lost: time for the national suicide prevention program Wien Klin Wochenschr 25732917
  39. Fon EA Pothos EN Sun B-C Killeen N Sulzer D Edwards RH 1997 Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action Neuron 19 6 1271 1283 9427250
  40. Fukui M Rodriguiz RM Zhou J Jiang SX Phillips LE Caron MG Wetsel WC 2007 Vmat2 heterozygous mutant mice display a depressive-like phenotype J Neurosci 27 39 10520 10529 17898223 PMC2855647
  41. Gold PW Goodwin FK Chrousos GP 1988 Clinical and biochemical manifestations of depression N Engl J Med 319 6 348 353 3292920
  42. Gregus A Wintink AJ Davis AC Kalynchuk LE 2005 Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats Behav Brain Res 156 1 105 114 15474655
  43. Gutknecht L Popp S Waider J Sommerlandt FM Göppner C Post A Reif A van den Hove D Strekalova T Schmitt A 2015 Interaction of brain 5-HT synthesis deficiency, chronic stress and sex differentially impact emotional behavior in Tph2 knockout mice Psychopharmacology (Berl) 232 14 2429 2441 25716307 PMC4480945
  44. Hall RD Macrides F 1983 Olfactory bulbectomy impairs the rat’s radial-maze behavior Physiol Behav 30 5 797 803 6878484
  45. Harkin A Kelly JP Leonard BE 2003 A review of the relevance and validity of olfactory bulbectomy as a model of depression Clin Neurosci Res 3 4 253 262
  46. Hellweg R Zueger M Fink K Hörtnagl H Gass P 2007 Olfactory bulbectomy in mice leads to increased BDNF levels and decreased serotonin turnover in depression-related brain areas Neurobiol Dis 25 1 1 7 16990008
  47. Helmstetter FJ Bellgowan PS 1994 Effects of muscimol applied to the basolateral amygdala on acquisition and expression of contextual fear conditioning in rats Behav Neurosci 108 5 1005 7826507
  48. Heninger GR Charney DS Sternberg DE 1984 Serotonergic function in depression: prolactin response to intravenous tryptophan in depressed patients and healthy subjects Arch Gen Psychiatry 41 4 398 402 6703856
  49. Huhman KL 2006 Social conflict models: can they inform us about human psychopathology? Horm Behav 50 4 640 646 16870189
  50. Ilango A Shumake J Wetzel W Scheich H Ohl FW 2012 The role of dopamine in the context of aversive stimuli with particular reference to acoustically signaled avoidance learning Front Neurosci 6 132 23049495 PMC3442182
  51. Jancsar S Leonard B 1984 The effect of (±) mianserin and its enantiomers on the behavioural hyperactivity of the olfactory-bulbectomized rat Neuropharmacology 23 9 1065 1070 6083502
  52. Jarosik J Legutko B Unsicker K Halbach OvB 2007 Antidepressant-mediated reversal of abnormal behavior and neurodegeneration in mice following olfactory bulbectomy Exp Neurol 204 1 20 28 17059819
  53. Jiao L Zhang J Li Z Liu H Chen Y Xu S 2011 Edaravone alleviates delayed neuronal death and long-dated cognitive dysfunction of hippocampus after transient focal ischemia in Wistar rat brains Neuroscience 182 177 183 21241778
  54. Katz R Roth K Carroll B 1981 Acute and chronic stress effects on open field activity in the rat: implications for a model of depression Neurosci Biobehav Rev 5 2 247 251 7196554
  55. Kelly J Wrynn A Leonard B 1997 The olfactory bulbectomized rat as a model of depression: an update Pharmacol Ther 74 3 299 316 9352586
  56. Kember R Dempster E Lee T Schalkwyk LC Mill J Fernandes C 2012 Maternal separation is associated with strain-specific responses to stress and epigenetic alterations to Nr3c1, Avp, and Nr4a1 in mouse Brain Behav 2 4 455 467 22950049 PMC3432968
  57. Kendler KS Gardner CO Prescott CA 2002 Toward a comprehensive developmental model for major depression in women Am J Psychiatry 159 7 1133 1145 12091191
  58. Kim H Lee H Rowan J Brahim J Dionne RA 2006 Genetic polymorphisms in monoamine neurotransmitter systems show only weak association with acute post-surgical pain in humans Mol Pain 2 1 1 16848906 PMC1543620
  59. Klein DF 1974 Endogenomorphic depression: a conceptual and terminological revision Arch Gen Psychiatry 31 4 447 454 4420562
  60. Kohen R Kirov S Navaja G Happe HK Hamblin M Snoddy J Neumaier J Petty F 2005 Gene expression profiling in the hippocampus of learned helpless and nonhelpless rats Pharmacogenomics J 5 5 278 291 16010284
  61. Koolhaas J Meerlo P De Boer S Strubbe J Bohus B 1997 The temporal dynamics of the stress response Neurosci Biobehav Rev 21 6 775 782 9415902
  62. Kovacs M Garrison B 1985 Hopelessness and eventual suicide: a 10-year prospective study of patients hospitalized with suicidal ideation Am J Psychiatry 1 42 559 563 3985195
  63. Krishnan V Nestler EJ 2008 The molecular neurobiology of depression Nature 455 7215 894 902 18923511 PMC2721780
  64. LeDoux JE Cicchetti P Xagoraris A Romanski LM 1990 The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning J Neurosci 10 4 1062 1069 2329367 PMC6570227
  65. LeDoux JE Thompson ME Iadecola C Tucker LW Reis DJ 1983 Local cerebral blood flow increases during auditory and emotional processing in the conscious rat Science 221 4610 576 578 6867731
  66. Lee J-H Kim HJ Kim JG Ryu V Kim B-T Kang D-W Jahng JW 2007 Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation Neurosci Res 58 1 32 39 17298851
  67. Leonard B Tuite M 1981 Anatomical, physiological, and behavioral aspects of olfactory bulbectomy in the rat Int Rev Neurobiol 22 251 286 7024168
  68. Levine S 1967 Maternal and environmental influences on the adrenocortical response to stress in weanling rats Science 156 3772 258 260 6021047
  69. Levine S 2005 Developmental determinants of sensitivity and resistance to stress Psychoneuroendocrinology 30 10 939 946 15958281
  70. Lewis DA 2002 The human brain revisited: opportunities and challenges in postmortem studies of psychiatric disorders Neuropsychopharmacology 26 143 154 11790510
  71. Li K Zhou T Liao L Yang Z Wong C Henn F Malinow R Yates JR Hu H 2013 βCaMKII in lateral habenula mediates core symptoms of depression Science 341 6149 1016 1020 23990563 PMC3932364
  72. Lloyd C 1980 Life events and depressive disorder reviewed: II. Events as precipitating factors Arch Gen Psychiatry 37 5 541 548 7377910
  73. Lotrich F 2012 Inflammatory cytokines, growth factors, and depression Curr Pharm Des 18 36 5920 5935 22681170
  74. Lumia AR Teicher MH Salchli F Ayers E Possidente B 1992 Olfactory bulbectomy as a model for agitated hyposerotonergic depression Brain Res 587 2 181 185 1525654
  75. Lyons DM Kim S Schatzberg AF Levine S 1998 Postnatal foraging demands alter adrenocortical activity and psychosocial development Dev Psychobiol 32 4 285 291 9589217
  76. MacQueen GM Ramakrishman K Croll SD Siuciak JA Yu G Young T Fahnestock M 2001 Performance of heterozygous brain-derived neurotrophic factor knockout mice on behavioral analogues of anxiety, nociception, and depression Behav Neurosci 115 5 1145 11584927
  77. Magarin A McEwen B 1995 Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors Neuroscience 69 1 89 98 8637636
  78. Magariños AM Deslandes A McEwen BS 1999 Effects of antidepressants and benzodiazepine treatments on the dendritic structure of CA3 pyramidal neurons after chronic stress Eur J Pharmacol 371 2 113 122 10357248
  79. Mahata S Mahata M Fischer-Colbrie R Winkler H 1993 Vesicle monoamine transporters 1 and 2: differential distribution and regulation of their mRNAs in chromaffin and ganglion cells of rat adrenal medulla Neurosci Lett 156 1 70 72 8414192
  80. Martinez M Phillips PJ Herbert J 1998 Adaptation in patterns of c-fos expression in the brain associated with exposure to either single or repeated social stress in male rats Eur J Neurosci 10 1 20 33 9753110
  81. Martinowich K Manji H Lu B 2007 New insights into BDNF function in depression and anxiety Nat Neurosci 10 9 1089 1093 17726474
  82. McGonagle KA Kessler RC 1990 Chronic stress, acute stress, and depressive symptoms Am J Community 18 5 681 706 2075897
  83. McKernan DP Dinan TG Cryan JF 2009 “Killing the Blues”: a role for cellular suicide (apoptosis) in depression and the antidepressant response? Prog Neurobiol 88 4 246 263 19427352
  84. Meerlo P Overkamp G Daan S Van Den Hoofdakker R Koolhaas J 1996 Changes in behaviour and body weight following a single or double social defeat in rats Stress 1 1 21 32 9807059
  85. Morgan C Kirkbride J Leff J Craig T Hutchinson G McKenzie K Morgan K Dazzan P Doody GA Jones P 2007 Parental separation, loss and psychosis in different ethnic groups: a case-control study Psychol Med 37 04 495 503 17094816
  86. Mueller BR Bale TL 2008 Sex-specific programming of offspring emotionality after stress early in pregnancy J Neurosci 28 36 9055 9065 18768700 PMC2731562
  87. Murgatroyd C Patchev AV Wu Y Micale V Bockmühl Y Fischer D Holsboer F Wotjak CT Almeida OF Spengler D 2009 Dynamic DNA methylation programs persistent adverse effects of early-life stress Nat Neurosci 12 12 1559 1566 19898468
  88. Nam H Clinton SM Jackson NL Kerman IA 2014 Learned helplessness and social avoidance in the Wistar-Kyoto rat Front Behav Neurosci 8 109 127 24744709 PMC3978372
  89. Nestler EJ Hyman SE 2010 Animal models of neuropsychiatric disorders Nat Neurosci 13 10 1161 1169 20877280 PMC3750731
  90. Newport DJ Stowe ZN Nemeroff CB 2002 Parental depression: animal models of an adverse life event Am J Psychiatry 159 8 1265 1283 12153816
  91. Nishi K Kanemaru K Hasegawa S Watanabe A Diksic M 2009 Both acute and chronic buspirone treatments have different effects on regional 5-HT synthesis in Flinders Sensitive Line rats (a rat model of depression) than in control rats Neurochem Int 54 3 205 214 19084042 PMC2693024
  92. Nishi M Horii-Hayashi N Sasagawa T Matsunaga W 2013 Effects of early life stress on brain activity: implications from maternal separation model in rodents Gen Comp Endocrinol 181 306 309 23032077
  93. Ohadi M Mirabzadeh A Esmaeilzadeh-Gharehdaghi E Rezazadeh M Hosseinkhanni S Oladnabi M Firouzabadi SG Darvish H 2012 Novel evidence of the involvement of calreticulin in major psychiatric disorders Prog Neuropsychopharmacol Biol Psychiatry 37 2 276 281 22507216
  94. Overstreet D Russell R 1982 Selective breeding for diisopropyl fluorophosphate-sensitivity: behavioural effects of cholinergic agonists and antagonists Psychopharmacology (Berl) 78 2 150 155 6817373
  95. Overstreet DH Friedman E Mathé AA Yadid G 2005 The Flinders Sensitive Line rat: a selectively bred putative animal model of depression Neurosci Biobehav Rev 29 4 739 759 15925699
  96. Padilla E Barrett D Shumake J Gonzalez-Lima F 2009 Strain, sex, and open-field behavior: factors underlying the genetic susceptibility to helplessness Behav Brain Res 201 2 257 264 19428642 PMC2730204
  97. Padilla E Shumake J Barrett DW Holmes G Sheridan EC Gonzalez-Lima F 2010 Novelty-evoked activity in open field predicts susceptibility to helpless behavior Physiol Behav 101 5 746 754 20804778 PMC2975894
  98. Pause BM Miranda A Göder R Aldenhoff JB Ferstl R 2001 Reduced olfactory performance in patients with major depression J Psychiatr Res 35 5 271 277 11591429
  99. Pellow S Chopin P File SE Briley M 1985 Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat J Neurosci Methods 14 3 149 167 2864480
  100. Peters JE Finch SB 1961 Short-and long-range effects on the rat of a fear-provoking stimulus Psychosom Med 23 2 138 152 13734773
  101. Plotsky PM Thrivikraman K Nemeroff CB Caldji C Sharma S Meaney MJ 2005 Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring Neuropsychopharmacology 30 12 2192 2204 15920504
  102. Ponomarev I Wang S Zhang L Harris RA Mayfield RD 2012 Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence J Neurosci 32 5 1884 1897 22302827 PMC3564514
  103. Porsolt R Bertin A Jalfre M 1977 Behavioral despair in mice: a primary screening test for antidepressants Arch Int Pharmacodyn Ther 229 2 327 336 596982
  104. Pryce CR Rüedi-Bettschen D Dettling AC Weston A Russig H Ferger B Feldon J 2005 Long-term effects of early-life environmental manipulations in rodents and primates: potential animal models in depression research Neurosci Biobehav Rev 29 4 649 674 15925698
  105. Pucilowski O Overstreet DH 1993 Effect of chronic antidepressant treatment on responses to apomorphine in selectively bred rat strains Brain Res Bull 32 5 471 475 8221139
  106. Quesseveur G Portal B Basile J-A Ezan P Mathou A Halley H Leloup C Fioramonti X Déglon N Giaume C 2015 Attenuated levels of hippocampal connexin 43 and its phosphorylation correlate with antidepressant-and anxiolytic- like activities in mice Front Cell Neurosci 9 26733815 PMC4686612
  107. Rao TS Asha M Ramesh B Rao KJ 2008 Understanding nutrition, depression and mental illnesses Indian J Psychiatry 50 2 77 19742217 PMC2738337
  108. Ritter RC Balch OK 1978 Feeding in response to insulin but not to 2-deoxy-D-glucose in the hamster Am J Physiol Endocrinol Metab 234 1 E20 623243
  109. Ryu V Yoo SB Kang D-W Lee J-H Jahng JW 2009 Post-weaning isolation promotes food intake and body weight gain in rats that experienced neonatal maternal separation Brain Res 1295 127 134 19666012
  110. Schmidt MV 2011 Animal models for depression and the mismatch hypothesis of disease Psychoneuroendocrinology 36 3 330 338 20674180
  111. Schulte-Herbrüggen O Chourbaji S Ridder S Brandwein C Gass P Hörtnagl H Hellweg R 2006 Stress-resistant mice overexpressing glucocorticoid receptors display enhanced BDNF in the amygdala and hippocampus with unchanged NGF and serotonergic function Psychoneuroendocrinology 31 10 1266 1277 17098367
  112. Seligman ME 1972 Learned helplessness Annu Rev Med 23 1 407 412 4566487
  113. Sherman A Petty F 1982 Additivity of neurochemical changes in learned helplessness and imipramine Behav Neural Biol 35 4 344 353 6299264
  114. Shi J Potash J Knowles J Weissman M Coryell W Scheftner W Lawson W DePaulo J Gejman P Sanders A 2011 Genome-wide association study of recurrent early-onset major depressive disorder Mol Psychiatry 16 2 193 201 20125088 PMC6486400
  115. Shumake J Colorado RA Barrett DW Gonzalez-Lima F 2010 Metabolic mapping of the effects of the antidepressant fluoxetine on the brains of congenitally helpless rats Brain Res 1343 218 225 20470763 PMC2900439
  116. Smalheiser NR Lugli G Rizavi HS Zhang H Torvik VI Pandey GN Davis JM Dwivedi Y 2011 MicroRNA expression in rat brain exposed to repeated inescapable shock: differential alterations in learned helplessness vs. non-learned helplessness Int J Neuropsychopharmacol 14 10 1315 1325 21275079
  117. Song C Leonard BE 2005 The olfactory bulbectomised rat as a model of depression Neurosci Biobehav Rev 29 4 627 647 15925697
  118. Sun H Kennedy PJ Nestler EJ 2013 Epigenetics of the depressed brain: role of histone acetylation and methylation Neuropsychopharmacology 38 1 124 137 22692567 PMC3521990
  119. Surís A North C Adinoff B Powell CM Greene R 2010 Effects of exogenous glucocorticoid on combat-related PTSD symptoms Ann Clin Psychiatry 22 4 274 279 21180658 PMC3917156
  120. Tran PV Bymaster FP McNamara RK Potter WZ 2003 Dual monoamine modulation for improved treatment of major depressive disorder J Clin Psychopharmacol 23 1 78 86 12544378
  121. Vollmayr B Faust H Lewicka S Henn F 2001 Brain-derived-neurotrophic- factor (BDNF) stress response in rats bred for learned helplessness Mol Psychiatry 6 4 471 474 11443536
  122. Vollmayr B Mahlstedt MM Henn FA 2007 Neurogenesis and depression: what animal models tell us about the link Eur Arch Psychiatry Clin Neurosci 257 5 300 303 17401725
  123. Walker C-d Scribner KA Cascio CS Dallman MF 1991 The Pituitary-Adrenocortical System of Neonatal Rats Is Responsive to Stress throughout Development in a Time-Dependent and Stressor-Specific Fashion* Endocrinology 128 3 1385 1395 1847856
  124. Walther DJ Peter J-U Bashammakh S Hörtnagl H Voits M Fink H Bader M 2003 Synthesis of serotonin by a second tryptophan hydroxylase isoform Science 299 5603 76 76 12511643
  125. Wang Y-M Gainetdinov RR Fumagalli F Xu F Jones SR Bock CB Miller GW Wightman RM Caron MG 1997 Knockout of the vesicular monoamine transporter 2 gene results in neonatal death and supersensitivity to cocaine and amphetamine Neuron 19 6 1285 1296 9427251
  126. Watanabe Y Gould E Cameron HA Daniels DC McEwen BS 1992 Phenytoin prevents stress-and corticosterone-induced atrophy of CA3 pyramidal neurons Hippocampus 2 4 431 435 1308199
  127. Weaver IC Cervoni N Champagne FA D’Alessio AC Sharma S Seckl JR Dymov S Szyf M Meaney MJ 2004 Epigenetic programming by maternal behavior Nat Neurosci 7 8 847 854 15220929
  128. Weiss J Bailey W Pohorecky L Korzeniowski D Grillione G 1980 Stress-induced depression of motor activity correlates with regional changes in brain norepinephrine but not in dopamine Neurochem Res 5 1 9 22 7366796
  129. Weiss J Simson PG 1986 Depression in an animal model: Focus on the locus coeruleus Ciba Found Symp 123 191 215 3028724
  130. Will C Aird F Redei E 2003 Selectively bred Wistar–Kyoto rats: an animal model of depression and hyper-responsiveness to antidepressants Mol Psychiatry 8 11 925 932 14593430
  131. Willner P 1991 Animal models as simulations of depression Trends Pharmacol Sci 12 131 136 2063478
  132. Willner P Belzung C 2015 Treatment-resistant depression: are animal models of depression fit for purpose? Psychopharmacology 232 19 3473 3495 26289353
  133. Willner P Mitchell P 2002 The validity of animal models of predisposition to depression Behav Pharmacol 13 3 169 188 12122308
  134. Wong M-L Licinio J 2001 Research and treatment approaches to depression Nat Rev Neurosci 2 5 343 351 11331918
  135. Wood GE Young LT Reagan LP McEwen BS 2003 Acute and chronic restraint stress alter the incidence of social conflict in male rats Horm Behav 43 1 205 213 12614651
  136. You Z Luo C Zhang W Chen Y He J Zhao Q Zuo R Wu Y 2011 Pro- and anti-inflammatory cytokines expression in rat’s brain and spleen exposed to chronic mild stress: involvement in depression Behavioural brain research 225 1 135 141 21767575
  137. Zacharko RM Bowers WJ Kokkinidis L Anisman H 1983 Region-specific reductions of intracranial self-stimulation after uncontrollable stress: possible effects on reward processes Behav Brain Res 9 2 129 141 6603854
  138. Zangen A Overstreet DH Yadid G 1997 High Serotonin and 5-Hydroxyindoleacetic Acid Levels in Limbic Brain Regions in a Rat Model of Depression; Normalization by Chronic Antidepressant Treatment J Neurochem 69 6 2477 2483 9375680
  139. Zhang L Luo J Zhang M Yao W Ma X Yu SY 2014 Effects of curcumin on chronic, unpredictable, mild, stress-induced depressive-like behaviour and structural plasticity in the lateral amygdala of rats Int J Neuropsychopharmacol 17 5 793 806 24405689

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Authors
Wang, Q., Timberlake, M. A., Prall, K., & Dwivedi, Y.
Affiliations
University of Alabama at Birmingham (US)
Corresponding author
Dwivedi, Yogesh
ORCID
Venue
Progress in Neuro-Psychopharmacology and Biological Psychiatry
Publisher
Elsevier BV
Published
2017-07
Volume
77
Pages
99-109
ISSN
0278-5846 (ISSN-L)
DOI
10.1016/j.pnpbp.2017.04.008
PMC
PMC5605906
OpenAlex
W2604652480
Cited by
370
References
20
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FWCI
2.93
Type
journal article
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
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  • Progress in Neuro-Psychopharmacology and Biological Psychiatry (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of Mental Health (R01MH082802, R21MH081099, 1R01MH101890, R01MH100616, 1R01MH107183)
  • American Foundation for Suicide Prevention (SRG-XXXX-001778-1209)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords
major depressive disorder, animal models of depression, pharmacological manipulation, genome editing, neural circuits
MeSH terms
Animals, Behavior, Animal, Depressive Disorder, Major, Major Depressive Disorder, Disease Models, Animal

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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