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Does Stress Elicit Depression? Evidence From Clinical and Preclinical Studies

  • Helle M. Sickmann
  • Yan Li
  • Arne Mørk
  • Connie Sanchez
  • Maria Gulinello
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 18)

Abstract

Exposure to stressful situations may induce or deteriorate an already existing depression. Stress-related depression can be elicited at an adolescent/adult age but evidence also shows that early adverse experiences even at the fetal stage may predispose the offspring for later development of depression. The hypothalamus–pituitary–adrenal axis (HPA-axis) plays a key role in regulating the stress response and dysregulation in the system has been linked to depression both in humans and in animal models. This chapter critically reviews clinical and preclinical findings that may explain how stress can cause depression, including HPA-axis changes and alterations beyond the HPA-axis. As stress does not elicit depression in the majority of the population, this motivated research to focus on understanding the biology underlying resilient versus sensitive subjects. Animal models of depression have contributed to a deeper understanding of these mechanisms. Findings from these models will be presented.

Keywords

Depression Clinical studies Animal models Stress resilience Vulnerability factors 

References

  1. Abdul Aziz NH, Kendall DA, Pardon MC (2012) Prenatal exposure to chronic mild stress increases corticosterone levels in the amniotic fluid and induces cognitive deficits in female offspring, improved by treatment with the antidepressant drug amitriptyline. Behav Brain Res 231(1):29–39PubMedGoogle Scholar
  2. Adachi M, Barrot M, Autry AE, Theobald D, Monteggia LM (2008) Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol Psychiatry 63(7):642–649PubMedCentralPubMedGoogle Scholar
  3. Aguilera G, Subburaju S, Young S, Chen J (2008) The parvocellular vasopressinergic system and responsiveness of the hypothalamic pituitary adrenal axis during chronic stress. Prog Brain Res 170:29–39PubMedCentralPubMedGoogle Scholar
  4. Albonetti ME, Farabollini F (1994) Social stress by repeated defeat: effects on social behaviour and emotionality. Behav Brain Res 62(2):187–193PubMedGoogle Scholar
  5. Almeida OF, Conde GL, Crochemore C, Demeneix BA, Fischer D, Hassan AH, Meyer M, Holsboer F, Michaelidis TM (2000) Subtle shifts in the ratio between pro- and antiapoptotic molecules after activation of corticosteroid receptors decide neuronal fate. FASEB J 14(5):779–790Google Scholar
  6. Anisman H, Zaharia MD, Meaney MJ, Merali Z (1998) Do early-life events permanently alter behavioral and hormonal responses to stressors? Int J Dev Neurosci 16(3–4):149–164PubMedGoogle Scholar
  7. Aonurm-Helm A, Jurgenson M, Zharkovsky T, Sonn K, Berezin V, Bock E, Zharkovsky A (2008) Depression-like behaviour in neural cell adhesion molecule (NCAM)-deficient mice and its reversal by an NCAM-derived peptide, FGL. Eur J Neurosci 28(8):1618–1628Google Scholar
  8. Armario A, Gil M, Marti J, Pol O, Balasch J (1991) Influence of various acute stressors on the activity of adult male rats in a holeboard and in the forced swim test. Pharmacol Biochem Behav 39(2):373–377PubMedGoogle Scholar
  9. Austin MP, Hadzi-Pavlovic D, Leader L, Saint K, Parker G (2005) Maternal trait anxiety, depression and life event stress in pregnancy: relationships with infant temperament. Early Hum Dev 81(2):183–190PubMedGoogle Scholar
  10. Autry AE, Adachi M, Cheng P, Monteggia LM (2009) Gender-specific impact of brain-derived neurotrophic factor signaling on stress-induced depression-like behavior. Biol Psychiatry 66(1):84–90PubMedCentralPubMedGoogle Scholar
  11. Axelson DA, Doraiswamy PM, McDonald WM, Boyko OB, Tupler LA, Patterson LJ, Nemeroff CB, Ellinwood EH Jr, Krishnan KR (1993) Hypercortisolemia and hippocampal changes in depression. Psychiatry Res 47(2):163–173PubMedGoogle Scholar
  12. Baker SL, Kentner AC, Konkle ATM, Barbagallo LS-M, Bielajew C (2006) Behavioral and physiological effects of chronic mild stress in female rats. Physiol Behav 87(2):314–322PubMedGoogle Scholar
  13. Bao AM, Hestiantoro A, Van Someren EJ, Swaab DF, Zhou JN (2005) Colocalization of corticotropin-releasing hormone and oestrogen receptor-alpha in the paraventricular nucleus of the hypothalamus in mood disorders. Brain 128(Pt 6):1301–1313PubMedGoogle Scholar
  14. Barr AM, Brotto LA, Phillips AG (2000) Chronic corticosterone enhances the rewarding effect of hypothalamic self-stimulation in rats. Brain Res 875(1–2):196–201PubMedGoogle Scholar
  15. Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R, Parmigiani S (2005) Social factors and individual vulnerability to chronic stress exposure. Neurosci Biobehav Rev 29(1):67–81PubMedGoogle Scholar
  16. Bergman K, Sarkar P, O’Connor TG, Modi N, Glover V (2007) Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J Am Acad Child Adolesc Psychiatry 46(11):1454–1463PubMedGoogle Scholar
  17. Bergström A, Jayatissa MN, Mørk A, Wiborg O (2008) Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study. Brain Res 1196:41–52PubMedGoogle Scholar
  18. Berry A, Bellisario V, Capoccia S, Tirassa P, Calza A, Alleva E, Cirulli F (2012) Social deprivation stress is a triggering factor for the emergence of anxiety- and depression-like behaviours and leads to reduced brain BDNF levels in C57BL/6J mice. Psychoneuroendocrinology 37(6):762–772PubMedGoogle Scholar
  19. Bhatnagar S, Vining C (2003) Facilitation of hypothalamic-pituitary-adrenal responses to novel stress following repeated social stress using the resident/intruder paradigm. Horm Behav 43(1):158–165PubMedGoogle Scholar
  20. Bielajew C, Konkle AT, Merali Z (2002) The effects of chronic mild stress on male Sprague-Dawley and Long Evans rats: I. Biochemical and physiological analyses. Behav Brain Res 136(2):583–592PubMedGoogle Scholar
  21. Björkqvist K (2001) Social defeat as a stressor in humans. Physiol Behav 73(3):435–442PubMedGoogle Scholar
  22. Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwen B, Sakai RR (1995) Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 20(2):117–134PubMedGoogle Scholar
  23. Blanchard RJ, McKittrick CR, Blanchard DC (2001) Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol Behav 73(3):261–271PubMedGoogle Scholar
  24. Bonanno GA (2004) Loss, trauma, and human resilience: have we underestimated the human capacity to thrive after extremely aversive events? Am psychol 59(1):20–28PubMedGoogle Scholar
  25. Borsonelo EC, Suchecki D, Galduroz JC (2011) Effect of fish oil and coconut fat supplementation on depressive-type behavior and corticosterone levels of prenatally stressed male rats. Brain Res 1385:144–150PubMedGoogle Scholar
  26. Bowens N, Heydendael W, Bhatnagar S, Jacobson L (2012) Lack of elevations in glucocorticoids correlates with dysphoria-like behavior after repeated social defeat. Physiol Behav 105(4):958–965PubMedCentralPubMedGoogle Scholar
  27. Bowers SL, Bilbo SD, Dhabhar FS, Nelson RJ (2008) Stressor-specific alterations in corticosterone and immune responses in mice. Brain Behav Immun 22(1):105–113PubMedCentralPubMedGoogle Scholar
  28. Brindle RC, Ginty AT, Conklin SM (2013) Is the association between depression and blunted cardiovascular stress reactions mediated by perceptions of stress? Int J psychophysiol: Off J Int Org Psychophysiol 90(1):66–72Google Scholar
  29. Brotto LA, Gorzalka BB, Barr AM (2001) Paradoxical effects of chronic corticosterone on forced swim behaviours in aged male and female rats. Eur J Pharmacol 424(3):203–209PubMedGoogle Scholar
  30. Brown GW, Bifulco A, Harris TO (1987) Life events, vulnerability and onset of depression: some refinements. Br J Psychiatry 150(1):30–42Google Scholar
  31. Brunton PJ, Russell JA (2010) Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex-specific effects. J Neuroendocrinol 22(4):258–271PubMedGoogle Scholar
  32. Burke HM, Davis MC, Otte C, Mohr DC (2005) Depression and cortisol responses to psychological stress: a meta-analysis. Psychoneuroendocrinology 30(9):846–856PubMedGoogle Scholar
  33. Caldarone BJ, George TP, Zachariou V, Picciotto MR (2000) Gender differences in learned helplessness behavior are influenced by genetic background. Pharmacol Biochem Behav 66(4):811–817PubMedGoogle Scholar
  34. Calvo N, Cecchi M, Kabbaj M, Watson SJ, Akil H (2011) Differential effects of social defeat in rats with high and low locomotor response to novelty. Neuroscience 183:81–89PubMedCentralPubMedGoogle Scholar
  35. Cancela LM, Rossi S, Molina VA (1991) Effect of different restraint schedules on the immobility in the forced swim test: modulation by an opiate mechanism. Brain Res Bull 26(5):671–675PubMedGoogle Scholar
  36. Carnevali L, Mastorci F, Graiani G, Razzoli M, Trombini M, Pico-Alfonso MA, Arban R, Grippo AJ, Quaini F, Sgoifo A (2012) Social defeat and isolation induce clear signs of a depression-like state, but modest cardiac alterations in wild-type rats. Physiol Behav 106(2):142–150PubMedGoogle Scholar
  37. Casarotto PC, Andreatini R (2007) Repeated paroxetine treatment reverses anhedonia induced in rats by chronic mild stress or dexamethasone. Eur Neuropsychopharmacol 17(11):735–742PubMedGoogle Scholar
  38. Casarotto PC, de Bortoli VC, Zangrossi H Jr (2012) Intrahippocampal injection of brain-derived neurotrophic factor increases anxiety-related, but not panic-related defensive responses: involvement of serotonin. Behav Pharmacol 23(1):80–88PubMedGoogle Scholar
  39. Castren E, Rantamaki T (2008) Neurotrophins in depression and antidepressant effects. Novartis Found symp 289:43–52; discussion 53–49, 87–93Google Scholar
  40. Castren E, Rantamaki T (2010) The role of BDNF and its receptors in depression and antidepressant drug action: reactivation of developmental plasticity. Dev Neurobiol 70(5):289–297PubMedGoogle Scholar
  41. Castro JE, Diessler S, Varea E, Marquez C, Larsen MH, Cordero MI, Sandi C (2012) Personality traits in rats predict vulnerability and resilience to developing stress-induced depression-like behaviors, HPA axis hyper-reactivity and brain changes in pERK1/2 activity. Psychoneuroendocrinology 37(8):1209–1223PubMedGoogle Scholar
  42. Chen J, Young S, Subburaju S, Sheppard J, Kiss A, Atkinson H, Wood S, Lightman S, Serradeil-Le Gal C, Aguilera G (2008) Vasopressin does not mediate hypersensitivity of the hypothalamic pituitary adrenal axis during chronic stress. Ann N Y Acad Sci 1148:349–359PubMedCentralPubMedGoogle Scholar
  43. Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H (2012) Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 39(1):112–119PubMedGoogle Scholar
  44. Cory-Slechta DA, Merchant-Borna K, Allen JL, Liu S, Weston D, Conrad K (2013) Variations in the nature of behavioral experience can differentially alter the consequences of developmental exposures to lead, prenatal stress, and the combination. Toxicol Sci 131(1):194–205PubMedCentralPubMedGoogle Scholar
  45. Couch Y, Anthony DC, Dolgov O, Revischin A, Festoff B, Santos AI, Steinbusch HW, Strekalova T (2013) Microglial activation, increased TNF and SERT expression in the prefrontal cortex define stress-altered behaviour in mice susceptible to anhedonia. Brain Behav Immun 29:136–146PubMedGoogle Scholar
  46. Covington HE 3rd, Maze I, LaPlant QC, Vialou VF, Ohnishi YN, Berton O, Fass DM, Renthal W, Rush AJ 3rd, Wu EY, Ghose S, Krishnan V, Russo SJ, Tamminga C, Haggarty SJ, Nestler EJ (2009) Antidepressant actions of histone deacetylase inhibitors. J Neurosci 29(37):11451–11460Google Scholar
  47. Crema LM, Pettenuzzo LF, Schlabitz M, Diehl L, Hoppe J, Mestriner R, Laureano D, Salbego C, Dalmaz C, Vendite D (2013) The effect of unpredictable chronic mild stress on depressive-like behavior and on hippocampal A1 and striatal A2A adenosine receptors. Physiol Behav 109:1–7PubMedGoogle Scholar
  48. Croes S, Merz P, Netter P (1993) Cortisol reaction in success and failure condition in endogenous depressed patients and controls. Psychoneuroendocrinology 18(1):23–35PubMedGoogle Scholar
  49. Cui M, Yang Y, Yang J, Zhang J, Han H, Ma W, Li H, Mao R, Xu L, Hao W, Cao J (2006) Enriched environment experience overcomes the memory deficits and depressive-like behavior induced by early life stress. Neurosci Lett 404(1–2):208–212PubMedGoogle Scholar
  50. D’Aquila PS, Brain P, Willner P (1994) Effects of chronic mild stress on performance in behavioural tests relevant to anxiety and depression. Physiol Behav 56(5):861–867PubMedGoogle Scholar
  51. Dadomo H, Sanghez V, Di Cristo L, Lori A, Ceresini G, Malinge I, Parmigiani S, Palanza P, Sheardown M, Bartolomucci A (2011) Vulnerability to chronic subordination stress-induced depression-like disorders in adult 129SvEv male mice. Prog Neuropsychopharmacol Biol Psychiatry 35(6):1461–1471PubMedGoogle Scholar
  52. Dalla C, Antoniou K, Drossopoulou G, Xagoraris M, Kokras N, Sfikakis A, Papadopoulou-Daifoti Z (2005) Chronic mild stress impact: are females more vulnerable? Neuroscience 135(3):703–714PubMedGoogle Scholar
  53. Dalla C, Antoniou K, Kokras N, Drossopoulou G, Papathanasiou G, Bekris S, Daskas S, Papadopoulou-Daifoti Z (2008) Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiol Behav 93(3):595–605PubMedGoogle Scholar
  54. Daniels WM, Richter L, Stein DJ (2004) The effects of repeated intra-amygdala CRF injections on rat behavior and HPA axis function after stress. Metab Brain Dis 19(1–2):15–23PubMedGoogle Scholar
  55. David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, Mendez I, Drew M, Craig DA, Guiard BP, Guilloux JP, Artymyshyn RP, Gardier AM, Gerald C, Antonijevic IA, Leonardo ED, Hen R (2009) Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62(4):479–493PubMedCentralPubMedGoogle Scholar
  56. Davis EP, Sandman CA (2012) Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology 37(8):1224–1233PubMedCentralPubMedGoogle Scholar
  57. de Kloet ER, Oitzl MS, Joëls M (1999) Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 22(10):422–426PubMedGoogle Scholar
  58. De Vry J, Prickaerts J, Jetten M, Hulst M, Steinbusch HW, van den Hove DL, Schuurman T, van der Staay FJ (2012) Recurrent long-lasting tethering reduces BDNF protein levels in the dorsal hippocampus and frontal cortex in pigs. Horm Behav 62(1):10–17PubMedGoogle Scholar
  59. Deis RP, Leguizamon E, Jahn GA (1989) Feedback regulation by progesterone of stress-induced prolactin release in rats. J Endocrinol 120(1):37–43PubMedGoogle Scholar
  60. Del Cerro MC, Perez-Laso C, Ortega E, Martin JL, Gomez F, Perez-Izquierdo MA, Segovia S (2010) Maternal care counteracts behavioral effects of prenatal environmental stress in female rats. Behav Brain Res 208(2):593–602PubMedGoogle Scholar
  61. Detanico BC, Piato AL, Freitas JJ, Lhullier FL, Hidalgo MP, Caumo W, Elisabetsky E (2009) Antidepressant-like effects of melatonin in the mouse chronic mild stress model. Eur J Pharmacol 607(1–3):121–125PubMedGoogle Scholar
  62. Djordjevic A, Adzic M, Djordjevic J, Radojcic MB (2009) Stress type dependence of expression and cytoplasmic-nuclear partitioning of glucocorticoid receptor, hsp90 and hsp70 in Wistar rat brain. Neuropsychobiology 59(4):213–221PubMedGoogle Scholar
  63. Dubrovsky B (2000) The specificity of stress responses to different nocuous stimuli: neurosteroids and depression. Brain Res Bull 51(6):443–455PubMedGoogle Scholar
  64. Ducottet C, Belzung C (2005) 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(1):153–162PubMedGoogle Scholar
  65. Dugovic C, Maccari S, Weibel L, Turek FW, Van Reeth O (1999) High corticosterone levels in prenatally stressed rats predict persistent paradoxical sleep alterations. J Neurosci 19(19):8656–8664Google Scholar
  66. Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59(12):1116–1127PubMedGoogle Scholar
  67. Duric V, McCarson KE (2005) Hippocampal neurokinin-1 receptor and brain-derived neurotrophic factor gene expression is decreased in rat models of pain and stress. Neuroscience 133(4):999–1006PubMedGoogle Scholar
  68. Egashira N, Tanoue A, Matsuda T, Koushi E, Harada S, Takano Y, Tsujimoto G, Mishima K, Iwasaki K, Fujiwara M (2007) Impaired social interaction and reduced anxiety-related behavior in vasopressin V1a receptor knockout mice. Behav Brain Res 178(1):123–127PubMedGoogle Scholar
  69. Ely DR, Dapper V, Marasca J, Correa JB, Gamaro GD, Xavier MH, Michalowski MB, Catelli D, Rosat R, Ferreira MB, Dalmaz C (1997) Effect of restraint stress on feeding behavior of rats. Physiol Behav 61(3):395–398PubMedGoogle Scholar
  70. Fan Y, Chen P, Li Y, Cui K, Noel DM, Cummins ED, Peterson DJ, Brown RW, Zhu MY (2013) Corticosterone administration up-regulated expression of norepinephrine transporter and dopamine beta-hydroxylase in rat locus coeruleus and its terminal regions. J Neurochem 128(3):445–458Google Scholar
  71. ffrench-Mullen J (1995) Cortisol inhibition of calcium currents in guinea pig hippocampal CA1 neurons via G-protein-coupled activation of protein kinase C. J Neurosci 15(1):903–911PubMedGoogle Scholar
  72. Forbes NF, Stewart CA, Matthews K, Reid IC (1996) Chronic mild stress and sucrose consumption: validity as a model of depression. Physiol Behav 60(6):1481–1484PubMedGoogle Scholar
  73. Frodl T, Meisenzahl EM, Zetzsche T, Born C, Groll C, Jager M, Leinsinger G, Bottlender R, Hahn K, Moller HJ (2002) Hippocampal changes in patients with a first episode of major depression. Am J psychiatry 159(7):1112–1118PubMedGoogle Scholar
  74. Frodl T, Reinhold E, Koutsouleris N, Reiser M, Meisenzahl EM (2010) Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression. J Psychiatr Res 44(13):799–807PubMedGoogle Scholar
  75. Froger N, Palazzo E, Boni C, Hanoun N, Saurini F, Joubert C, Dutriez-Casteloot I, Enache M, Maccari S, Barden N, Cohen-Salmon C, Hamon M, Lanfumey L (2004) Neurochemical and behavioral alterations in glucocorticoid receptor-impaired transgenic mice after chronic mild stress. J Neurosci 24(11):2787–2796Google Scholar
  76. Fuchs E, Czeh B, Kole MH, Michaelis T, Lucassen PJ (2004) Alterations of neuroplasticity in depression: the hippocampus and beyond. European Neuropsychopharmacol: J Eur Coll Neuropsychopharmacol 14(Suppl 5):S481–S490Google Scholar
  77. Geracioti TD Jr, Loosen PT, Gold PW, Kling MA (1992) Cortisol, thyroid hormone, and mood in atypical depression: a longitudinal case study. Biol Psychiatry 31(5):515–519PubMedGoogle Scholar
  78. Gomez-Lazaro E, Garmendia L, Beitia G, Perez-Tejada J, Azpiroz A, Arregi A (2012) Effects of a putative antidepressant with a rapid onset of action in defeated mice with different coping strategies. Prog Neuropsychopharmacol Biol Psychiatry 38(2):317–327PubMedGoogle Scholar
  79. Gourley SL, Kedves AT, Olausson P, Taylor JR (2009) A history of corticosterone exposure regulates fear extinction and cortical NR2B, GluR2/3, and BDNF. Neuropsychopharmacology 34(3):707–716PubMedCentralPubMedGoogle Scholar
  80. Gourley SL, Kiraly DD, Howell JL, Olausson P, Taylor JR (2008a) Acute hippocampal brain-derived neurotrophic factor restores motivational and forced swim performance after corticosterone. Biol Psychiatry 64(10):884–890PubMedCentralPubMedGoogle Scholar
  81. Gourley SL, Wu FJ, Kiraly DD, Ploski JE, Kedves AT, Duman RS, Taylor JR (2008b) Regionally specific regulation of ERK MAP kinase in a model of antidepressant-sensitive chronic depression. Biol Psychiatry 63(4):353–359PubMedCentralPubMedGoogle Scholar
  82. Green MK, Rani CS, Joshi A, Soto-Pina AE, Martinez PA, Frazer A, Strong R, Morilak DA (2011) Prenatal stress induces long term stress vulnerability, compromising stress response systems in the brain and impairing extinction of conditioned fear after adult stress. Neuroscience 192:438–451PubMedGoogle Scholar
  83. Greenwood BN, Strong PV, Foley TE, Thompson RS, Fleshner M (2007) Learned helplessness is independent of levels of brain-derived neurotrophic factor in the hippocampus. Neuroscience 144(4):1193–1208Google Scholar
  84. 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):105–114PubMedGoogle Scholar
  85. Griebel G, Holsboer F (2012) Neuropeptide receptor ligands as drugs for psychiatric diseases: the end of the beginning? Nat Rev Drug Discov 11(6):462–478PubMedGoogle Scholar
  86. Griebel G, Simiand J, Steinberg R, Jung M, Gully D, Roger P, Geslin M, Scatton B, Maffrand JP, Soubrie P (2002) 4-(2-Chloro-4-methoxy-5-methylphenyl)-N-[(1S)-2-cyclopropyl-1-(3-fluoro-4-methylp henyl)ethyl]5-methyl-N-(2-propynyl)-1, 3-thiazol-2-amine hydrochloride (SSR125543A), a potent and selective corticotrophin-releasing factor(1) receptor antagonist. II. Characterization in rodent models of stress-related disorders. J Pharmacol Exp Ther 301(1):333–345PubMedGoogle Scholar
  87. Grippo AJ, Francis J, Beltz TG, Felder RB, Johnson AK (2005) Neuroendocrine and cytokine profile of chronic mild stress-induced anhedonia. Physiol Behav 84(5):697–706PubMedGoogle Scholar
  88. Grippo AJ, Gerena D, Huang J, Kumar N, Shah M, Ughreja R, Sue Carter C (2007) Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinology 32(8–10):966–980PubMedCentralPubMedGoogle Scholar
  89. Gronli J, Murison R, Bjorvatn B, Sorensen E, Portas CM, Ursin R (2004) Chronic mild stress affects sucrose intake and sleep in rats. Behav Brain Res 150(1–2):139–147PubMedGoogle Scholar
  90. Halbreich U, Asnis GM, Shindledecker R, Zumoff B, Nathan R (1985) Cortisol secretion in endogenous depression: I. basal plasma levels. Arch Gen Psychiatry 42(9):904–908PubMedGoogle Scholar
  91. Hamilton JL, Stange JP, Shapero BG, Connolly SL, Abramson LY, Alloy LB (2013) Cognitive vulnerabilities as predictors of stress generation in early adolescence: pathway to depressive symptoms. J Abnorm Child Psychol 41(7):1027–1039PubMedCentralPubMedGoogle Scholar
  92. Hammack SE, Cooper MA, Lezak KR (2012) Overlapping neurobiology of learned helplessness and conditioned defeat: implications for PTSD and mood disorders. Neuropharmacology 62(2):565–575PubMedCentralPubMedGoogle Scholar
  93. Hammen C (1991) Generation of stress in the course of unipolar depression. J Abnorm Psychol 100(4):555–561PubMedGoogle Scholar
  94. Hammen C, Davila J, Brown G, Ellicott A, Gitlin M (1992) Psychiatric history and stress: predictors of severity of unipolar depression. J Abnorm Psychol 101(1):45–52PubMedGoogle Scholar
  95. Hanson ND, Owens MJ, Nemeroff CB (2011) Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology 36(13):2589–2602PubMedCentralPubMedGoogle Scholar
  96. Harris A, Seckl J (2011) Glucocorticoids, prenatal stress and the programming of disease. Horm Behav 59(3):279–289PubMedGoogle Scholar
  97. Hata T, Nishikawa H, Itoh E, Watanabe A (1999) Depressive state with anxiety in repeated cold-stressed mice in forced swimming tests. Jpn J Pharmacol 79(2):243–249PubMedGoogle Scholar
  98. Hayase T (2011) Depression-related anhedonic behaviors caused by immobilization stress: a comparison with nicotine-induced depression-like behavioral alterations and effects of nicotine and/or “antidepressant” drugs. J Toxicol Sci 36(1):31–41PubMedGoogle Scholar
  99. Hayashida S, Oka T, Mera T, Tsuji S (2010) Repeated social defeat stress induces chronic hyperthermia in rats. Physiol Behav 101(1):124–131PubMedGoogle Scholar
  100. Haynes LE, Griffiths MR, Hyde RE, Barber DJ, Mitchell IJ (2001) Dexamethasone induces limited apoptosis and extensive sublethal damage to specific subregions of the striatum and hippocampus: implications for mood disorders. Neuroscience 104(1):57–69PubMedGoogle Scholar
  101. Hegde P, Singh K, Chaplot S, Rao BSS, Chattarji S, Kutty BM, Laxmi TR (2008) Stress-induced changes in sleep and associated neuronal activity in rat hippocampus and amygdala. Neuroscience 153(1):20–30PubMedGoogle Scholar
  102. Henn F, Vollmayr B, Sartorius A (2004) Mechanisms of depression: the role of neurogenesis. Drug Discov Today: Dis Mech 1(4):407–411Google Scholar
  103. Henn FA, Vollmayr B (2004) Neurogenesis and depression: etiology or epiphenomenon? Biol Psychiatry 56(3):146–150PubMedGoogle Scholar
  104. Herman JP, Adams D, Prewitt C (1995) Regulatory changes in neuroendocrine stress-integrative circuitry produced by a variable stress paradigm. Neuroendocrinology 61(2):180–190PubMedGoogle Scholar
  105. Herman JP, Spencer R (1998) Regulation of hippocampal glucocorticoid receptor gene transcription and protein expression in vivo. J Neurosci 18(18):7462–7473Google Scholar
  106. Heuser I, Yassouridis A, Holsboer F (1994) The combined dexamethasone/CRH test: a refined laboratory test for psychiatric disorders. J Psychiatr Res 28(4):341–356PubMedGoogle Scholar
  107. Hill MN, Hellemans KG, Verma P, Gorzalka BB, Weinberg J (2012) Neurobiology of chronic mild stress: parallels to major depression. Neurosci Biobehav Rev 36(9):2085–2117PubMedGoogle Scholar
  108. Hodes GE, Brookshire BR, Hill-Smith TE, Teegarden SL, Berton O, Lucki I (2012) Strain differences in the effects of chronic corticosterone exposure in the hippocampus. Neuroscience 222:269–280PubMedCentralPubMedGoogle Scholar
  109. Hodes GE, Hill-Smith TE, Suckow RF, Cooper TB, Lucki I (2010) Sex-specific effects of chronic fluoxetine treatment on neuroplasticity and pharmacokinetics in mice. J Pharmacol Exp Ther 332(1):266–273PubMedCentralPubMedGoogle Scholar
  110. Hollis F, Wang H, Dietz D, Gunjan A, Kabbaj M (2010) The effects of repeated social defeat on long-term depressive-like behavior and short-term histone modifications in the hippocampus in male Sprague-Dawley rats. Psychopharmacology 211(1):69–77PubMedGoogle Scholar
  111. Holsboer F (2000) The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23(5):477–501PubMedGoogle Scholar
  112. Holsboer F (2001) Stress, hypercortisolism and corticosteroid receptors in depression: implicatons for therapy. J Affect Disord 62(1–2):77–91PubMedGoogle Scholar
  113. Holsboer F, Bender W, Benkert O, Klein HE, Schmauss M (1980) Diagnostic value of dexamethasone suppression test in depression. Lancet 2(8196):706PubMedGoogle Scholar
  114. Holson RR, Gough B, Sullivan P, Badger T, Sheehan DM (1995) Prenatal dexamethasone or stress but not ACTH or corticosterone alter sexual behavior in male rats. Neurotoxicol Teratol 17(4):393–401PubMedGoogle Scholar
  115. Howell KR, Kutiyanawalla A, Pillai A (2011) Long-term continuous corticosterone treatment decreases VEGF receptor-2 expression in frontal cortex. PLoS ONE 6(5):e20198PubMedCentralPubMedGoogle Scholar
  116. Huizink AC, de Medina PGR, Mulder EJ, Visser GH, Buitelaar JK (2003) Stress during pregnancy is associated with developmental outcome in infancy. J Child Psychol Psychiatry 44(6):810–818PubMedGoogle Scholar
  117. Huynh TN, Krigbaum AM, Hanna JJ, Conrad CD (2011) Sex differences and phase of light cycle modify chronic stress effects on anxiety and depressive-like behavior. Behav Brain Res 222(1):212–222PubMedGoogle Scholar
  118. Ibarguen-Vargas Y, Surget A, Vourc’h P, Leman S, Andres CR, Gardier AM, Belzung C (2009) Deficit in BDNF does not increase vulnerability to stress but dampens antidepressant-like effects in the unpredictable chronic mild stress. Behav Brain Res 202(2):245–251PubMedGoogle Scholar
  119. Iio W, Matsukawa N, Tsukahara T, Kohari D, Toyoda A (2011) Effects of chronic social defeat stress on MAP kinase cascade. Neurosci Lett 504(3):281–284PubMedGoogle Scholar
  120. Jacobs BL (2002) Adult brain neurogenesis and depression. Brain Behav Immun 16(5):602–609PubMedGoogle Scholar
  121. Jayatissa MN, Bisgaard CF, West MJ, Wiborg O (2008) The number of granule cells in rat hippocampus is reduced after chronic mild stress and re-established after chronic escitalopram treatment. Neuropharmacology 54(3):530–541PubMedGoogle Scholar
  122. Jayatissa MN, Henningsen K, West MJ, Wiborg O (2009) Decreased cell proliferation in the dentate gyrus does not associate with development of anhedonic-like symptoms in rats. Brain Res 1290:133–141PubMedGoogle Scholar
  123. Kanarik M, Alttoa A, Matrov D, Kõiv K, Sharp T, Panksepp J, Harro J (2011) Brain responses to chronic social defeat stress: effects on regional oxidative metabolism as a function of a hedonic trait, and gene expression in susceptible and resilient rats. Eur Neuropsychopharmacol 21(1):92–107PubMedGoogle Scholar
  124. Kant GJ, Leu JR, Anderson SM, Mougey EH (1987) Effects of chronic stress on plasma corticosterone ACTH and prolactin. Physiol Behav 40(6):775–779PubMedGoogle Scholar
  125. Kehne JH, Cain CK (2010) Therapeutic utility of non-peptidic CRF1 receptor antagonists in anxiety, depression, and stress-related disorders: evidence from animal models. Pharmacol Ther 128(3):460–487PubMedCentralPubMedGoogle Scholar
  126. Kemble ED (1993) 8—Resident–Intruder Paradigms for the Study of Rodent Aggression. In: Conn PM (ed) Methods in neurosciences, vol 14. Academic press, pp 138–150Google Scholar
  127. Kendler KS, Gardner CO, Prescott CA (2002) Toward a comprehensive developmental model for major depression in women. Am J psychiatry 159(7):1133–1145PubMedGoogle Scholar
  128. Kendler KS, Gardner CO, Prescott CA (2006) Toward a comprehensive developmental model for major depression in men. Am J psychiatry 163(1):115–124PubMedGoogle Scholar
  129. Kendler KS, Karkowski LM, Prescott CA (1999) Causal relationship between stressful life events and the onset of major depression. Am J psychiatry 156(6):837–841PubMedGoogle Scholar
  130. Keshet GI, Weinstock M (1995) Maternal naltrexone prevents morphological and behavioral alterations induced in rats by prenatal stress. Pharmacol Biochem Behav 50(3):413–419PubMedGoogle Scholar
  131. Kessler RC (1997) The effects of stressful life events on depression. Annu Rev Psychol 48(1):191–214PubMedGoogle Scholar
  132. Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, Kenny LC, Mortensen PB (2008) Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry 65(2):146–152PubMedGoogle Scholar
  133. Kim BS, Kim MY, Leem YH (2011) Hippocampal neuronal death induced by kainic acid and restraint stress is suppressed by exercise. Neuroscience 194:291–301PubMedGoogle Scholar
  134. Kim CK, Yu W, Edin G, Ellis L, Osborn JA, Weinberg J (1999) Chronic intermittent stress does not differentially alter brain corticosteroid receptor densities in rats prenatally exposed to ethanol. Psychoneuroendocrinology 24(6):585–611PubMedGoogle Scholar
  135. Kim EJ, Kim WR, Chi SE, Lee KH, Park EH, Chae JH, Park SK, Kim HT, Choi JS (2006) Repetitive transcranial magnetic stimulation protects hippocampal plasticity in an animal model of depression. Neurosci Lett 405(1–2):79–83PubMedGoogle Scholar
  136. Kim JW, Kirkpatrick B (1996) Social isolation in animal models of relevance to neuropsychiatric disorders. Biol Psychiatry 40(9):918–922PubMedGoogle Scholar
  137. Kinsey SG, Bailey MT, Sheridan JF, Padgett DA, Avitsur R (2007) Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice. Brain Behav Immun 21(4):458–466PubMedCentralPubMedGoogle Scholar
  138. Kleinhaus K, Harlap S, Perrin M, Manor O, Margalit-Calderon R, Opler M, Friedlander Y, Malaspina D (2013) Prenatal stress and affective disorders in a population birth cohort. Bipolar Disord 15(1):92–99PubMedGoogle Scholar
  139. Koolhaas JM, Coppens CM, de Boer SF, Buwalda B, Meerlo P, Timmermans PJ (2013) The resident-intruder paradigm: a standardized test for aggression, violence and social stress. J Vis Exp 77:e4367 (JoVE)PubMedGoogle Scholar
  140. Koolhaas JM, De Boer SF, De Rutter AJ, Meerlo P, Sgoifo A (1997) Social stress in rats and mice. Acta Physiol Scand Suppl 640:69–72PubMedGoogle Scholar
  141. Kormos V, Gaszner B (2013) Role of neuropeptides in anxiety, stress, and depression: from animals to humans. Neuropeptides 47(6):401–419Google Scholar
  142. Krishnan V, Graham A, Mazei-Robison MS, Lagace DC, Kim KS, Birnbaum S, Eisch AJ, Han PL, Storm DR, Zachariou V, Nestler EJ (2008) Calcium-sensitive adenylyl cyclases in depression and anxiety: behavioral and biochemical consequences of isoform targeting. Biol Psychiatry 64(4):336–343PubMedCentralPubMedGoogle Scholar
  143. Krishnan V, Han MH, Graham DL, Berton O, Renthal W, Russo SJ, Laplant Q, Graham A, Lutter M, Lagace DC, Ghose S, Reister R, Tannous P, Green TA, Neve RL, Chakravarty S, Kumar A, Eisch AJ, Self DW, Lee FS, Tamminga CA, Cooper DC, Gershenfeld HK, Nestler EJ (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131(2):391–404PubMedGoogle Scholar
  144. Kulisch C, Albrecht D (2013) Effects of single swim stress on changes in TRPV1-mediated plasticity in the amygdala. Behav Brain Res 236(1):344–349PubMedGoogle Scholar
  145. Lee AL, Ogle WO, Sapolsky RM (2002) Stress and depression: possible links to neuron death in the hippocampus. Bipolar Disord 4(2):117–128PubMedGoogle Scholar
  146. Lee B, Shim I, Lee H-J, Yang Y, Hahm D-H (2009) Effects of acupuncture on chronic corticosterone-induced depression-like behavior and expression of neuropeptide Y in the rats. Neurosci Lett 453(3):151–156PubMedGoogle Scholar
  147. Lee B, Yun HY, Shim I, Lee H, Hahm DH (2012) Bupleurum falcatum prevents depression and anxiety-like behaviors in rats exposed to repeated restraint stress. J Microbiol Biotechnol 22(3):422–430PubMedGoogle Scholar
  148. Lee EJ, Son GH, Chung S, Lee S, Kim J, Choi S, Kim K (2011) Impairment of fear memory consolidation in maternally stressed male mouse offspring: evidence for nongenomic glucocorticoid action on the amygdala. J Neurosci 31(19):7131–7140Google Scholar
  149. Lehmann ML, Mustafa T, Eiden AM, Herkenham M, Eiden LE (2013) PACAP-deficient mice show attenuated corticosterone secretion and fail to develop depressive behavior during chronic social defeat stress. Psychoneuroendocrinology 38(5):702–715PubMedCentralPubMedGoogle Scholar
  150. Lewinsohn PM, Allen NB, Seeley JR, Gotlib IH (1999) First onset versus recurrence of depression: differential processes of psychosocial risk. J Abnorm Psychol 108(3):483–489PubMedGoogle Scholar
  151. Li W, Li QJ, An SC (2010a) Preventive effect of estrogen on depression-like behavior induced by chronic restraint stress. Neurosci Bull 26(2):140–146PubMedGoogle Scholar
  152. Li Y, Zheng X, Liang J, Peng Y (2010b) Coexistence of anhedonia and anxiety-independent increased novelty-seeking behavior in the chronic mild stress model of depression. Behav Process 83(3):331–339Google Scholar
  153. Lightman SL (2008) The neuroendocrinology of stress: a never ending story. J Neuroendocrinol 20(6):880–884PubMedGoogle Scholar
  154. Lin D, Bruijnzeel AW, Schmidt P, Markou A (2002) Exposure to chronic mild stress alters thresholds for lateral hypothalamic stimulation reward and subsequent responsiveness to amphetamine. Neuroscience 114(4):925–933PubMedGoogle Scholar
  155. Litvin Y, Murakami G, Pfaff DW (2011) Effects of chronic social defeat on behavioral and neural correlates of sociality: Vasopressin, oxytocin and the vasopressinergic V1b receptor. Physiol Behav 103(3–4):393–403PubMedGoogle Scholar
  156. Liu RT, Alloy LB (2010) Stress generation in depression: a systematic review of the empirical literature and recommendations for future study. Clin Psychol Rev 30(5):582–593PubMedCentralPubMedGoogle Scholar
  157. Lopez JF, Chalmers DT, Little KY, Watson SJ (1998) A.E. Bennett Research Award. Regulation of serotonin1A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol Psychiatry 43(8):547–573PubMedGoogle Scholar
  158. Lucassen PJ, Muller MB, Holsboer F, Bauer J, Holtrop A, Wouda J, Hoogendijk WJ, De Kloet ER, Swaab DF (2001a) Hippocampal apoptosis in major depression is a minor event and absent from subareas at risk for glucocorticoid overexposure. Am J Pathol 158(2):453–468PubMedCentralPubMedGoogle Scholar
  159. Lucassen PJ, Vollmann-Honsdorf GK, Gleisberg M, Czeh B, De Kloet ER, Fuchs E (2001b) Chronic psychosocial stress differentially affects apoptosis in hippocampal subregions and cortex of the adult tree shrew. Eur J Neurosci 14(1):161–166PubMedGoogle Scholar
  160. Lyubomirsky S, Caldwell ND, Nolen-Hoeksema S (1998) Effects of ruminative and distracting responses to depressed mood on retrieval of autobiographical memories. J Pers Soc Psychol 75(1):166–177PubMedGoogle Scholar
  161. Maciag CM, Dent G, Gilligan P, He L, Dowling K, Ko T, Levine S, Smith MA (2002) Effects of a non-peptide CRF antagonist (DMP696) on the behavioral and endocrine sequelae of maternal separation. Neuropsychopharmacology 26(5):574–582PubMedGoogle Scholar
  162. Maes M, Calabrese J, Meltzer HY (1994) The relevance of the in- versus outpatient status for studies on HPA-axis in depression: Spontaneous hypercortisolism is a feature of major depressed inpatients and not of major depression per se. Prog Neuropsychopharmacol Biol Psychiatry 18(3):503–517PubMedGoogle Scholar
  163. Makino S, Smith MA, Gold PW (1995) Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology 136(8):3299–3309PubMedGoogle Scholar
  164. Maniam J, Morris MJ (2010) Voluntary exercise and palatable high-fat diet both improve behavioural profile and stress responses in male rats exposed to early life stress: role of hippocampus. Psychoneuroendocrinology 35(10):1553–1564PubMedGoogle Scholar
  165. Mao QQ, Ip SP, Ko KM, Tsai SH, Che CT (2009) Peony glycosides produce antidepressant-like action in mice exposed to chronic unpredictable mild stress: effects on hypothalamic-pituitary-adrenal function and brain-derived neurotrophic factor. Prog Neuropsychopharmacol Biol Psychiatry 33(7):1211–1216PubMedGoogle Scholar
  166. Marais L, Stein DJ, Daniels WM (2009) Exercise increases BDNF levels in the striatum and decreases depressive-like behavior in chronically stressed rats. Metab Brain Dis 24(4):587–597PubMedGoogle Scholar
  167. Martin AL, Brown RE (2010) The lonely mouse: verification of a separation-induced model of depression in female mice. Behav Brain Res 207(1):196–207PubMedGoogle Scholar
  168. Matthews K, Forbes N, Reid IC (1995) Sucrose consumption as an hedonic measure following chronic unpredictable mild stress. Physiol Behav 57(2):241–248PubMedGoogle Scholar
  169. McCormick CM, Smith C, Mathews IZ (2008) Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 187(2):228–238PubMedGoogle Scholar
  170. McEwen BS (1998) Protective and damaging effects of stress mediators. N Engl J Med 338(3):171–179PubMedGoogle Scholar
  171. McEwen BS (2000) Allostasis and allostatic load: implications for neuropsychopharmacology. Neuropsychopharmacology 22(2):108–124PubMedGoogle Scholar
  172. Mitchell PJ, Fletcher A (1993) Venlafaxine exhibits pre-clinical antidepressant activity in the resident-intruder social interaction paradigm. Neuropharmacology 32(10):1001–1009PubMedGoogle Scholar
  173. Mlynarik M, Zelena D, Bagdy G, Makara GB, Jezova D (2007) Signs of attenuated depression-like behavior in vasopressin deficient Brattleboro rats. Horm Behav 51(3):395–405PubMedGoogle Scholar
  174. Monteggia LM, Luikart B, Barrot M, Theobold D, Malkovska I, Nef S, Parada LF, Nestler EJ (2007) Brain-derived neurotrophic factor conditional knockouts show gender differences in depression-related behaviors. Biol Psychiatry 61(2):187–197PubMedGoogle Scholar
  175. Monteleone MC, Adrover E, Pallares ME, Antonelli MC, Frasch AC, Brocco MA (2013) Prenatal stress changes the glycoprotein GPM6A gene expression and induces epigenetic changes in rat offspring brain. Epigenetics 9(1):152–160Google Scholar
  176. Moreau JL, Jenck F, Martin JR, Mortas P, Haefely WE (1992) Antidepressant treatment prevents chronic unpredictable mild stress-induced anhedonia as assessed by ventral tegmentum self-stimulation behavior in rats. Eur Neuropsychopharmacol 2(1):43–49PubMedGoogle Scholar
  177. Morley-Fletcher S, Darnaudery M, Koehl M, Casolini P, Van Reeth O, Maccari S (2003) Prenatal stress in rats predicts immobility behavior in the forced swim test. effects of a chronic treatment with tianeptine. Brain Res 989(2):246–251PubMedGoogle Scholar
  178. Morley-Fletcher S, Mairesse J, Soumier A, Banasr M, Fagioli F, Gabriel C, Mocaer E, Daszuta A, McEwen B, Nicoletti F, Maccari S (2011) Chronic agomelatine treatment corrects behavioral, cellular, and biochemical abnormalities induced by prenatal stress in rats. Psychopharmacology 217(3):301–313PubMedGoogle Scholar
  179. Mozhui K, Karlsson RM, Kash TL, Ihne J, Norcross M, Patel S, Farrell MR, Hill EE, Graybeal C, Martin KP, Camp M, Fitzgerald PJ, Ciobanu DC, Sprengel R, Mishina M, Wellman CL, Winder DG, Williams RW, Holmes A (2010) Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 30(15):5357–5367Google Scholar
  180. Mueller BR, Bale TL (2008) Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28(36):9055–9065Google Scholar
  181. Muglia L, Jacobson L, Dikkes P, Majzoub JA (1995) Corticotropin-releasing hormone deficiency reveals major fetal but not adult glucocorticoid need. Nature 373(6513):427–432PubMedGoogle Scholar
  182. Mullen PE, Martin JL, Anderson JC, Romans SE, Herbison GP (1996) The long-term impact of the physical, emotional, and sexual abuse of children: a community study. Child Abuse Negl 20(1):7–21PubMedGoogle Scholar
  183. Muller MB, Lucassen PJ, Yassouridis A, Hoogendijk WJ, Holsboer F, Swaab DF (2001) Neither major depression nor glucocorticoid treatment affects the cellular integrity of the human hippocampus. Eur J Neurosci 14(10):1603–1612PubMedGoogle Scholar
  184. Murray F, Smith DW, Hutson PH (2008) Chronic low dose corticosterone exposure decreased hippocampal cell proliferation, volume and induced anxiety and depression like behaviours in mice. Eur J Pharmacol 583(1):115–127PubMedGoogle Scholar
  185. Myles K, Funder JW (1996) Progesterone binding to mineralocorticoid receptors: in vitro and in vivo studies. Am J Physiol—Endocrinol Metab 270(4):E601–E607Google Scholar
  186. Naert G, Ixart G, Maurice T, Tapia-Arancibia L, Givalois L (2011) Brain-derived neurotrophic factor and hypothalamic-pituitary-adrenal axis adaptation processes in a depressive-like state induced by chronic restraint stress. Mol Cell Neurosci 46(1):55–66PubMedGoogle Scholar
  187. Nemeroff CB (2004) Neurobiological consequences of childhood trauma. J Clin Psychiatry 65(1):18–28PubMedGoogle Scholar
  188. Nemeroff CB, Widerlov E, Bissette G, Walleus H, Karlsson I, Eklund K, Kilts CD, Loosen PT, Vale W (1984) Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science 226(4680):1342–1344PubMedGoogle Scholar
  189. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM (2002) Neurobiology of depression. Neuron 34(1):13–25PubMedGoogle Scholar
  190. Nielsen CK, Arnt J, Sanchez C (2000) Intracranial self-stimulation and sucrose intake differ as hedonic measures following chronic mild stress: interstrain and interindividual differences. Behav Brain Res 107(1–2):21–33PubMedGoogle Scholar
  191. Nielsen DM, Carey GJ, Gold LH (2004) Antidepressant-like activity of corticotropin-releasing factor type-1 receptor antagonists in mice. Eur J Pharmacol 499(1–2):135–146PubMedGoogle Scholar
  192. O’Mahony CM, Clarke G, Gibney S, Dinan TG, Cryan JF (2011) Strain differences in the neurochemical response to chronic restraint stress in the rat: relevance to depression. Pharmacol Biochem Behav 97(4):690–699PubMedGoogle Scholar
  193. Okuyama S, Chaki S, Kawashima N, Suzuki Y, Ogawa S, Nakazato A, Kumagai T, Okubo T, Tomisawa K (1999) Receptor binding, behavioral, and electrophysiological profiles of nonpeptide corticotropin-releasing factor subtype 1 receptor antagonists CRA1000 and CRA1001. J Pharmacol Exp Ther 289(2):926–935PubMedGoogle Scholar
  194. 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):746–754PubMedCentralPubMedGoogle Scholar
  195. Pan Y, Wang FM, Qiang LQ, Zhang DM, Kong LD (2010) Icariin attenuates chronic mild stress-induced dysregulation of the LHPA stress circuit in rats. Psychoneuroendocrinology 35(2):272–283PubMedGoogle Scholar
  196. Paternain L, Garcia-Diaz DF, Milagro FI, Gonzalez-Muniesa P, Martinez JA, Campion J (2011) Regulation by chronic-mild stress of glucocorticoids, monocyte chemoattractant protein-1 and adiposity in rats fed on a high-fat diet. Physiol Behav 103(2):173–180PubMedGoogle Scholar
  197. Paul ED, Hale MW, Lukkes JL, Valentine MJ, Sarchet DM, Lowry CA (2011) Repeated social defeat increases reactive emotional coping behavior and alters functional responses in serotonergic neurons in the rat dorsal raphe nucleus. Physiol Behav 104(2):272–282PubMedCentralPubMedGoogle Scholar
  198. Pechnick RN, Kariagina A, Hartvig E, Bresee CJ, Poland RE, Chesnokova VM (2006) Developmental exposure to corticosterone: behavioral changes and differential effects on leukemia inhibitory factor (LIF) and corticotropin-releasing hormone (CRH) gene expression in the mouse. Psychopharmacology 185(1):76–83PubMedGoogle Scholar
  199. Platt JE, Stone EA (1982) Chronic restraint stress elicits a positive antidepressant response on the forced swim test. Eur J Pharmacol 82(3–4):179–181PubMedGoogle Scholar
  200. Pothion S, Bizot J-C, Trovero F, Belzung C (2004) Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav Brain Res 155(1):135–146PubMedGoogle Scholar
  201. Power RA, Wingenbach T, Cohen-Woods S, Uher R, Ng MY, Butler AW, Ising M, Craddock N, Owen MJ, Korszun A, Jones L, Jones I, Gill M, Rice JP, Maier W, Zobel A, Mors O, Placentino A, Rietschel M, Lucae S, Holsboer F, Binder EB, Keers R, Tozzi F, Muglia P, Breen G, Craig IW, Muller-Myhsok B, Kennedy JL, Strauss J, Vincent JB, Lewis CM, Farmer AE, McGuffin P (2013) Estimating the heritability of reporting stressful life events captured by common genetic variants. Psychol Med 43(9):1965–1971PubMedGoogle Scholar
  202. Quinkler M, Meyer B, Bumke-Vogt C, Grossmann C, Gruber U, Oelkers W, Diederich S, Bahr V (2002) Agonistic and antagonistic properties of progesterone metabolites at the human mineralocorticoid receptor. Eur J Endocrinol 146(6):789–799Google Scholar
  203. Rabasa C, Delgado-Morales R, Gomez-Roman A, Nadal R, Armario A (2013) Adaptation of the pituitary-adrenal axis to daily repeated forced swim exposure in rats is dependent on the temperature of water. Stress 16(6):698–705Google Scholar
  204. Radtke KM, Ruf M, Gunter HM, Dohrmann K, Schauer M, Meyer A, Elbert T (2011) Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl Psychiatry 1:e21PubMedCentralPubMedGoogle Scholar
  205. Rantamaki T, Hendolin P, Kankaanpaa A, Mijatovic J, Piepponen P, Domenici E, Chao MV, Mannisto PT, Castren E (2007) Pharmacologically diverse antidepressants rapidly activate brain-derived neurotrophic factor receptor TrkB and induce phospholipase-Cgamma signaling pathways in mouse brain. Neuropsychopharmacology 32(10):2152–2162PubMedGoogle Scholar
  206. Razzoli M, Andreoli M, Maraia G, Di Francesco C, Arban R (2010) Functional role of calcium-stimulated adenylyl cyclase 8 in adaptations to psychological stressors in the mouse: implications for mood disorders. Neuroscience 170(2):429–440PubMedGoogle Scholar
  207. Razzoli M, Carboni L, Andreoli M, Ballottari A, Arban R (2011a) Different susceptibility to social defeat stress of BalbC and C57BL6/J mice. Behav Brain Res 216(1):100–108PubMedGoogle Scholar
  208. Razzoli M, Carboni L, Andreoli M, Michielin F, Ballottari A, Arban R (2011b) Strain-specific outcomes of repeated social defeat and chronic fluoxetine treatment in the mouse. Pharmacol Biochem Behav 97(3):566–576PubMedGoogle Scholar
  209. Razzoli M, Carboni L, Arban R (2009) Alterations of behavioral and endocrinological reactivity induced by 3 brief social defeats in rats: relevance to human psychopathology. Psychoneuroendocrinology 34(9):1405–1416PubMedGoogle Scholar
  210. Razzoli M, Domenici E, Carboni L, Rantamaki T, Lindholm J, Castren E, Arban R (2011c) A role for BDNF/TrkB signaling in behavioral and physiological consequences of social defeat stress. Genes Brain Behav 10(4):424–433Google Scholar
  211. Regev L, Neufeld-Cohen A, Tsoory M, Kuperman Y, Getselter D, Gil S, Chen A (2011) Prolonged and site-specific over-expression of corticotropin-releasing factor reveals differential roles for extended amygdala nuclei in emotional regulation. Mol psychiatry 16(7):714–728PubMedGoogle Scholar
  212. Reus VI, Wolkowitz OM (2001) Antiglucocorticoid drugs in the treatment of depression. Expert Opin Investig Drugs 10(10):1789–1796PubMedGoogle Scholar
  213. Risch N, Herrell R, Lehner T, Liang KY, Eaves L, Hoh J, Griem A, Kovacs M, Ott J, Merikangas KR (2009) Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: a meta-analysis. JAMA 301(23):2462–2471PubMedCentralPubMedGoogle Scholar
  214. Rubin RT, Poland RE, Lesser IM, Winston RA, Blodgett AL (1987) Neuroendocrine aspects of primary endogenous depression. I. Cortisol secretory dynamics in patients and matched controls. Arch Gen Psychiatry 44(4):328–336PubMedGoogle Scholar
  215. Rygula R, Abumaria N, Flugge G, Fuchs E, Ruther E, Havemann-Reinecke U (2005) Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res 162(1):127–134PubMedGoogle Scholar
  216. Saarelainen T, Hendolin P, Lucas G, Koponen E, Sairanen M, MacDonald E, Agerman K, Haapasalo A, Nawa H, Aloyz R, Ernfors P, Castren E (2003) Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J Neurosci 23(1):349–357Google Scholar
  217. Salomon S, Bejar C, Schorer-Apelbaum D, Weinstock M (2011) Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats. J Neuroendocrinol 23(2):118–128PubMedGoogle Scholar
  218. Sandi C (2004) Stress, cognitive impairment and cell adhesion molecules. Nat Rev Neurosci 5(12):917–930PubMedGoogle Scholar
  219. Sapolsky RM (1999) Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp Gerontol 34(6):721–732PubMedGoogle Scholar
  220. Sapolsky RM (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57(10):925–935PubMedGoogle Scholar
  221. Savignac HM, Finger BC, Pizzo RC, O’Leary OF, Dinan TG, Cryan JF (2011) Increased sensitivity to the effects of chronic social defeat stress in an innately anxious mouse strain. Neuroscience 192:524–536PubMedGoogle Scholar
  222. Schmidt MV, Scharf SH, Liebl C, Harbich D, Mayer B, Holsboer F, Müller MB (2010a) A novel chronic social stress paradigm in female mice. Horm Behav 57(4–5):415–420PubMedGoogle Scholar
  223. Schmidt MV, Scharf SH, Sterlemann V, Ganea K, Liebl C, Holsboer F, Muller MB (2010b) High susceptibility to chronic social stress is associated with a depression-like phenotype. Psychoneuroendocrinology 35(5):635–643PubMedGoogle Scholar
  224. Schweizer MC, Henniger MS, Sillaber I (2009) Chronic mild stress (CMS) in mice: of anhedonia, ‘anomalous anxiolysis’ and activity. PLoS ONE 4(1):e4326PubMedCentralPubMedGoogle Scholar
  225. Secoli SR, Teixeira NA (1998) Chronic prenatal stress affects development and behavioral depression in rats. Stress 2(4):273–280Google Scholar
  226. Shors TJ, Seib TB, Levine S, Thompson RF (1989) Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244(4901):224–226PubMedGoogle Scholar
  227. Siegle GJ, Granholm E, Ingram RE, Matt GE (2001) Pupillary and reaction time measures of sustained processing of negative information in depression. Biol Psychiatry 49(7):624–636PubMedGoogle Scholar
  228. Silver H (1986) Physical complaints correlate better with depression than do dexamethasone suppression test results. J Clin Psychiatry 47(4):179–181PubMedGoogle Scholar
  229. Slattery DA, Uschold N, Magoni M, Bar J, Popoli M, Neumann ID, Reber SO (2012) Behavioural consequences of two chronic psychosocial stress paradigms: anxiety without depression. Psychoneuroendocrinology 37(5):702–714PubMedGoogle Scholar
  230. Spencer SJ, Xu L, Clarke MA, Lemus M, Reichenbach A, Geenen B, Kozicz T, Andrews ZB (2012) Ghrelin regulates the hypothalamic-pituitary-adrenal axis and restricts anxiety after acute stress. Biol Psychiatry 72(6):457–465PubMedGoogle Scholar
  231. Stetler C, Miller GE (2011) Depression and hypothalamic-pituitary-adrenal activation: a quantitative summary of four decades of research. Psychosom Med 73(2):114–126PubMedGoogle Scholar
  232. Stone EA, Zhang Y, Quartermain D (1997) The effect of stress on spontaneous nest leaving behavior in the mouse: an improved model of stress-induced behavioral pathology. Stress 1(3):145–154Google Scholar
  233. Strauss K, Dapp U, Anders J, von Renteln-Kruse W, Schmidt S (2011) Range and specificity of war-related trauma to posttraumatic stress; depression and general health perception: displaced former World War II children in late life. J Affect Disord 128(3):267–276PubMedGoogle Scholar
  234. Strekalova T, Spanagel R, Bartsch D, Henn FA, Gass P (2004) Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29(11):2007–2017PubMedGoogle Scholar
  235. Strekalova T, Steinbusch HW (2010) Measuring behavior in mice with chronic stress depression paradigm. Prog Neuropsychopharmacol Biol Psychiatry 34(2):348–361PubMedGoogle Scholar
  236. Suo L, Zhao L, Si J, Liu J, Zhu W, Chai B, Zhang Y, Feng J, Ding Z, Luo Y, Shi H, Shi J, Lu L (2013) Predictable chronic mild stress in adolescence increases resilience in adulthood. Neuropsychopharmacology 38(8):1387–1400PubMedCentralPubMedGoogle Scholar
  237. Suvrathan A, Tomar A, Chattarji S (2010) Effects of chronic and acute stress on rat behaviour in the forced-swim test. Stress 13(6):533–540Google Scholar
  238. Swaab DF, Bao AM, Lucassen PJ (2005) The stress system in the human brain in depression and neurodegeneration. Ageing Res Rev 4(2):141–194PubMedGoogle Scholar
  239. Swiergiel AH, Leskov IL, Dunn AJ (2008) Effects of chronic and acute stressors and CRF on depression-like behavior in mice. Behav Brain Res 186(1):32–40PubMedGoogle Scholar
  240. Swiergiel AH, Zhou Y, Dunn AJ (2007) Effects of chronic footshock, restraint and corticotropin-releasing factor on freezing, ultrasonic vocalization and forced swim behavior in rats. Behav Brain Res 183(2):178–187PubMedGoogle Scholar
  241. Szyf M (2013) DNA methylation, behavior and early life adversity. J Genet Genomics 40(7):331–338PubMedGoogle Scholar
  242. Taksande BG, Faldu DS, Dixit MP, Sakaria JN, Aglawe MM, Umekar MJ, Kotagale NR (2013) Agmatine attenuates chronic unpredictable mild stress induced behavioral alteration in mice. Eur J Pharmacol 720(1–3):115–120Google Scholar
  243. Tao M, Li Y, Xie D, Wang Z, Qiu J, Wu W, Sun J, Wang Z, Tao D, Zhao H, Tian T, Zhang J, Gao C, Niu Q, Li Q, Liu S, Liu J, Zhang Y, He Q, Rong H, Gan Z, Li J, Chen X, Pan J, Li Y, Cui Y, Han W, Ma H, Xie S, Jin G, Li L, Zhang R, Tan Q, Zhang J, Guan J, Shi S, Chen Y, Kendler KS, Flint J, Gao J (2011) Examining the relationship between lifetime stressful life events and the onset of major depression in Chinese women. J Affect Disord 135(1–3):95–99PubMedCentralPubMedGoogle Scholar
  244. Teixeira JM, Fisk NM, Glover V (1999) Association between maternal anxiety in pregnancy and increased uterine artery resistance index: cohort based study. BMJ 318(7177):153–157PubMedCentralPubMedGoogle Scholar
  245. Thorsell A, Slawecki CJ, El Khoury A, Mathe AA, Ehlers CL (2006) The effects of social isolation on neuropeptide Y levels, exploratory and anxiety-related behaviors in rats. Pharmacol Biochem Behav 83(1):28–34PubMedGoogle Scholar
  246. Torner L, Neumann ID (2002) The brain prolactin system: involvement in stress response adaptations in lactation. Stress 5(4):249–257Google Scholar
  247. Towle AC, Sze PY (1983) Steroid binding to synaptic plasma membrane: differential binding of glucocorticoids and gonadal steroids. J Steroid Biochem 18(2):135–143PubMedGoogle Scholar
  248. Trestman RL, Coccaro EF, Bernstein D, Lawrence T, Gabriel SM, Horvath TB, Siever LJ (1991) Cortisol responses to mental arithmetic in acute and remitted depression. Biol Psychiatry 29(10):1051–1054PubMedGoogle Scholar
  249. Uchida S, Hara K, Kobayashi A, Otsuki K, Hobara T, Yamagata H, Watanabe Y (2010) Maternal and genetic factors in stress-resilient and -vulnerable rats: a cross-fostering study. Brain Res 1316:43–50PubMedGoogle Scholar
  250. Ulloa JL, Castaneda P, Berrios C, Diaz-Veliz G, Mora S, Bravo JA, Araneda K, Menares C, Morales P, Fiedler JL (2010) Comparison of the antidepressant sertraline on differential depression-like behaviors elicited by restraint stress and repeated corticosterone administration. Pharmacol Biochem Behav 97(2):213–221PubMedGoogle Scholar
  251. Uschold-Schmidt N, Nyuyki KD, Füchsl AM, Neumann ID, Reber SO (2012) Chronic psychosocial stress results in sensitization of the HPA axis to acute heterotypic stressors despite a reduction of adrenal in vitro ACTH responsiveness. Psychoneuroendocrinology 37(10):1676–1687PubMedGoogle Scholar
  252. Vamvakopoulos NC, Chrousos GP (1993) Evidence of direct estrogenic regulation of human corticotropin-releasing hormone gene expression. Potential implications for the sexual dimophism of the stress response and immune/inflammatory reaction. J Clin Investig 92(4):1896–1902PubMedCentralPubMedGoogle Scholar
  253. Van den Bergh BR, Van Calster B, Smits T, Van Huffel S, Lagae L (2008) Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 33(3):536–545PubMedGoogle Scholar
  254. Van den Hove DL, Kenis G, Brass A, Opstelten R, Rutten BP, Bruschettini M, Blanco CE, Lesch KP, Steinbusch HW, Prickaerts J (2013) Vulnerability versus resilience to prenatal stress in male and female rats; Implications from gene expression profiles in the hippocampus and frontal cortex. Eur Neuropsychopharmacol 23(10):1226–1246Google Scholar
  255. van der Staay FJ, de Groot J, Schuurman T, Korte SM (2008) Repeated social defeat in female pigs does not induce neuroendocrine symptoms of depression, but behavioral adaptation. Physiol Behav 93(3):453–460PubMedGoogle Scholar
  256. van Praag HM (2004) Can stress cause depression? Prog Neuropsychopharmacol Biol Psychiatry 28(5):891–907PubMedGoogle Scholar
  257. van Riel E, Meijer OC, Steenbergen PJ, Joels M (2003) Chronic unpredictable stress causes attenuation of serotonin responses in cornu ammonis 1 pyramidal neurons. Neuroscience 120(3):649–658PubMedGoogle Scholar
  258. Venzala E, Garcia-Garcia AL, Elizalde N, Tordera RM (2013) Social vs. environmental stress models of depression from a behavioural and neurochemical approach. Eur Neuropsychopharmacol 23(7):697–708Google Scholar
  259. Ver Hoeve ES, Kelly G, Luz S, Ghanshani S, Bhatnagar S (2013) Short-term and long-term effects of repeated social defeat during adolescence or adulthood in female rats. Neuroscience 249:63–73PubMedCentralPubMedGoogle Scholar
  260. Vollmann-Honsdorf GK, Flügge G, Fuchs E (1997) Chronic psychosocial stress does not affect the number of pyramidal neurons in tree shrew hippocampus. Neurosci Lett 233(2–3):121–124PubMedGoogle Scholar
  261. Wang CC, Wang SJ (2009) Modulation of presynaptic glucocorticoid receptors on glutamate release from rat hippocampal nerve terminals. Synapse 63(9):745–751PubMedGoogle Scholar
  262. Watson S, Gallagher P, Smith MS, Ferrier IN, Young AH (2006) The dex/CRH test—is it better than the DST? Psychoneuroendocrinology 31(7):889–894PubMedGoogle Scholar
  263. Weinstock M (2005) The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 19(4):296–308PubMedGoogle Scholar
  264. Weninger SC, Muglia LJ, Jacobson L, Majzoub JA (1999) CRH-deficient mice have a normal anorectic response to chronic stress. Regul Pept 84(1–3):69–74PubMedGoogle Scholar
  265. Wiborg O (2013) Chronic mild stress for modeling anhedonia. Cell Tissue Res 354(1):155–169PubMedGoogle Scholar
  266. Wilkinson MB, Xiao G, Kumar A, LaPlant Q, Renthal W, Sikder D, Kodadek TJ, Nestler EJ (2009) Imipramine treatment and resiliency exhibit similar chromatin regulation in the mouse nucleus accumbens in depression models. J Neurosci 29(24):7820–7832Google Scholar
  267. Willner P (2005) Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52(2):90–110PubMedGoogle Scholar
  268. Willner P, Mitchell PJ (2002) The validity of animal models of predisposition to depression. Behav Pharmacol 13(3):169–188PubMedGoogle Scholar
  269. Willner P, Muscat R, Papp M (1992) Chronic mild stress-induced anhedonia: a realistic animal model of depression. Neurosci Biobehav Rev 16(4):525–534PubMedGoogle Scholar
  270. Willner P, Scheel-Kruger J, Belzung C (2013) The neurobiology of depression and antidepressant action. Neurosci Biobehav Rev 37(10 Pt 1):2331–2371PubMedGoogle Scholar
  271. Wilson CL, Weber ET (2013) Chemotherapy drug thioTEPA exacerbates stress-induced anhedonia and corticosteroid responses but not impairment of hippocampal cell proliferation in adult mice. Behav Brain Res 236(1):180–185PubMedCentralPubMedGoogle Scholar
  272. Wood GE, Norris EH, Waters E, Stoldt JT, McEwen BS (2008) Chronic immobilization stress alters aspects of emotionality and associative learning in the rat. Behav Neurosci 122(2):282–292Google Scholar
  273. Wu HH, Wang S (2010) Strain differences in the chronic mild stress animal model of depression. Behav Brain Res 213(1):94–102PubMedGoogle Scholar
  274. Wu T-C, Chen H-T, Chang H-Y, Yang C-Y, Hsiao M-C, Cheng M-L, Chen J-C (2013) Mineralocorticoid receptor antagonist spironolactone prevents chronic corticosterone induced depression-like behavior. Psychoneuroendocrinology 38(6):871–883PubMedGoogle Scholar
  275. Wuttke W, Duker E, Vaupel R, Jarry H (1987) The neuroendocrinology of stress. Stress Med 3(3):217–225Google Scholar
  276. Xu Y, Ku B, Tie L, Yao H, Jiang W, Ma X, Li X (2006) Curcumin reverses the effects of chronic stress on behavior, the HPA axis, BDNF expression and phosphorylation of CREB. Brain Res 1122(1):56–64PubMedGoogle Scholar
  277. Xu Z, Zhang Y, Hou B, Gao Y, Wu Y, Zhang C (2011) Chronic corticosterone administration from adolescence through early adulthood attenuates depression-like behaviors in mice. J Affect Disord 131(1–3):128–135PubMedGoogle Scholar
  278. Yau JL, Noble J, Seckl JR (2001) Acute restraint stress increases 5-HT7 receptor mRNA expression in the rat hippocampus. Neurosci Lett 309(3):141–144PubMedGoogle Scholar
  279. Yehuda R, Boisoneau D, Lowy MT, Giller EL Jr (1995) Dose-response changes in plasma cortisol and lymphocyte glucocorticoid receptors following dexamethasone administration in combat veterans with and without posttraumatic stress disorder. Arch Gen Psychiatry 52(7):583–593PubMedGoogle Scholar
  280. Young EA (1995) Normal glucocorticoid fast feedback following chronic 50 % corticosterone pellet treatment. Psychoneuroendocrinology 20(7):771–784PubMedGoogle Scholar
  281. Young EA, Haskett RF, Grunhaus L, Pande A, Weinberg VM, Watson SJ, Akil H (1994) Increased evening activation of the hypothalamic-pituitary-adrenal axis in depressed patients. Arch Gen Psychiatry 51(9):701–707PubMedGoogle Scholar
  282. Young EA, Lopez JF, Murphy-Weinberg V, Watson SJ, Akil H (2000) Hormonal evidence for altered responsiveness to social stress in major depression. Neuropsychopharmacology 23(4):411–418PubMedGoogle Scholar
  283. Yu S, Holsboer F, Almeida OFX (2008) Neuronal actions of glucocorticoids: focus on depression. J Steroid Biochem Mol Biol 108(3–5):300–309PubMedGoogle Scholar
  284. Zannas AS, McQuoid DR, Payne ME, Steffens DC, MacFall JR, Ashley-Koch A, Taylor WD (2013) Negative life stress and longitudinal hippocampal volume changes in older adults with and without depression. J Psychiatr Res 47(6):829–834PubMedCentralPubMedGoogle Scholar
  285. Zelena D, Haller J, Halasz J, Makara GB (1999) Social stress of variable intensity: physiological and behavioral consequences. Brain Res Bull 48(3):297–302PubMedGoogle Scholar
  286. Zhang L, Zhang J, Sun H, Liu H, Yang Y, Yao Z (2011) Exposure to enriched environment restores the mRNA expression of mineralocorticoid and glucocorticoid receptors in the hippocampus and ameliorates depressive-like symptoms in chronically stressed rats. Current Neurovascul Res 8(4):286–293Google Scholar
  287. Zhao Y, Liu L-J, Wang C, Li S-X (2012a) Swimming exercise may not alleviate the depressive-like behaviors and circadian alterations of neuroendocrine induced by chronic unpredictable mild stress in rats. Neurology, Psychiatry Brain Res 18(4):202–207Google Scholar
  288. Zhao Y, Wang Z, Dai J, Chen L, Huang Y, Zhan Z (2012b) Beneficial effects of benzodiazepine diazepam on chronic stress-induced impairment of hippocampal structural plasticity and depression-like behavior in mice. Behav Brain Res 228(2):339–350PubMedGoogle Scholar
  289. Zheng H, Liu Y, Li W, Yang B, Chen D, Wang X, Jiang Z, Wang H, Wang Z, Cornelisson G, Halberg F (2006) Beneficial effects of exercise and its molecular mechanisms on depression in rats. Behav Brain Res 168(1):47–55PubMedCentralPubMedGoogle Scholar
  290. Zhou QG, Zhu LJ, Chen C, Wu HY, Luo CX, Chang L, Zhu DY (2011) Hippocampal neuronal nitric oxide synthase mediates the stress-related depressive behaviors of glucocorticoids by downregulating glucocorticoid receptor. J Neurosci 31(21):7579–7590Google Scholar
  291. Zorrilla EP, Valdez GR, Nozulak J, Koob GF, Markou A (2002) Effects of antalarmin, a CRF type 1 receptor antagonist, on anxiety-like behavior and motor activation in the rat. Brain Res 952(2):188–199PubMedGoogle Scholar
  292. Zunszain PA, Anacker C, Cattaneo A, Carvalho LA, Pariante CM (2011) Glucocorticoids, cytokines and brain abnormalities in depression. Prog Neuropsychopharmacol Biol Psychiatry 35(3):722–729PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Helle M. Sickmann
    • 1
    • 2
  • Yan Li
    • 3
  • Arne Mørk
    • 2
  • Connie Sanchez
    • 3
  • Maria Gulinello
    • 4
  1. 1.Department of Drug Design and Pharmacology, Faculty of Health and Medical SciencesUniversity of CopenhagenCopenhagenDenmark
  2. 2.Lundbeck Research DKCopenhagenDenmark
  3. 3.Lundbeck Research USAParamusUSA
  4. 4.Albert Einstein College of Medicine, Yeshiva UniversityBronxUSA

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