Predictable chronic mild stress improves mood, hippocampal neurogenesis and memory

Molecular Psychiatry

Volumn 16, Issue 2, 2011, Pages 171-183

  Parihar, V K ^a,b   Hattiangady, B ^a,b   Kuruba, R ^a,b   Shuai, B ^a,b   Shetty, A K ^a,b  

^a DURHAM VA MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

dentate neurogenesis; depression; hippocampal plasticity; stem cells; stress and neurogenesis

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; BRAIN FUNCTION; CHRONIC STRESS; COGNITION; DEPRESSION; HIPPOCAMPUS; MEMORY; MOOD; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT;

AFFECT; ANIMALS; BROMODEOXYURIDINE; CELL COUNT; CHOICE BEHAVIOR; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MICROTUBULE-ASSOCIATED PROTEINS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; PREDICTIVE VALUE OF TESTS; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; SWIMMING; TIME FACTORS;

EID: 79151480276     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2009.130     Document Type: Article

References (75)

1. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996; 16: 2027-2033.
2. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA et al. Neurogenesis in the adult human hippocampus. Nat Med 1998; 4: 1313-1317.
3. Gould E, Tanapat P, Hastings NB, Shors TJ. Neurogenesis in adulthood: a possible role in learning. Trends Cogn Sci 1999; 3: 186-192.
4. Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 2005; 21: 464-476.
5. Rao MS, Hattiangady B, Shetty AK. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 2006; 5: 545-558.
6. Van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. Functional neurogenesis in the adult hippocampus. Nature 2002; 415: 1030-1034.
7. Abrous DN, Koehl M, Le Moal M. Adult neurogenesis: from precursors to network and physiology. Physiol Rev 2005; 85: 523-569.
8. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH et al. Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 2008; 11: 901-907.
9. Feng R, Rampon C, Tang YP, Shrom D, Jin J, Kyin M et al. Deficient neurogenesis in forebrain-specific presenilin-1 knockout mice is associated with reduced clearance of hippocampal memory traces. Neuron 2001; 32: 911-926.
10. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001; 410: 372-376.
11. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E. Neurogenesis may relate to some but not all types of hippocampaldependent learning. Hippocampus 2002; 12: 578-584.
12. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 2003; 100: 14385-14390.
13. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003; 301: 805-809.
14. Van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005; 25: 8680-8685.
15. Kee N, Teixeira CM, Wang AH, Frankland PW. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 2007; 10: 355-362.
16. Bizon JL, Lee HJ, Gallagher M. Neurogenesis in a rat model of agerelated cognitive decline. Aging Cell 2004; 3: 227-234.
17. Leuner B, Gould E, Shors TJ. Is there a link between adult neurogenesis and learning? Hippocampus 2006; 16: 216-224.
18. Thomas RM, Hotsenpiller G, Peterson DA. Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J Neurosci 2007; 27: 2734-2743.
19. Pollak DD, Monje FJ, Zuckerman L, Denny CA, Drew MR, Kandel ER. An animal model of a behavioral intervention for depression. Neuron 2008; 60: 149-161.
20. Revest JM, Dupret D, Koehl M, Funk-Reiter C, Grosjean N, Piazza PV et al. Adult hippocampal neurogenesis is involved in anxietyrelated behaviors. Mol Psychiatry 2009; 14: 959-967.
21. Taliaz D, Stall N, Dar DE, Zangen A. Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol Psychiatry 2009; e-pub ahead of print.
22. Dupret D, Revest JM, Koehl M, Ichas F, De Giorgi F, Costet P et al. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 2008; 3: e1959.
23. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 2008; 11: 1153-1161.
24. Clelland CD, Choi M, Romberg C, Clemenson Jr GD, Fragniere A, Tyers P et al. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009; 325: 210-213.
25. Jessberger S, Clark RE, Broadbent NJ, Clemenson Jr GD, Consiglio A, Lie DC et al. Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 2009; 16: 147-154.
26. Vollmayr B, Mahlstedt MM, Henn FA. Neurogenesis and depression: what animal models tell us about the link. Eur Arch Psychiatry Clin Neurosci 2007; 257: 300-303.
27. Kempermann G, Gage FH. Closer to neurogenesis in adult humans. Nat Med 1998; 4: 555-557.
28. Warner-Schmidt JL, Duman RS. Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 2006; 16: 239-249.
29. Montaron MF, Drapeau E, Dupret D, Kitchener P, Aurousseau C, Le Moal M et al. Lifelong corticosterone level determines agerelated decline in neurogenesis and memory. Neurobiol Aging 2006; 27: 645-654.
30. Hitoshi S, Maruta N, Higashi M, Kumar A, Kato N, Ikenaka K. Antidepressant drugs reverse the loss of adult neural stem cells following chronic stress. J Neurosci Res 2007; 85: 3574-3585.
31. Li S, Wang C, Wang W, Dong H, Hou P, Tang Y. Chronic mild stress impairs cognition in mice: from brain homeostasis to behavior. Life Sci 2008; 82: 934-942.
32. Liu Q, Yu J, Mao-Ying QL, Mi WL, Li B, Wang YQ et al. Repeated clomipramine treatment reversed the inhibition of cell proliferation in adult hippocampus induced by chronic unpredictable stress. Pharmacogenomics J 2008; 8: 375-383.
33. Stambor Z. Stressed out nation. Monit Psychol 2006; 37: 28.
34. Joels M, Karst H, Alfarez D, Heine VM, Qin Y, Van Riel E et al. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004; 7: 221-231.
35. Heine VM, Zareno J, Maslam S, Joels M, Lucassen PJ. Chronic stress in the adult dentate gyrus reduces cell proliferation near the vasculature and VEGF and Flk-1 protein expression. Eur J Neurosci 2005; 21: 1304-1314.
36. Galea LA, WiDe JK, Barr AM. Estradiol alleviates depressive-like symptoms in a novel animal model of post-partum depression. Behav Brain Res 2001; 122: 1-9.
37. Pellow S, Chopin P, File SE, Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 1985; 14: 149-167.
38. Rao MS, Hattiangady B, Reddy DS, Shetty AK. Hippocampal neurodegeneration, spontaneous seizures, and mossy fiber sprouting in the F344 rat model of temporal lobe epilepsy. J Neurosci Res 2006; 83: 1088-1105.
39. Abdel-Rahman A, Rao MS, Shetty AK. Nestin expression in hippocampal astrocytes after injury depends on the age of the hippocampus. Glia 2004; 47: 299-313.
40. Hattiangady B, Rao MS, Shetty AK. Plasticity of hippocampal stem/progenitor cells to enhance neurogenesis in response to kainate-induced injury is lost by middle age. Aging Cell 2008; 7: 207-224.
41. Rao MS, Shetty AK. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 2004; 19: 234-246.
42. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 2003; 130: 391-399.
43. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984; 11: 47-60.
44. Gourley SL, Kiraly DD, Howell JL, Olausson P, Taylor JR. Acute hippocampal brain-derived neurotrophic factor restores motivational and forced swim performance after corticosterone. Biol Psychiatry 2008; 64: 884-890.
45. Wang SH, Zhang ZJ, Guo YJ, Teng GJ, Chen BA. Hippocampal neurogenesis and behavioural studies on adult ischemic rat response to chronic mild stress. Behav Brain Res 2008; 189: 9-16.
46. Borcel E, Perez-Alvarez L, Herrero AI, Brionne T, Varea E, Berezin V et al. Chronic stress in adulthood followed by intermittent stress impairs spatial memory and the survival of newborn hippocampal cells in aging animals: prevention by FGL, a peptiDe mimetic of neural cell adhesion molecule. Behav Pharmacol 2008; 19: 41-49.
47. Lucassen PJ, Heine VM, Muller MB, Van der Beek EM, Wiegant VM, De Kloet ER et al. Stress, depression and hippocampal apoptosis. CNS Neurol Disord Drug Targets 2006; 5: 531-546.
48. Pham K, Nacher J, Hof PR, McEwen BS. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur J Neurosci 2003; 17: 879-886.
49. Becker S, Macqueen G, Wojtowicz JM. Computational modeling and empirical studies of hippocampal neurogenesis-dependent memory: effects of interference, stress and depression. Brain Res 2009; 1299: 45-54.
50. Sahay A, Hen R. Hippocampal neurogenesis and depression. Novartis Found Symp 2008; 289: 152-160; discussion 160-154, 193-155.
51. Boldrini M, Underwood MD, Hen R, Rosoklija GB, Dwork AJ, John Mann J et al. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 2009; 34: 2376-2389.
52. Ageta H, Murayama A, Migishima R, Kida S, Tsuchida K, Yokoyama M et al. Activin in the brain modulates anxiety-related behavior and adult neurogenesis. PLoS One 2008; 3: e1869.
53. Bergami M, Rimondini R, Santi S, Blum R, Gotz M, Canossa M. Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc Natl Acad Sci USA 2008; 105: 15570-15575.
54. Smith SM, Vale WW. The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci 2006; 8: 383-395.
55. Yuen EY, Liu W, Karatsoreos IN, Feng J, McEwen BS, Yan Z. Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proc Natl Acad Sci USA 2009; 106: 17552-17557.
56. Joels M, Pu Z, Wiegert O, Oitzl MS, Krugers HJ. Learning under stress: how does it work? Trends Cogn Sci 2006; 10: 152-158.
57. McEwen BS. The neurobiology of stress: from serendipity to clinical relevance. Brain Res 2000; 886: 172-189.
58. Joels M, Krugers H, Karst H. Stress-induced changes in hippocampal function. Prog Brain Res 2008; 167: 3-15.
59. Muscatell KA, Slavich GM, Monroe SM, Gotlib IH. Stressful life events, chronic difficulties, and the symptoms of clinical depression. J Nerv Ment Dis 2009; 197: 154-160.
60. Gould E, Tanapat P, Rydel T, Hastings N. Regulation of hippocampal neurogenesis in adulthood. Biol Psychiatry 2000; 48: 715-720.
61. Mirescu C, Peters JD, Gould E. Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 2004; 7: 841-846.
62. Garcia A, Steiner B, Kronenberg G, Bick-Sander A, Kempermann G. Age-dependent expression of glucocorticoid and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell 2004; 3: 363-371.
63. Yu IT, Lee SH, Lee YS, Son H. Differential effects of corticosterone and dexamethasone on hippocampal neurogenesis in vitro. Biochem Biophys Res Commun 2004; 317: 484-490. (Pubitemid 38452508)
64. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, Malenka RC. Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 2004; 42: 535-552.
65. Nakamichi N, Takarada T, Yoneda Y. Neurogenesis mediated by gamma-aminobutyric acid and glutamate signaling. J Pharmacol Sci 2009; 110: 133-149.
66. Lupien SJ, Wilkinson CW, Briere S, Menard C, Ng Ying Kin NM, Nair NP. The modulatory effects of corticosteroids on cognition: studies in young human populations. Psychoneuroendocrinology 2002; 27: 401-416.
67. Joels M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol Sci 2006; 27: 244-250.
68. Molteni R, Fumagalli F, Magnaghi V, Roceri M, Gennarelli M, Racagni G et al. Modulation of fibroblast growth factor-2 by stress and corticosteroids: from developmental events to adult brain plasticity. Brain Res Brain Res Rev 2001; 37: 249-258.
69. Molteni R, Calabrese F, Cattaneo A, Mancini M, Gennarelli M, Racagni G et al. Acute stress responsiveness of the neurotrophin BDNF in the rat hippocampus is modulated by chronic treatment with the antidepressant duloxetine. Neuropsychopharmacology 2009; 34: 1523-1532.
70. Jin K, Sun Y, Xie L, Batteur S, Mao XO, Smelick C et al. Neurogenesis and aging: FGF-2 and HB-EGF restore neurogenesis in hippocampus and subventricular zone of aged mice. Aging Cell 2003; 2: 175-183.
71. Lichtenwalner RJ, Forbes ME, Bennett SA, Lynch CD, Sonntag WE, Riddle DR. Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 2001; 107: 603-613.
72. Lee J, Seroogy KB, Mattson MP. Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. J Neurochem 2002; 80: 539-547.
73. Decressac M, Prestoz L, Veran J, Cantereau A, Jaber M, Gaillard A. NeuropeptiDe Y stimulates proliferation, migration and differentiation of neural precursors from the subventricular zone in adult mice. Neurobiol Dis 2009; 34: 441-449.
74. Howell OW, Silva S, Scharfman HE, Sosunov AA, Zaben M, Shatya A et al. NeuropeptiDe Y is important for basal and seizureinduced precursor cell proliferation in the hippocampus. Neurobiol Dis 2007; 26: 174-188.
75. Lee JS, Jang DJ, Lee N, Ko HG, Kim H, Kim YS et al. Induction of neuronal vascular endothelial growth factor expression by cAMP in the dentate gyrus of the hippocampus is required for antidepressant-like behaviors. J Neurosci 2009; 29: 8493-8505.