Increased stress reactivity is associated with cognitive deficits and decreased hippocampal brain-derived neurotrophic factor in a mouse model of affective disorders

Journal of Psychiatric Research

Volumn 44, Issue 9, 2010, Pages 566-575

  Knapman, A ^a   Heinzmann, J M ^a   Hellweg, R ^b   Holsboer, F ^a   Landgraf, R ^a   Touma, C ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Animal model; BDNF; Cognition; Depression; Hippocampus; Stress

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BREEDING LINE; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; EXPERIMENTAL MOUSE; FEMALE; HIPPOCAMPUS; MAJOR DEPRESSION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECOGNITION; SPATIAL MEMORY; STRESS;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; COGNITION DISORDERS; CORTICOSTERONE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MOOD DISORDERS; NEUROPSYCHOLOGICAL TESTS; RECOGNITION (PSYCHOLOGY); STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 77952542665     PISSN: 00223956     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2009.11.014     Document Type: Article

References (82)

1. Airaksinen E., Wahlin A., Forsell Y., Larsson M. Low episodic memory performance as a premorbid marker of depression: evidence from a 3-year follow-up. Acta Psychiatrica Scandinavica 2007, 115:458-465.
2. Angst J., Gamma A., Sellaro R., Zhang H., Merikangas K. Toward validation of atypical depression in the community: results of the Zurich cohort study. Journal Affective Disorders 2002, 72:125-138.
3. Antonijevic I.A. Depressive disorders - is it time to endorse different pathophysiologies?. Psychoneuroendocrinology 2006, 31:1-15.
4. Austin M.P., Mitchell P., Goodwin G.M. Cognitive deficits in depression: possible implications for functional neuropathology. Brittish Journal of Psychiatry 2001, 178:200-206.
5. Belanoff J.K., Kalehzan M., Sund B., Fleming Ficek S.K., Schatzberg A.F. Schatzberg: cortisol activity and cognitive changes in psychotic major depression. American Journal Psychiatry 2001, 158:1612-1616.
6. Bredy T.W., Lee A.W., Meaney M.J., Brown R.E. Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus). Hormones and Behavior 2004, 46:30-38.
7. Bremner J.D., Narayan M., Anderson E.R., Staib L.H., Miller H.L., Charney D.S. Hippocampal volume reduction in major depression. American Journal of Psychiatry 2000, 157:115-118.
8. Bremner J.D., Vythilingam M., Vermetten E., Anderson G., Newcomer J.W., Charney D.S. Effects of glucocorticoids on declarative memory function in major depression. Biological Psychiatry 2004, 55:811-815.
9. Buchanan T.W., Lovallo W.R. Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 2001, 26:307-317.
10. Chen G., Kolbeck R., Barde Y.A., Bonhoeffer T., Kossel A. Relative contribution of endogenous neurotrophins in hippocampal long-term potentiation. Journal of Neuroscience 1999, 19:7983-7990.
11. Chen G.H., Wang Y.J., Zhang L.Q., Zhou J.N. Age- and sex-related disturbance in a battery of sensorimotor and cognitive tasks in Kunming mice. Physiological Behavior 2004, 83:531-541.
12. Clinton L.K., Billings L.M., Green K.N., Caccamo A., Ngo J., Oddo S., et al. Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice. Neurobiology of Disease 2007, 28:76-82.
13. Cryan J.F., Holmes A. The ascent of mouse: advances in modelling human depression and anxiety. Nature Reviews Drug Discovery 2005, 4:775-790.
14. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
15. Dellu F., Contarino A., Simon H., Koob G.F., Gold L.H. Genetic differences in response to novelty and spatial memory using a two-trial recognition task in mice. Neurobiology Learning and Memory 2000, 73:31-48.
16. Dellu F., Mayo W., Cherkaoui J., Le Moal M., Simon H. A two-trial memory task with automated recording: study in young and aged rats. Brain Research 1992, 588:132-139.
17. Egan M.F., Kojima M., Callicott J.H., Goldberg T.E., Kolachana B.S., Bertolino A., et al. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell 2003, 112:257-269.
18. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience 2000, 1:41-50.
19. Eichenbaum H., Yonelinas A.P., Ranganath C. The medial temporal lobe and recognition memory. Annuual Review of Neuroscience 2007, 30:123-152.
20. Exner C., Lange C., Irle E. Impaired implicit learning and reduced pre-supplementary motor cortex size in early-onset major depression with melancholic features. Journal of Affective Disorders 2009, 119:156-192.
21. Figurov A., Pozzo-Miller L.D., Olafsson P., Wang T., Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 1996, 381:706-709.
22. Flood J.F., Vidal D., Bennett E.L., Orme A.E., Vasquez S., Jarvik M.E. Memory facilitating and anti-amnesic effects of corticosteroids. Pharmacology Biochemistry and Behavior 1978, 8:81-87.
23. Frodl T., Schaub A., Banac S., Charypar M., Jager M., Kummler P., et al. Reduced hippocampal volume correlates with executive dysfunctioning in major depression. Journal of Psychiatry and Neuroscience 2006, 31:316-323.
24. Gold P.W., Chrousos G.P. Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Molecular Psychiatry 2002, 7:254-275.
25. Gold P.W., Licinio J., Wong M.L., Chrousos G.P. Corticotropin releasing hormone in the pathophysiology of melancholic and atypical depression and in the mechanism of action of antidepressant drugs. Annals of the NewYork Academy of Sciences 1995, 771:716-729.
26. Gorski J.A., Balogh S.A., Wehner J.M., Jones K.R. Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice. Neuroscience 2003, 121:341-354.
27. Grassi-Oliveira R., Stein L.M., Lopes R.P., Teixeira A.L., Bauer M.E. Low plasma brain-derived neurotrophic factor and childhood physical neglect are associated with verbal memory impairment in major depression - a preliminary report. Biological Psychiatry 2008, 64:281-285.
28. Greden J.F., Gardner R., King D., Grunhaus L., Carroll B.J., Kronfol Z. Dexamethasone suppression tests in antidepressant treatment of melancholia. The process of normalization and test-retest reproducibility. Archives of General Psychiatry 1983, 40:493-500.
29. Hasler G., Drevets W.C., Manji H.K., Charney D.S. Discovering endophenotypes for major depression. Neuropsychopharmacology 2004, 29:1765-1781.
30. Hellweg R., Lohmann P., Huber R., Kuhl A., Riepe M.W. Spatial navigation in complex and radial mazes in APP23 animals and neurotrophin signaling as a biological marker of early impairment. Learning and Memory 2006, 13:63-71.
31. Hellweg R., von Arnim C.A., Buchner M., Huber R., Riepe M.W. Neuroprotection and neuronal dysfunction upon repetitive inhibition of oxidative phosphorylation. Experimental Neurology 2003, 183:346-354.
32. Holsboer F. The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 2000, 23:477-501.
33. Holsboer F., Ising M. Stress hormones and stress hormone regulation: biological role and translation into therapy. Annual Review of Psychology 2010, 61.
34. Holsboer F., Liebl R., Hofschuster E. Repeated dexamethasone suppression test during depressive illness. Normalisation of test result compared with clinical improvement. Journal of Affective Disorders 1982, 4:93-101.
35. Huang T.L., Lee C.T., Liu Y.L. Serum brain-derived neurotrophic factor levels in patients with major depression: effects of antidepressants. Journal of Psychiatric Research 2008, 42:521-525.
36. Ising M., Horstmann S., Kloiber S., Lucae S., Binder E.B., Kern N., et al. Combined dexamethasone/corticotropin releasing hormone test predicts treatment response in major depression - a potential biomarker?. Biological Psychiatry 2007, 62:47-54.
37. Ising M., Kunzel H.E., Binder E.B., Nickel T., Modell S., Holsboer F. The combined dexamethasone/CRH test as a potential surrogate marker in depression. Prog Neuropsychopharmacol Biological Psychiatry 2005, 29:1085-1093.
38. Jacobsen J.P., Mork A. Chronic corticosterone decreases brain-derived neurotrophic factor (BDNF) mRNA and protein in the hippocampus, but not in the frontal cortex, of the rat. Brain Research 2006, 1110:221-225.
39. Karege F., Schwald M., Cisse M. Postnatal developmental profile of brain-derived neurotrophic factor in rat brain and platelets. Neuroscience Letters 2002, 328:261-264.
40. Kirschbaum C., Wolf O.T., May M., Wippich W., Hellhammer D.H. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Science 1996, 58:1475-1483.
41. Korte M., Staiger V., Griesbeck O., Thoenen H., Bonhoeffer T. The involvement of brain-derived neurotrophic factor in hippocampal long-term potentiation revealed by gene targeting experiments. Journal of Physiology Paris 1996, 90:157-164.
42. Kovacs G.L., Telegdy G., Lissak K. Dose-dependent action of corticosteroids on brain serotonin content and passive avoidance behavior. Hormones and Behavior 1977, 8:155-165.
43. Kubo T., Nonomura T., Enokido Y., Hatanaka H. Brain-derived neurotrophic factor (BDNF) can prevent apoptosis of rat cerebellar granule neurons in culture. Brain Research Developmental Brain Research 1995, 85:249-258.
44. Kuhlmann S., Wolf O.T. Arousal and cortisol interact in modulating memory consolidation in healthy young men. Behavioral Neuroscience 2006, 120:217-223.
45. Lee B.H., Kim H., Park S.H., Kim Y.K. Decreased plasma BDNF level in depressive patients. Journal of Affective Disorders 2007, 101:239-244.
46. Lindholm D., Castren M., Hengerer B., Leingartner A., Castren E., Thoenen H. Glucocorticoids and neurotrophin gene regulation in the nervous system. Annals of NewYork Academy of Science 1994, 746:195-202. [discussion 202-3].
47. Luethi M., Meier B., Sandi C. Stress effects on working memory, explicit memory, and implicit memory for neutral and emotional stimuli in healthy men. Front Behavioral Neuroscience 2008, 2:5.
48. Lyons D.M., Parker K.J., Zeitzer J.M., Buckmaster C.L., Schatzberg A.F. Preliminary evidence that hippocampal volumes in monkeys predict stress levels of adrenocorticotropic hormone. Biological Psychiatry 2007, 62:1171-1174.
49. MacQueen G.M., Campbell S., McEwen B.S., Macdonald K., Amano S., Joffe R.T., et al. Course of illness, hippocampal function, and hippocampal volume in major depression. Proceedings of the National Academy of Sciences USA 2003, 100:1387-1392.
50. McKittrick C.R., Magarinos A.M., Blanchard D.C., Blanchard R.J., McEwen B.S., Sakai R.R. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 2000, 36:85-94.
51. Monteggia L.M., Barrot M., Powell C.M., Berton O., Galanis V., Gemelli T., et al. Essential role of brain-derived neurotrophic factor in adult hippocampal function. Proceedings of the National Academy of Sciences USA 2004, 101:10827-10832.
52. Monteleone P., Serritella C., Martiadis V., Maj M. Decreased levels of serum brain-derived neurotrophic factor in both depressed and euthymic patients with unipolar depression and in euthymic patients with bipolar I and II disorders. Bipolar Disorder 2008, 10:95-100.
53. Murakami S., Imbe H., Morikawa Y., Kubo C., Senba E. Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neuroscience Research 2005, 53:129-139.
54. Nibuya M., Nestler E.J., Duman R.S. Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. Journal of Neuroscience 1996, 16:2365-2372.
55. Nierenberg A.A., Alpert J.E., Pava J., Rosenbaum J.F., Fava M. Course and treatment of atypical depression. Journal of Clinical Psychiatry 1998, 59(Suppl. 18):5-9.
56. Oitzl M.S., Fluttert M., Sutanto W., de Kloet E.R. Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. European Journal of Neuroscience 1998, 10:3759-3766.
57. Okuda S., Roozendaal B., McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proceedings of the National Academy of Sciences USA 2004, 101:853-858.
58. Palchykova S., Winsky-Sommerer R., Meerlo P., Durr R., Tobler I. Sleep deprivation impairs object recognition in mice. Neurobiology of Learning and Memory 2006, 85:263-271.
59. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 1996, 16:1137-1145.
60. Porsolt R.D., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Archives of International Pharmacodynamics Ther 1977, 229:327-336.
61. Porter R.J., Gallagher P., Thompson J.M., Young A.H. Neurocognitive impairment in drug-free patients with major depressive disorder. Brittish Journal of Psychiatry 2003, 182:214-220.
62. Reppermund S., Ising M., Lucae S., Zihl J. Cognitive impairment in unipolar depression is persistent and non-specific: further evidence for the final common pathway disorder hypothesis. Psychological Medicine 2009, 39:603-614.
63. Reppermund S., Zihl J., Lucae S., Horstmann S., Kloiber S., Holsboer F., et al. Persistent cognitive impairment in depression: the role of psychopathology and altered hypothalamic-pituitary-adrenocortical (HPA) system regulation. Biological Psychiatry 2007, 62:400-406.
64. Roozendaal B. Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 1999, 2000(25):213-238.
65. Sanderson D.J., Good M.A., Skelton K., Sprengel R., Seeburg P.H., Rawlins J.N., et al. Enhanced long-term and impaired short-term spatial memory in GluA1 AMPA receptor subunit knockout mice: evidence for a dual-process memory model. Learning and Mem 2009, 16:379-386.
66. 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.
67. Sapolsky R.M., Uno H., Rebert C.S., Finch C.E. Hippocampal damage associated with prolonged glucocorticoid exposure in primates. Journal of Neuroscience 1990, 10:2897-2902.
68. Schaaf M.J., de Jong J., de Kloet E.R., Vreugdenhil E. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Research 1998, 813:112-120.
69. Schaaf M.J., Hoetelmans R.W., de Kloet E.R., Vreugdenhil E. Corticosterone regulates expression of BDNF and trkB but not NT-3 and trkC mRNA in the rat hippocampus. Journal of Neuroscience Research 1997, 48:334-341.
70. Schaaf M.J., Workel J.O., Lesscher H.M., Vreugdenhil E., Oitzl M.S., de Kloet E.R. Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats. Brain Research 2001, 915:227-233.
71. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry 1957, 20:11-21.
72. Sheline Y.I., Wang P.W., Gado M.H., Csernansky J.G., Vannier M.W. Hippocampal atrophy in recurrent major depression. Proceedings of the National Academy of Sciences USA 1996, 93:3908-3913.
73. Sossin W.S., Barker P.A. Something old, something new: BDNF-induced neuron survival requires TRPC channel function. Nature Neuroscience 2007, 10:537-538.
74. Sousa N., Madeira M.D., Paula-Barbosa M.M. Corticosterone replacement restores normal morphological features to the hippocampal dendrites, axons and synapses of adrenalectomized rats. Journal of Neurocytology 1999, 28:541-558.
75. Starkman M.N., Gebarski S.S., Berent S., Schteingart D.E. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biological Psychiatry 1992, 32:756-765.
76. Stern A.J., Savostyanova A.A., Goldman A., Barnett A.S., van der Veen J.W., Callicott J.H., et al. Impact of the brain-derived neurotrophic factor Val66Met polymorphism on levels of hippocampal N-acetyl-aspartate assessed by magnetic resonance spectroscopic imaging at 3 Tesla. Biological Psychiatry 2008, 64:856-862.
77. Tordera R.M., Totterdell S., Wojcik S.M., Brose N., Elizalde N., Lasheras B., et al. Enhanced anxiety, depressive-like behaviour and impaired recognition memory in mice with reduced expression of the vesicular glutamate transporter 1 (VGLUT1). European Journal of Neuroscience 2007, 25:281-290.
78. Touma C., Bunck M., Glasl L., Nussbaumer M., Palme R., Stein H., et al. Mice selected for high versus low stress reactivity: a new animal model for affective disorders. Psychoneuroendocrinology 2008, 33:839-862.
79. Touma C., Fenzl T., Ruschel J., Palme R., Holsboer F., Kimura M. Rhythmicity in mice selected for extremes in stress reactivity: behavioural, endocrine and sleep changes resembling endophenotypes of major depression. PLoS ONE 2009, 4:e4325.
80. Villasana L., Acevedo S., Poage C., Raber J. Sex- and APOE isoform-dependent effects of radiation on cognitive function. Radiation Research 2006, 166:883-891.
81. Wang J.W., Dranovsky A., Hen R. The when and where of BDNF and the antidepressant response. Biological Psychiatry 2008, 63:640-641.
82. Watanabe Y., Gould E., McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Research 1992, 588:341-345.