Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: Effects on learning and memory

Hippocampus

Volumn 18, Issue 7, 2008, Pages 655-667

  Choy, Kwok Ho Christopher ^a,b   De Visser, Yvonne ^a   Nichols, Nancy R ^c   Van Den Buuse, Maarten ^a,b  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

Author keywords

BDNF; Cognition; Corticosterone; Depression; Development; Maternal deprivation; Schizophrenia

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLUCOCORTICOID; MESSENGER RNA; STRESS HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; IN SITU HYBRIDIZATION; LEARNING; MALE; MATERNAL DEPRIVATION; MAZE TEST; MEMORY; NEONATAL STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPATIAL MEMORY; WORKING MEMORY;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANIMALS, OUTBRED STRAINS; ANTI-INFLAMMATORY AGENTS; BODY WEIGHT; BRAIN-DERIVED NEUROTROPHIC FACTOR; CORTICOSTERONE; GENE EXPRESSION; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; MEMORY, SHORT-TERM; RATS; RATS, WISTAR; REACTION TIME; STRESS, PSYCHOLOGICAL;

EID: 47749135849     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20425     Document Type: Article

References (63)

1. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T. 2007. Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res 85:525-535.
2. Aisa B, Tordera R, Lasheras B, Del Río J, Ramírez MJ. 2005. Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32:256-266.
3. Angelucci F, Brene S, Mathe AA. 2005. BDNF in schizophrenia, depression and corresponding animal models. Mol Psychiatry 10:345-352.
4. Arango C, Kirkpatrick B, Koenig J. 2001. At issue: Stress, hippocampal neuronal turnover, and neuropsychiatric disorders. Schizophrenia Bull 27:477-480.
5. Bayer TA, Falkai P, Maier W. 1999. Genetic and non-genetic vulnerability factors in schizophrenia: The basis of the "Two hit hypothesis". J Psychiatr Res 33:543-548.
6. Brandeis R, Brandys Y, Yehuda S. 1989. The use of the Morris Water Maze in the study of memory and learning. Int J Neurosci 48:29-69.
7. Bye N, Zieba M, Wreford NG, Nichols NR. 2001. Resistance of the dentate gyrus to induced apoptosis during ageing is associated with increases in transforming growth factor-β1 messenger RNA. Neuroscience 105:853-862.
8. Canal CE, Stutz SJ, Gold PE. 2005. Glucose injections into the dorsal hippocampus or dorsolateral striatum of rats prior to T-maze training: Modulation of learning rates and strategy selection. Learn Mem 12:367-374.
9. Choy KH, van den Buuse M. 2008. Attenuated disruption of prepulse inhibition by dopaminergic stimulation after maternal deprivation and adolescent corticosterone treatment in rats. Eur Neuropsychopharmacol 18:1-13.
10. Conrad CD, Lupien SJ, Thanasoulis LC, McEwen BS. 1997. The effects of type I, type II corticosteroid receptor agonists on exploratory behavior and spatial memory in the Y-maze. Brain Res 759:76-83.
11. Conrad CD, Lupien SJ, McEwen BS. 1999. Support for a bimodal role for type II adrenal steroid receptors in spatial memory. Neurobiol Learn Mem 72:39-46.
12. Deacon RM, Bannerman DM, Kirby BP, Croucher A, Rawlins JN. 2002. Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav Brain Res 133:57-68.
13. Dellu F, Mayo W, Cherkaoui J, Le Moal M, Simon H. 1992. A two-trial memory task with automated recording: Study in young and aged rats. Brain Res 588:132-139.
14. Dellu F, Fauchey V, Le Moal M, Simon H. 1997. Extension of a new two-trial memory task in the rat: Influence of environmental context on recognition processes. Neurobiol Learning Memory 67: 112-120.
15. D'Hooge R, De Deyn PP. 2001. Applications of the Morris water maze in the study of learning and memory. Brain Res Rev 36:60-90.
16. Durany N, Michel T, Zöchling R, Boissl KW, Cruz-Sánchez FF, Riederer P, Thome J. 2001. Brain-derived neurotrophic factor and neurotrophin 3 in schizophrenic psychoses. Schizophr Res 52:79-86.
17. Egan MF, Kojima M, Callicott JH, Goldberg TE, Kolachana BS, Bertolino A, Zaitsev E, Gold B, Goldman D, Dean M, Lu B, Weinberger DR. 2003. The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell Mol Neurobiol 112:257-269.
18. Ellenbroek BA, van den Kroonenberg PTJM, Cools AR. 1998. The effects of an early stressful life event on sensorimotor gating in adult rats. Schizophr Res 30:251-260.
19. Ellenbroek BA, Cools AR. 2002. Early maternal deprivation and pre-pulse inhibition. The role of postdeprivation environment. Pharmacol Biochem Behav 73:177-184.
20. Falkenberg T, Mohammed AK, Henriksson B, Persson H, Winblad B, Lindefors N. 1992. Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci Lett 138:153-156.
21. Fumagalli F, Molteni R, Racagni G, Riva MA. 2007. Stress during development: Impact on neuroplasticity and relevance to psychopathology. Progr Neurobiol 81:197-217.
22. Garner B, Wood SJ, Pantelis C, van den Buuse M. 2006. Early maternal deprivation reduces prepulse inhibition and impairs spatial learning ability in adulthood: No further effect of post-pubertal chronic corticosterone treatment. Behav Brain Res 176:323-332.
23. Gorski JA, Balogh SA, Wehner JM, Jones KR. 2003. Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice. Neuroscience 121:341-354.
24. Hariri AR, Goldberg TE, Mattay VS, Kolachana BS, Callicott JH, Egan MF, Weinberger DR. 2003. Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J Neurosci 23: 6690-6694.
25. Hashimoto T, Bergen SE, Nguyen QL, Xu B, Monteggia LM, Pierri JN, Sun Z, Sampson AR, Lewis DA. 2005. Relationship of brain-derived neurotrophic factor and its receptor TrkB to altered inhibitory prefrontal circuitry in schizophrenia. J Neurosci 25:372-383.
26. Heldt SA, Stanek L, Chhatwal JP, Ressler KJ. 2007. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12:656-670.
27. Iritani S, Niizato K, Nawa H, Ikeda H, Emson PC. 2003. Immunohistochemical study of brain-derived neurotrophic factor and its receptor, TrkB, in the hippocampal formation of schizophrenic brains. Progr Neuro-Psychopharmacol Biol Psych 27:810-807.
28. Lee I, Kensner RP. 2003. Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J Neurosci 23:1517-1523.
29. Lehmann J, Feldon J. 2000. Long-term biobehavioral effects of maternal separation in the rat: Consistent or confusing? Rev Neurosci 11:383-408.
30. Lehmann J, Pryce CR, Feldon J. 2000. Lack of effect of an early stressful life event on sensorimotor gating in adult rats. Schizophrenia Res 41:365-371.
31. Ma YL, Wang HL, Wu HC, Wei CL, Lee EH. 1998. Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 82:957-967.
32. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G, Sun YE. 2003. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302:890-893.
33. Matthews DB, Ilgen M, White AM, Best PJ. 1999. Acute ethanol administration impairs spatial performance while facilitating non-spatial performance in rats. Neurobiol Learn Mem 72:169-179.
34. Maynard TM, Sikich L, Lieberman JA, LaMantia AS. 2001. Neural development, cell-cell signaling, and the "two-hit" hypothesis of schizophrenia. Schizophrenia Bull 27:457-476.
35. McGrath JJ, Feron FP, Burne TH, Mackay-Sim A, Eyles DW. 2003. The neurodevelopmental hypothesis of schizophrenia: A review of recent developments. Ann Med 35:86-93.
36. Meyer JS, Micco DJ, Stephenson BS, Krey LC, McEwen BS. 1979. Subcutaneous implantation method for chronic glucocorticoid replacement therapy. Physiol Behav 22:867-870.
37. Moran PM. 1993. Differential effects of scopolamine and mecamylamine on working and reference memory in the rat. Pharmacol Biochem Behav 45:533-538.
38. Morgan TE, Nichols NR, Pasinetti GM, Finch CE. 1993. TGF-β 1 mRNA increases in macrophage/microglial cells of the hippocampus in response to deafferentation and kainic acid-induced neurodegeneration. Exp Neurol 120:291-301.
39. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
40. Pantelis C, Yucel M, Wood SJ, McGorry PD, Velakoulis D. 2003. Early and late neurodevelopmental disturbances in schizophrenia and their functional consequences. Aust N Z J Psychiatry 37:399-406.
41. Pantelis C, Yucel M, Wood SJ, Velakoulis D, Sun D, Berger G, Stuart GW, Yung A, Phillips L, McGorry PD. 2005. Structural brain imaging evidence for multiple pathological processes at different stages of brain development in schizophrenia. Schizophr Bull 31:672-696.
42. Paxinos G, Watson C. 1986. The Rat Brain in Stereotaxic Co-Ordinates, 2nd ed. New York: Academic press.
43. Phillips HS, Hains JM, Laramee GR, Rosenthal A, Winslow JW. 1990. Widespread expression of BDNF but not NT3 by target areas of basal forebrain cholinergic neurons. Science 250:290-294.
44. Poldrack RA, Packard MG. 2003. Competition among multiple memory systems: Converging evidence from animal and human brain studies. Neuropsychologia 41:245-251.
45. Radecki DT, Brown LM, Martinez J, Teyler TJ. 2005. BDNF protects against stress-induced impairments in spatial learning and memory and LTP. Hippocampus 15:246-253.
46. Roceri M, Cirulli F, Pessina C, Peretto P, Racagni G, Riva MA. 2004. Postnatal repeated maternal deprivation produces age-dependent changes of brain-derived neurotrophic factor expression in selected rat brain regions. Biol Psychiatry 55:708-714.
47. Rüedi-Bettschen D, Zhang W, Russig H, Ferger B, Weston A, Pedersen E-M, Feldon J, Pryce CR. 2006. Early deprivation leads to altered behavioural, autonomic and endocrine responses to environmental challenge in adult Fischer rats. Eur J Neurosci 24:2879-2893.
48. Schaaf MJ, de Jong J, de Kloet ER, Vreugdenhil E. 1998. Downregulation of BDNF mRNA and protein in the rat hippocampus by corticosterone. Brain Res 813:112-120.
49. Schaaf MJ, Sibug RM, Duurland R, Fluttert MF, Oitzl MS, De Kloet ER, Vreugdenhil E. 1999. Corticosterone effects on BDNF mRNA expression in the rat hippocampus during morris water maze training. Stress 3:173-183.
50. Schaaf MJ, De Kloet ER, Vreugdenhil E. 2000. Corticosterone effects on BDNF expression in the hippocampus. Implications for memory formation. Stress 3:201-208.
51. Schaaf MJ, Workel JO, Lesscher HM, Vreugdenhil E, Oitzl MS, de Kloet ER. 2001. Correlation between hippocampal BDNF mRNA expression and memory performance in senescent rats. Brain Res 915:227-233.
52. Shoval G, Weizman A. 2005. The possible role of neurotrophins in the pathogenesis and therapy of schizophrenia. Eur Neuropsychopharmacol 15:319-329.
53. Smith MA, Makino S, Kvetnansky R, Post RM. 1995. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 15:1768-1777.
54. Song L, Che W, Min-Wei W, Murakami Y, Matsumoto K. 2006. Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol Biochem Behav 83:186-193.
55. Szeszko PR, Lipsky R, Mentschel C, Robinson D, Gunduz-Bruce H, Sevy S, Ashtari M, Napolitano B, Bilder RM, Kane JM, Goldman D, Malhotra AK. 2005. Brain-derived neurotrophic factor val66-met polymorphism and volume of the hippocampal formation. Mol Psychiatry 10:631-636.
56. Takahashi M, Shirakawa O, Toyooka K, Kitamura N, Hashimoto T, Maeda K, Koizumi S, Wakabayashi K, Takahashi H, Someya T, Nawa H. 2000. Abnormal expression of brain-derived neurotrophic factor and its receptor in the corticolimbic system of schizophrenic patients. Mol Psychiatry 5:293-300.
57. Terry AV Jr. 2001. Spatial navigation (Water maze) tasks. In: Buccafusco JJ, editor. Methods of Behavior Analysis in Neuroscience, 1st ed. Washington DC: CRC. pp 153-166.
58. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ. 2006. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9: 519-525.
59. Weickert CS, Hyde TM, Lipska BK, Herman MM, Weinberger DR, Kleinman JE. 2003. Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol Psychiatry 8:592-610.
60. Weickert CS, Ligons DL, Romanczyk T, Ungaro G, Hyde TM, Herman MM, Weinberger DR, Kleinman JE. 2005. Reductions in neurotrophin receptor mRNAs in the prefrontal cortex of patients with schizophrenia. Mol Psychiatry 10:637-650.
61. Wilkinson DG. 1992. The theory and practice of in situ hybridization. In: Wilkinson DG, editor. In Situ Hybridization - A Practical Approach, 1st ed. Tokyo: IRL Press Oxford University Press. pp 1-14.
62. Yamada K, Mizuno M, Nabeshima T. 2002. Role of brain-derived neurotrophic factor in learning and memory. Life Sci 70:735-744.
63. Yoshida T, Goldsmith SK, Morgan TE, Stone DJ, Finch CE. 1996. Transcription supports age-related increases of GFAP gene expression in the male rat brain. Neurosci Lett 215:107-110.