Increased stress-induced intra-hippocampus corticosterone rise associated with memory impairments in middle-aged mice

Neurobiology of Learning and Memory

Volumn 93, Issue 3, 2010, Pages 343-351

  Tronche, C ^a,b   Pierard C ^a   Coutan, M ^a   Chauveau, F ^a   Liscia, P ^a   Beracochea D ^b  

^a INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Acute stress; Aging; Glucocorticoids; Memory retrieval; Mice; Microdialysis

Indexed keywords

CORTICOSTERONE; METYRAPONE;

ACUTE STRESS; AGING; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; HIPPOCAMPUS; HISTOLOGY; IN VIVO STUDY; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; MICRODIALYSIS; MOUSE; NONHUMAN; TASK PERFORMANCE;

EID: 77950692068     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2009.11.009     Document Type: Article

References (48)

1. Akirav I., Kozenicky M., Tal D., Sandi C., Venero C., Richter-Levin G. A facilitative role for corticosterone in the acquisition of a spatial task under moderate stress. Learning & Memory 2004, 11:188-195.
2. Azcoitia I., Perez-Martin M., Salazar V., Castillo C., Ariznavarreta C., Garcia-Segura L.M., et al. Growth hormone prevents neuronal loss in the aged rat hippocampus. Neurobiology of Aging 2005, 26:697-703.
3. Beracochea D., Boucard A., Trocme-Thibierge C., Morain P. Improvement of contextual memory by S 24795 in aged mice: Comparison with memantine. Psychopharmacology (Berlin) 2008, 196:555-564.
4. Beracochea D., Liscia P., Tronche C., Chauveau F., Jouanin J.C., Pierard C. Stress modulation of the memory retrograde-enhancing effects of the awakening drug modafinil in mice. Psychopharmacology (Berl) 2008, 196:1-13.
5. Celerier A., Pierard C., Beracochea D. Effects of ibotenic acid lesions of the dorsal hippocampus on contextual fear conditioning in mice: Comparison with mammillary body lesions. Behavioral Brain Research 2004, 151:65-72.
6. Celerier A., Pierard C., Rachbauer D., Sarrieau A., Beracochea D. Contextual and serial discriminations: A new learning paradigm to assess simultaneously the effects of acute stress on retrieval of flexible or stable information in mice. Learning & Memory 2004, 11:196-204.
7. Chauveau, F., Tronche, C., Pierard, C., Liscia, P., Drouet, I., Coutan, M. et al. (2009). Rapid stress-induced corticosterone rise in the hippocampus reverses serial memory retrieval pattern. Hippocampus (April 9, Epub ahead of print).
8. Chauveau F., Pierard C., Tronche C., Coutan M., Drouet I., Liscia P., et al. The hippocampus and prefrontal cortex are differentially involved in serial memory retrieval in non-stress and stress conditions. Neurobiology of Learning and Memory 2009, 91:447-455.
9. Cizza G., Calogero A.E., Brady L.S., Bagdy G., Bergamini E., Blackman M.R., et al. Male Fischer 344/N rats show a progressive central impairment of the hypothalamic-pituitary-adrenal axis with advancing age. Endocrinology 1994, 134:1611-1620.
10. Cizza G., Gold P.W., Chrousos G.P. Aging is associated in the 344/N Fischer rat with decreased stress responsivity of central and peripheral catecholaminergic systems and impairment of the hypothalamic-pituitary-adrenal axis. Annals of the New York Academy of Sciences 1995, 771:491-511.
11. Cordero M.I., Kruyt N.D., Merino J.J., Sandi C. Glucocorticoid involvement in memory formation in a rat model for traumatic memory. Stress 2002, 5:73-79.
12. Dallman M.F. Fast glucocorticoid actions on brain: Back to the future. Front Neuroendocrinology 2005, 26:103-108.
13. de Quervain D.J., Henke K., Aerni A., Treyer V., McGaugh J.L., Berthold T., et al. Glucocorticoid-induced impairment of declarative memory retrieval is associated with reduced blood flow in the medial temporal lobe. European Journal of Neuroscience 2003, 17:1296-1302.
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. Droste S.K., de Groote L., Atkinson H.C., Lightman S.L., Reul J.M., Linthorst A.C. Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology 2008, 149:3244-3253.
16. Etchamendy N., Enderlin V., Marighetto A., Vouimba R.M., Pallet V., Jaffard R., et al. Alleviation of a selective age-related relational memory deficit in mice by pharmacologically induced normalization of brain retinoid signaling. Journal of Neuroscience 2001, 21:6423-6429.
17. Ferrari E., Magri F. Role of neuroendocrine pathways in cognitive decline during aging. Ageing Research Review 2008, 7:225-233.
18. Golier J.A., Schmeidler J., Yehuda R. Pituitary response to metyrapone in Gulf War veterans: Relationship to deployment, PTSD, and unexplained health symptoms. Psychoneuroendocrinology 2009, 34:1338-1345.
19. Groc L., Choquet D., Chaouloff F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nature Neuroscience 2008, 11:868-870.
20. Herman J.P., Larson B.R., Speert D.B., Seasholtz A.F. Hypothalamo-pituitary-adrenocortical dysregulation in aging F344/Brown-Norway F1 hybrid rats. Neurobiology of Aging 2001, 22:323-332.
21. Holmes M.C., Yau J.L., Kotelevtsev Y., Mullins J.J., Seckl J.R. 11beta-hydroxysteroid dehydrogenases in the brain: Two enzymes two roles. Annals of the New York Academy of Sciences 2003, 1007:357-366.
22. Joels M., de Kloet E.R. Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems. Progress in Neurobiology 1994, 43:1-36.
23. Kasckow J.W., Segar T.M., Xiao C., Furay A.R., Evanson N.K., Ostrander M.M., et al. Stability of neuroendocrine and behavioral responsiveness in aging Fischer 344/Brown-Norway hybrid rats. Endocrinology 2005, 146:3105-3112.
24. Lupien S.J., Nair N.P., Briere S., Maheu F., Tu M.T., Lemay M., et al. Increased cortisol levels and impaired cognition in human aging: Implication for depression and dementia in later life. Review Neuroscience 1999, 10:117-139.
25. Lye T.C., Piguet O., Grayson D.A., Creasey H., Ridley L.J., Bennett H.P., et al. Hippocampal size and memory function in the ninth and tenth decades of life: The Sydney Older Persons Study. Journal of Neurology Neurosurgery Psychiatry 2004, 75:548-554.
26. Mason S.R., Ward L.C., Reilly P.E. Fluorimetric detection of serum corticosterone using high-performance liquid chromatography. Journal of Chromatography 1992, 581:267-271.
27. Mattson M.P., Maudsley S., Martin B. A neural signaling triumvirate that influences ageing and age-related disease: Insulin/IGF-1, BDNF and serotonin. Ageing Research Review 2004, 3:445-464.
28. Miller D.B., O'Callaghan J.P. Effects of aging and stress on hippocampal structure and function. Metabolism 2003, 52:17-21.
29. Miller D.B., O'Callaghan J.P. Aging, stress and the hippocampus. Ageing Research Review 2005, 4:123-140.
30. Nichols N.R., Zieba M., Bye N. Do glucocorticoids contribute to brain aging?. Brain Research Review 2001, 37:273-286.
31. Oitzl M.S., Reichardt H.M., Joëls M., Kloet De. Point mutation in the mouse glucocorticoids receptors preventing DNA binding impairs spatial memory. Proceedings of the National Academy of Sciences USA 2001, 98:12790-12795.
32. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2001, Academic Press, San Diego. 2nd ed.
33. Pierard C., Tronche C., Liscia P., Chauveau F., Beracochea D. Combined effects of acute stress and amphetamine on serial memory retrieval pattern in mice. Psychopharmacology (Berl) 2009, 203:463-473.
34. Rapp P.R., Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proceedings of the National Academy of Sciences USA 1996, 93:9926-9930.
35. Raz N., Lindenberger U., Rodrigue K.M., Kennedy K.M., Head D., Williamson A., et al. Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cerebral Cortex 2005, 15:1676-1689.
36. Roozendaal B. Systems mediating acute glucocorticoid effects on memory consolidation and retrieval. Progress in Neuropsychopharmacology and Biological Psychiatry 2003, 27:1213-1223.
37. Roozendaal B., de Quervain D.J., Ferry B., Setlow B., McGaugh J.L. Basolateral amygdala-nucleus accumbens interactions in mediating glucocorticoid enhancement of memory consolidation. Journal of Neuroscience 2001, 21:2518-2525.
38. Roozendaal B., Griffith Q.K., Buranday J., De Quervain D.J., McGaugh J.L. The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: Dependence on the basolateral amygdala. Proceedings of the National Academy of Sciences USA 2003, 100:1328-1333.
39. Roozendaal B., Phillips R.G., Power A.E., Brooke S.M., Sapolsky R.M., McGaugh J.L. Memory retrieval impairment induced by hippocampal CA3 lesions is blocked by adrenocortical suppression. Nature Neuroscience 2001, 4:1169-1171.
40. Sandi C., Pinelo-Nava M.T. Stress and memory: Behavioral effects and neurobiological mechanisms. Neural Plasticity 2007, 2007:78970.
41. Sapolsky R.M., Krey L.C., Mc Ewen B. The neuroendocrinology of stress and aging: The glucocorticoid cascade hypothesis. Endocrine Reviews 1986, 7:284-301.
42. Stein B.A., Sapolsky R.M. Chemical adrenalectomy reduces hippocampal damage induced by kainic acid. Brain Research 1988, 473:175-180.
43. Stein-Behrens B., Mattson M.P., Chang I., Yeh M., Sapolsky R. Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus. Journal of Neuroscience 1994, 14:5373-5380.
44. Touzani K., Marighetto A., Jaffard R. Fos imaging reveals ageing-related changes in hippocampal response to radial maze discrimination testing in mice. European Journal of Neuroscience 2003, 17:628-640.
45. Vallee M., Purdy R.H., Mayo W., Koob G.F., Le Moal M. Neuroactive steroids: New biomarkers of cognitive aging. Journal of Steroid Biochemistry and Molecular Biology 2003, 85:329-335.
46. Wan S.L., Liao M.Y., Sun K. Postnatal development of 11beta-hydroxysteroid dehydrogenase type 1 in the rat hippocampus. Journal of Neuroscience Research 2002, 69:681-686.
47. Yarom O., Maroun M., Richter-Levin G. Exposure to forced swim stress alters local circuit activity and plasticity in the dentate gyrus of the hippocampus. Neural Plasticity 2008, 2008:194097.
48. Yehuda R., Bierer L.M., Sarapas C., Makotkine I., Andrew R., Seckl J.R. Cortisol metabolic predictors of responses to psychotherapy for symptoms of PTSD in survivors of the World Trade Center attacks on September 11, 2001. Psychoneuroendocrinology 2009, 34:1304-1313.