Enhanced cell death in hippocampus and emergence of cognitive impairments following a localized mini-stroke in hippocampus if preceded by a previous episode of acute stress

European Journal of Neuroscience

Volumn 27, Issue 8, 2008, Pages 2197-2209

  McDonald, Robert J ^a   Craig, Laura A ^a   Hong, Nancy S ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Alzheimer's disease; Cofactors; Glucocorticoids; Mini stroke; Necrosis; Spatial memory; Stress

Indexed keywords

CORTICOSTERONE; ENDOTHELIN 1; GLUCOCORTICOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; STROKE;

ANIMALS; BEHAVIOR, ANIMAL; CELL DEATH; COGNITION DISORDERS; CORTICOSTERONE; ENDOTHELIN-1; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NERVE DEGENERATION; RATS; RATS, LONG-EVANS; STRESS, PSYCHOLOGICAL; STROKE;

EID: 42049086996     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06151.x     Document Type: Article

References (67)

1. Adachi, N., Chen, J., Liu, K., Tsubota, S. Arai, T. (1998) Dexamethasone aggravates ischemia-induced neuronal damage by facilitating onset of anoxic depolarization and the increase in the intracellular Ca2+ concentration in gerbil hippocampus. J. Cereb. Blood Flow Metab., 18, 274 280.
2. Adachi, N., Namba, C., Nagaro, T. Arai, T. (2001) Dexamethasone reduces energy utilization in ischemic gerbil brain. Eur. J. Pharmacol., 427, 119 123.
3. American Heart Association (2005) Heart Disease and Stroke Statistics. American Heart Association, Dallas, TX.
4. Armanini, M.P., Hutchins, C., Stein, B.A. Sapolsky, R.M. (1990) Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Res., 532, 7 12.
5. Back, T., Hemmen, T. Schuler, O.G. (2004) Lesion evolution in cerebral ischemia. J. Neurol., 251, 388 397.
6. Ball, M.J., Fisman, M., Hachinski, V., Blume, W., Fox, A., Kral, V.A., Kirshen, A.J., Fox, H. Merskey, H. (1985) A new definition of Alzheimer's disease: an hippocampal dementia. Lancet, 8419, 14 16.
7. Braak, H. Braak, E. (1991) Neuropathological staging of Alzheimer-related changes. Acta Neuropath., 82, 239 259.
8. Caplan, L.R. (1994) Silent brain infarcts. Cerebrovasc. Dis., 4, 32 39.
9. Corder, E.H., Saunders, A.M., Strittmatter, W.J., Schmechel, D.E., Gaskell, P.C., Small, G.W., Roses, A.D., Haines, J.L. Pericak-Vance, M.A. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science, 261, 921 923.
10. Dahlqvist, P., Ronnback, A., Bergstrom, S.A., Soderstrom, I. Olsson, T. (2004) Environmental enrichment reverses learning impairment in the Morris water maze after focal cerebral ischemia in rats. Eur. J. Neurosci., 19, 2288 2298.
11. de la Torre, J.C. (2002) Alzheimer's disease as a vascular disorder: Nosological evidence. Stroke, 33, 1152 1162.
12. Del Ser, T., Hachinski, V., Merskey, H. Munoz, D.G. (2005) Alzheimer's disease with and without cerebral infarcts. J. Neurol. Sci., 231, 3 11.
13. Delaney, G. Potter, P. (1993) Disability post-stroke. In Teasell, R.W. (Ed.), Long-Term Consequences of Stroke. Physical Medicine and Rehabilitation: State of the Art Reviews. Hanley and Belfus, Philadelphia, Vol. 7 (20), pp. 27 42.
14. Devries, A.C., Joh, H.D., Bernard, O., Hattori, K., Hurn, P.D. Traystman, R.J. Alkayed, N.J. (2001) Social stress exacerbates stroke outcome by suppressing Bcl-2 expression. Proc. Natl Acad. Sci. USA, 98, 11824 11828.
15. Driscoll, I., Hong, N.S., Craig, L.A., Sutherland, R.J. McDonald, R.J. (2007) Enhanced cell death and learning deficits after a mini-stroke in aged hippocampus. Neurobiol. Aging, In press doi : Pennypacker, K.R. (2005) Temporary focal ischemia in the mouse: technical aspects and patterns of Fluoro-Jade evident neurodegeneration. Brain Res., 1042, 29 36.
16. Farr, S.A., Banks, W.A., Uezu, K., Sano, A., Gaskin, F.S. Morley, J.E. (2003) Antibody to beta-amyloid protein increases acetylcholine in the hippocampus of 12 month SAMP8 male mice. Life Sci., 73, 555 562.
17. Fein, G., Di-Sciafani, V., Tanabe, J., Cardenas, V., Weiner, M.W., Jagust, W.J., Reed, B.R., Norman, D., Schuff, N., Kusdra, L., Greenfield, T. Chui, H. (2000) Hippocampal and cortical atrophy predict dementia in subcortical ischemic vascular disease. Neurology, 55, 1626 1635.
18. Finch, T.E. Tanzi, R.E. (1997) Genetics of aging. Science, 278, 407 411.
19. Fujikawa, T., Yanai, I. Yamawaki, S. (1997) Psychosocial stressors in patients with major depression and silent cerebral infarction. Stroke, 28, 1123 1125.
20. Gainotti, G., Acciarri, A., Bizzarro, A., Marra, C., Masullo, C., Misciagna, S., Taraglione, T., Valenza, A. Colosimo, C. (2004) The role of brain infarcts and hippocampal atrophy in subcortical ischemic vascular dementia. Neurol. Sci., 25, 192 197.
21. Goedert, M. (1996) Tau protein and the neurofibrillary pathology of Alzheimer's disease. Ann. N Y Acad. Sci., 777, 121 131.
22. Grau-Olivares, M., Bartres-Faz, D., Arboix, A., Soliva, J.C., Rovira, M., Targa, C. Junque, C. (2007) Mild cognitive impairment after lacunar infarction: voxel-based morphometry and neuropsychological assessment. Cerebrovasc. Dis., 23, 353 361.
23. Growdon, J.H. (1995) Advances in the diagnosis of Alzheimer's disease. In Izbal, K., Mortimer, J.A., Winblad, B. Wisniewski, H.M. (Eds), Research Advances in Alzheimer's Disease and Related Disorders. John Wiley, Chichester, pp. 139 153.
24. Herderschee, D., Hijdra, A., Algra, A., Kappelle, L.J., Koudstaal, P.J. van Gijn, J. (1994) Silent infarction on a second CT scan in 91 patients without manifest stroke in the Dutch TIA trial. Clin. Neurol. Neurosurg., 96, 219 221.
25. Hirano, A. Zimmerman, H.M. (1962) Alzheimer's neurofibrillary changes: a topographic study. Arch. Neurol., 7, 227 233.
26. Hoane, M.R., Wolyniak, J.G. Akstulewicz, S.L. (2005) Administration of riboflavin improves behavioural outcome and reduces edema formation and glial fibrillary acidic protein expression after traumatic brain injury. J. Neurotrauma, 22, 1112 1122.
27. Honkaniemi, J., Massa, S.M., Breckinridge, M. Sharp, F.R. (1996) Global ischemia induces apoptosis-associated genes in hippocampus. Brain Res. Mol. Brain Res., 42, 79 88.
28. Jorgensen, H.S., Nakayama, H., Raaschou, H.O., Gam, J. Olsen, T.S. (1994) Silent infarction in acute stroke patients. Prevalence, localization, risk factors, and clinical significance: the Copenhagen Stroke Study. Stroke, 25, 97 104.
29. Joseph, J., Shukitt-Hale, B., Denisova, N.A., Martin, A., Perry, G. Smith, M.A. (2001) Copernicus revisited: amyloid beta in Alzheimer's disease. Neurobiol. Aging, 22, 131 146.
30. Karhunen, H., Pitkanen, A., Virtanen, T., Gureviciene, I., Pussinen, R., Ylinen, A., Sivenius, J., Nissinen, J. Jolkkonen, J. (2003) Long-term functional consequences of transient occlusion of the middle cerebral artery in rats: a 1 year follow-up of the development of epileptogenesis and memory impairment in relation to sensorimotor deficits. Epilepsy Res., 54, 1 10.
31. Koide, T., Wieloch, T.W. Siesjo, B.K. (1986) Chronic dexamethasone pretreatment aggravates ischemic neuronal necrosis. J. Cereb. Blood Flow Metab., 6, 395 404.
32. Korf, E.S.C., White, L.R., Scheltens, P. Launer, L.J. (2004) Midlife blood pressure and the risk of hippocampal atrophy. Hypertension, 44, 29 34.
33. Liu, C.Z., Yu, J.C., Zhang, X.Z., Fu, W.W., Wang, T. Han, J.X. (2006) Acupuncture prevents cognitive deficits and oxidative stress in cerebral multi-infarction rats. Neurosci. Lett., 393, 45 50.
34. Lupien, S., Gaudreau, S., Tchiteya, B.M., Maheu, F., Sharma, S., Nair, N.P.V., Hauger, R.L. Meaney, M.J. (1997) Stress-induced declarative memory impairments in healthy elderly subjects: Relationships with cortisol reactivity. J. Clin. Endocrin Metabolism, 82, 2070 2075.
35. Lupien, S.J., de Leon, M., de Santi, S., Convit, A., Tarshish, C., Nair, N.P.V., Thakur, M., McEwen, B.S., Hauger, R.L. Meaney, M.J. (1998) Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neurosci., 1, 69 73.
36. Madrigal, J.L.M., Caso, J.R., de Cristobal, J., Cardenas, A., Leza, J.C., Lizasoain, I., Lorenzo, P. Moro, M.A. (2003) Effect of subacute and chronic immobilization stress on the outcome of permanent focal cerebral ischemia in rats. Brain Res., 979, 137 145.
37. McDonald, R.J. (2002) Multiple combinations of co-factors produce variants of age-related cognitive decline: a theory. Can. J. Exp. Psychol., 56, 221 239.
38. McDonald, R.J., Hong, N.S., Craig, L.A., Holahan, M.R., Louis, M. Muller, R.U. (2005) NMDA-receptor blockade by CPP impairs post-training consolidation of a rapidly acquired spatial representation in rat hippocampus. Eur. J. Neurosci., 22, 1201 1213.
39. McDonald, R.J., Hong, N.S. Devan, B.D. (2004) The challenges of understanding mammalian cognition and memory-based behaviours: an interacting learning and memory systems approach. Neurosci. Biobehav. Rev., 28, 719 746.
40. McIntosh, L.J., Cortopassi, K.M. Sapolsky, R.M. (1998) Glucocorticoids may alter antioxidant enzyme capacity in the brain: kainic acid studies. Brain Res., 791, 215 222.
41. McIntosh, L.J. Sapolsky, R.M. (1996) Glucocorticoids may enhance oxygen radical-mediated neurotoxicity. Neurotoxicology, 17, 873 882.
42. Miyakawa, T., Kimura, T., Hirata, S., Fujise, N., Ono, T., Ishizuka, K. Nakabayashi, J. (2000) Role of blood vessels in producing pathological changes in the brain with Alzheimer's disease. Ann. N Y Acad. Sci., 903, 46 54.
43. Morris, R.G.M. (1981) Spatial localization does not require the presence of local cues. Learn. Motivat., 12, 239 260.
44. Morris, R.G.M., Garrud, P., Rawlins, J.N.P. O'Keefe, J. (1982) Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681 683.
45. Moser, M.B., Moser, E.I., Forrest, E., Andersen, P. Morris, R.G. (1995) Spatial learning with a mini-slab in the dorsal hippocampus. Proc. Natl Acad. Sci. USA, 92, 9697 9701.
46. Paxinos, G. Watson, C. (1998) The Rat Brain in Stereotaxic. Coordinates, 4th edn. Academic Press, Toronto.
47. Robinson, R.G., Starr, L.B., Lipsey, J.R., Rao, K. Price, T.R. (1984) A two-year longitudinal study of post-stroke mood disorders: dynamic changes in associated variables over the first six months of follow-up. Stroke, 15, 510 517.
48. Ryan, C.L., Doucette, T.A., Gill, D.A., Langdon, K.D., Liu, Y., Perry, M.A. Tasker, R.A. (2006) An improved post-operative care protocol allows detection of long-term functional deficits following MCAO surgery in rats. J. Neurosci. Meth., January 16 [Epub ahead of print].
49. Sapolsky, R.M. (2001) Cellular defenses against excitotoxic insults. J. Neurochem., 76, 1601 1611.
50. Sapolsky, R.M. Pulsinelli, W.A. (1985) Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications. Science, 229, 1397 1400.
51. Schmued, L.C. Hopkins, K.J. (2000) Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res., 874, 123 130.
52. Schneider, J.A., Arvanitakis, Z., Bang, W. Bennett, D.A. (2007) Mixed brain pathologies account for most dementia cases in community-dwelling older persons. Neurol, June 13 [Epub ahead of print].
53. Shapira, S., Sapir, M., Wengier, A., Grauer, E. Kadar, T. (2002) Aging has a complex effect on a rat model of ischemic stroke. Brain Res., 925, 148 158.
54. Shi, J., Yang, S.H., Stubley, L., Day, A.L. Simpkins, J.W. (2000) Hypoperfusion induces overexpression of a β-amyloid precursdor protein mRNA in a focal ischemic rodent model. Brain Res., 853, 1 4.
55. Snowdon, D.A., Greiner, L.H., Mortimer, J.A., Riley, K.P., Greiner, P.A. Markesbery, W.R. (1997) Brain infarction and the clinical expression of Alzheimer's disease. The nun study. J. Am. Med. Assoc., 277, 813 817.
56. Sugo, N., Hurn, P.D., Morahan, B., Hattori, K., Traystman, R.J. Devries, A.C. (2002) Social stress exacerbates focal cerebral ischemia in mice. Stroke, 33, 1660 1664.
57. Sutherland, R.J., Kolb, B. Whishaw, I.Q. (1982) Definitive disruption by hippocampal and medial frontal cortical damage in the rat. Neurosci. Lett., 31, 271 276.
58. Sutherland, R.J., McDonald, R.J. Savage, D.D. (2000) Prenatal exposure to moderate levels of ethanol can have long-lasting effects on learning and memory in adult offspring. Psychobiology., 28, 532 539.
59. Sutherland, R.J. Rudy, J.W. (1989) Configural association theory: the role of the hippocampal formation in learning, memory, and amnesia. Psychobiology, 17, 129 144.
60. Sutherland, R.J., Whishaw, I.Q. Kolb, B. (1983) A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat. Behav. Brain Res., 7, 133 153.
61. Taraszewska, A., Zelman, I.B., Ogonowska, W. Chrzanowska, H. (2002) The pattern of irreversible brain changes after cardiac arrest in humans. Folia Neuropathol, 40, 133 141.
62. Terry, R.D., Masliah, E. Hansen, L.A. (1994) Structural basis of the cognitive alterations in Alzheimer's disease. In Terry, R.D., Katzman, R. Bick, K.I. (Eds), Alzheimer's Disease. Raven Press, New York.
63. Uehara, T., Tabuchi, M. Mori, E. (1999) Risk factors for silent cerebral infarcts in subcortical white matter and basal ganglia. Stroke, 30, 378 382.
64. Waldstein, S.R., Siegel, E.L., Lefkowitz, D., Maier, K.J., Pelletier-Brown, J.R., Obuchowski, A.M. Katzel, L.I. (2004) Stress-induced blood pressure reactivity and silent cerebrovascular disease. Stroke, 35, 1294 1298.
65. Wisniewski, H.M., Terry, R.D. Hirano, A. (1970) Neurofibrillary pathology. J. Neuropathol. Exp. Neurol., 29, 163 176.
66. Yager, J.Y., Shuaib, A. Thornhill, J. (1996) The effect of age on susceptibility to brain damage in a model of global hemispheric hypoxia-ischemia. Brain Res. Dev. Brain Res., 93, 143 154.
67. Yager, J.Y., Wright, S., Armstrong, E.A., Jahraus, C.M. Saucier, D.M. (2006) The influence of aging on recovery following ischemic brain damage. Behav. Brain Res., 173, 171 180.