Selective Neuronal Vulnerability in the Hippocampus: Relationship to Neurological Diseases and Mechanisms for Differential Sensitivity of Neurons to Stress

The Clinical Neurobiology of the Hippocampus: An Integrative view

Volumn , Issue , 2012, Pages

  Michaelis, Elias K ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Ageing; CA1 CA3 neurons; Calcium regulation; Energy metabolism; Genomic analyses; Glutamate transmission; Ischaemia reperfusion; Neurodegenerative diseases; Oxidative stress

Indexed keywords

EID: 84920417155     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1093/acprof:oso/9780199592388.003.0004     Document Type: Chapter

References (192)

1. Aoki, M., Volkmann, I., Tjernberg, L. O., Winblad, B., and Bogdanovic, N. (2008). Amyloid beta-peptide levels in laser capture microdissected cornu ammonis 1 pyramidal neurons of Alzheimer's brain. Neuroreport, 19, 1085-9.
2. Arnold, S. E., Franz, B. R., Gur, R. C., et al. (1995). Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions. Am J Psychiatry, 152, 738-48.
3. Balazs, R., Jorgensen, O. S., and Hack, N. (1988). N-methyl-D-aspartate promotes the survival of cerebellar granule cells in culture. Neuroscience, 27, 437-51.
4. Ball, M. J. (1979). Topography of Pick inclusion bodies in hippocampi of demented patients. A quantitative study. J Neuropathol Exp Neurol, 38, 614-20.
5. Bao, X., Pal, R., Hascup, K. N., et al. (2009). Transgenic expression of Glud1 (glutamate dehydrogenase 1) in neurons: in vivo model of enhanced glutamate release, altered synaptic plasticity, and selective neuronal vulnerability. J Neurosci, 29, 13929-44.
6. Barnes, C. A. (1979). Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol, 93, 74-104.
7. Barnes, C. A., and McNaughton, B. L. (1980). Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. J Physiol, 309, 473-85.
8. Barnes, C. A., and McNaughton, B. L. (1985). An age comparison of the rates of acquisition and forgetting of spatial information in relation to long-term enhancement of hippocampal synapses. Behav Neurosci, 99, 1040-8.
9. Barnes, C. A., Suster, M. S., Shen, J., and McNaughton, B. L. (1997). Multistability of cognitive maps in the hippocampus of old rats. Nature, 388, 272-5.
10. Barnes, J., Bartlett, J. W., van de Pol, L. A., et al. (2009). A meta-analysis of hippocampal atrophy rates in Alzheimer's disease. Neurobiol Aging, 30, 1711-23.
11. Behrens, M. I., Koh, J. Y., Muller, M. C., and Choi, D. W. (1996). NADPH diaphorase-containing striatal or cortical neurons are resistant to apoptosis. Neurobiol Dis, 3, 72-5.
12. Benes, F. M. (2007). Searching for unique endophenotypes for schizophrenia and bipolar disorder within neural circuits and their molecular regulatory mechanisms. Schizophr Bull, 33, 932-6.
13. Benes, F. M., Sorensen, I., and Bird, E. D. (1991). Reduced neuronal size in posterior hippocampus of schizophrenic patients. Schizophr Bull, 17, 597-608.
14. Benes, F. M., Kwok, E. W., Vincent, S. L., and Todtenkopf, M. S. (1998). A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol Psychiatry, 44, 88-97.
15. Benes, F. M., Lim, B., Matzilevich, D., Walsh, J. P., Subburaju, S., and Minns, M. (2007). Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc Natl Acad Sci U S A, 104, 10164-9.
16. Bensch, K. G., Mott, J. L., Chang, S. W., et al. (2009). Selective mtDNA mutation accumulation results in beta-cell apoptosis and diabetes development. Am J Physiol Endocrinol Metab, 296, E672-80.
17. Bernaudin, M., Nouvelot, A., MacKenzie, E. T., and Petit, E. (1998). Selective neuronal vulnerability and specific glial reactions in hippocampal and neocortical organotypic cultures submitted to ischemia. Exp Neurol, 150, 30-9.
18. Blümcke, I., Kistner, I., Clusmann, H., et al. (2009). Towards a clinicopathological classification of granule cell dispersion in human mesial temporal lobe epilepsies. Acta Neuropathol, 117, 535-44.
19. Braak, H., and Braak, E. (1991). Neuropathological stageing of Alzheimerrelated changes. Acta Neuropathol, 82, 239-59.
20. Braak, H., Del Tredici, K., Rub, U., de Vos, R. A., Jansen Steur, E. N., and Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging, 24, 197-211.
21. Braak, H., Ghebremedhin, E., Rub, U., Bratzke, H., and Del Tredici, K. (2004). Stages in the development of Parkinson's disease-related pathology. Cell Tissue Res, 318, 121-34.
22. Buchan, A. M., and Pulsinelli, W. A. (1990). Septo-hippocampal deafferentation protects CA1 neurons against ischemic injury. Brain Res, 512, 7-14.
23. Cadenas, E., and Davies, K. J. (2000). Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med, 29, 222-30.
24. Cajal, S. R. Y. (1894). Les nouvelles idées sur la structure du système nerveux chez l'homme et chez les vertébrés. Paris: C. Reinwald.
25. Carri, M. T., Ferri, A., Cozzolino, M., Calabrese, L., and Rotilio, G. (2003). Neurodegeneration in amyotrophic lateral sclerosis: the role of oxidative stress and altered homeostasis of metals. Brain Res Bull, 61, 365-74.
26. Castellani, R., Hirai, K., Aliev, G., et al. (2002). Role of mitochondrial dysfunction in Alzheimer's disease. J Neurosci Res, 70, 357-60.
27. Cataldo, A. M., Petanceska, S., Terio, N. B., et al. (2004). Abeta localization in abnormal endosomes: association with earliest Abeta elevations in AD and Down syndrome. Neurobiol Aging, 25, 1263-72.
28. Choi, D. W. (1992). Excitotoxic cell death. J Neurobiol, 23, 1261-76.
29. Choi, D. W., and Rothman, S. M. (1990). The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci, 13, 171-82.
30. Constantinidis, J., Richard, J., and Tissot, R. (1974). Pick's disease. Histological and clinical correlations. Eur Neurol, 11, 208-17.
31. Cotman, C. W., Monaghan, D. T., and Ganong, A. H. (1988). Excitatory amino acid neurotransmission: NMDA receptors and Hebb-type synaptic plasticity. Annu Rev Neurosci, 11, 61-80.
32. Cottrell, D. A., Blakely, E. L., Johnson, M. A., Ince, P. G., and Turnbull, D. M. (2001). Mitochondrial enzyme-deficient hippocampal neurons and choroidal cells in AD. Neurology, 57, 260-4.
33. Crook, T., Bartus, R. T., Ferris, S., Whitehouse, P., Cohen, G., and Gershon, S. (1986). Age-associated memory impairment: Proposed diagnostic criteria and measures of clinical change-Report of a National Institue of Mental Health Work Group. Dev Neuropsychiatry, 2, 261-76.
34. Damier, P., Hirsch, E. C., Agid, Y., and Graybiel, A. M. (1999). The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain, 122(Pt 8), 1437-48.
35. Dauer, W., and Przedborski, S. (2003). Parkinson's disease: mechanisms and models. Neuron, 39, 889-909.
36. Dawson, V. L., and Dawson, T. M. (1998). Nitric oxide in neurodegeneration. Prog Brain Res, 118, 215-29.
37. Dawson, V. L., Dawson, T. M., London, E. D., Bredt, D. S., and Snyder, S. H. (1991). Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci U S A, 88, 6368-71.
38. De Lacoste, M. C., and White, C. L., 3rd (1993). The role of cortical connectivity in Alzheimer's disease pathogenesis: a review and model system. Neurobiol Aging, 14, 1-16.
39. DeGracia, D. J., Rudolph, J., Roberts, G. G., Rafols, J. A., and Wang, J. (2007). Convergence of stress granules and protein aggregates in hippocampal cornu ammonis 1 at later reperfusion following global brain ischemia. Neuroscience, 146, 562-72.
40. Diemer, N.H., and Siemkowicz, E. (1981). Regional neurone damage after cerebral ischaemia in the normo-and hypoglycaemic rat. Neuropathol Appl Neurobiol, 7, 217-27.
41. Du, H., Guo, L., Fang F., et al. (2008). Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat Med, 14, 1097-105.
42. Duan, H., Wearne, S. L., Rocher, A. B., Macedo, A., Morrison, J. H., and Hof, P. R. (2003). Age-related dendritic and spine changes in corticocortically projecting neurons in macaque monkeys. Cereb Cortex, 13, 950-61.
43. Earle, K. M., Baldwin, M., and Penfield, W. (1953). Incisural sclerosis and temporal lobe seizures produced by hippocampal herniation at birth. AMA Arch Neurol Psychiatry, 69, 27-42.
44. Esposito, F., Ammendola, R., Faraonio, R., Russo, T., and Cimino, F. (2004). Redox control of signal transduction, gene expression and cellular senescence. Neurochem Res, 29, 617-28.
45. Evans, S. J., Choudary, P. V., Vawter, M. P., et al. (2003). DNA microarray analysis of functionally discrete human brain regions reveals divergent transcriptional profiles. Neurobiol Dis, 14, 240-50.
46. Fahn, S., and Cohen, G. (1992). The oxidant stress hypothesis in Parkinson's disease: evidence supporting it. Ann Neurol, 32, 804-12.
47. Falconer, M. A. (1974). Mesial temporal (Ammon's horn) sclerosis as a common cause of epilepsy. Aetiology, treatment, and prevention. Lancet, 2, 767-70.
48. Falconer, M. A., and Taylor, D. C. (1968). Surgical treatment of drug-resistant epilepsy due to mesial temporal sclerosis. Etiology and significance. Arch Neurol, 19, 353-61.
49. Ferrante, R. J., Kowall, N. W., Beal, M. F., Richardson, E. P., Jr., Bird, E. D., and Martin, J. B. (1985). Selective sparing of a class of striatal neurons in Huntington's disease. Science, 230, 561-3.
50. Ferriero, D. M., Arcavi, L. J., Sagar, S. M., McIntosh, T. K., and Simon, R. P. (1988). Selective sparing of NADPH-diaphorase neurons in neonatal hypoxiaischemia. Ann Neurol, 24, 670-6.
51. Finkel, T. (2003). Oxidant signals and oxidative stress. Curr Opin Cell Biol, 15, 247-54.
52. Friberg, H., Wieloch, T., and Castilho, R. F. (2002). Mitochondrial oxidative stress after global brain ischemia in rats. Neurosci Lett, 334, 111-14.
53. Fryd Johansen, F., Balslev Jorgensen, M., and Diemer, N. H. (1983). Resistance of hippocampal CA-1 interneurons to 20 min of transient cerebral ischemia in the rat. Acta Neuropathol, 61, 135-40.
54. Garthwaite, J. (1991). Glutamate, nitric oxide and cell-cell signalling in the nervous system. Trends Neurosci, 14, 60-7.
55. Gasic, G. P., and Hollmann, M. (1992). Molecular neurobiology of glutamate receptors. Annu Rev Physiol, 54, 507-36.
56. Gibson, G. E., Sheu, K. F., and Blass, J. P. (1998). Abnormalities of mitochondrial enzymes in Alzheimer disease. J Neural Transm, 105, 855-70.
57. Ginsberg, S. D., and Che, S. (2005). Expression profile analysis within the human hippocampus: comparison of CA1 and CA3 pyramidal neurons. J Comp Neurol, 487, 107-18.
58. Ginsberg, S. D., Alldred, M. J., Counts, S. E., et al. (2010). Microarray analysis of hippocampal CA1 neurons implicates early endosomal dysfunction during Alzheimer's disease progression. Biol Psychiatry, 68, 885-93.
59. Glazner, G. W., and Mattson, M. P. (2000). Differential effects of BDNF, ADNF9, and TNF[alpha] on levels of NMDA receptor subunits, calcium homeostasis, and neuronal vulnerability to excitotoxicity. Exp Neurol, 161, 442-52.
60. Grazina, M., Pratas, J., Silva, F., Oliveira, S., Santana, I., and Oliveira, C. (2006). Genetic basis of Alzheimer's dementia: role of mtDNA mutations. Genes Brain Behav, 5(Suppl 2), 92-107.
61. Greenwood, S. M., Mizielinska, S. M., Frenguelli, B. G., Harvey, J., and Connolly, C. N. (2007a). Mitochondrial dysfunction and dendritic beading during neuronal toxicity. J Biol Chem, 282, 26235-44.
62. Greenwood, S. M., Mizielinska, S. M., Frenguelli, B. G., Harvey, J., and Connolly, C. N. (2007b). Mitochondrial dysfunction and dendritic beading during neuronal toxicity. J Biol Chem, 282, 26235-44.
63. Halliwell, B., Gutteridge, J. M., and Cross, C. E (1992). Free radicals, antioxidants, and human disease: where are we now? J Lab Clin Med, 119, 598-620.
64. Harman, D. (1956). Aging: a theory based on free radical and radiation chemistry. J Gerontol, 11, 298-300.
65. Hascup, K. N., Bao, X., Hascup, E. R., et al. (2011). Differential levels of glutamate dehydrogenase 1 (GLUD1) in BALB/c and C57BL/6 mice and the effects of over-expression of Glud1 gene on glutamate release in striatum. ASN Neuro, 3(2), e00057.
66. Hirsch, E., Graybiel, A. M., and Agid, Y. A. (1988). Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature, 334, 345-8.
67. Hof, P. R., Cox, K., and Morrison, J. H. (1990). Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: I. Superior frontal and inferior temporal cortex. J Comp Neurol, 301, 44-54.
68. Horn, M., and Schlote, W. (1992). Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol, 85, 79-87.
69. Hoskison, M. M., and Shuttleworth, C. W. (2006). Microtubule disruption, not calpain-dependent loss of MAP2, contributes to enduring NMDA-induced dendritic dysfunction in acute hippocampal slices. Exp Neurol, 202, 302-12.
70. Hoskison, M. M., Yanagawa, Y., Obata, K., and Shuttleworth, C. W. (2007). Calcium-dependent NMDA-induced dendritic injury and MAP2 loss in acute hippocampal slices. Neuroscience, 145, 66-79.
71. Houser, C. R., Harris, A. B., and Vaughn, J. E. (1986). Time course of the reduction of GABA terminals in a model of focal epilepsy: a glutamic acid decarboxylase immunocytochemical study. Brain Res, 383, 129-45.
72. Hyman, B. T., Van Horsen, G. W., Damasio, A. R., and Barnes, C. L. (1984). Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science, 225, 1168-70.
73. Hyman, B. T., Marzloff, K., Wenniger, J. J., Dawson, T. M., Bredt, D. S., and Snyder, S. H. (1992). Relative sparing of nitric oxide synthase-containing neurons in the hippocampal formation in Alzheimer's disease. Ann Neurol, 32, 818-20.
74. Ince, P. G., Lowe, J., and Shaw, P. J. (1998). Amyotrophic lateral sclerosis:current issues in classification, pathogenesis and molecular pathology. Neuropathol Appl Neurobiol, 24, 104-17.
75. Jack, C. R., Jr., Petersen, R. C., Xu, Y., et al. (2000). Rates of hippocampal atrophy correlate with change in clinical status in aging and AD. Neurology, 55, 484-9.
76. Jenner, P. (2003). Oxidative stress in Parkinson's disease. Ann Neurol, 53(Suppl 3), S26-36; discussion S36-8.
77. Jorgensen, M. B., Finsen, B. R., Jensen, M. B., Castellano, B., Diemer, N. H., and Zimmer, J. (1993). Microglial and astroglial reactions to ischemic and kainic acid-induced lesions of the adult rat hippocampus. Exp Neurol, 120, 70-88.
78. Kamsler, A., and Segal, M. (2003). Paradoxical actions of hydrogen peroxide on long-term potentiation in transgenic superoxide dismutase-1 mice. J Neurosci, 23, 10359-67.
79. Khaitovich, P., Muetzel, B., She, X., et al. (2004). Regional patterns of gene expression in human and chimpanzee brains. Genome Res, 14, 1462-73.
80. Kintner, D. B., Chen, X., Currie, J., et al. (2010). Excessive Na+/H+ exchange in disruption of dendritic Na+ and Ca2+ homeostasis and mitochondrial dysfunction following in vitro ischemia. J Biol Chem, 285, 35155-68.
81. Kirino, T. (1982). Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res, 239, 57-69.
82. Kirino, T., Tamura, A., and Sano, K. (1984). Delayed neuronal death in the rat hippocampus following transient forebrain ischemia. Acta Neuropathol, 64, 139-47.
83. Kitao, Y., Ozawa, K., Miyazaki, M., et al. (2001). Expression of the endoplasmic reticulum molecular chaperone (ORP150) rescues hippocampal neurons from glutamate toxicity. J Clin Invest, 108, 1439-50.
84. Koh, J. Y., Peters, S., and Choi, D. W. (1986). Neurons containing NADPHdiaphorase are selectively resistant to quinolinate toxicity. Science, 234, 73-6.
85. Koh, J. Y., Suh, S. W., Gwag, B. J., He, Y. Y., Hsu, C. Y., and Choi, D. W. (1996). The role of zinc in selective neuronal death after transient global cerebral ischemia. Science, 272, 1013-16.
86. Kujoth, G. C., Hiona, A., Pugh, T. D., et al. (2005). Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science, 309, 481-4.
87. La Joie, R., Fouquet, M., Mezenge, F., et al. (2010). Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence. Neuroimage, 53, 506-14.
88. Lein, E. S., Zhao, X., and Gage, F. H. (2004). Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J Neurosci, 24, 3879-89.
89. Lenaz, G. (2001). The mitochondrial production of reactive oxygen species:mechanisms and implications in human pathology. IUBMB Life, 52, 159-64.
90. Li, S., Mallory, M., Alford, M., Tanaka, S., and Masliah, E. (1997). Glutamate transporter alterations in Alzheimer disease are possibly associated with abnormal APP expression. J Neuropathol Exp Neurol, 56, 901-11.
91. Liang, W. S., Dunckley, T., Beach, T. G., et al. (2007). Gene expression profiles in anatomically and functionally distinct regions of the normal aged human brain. Physiol Genomics, 28, 311-22.
92. Lipton, S. A., Sucher, N. J., Kaiser, P. K., and Dreyer, E. B. (1991). Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron, 7, 111-18.
93. Lokkegaard, A., Nyengaard, J. R., and West, M. J. (2001). Stereological estimates of number and length of capillaries in subdivisions of the human hippocampal region. Hippocampus, 11, 726-40.
94. Lu, T., Pan, Y., Kao, S. Y., et al. (2004). Gene regulation and DNA damage in the ageing human brain. Nature, 429, 883-91.
95. Madsen, P. L., Hasselbalch, S. G., Hagemann, L. P., et al. (1995). Persistent resetting of the cerebral oxygen/glucose uptake ratio by brain activation:evidence obtained with the Kety-Schmidt technique. J Cereb Blood Flow Metab, 15, 485-91.
96. Masliah, E., Mallory, M., Hansen, L., DeTeresa, R., and Terry, R. D. (1993). Quantitative synaptic alterations in the human neocortex during normal aging. Neurology, 43, 192-7.
97. Matsugami, T. R., Tanemura, K., Mieda, M., et al. (2006). From the Cover:Indispensability of the glutamate transporters GLAST and GLT1 to brain development. Proc Natl Acad Sci U S A, 103, 12161-6.
98. Mattson, M. P., and Magnus, T. (2006). Ageing and neuronal vulnerability. Nat Rev Neurosci, 7, 278-94.
99. McCormack, J. G., Halestrap, A. P., and Denton, R. M. (1990). Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev, 70, 391-425.
100. Mecocci, P., MacGarvey, U., and Beal, M. F. (1994). Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann Neurol, 36, 747-51.
101. Meencke, H. J. (2009). Clinical neuropathology of the epilepsies in the 100 years of the ILAE (1909-2009). Epilepsia, 50(Suppl 3), 8-16.
102. Meldrum, B. S., Vigouroux, R. A., and Brierley, J. B. (1973a). Systemic factors and epileptic brain damage. Prolonged seizures in paralyzed, artificially ventilated baboons. Arch Neurol, 29, 82-7.
103. Meldrum, B. S., Vigouroux, R. A., Rage, P., and Brierley, J. B. (1973b). Hippocampal lesions produced by prolonged seizures in paralyzed artificially ventilated baboons. Experientia, 29, 561-3.
104. Mello, L. E., Cavalheiro, E. A., Tan, A. M., et al. (1993). Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia, 34, 985-95.
105. Meyer, A. (1936). The selective regional vulnerability of the brain and its relation to psychiatric problems. Proc R Soc Med, 29, 1175-81.
106. Michaelis, E. K. (1998). Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging. Prog Neurobiol, 54, 369-415.
107. Michaelis, E. K., Wang, X., Pal, R., et al. (2011). Neuronal Glud1 (glutamate dehydrogenase 1) over-expressing mice: Increased glutamate formation and synaptic release, loss of synaptic activity, and adaptive changes in genomic expression. Neurochem Int, 59, 473-81.
108. Miclescu, A., Sharma, H. S., Martijn, C., and Wiklund, L. (2010). Methylene blue protects the cortical blood-brain barrier against ischemia/reperfusioninduced disruptions. Crit Care Med, 38, 2199-206.
109. Morrison, J. H., and Hof, P. R. (1997). Life and death of neurons in the aging brain. Science, 278, 412-19.
110. Mueller, S. G., Stables, L., Du, A. T., et al. (2007). Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T. Neurobiol Aging, 28, 719-26.
111. Nelson, M. D., Saykin, A. J., Flashman, L. A., and Riordan, H.J. (1998). Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging: a meta-analytic study. Arch Gen Psychiatry, 55, 433-40.
112. Newrzella, D., Pahlavan, P. S., Kruger, C., et al. (2007). The functional genome of CA1 and CA3 neurons under native conditions and in response to ischemia. BMC Genomics, 8, 370.
113. Nickell, J., Pomerleau, F., Allen, J., and Gerhardt, G. A. (2005). Age-related changes in the dynamics of potassium-evoked L-glutamate release in the striatum of Fischer 344 rats. J Neural Transm, 112, 87-96.
114. Olsson, T., Wieloch, T., and Smith, M. L. (2003). Brain damage in a mouse model of global cerebral ischemia. Effect of NMDA receptor blockade. Brain Res, 982, 260-9.
115. Parker, W. D., Jr., Filley, C. M., and Parks, J. K. (1990). Cytochrome oxidase deficiency in Alzheimer's disease. Neurology, 40, 1302-3.
116. Parker, W. D., Jr., Mahr, N. J., et al. (1994a). Reduced platelet cytochrome c oxidase activity in Alzheimer's disease. Neurology, 44, 1086-90.
117. Parker, W. D., Jr., Parks, J., Filley, C. M., and Kleinschmidt-DeMasters, B. K. (1994b). Electron transport chain defects in Alzheimer's disease brain. Neurology, 44, 1090-6.
118. Peng, P. L., Zhong, X., Tu, W., et al. (2006). ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron, 49, 719-33.
119. Petersen, R. C., Jack, C. R., Jr., Xu, Y. C., et al. (2000). Memory and MRI-based hippocampal volumes in aging and AD. Neurology, 54, 581-7.
120. Pulsinelli, W. A. (1985). Selective neuronal vulnerability: morphological and molecular characteristics. Prog Brain Res, 63, 29-37.
121. Pulsinelli, W. A., Brierley, J. B., and Plum, F. (1982). Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol, 11, 491-8.
122. Rajah, M. N., Kromas, M., Han, J. E., and Pruessner, J. C. (2010). Group differences in anterior hippocampal volume and in the retrieval of spatial and temporal context memory in healthy young versus older adults. Neuropsychologia, 48, 4020-30.
123. Reddy, P. H., and Beal, M. F. (2008). Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer's disease. Trends Mol Med, 14, 45-53.
124. Reddy, P. H., Williams, M., Charles, V., et al. (1998). Behavioural abnormalities and selective neuronal loss in HD transgenic mice expressing mutated full-length HD cDNA. Nat Genet, 20, 198-202.
125. Reddy, P. H., Charles, V., Williams, M., Miller, G., Whetsell, W. O., Jr., and Tagle, D. A. (1999). Transgenic mice expressing mutated full-length HD cDNA: a paradigm for locomotor changes and selective neuronal loss in Huntington's disease. Philos Trans R Soc Lond B Biol Sci, 354, 1035-45.
126. Ribak, C. E., Hunt, C. A., Bakay, R. A., and Oertel, W. H. (1986). A decrease in the number of GABAergic somata is associated with the preferential loss of GABAergic terminals at epileptic foci. Brain Res, 363, 78-90.
127. Rickhag, M., Wieloch, T., Gido, G., et al. (2006). Comprehensive regional and temporal gene expression profiling of the rat brain during the first 24 h after experimental stroke identifies dynamic ischemia-induced gene expression patterns, and reveals a biphasic activation of genes in surviving tissue. J Neurochem, 96, 14-29.
128. Rival, T., Soustelle, L., Strambi, C., Besson, M. T., Iche, M., and Birman, S. (2004). Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in the Drosophila brain. Curr Biol, 14, 599-605.
129. Rizzuto, R., Bernardi, P., and Pozzan, T. (2000). Mitochondria as all-round players of the calcium game. J Physiol, 529(Pt 1), 37-47.
130. Rosenzweig, E. S., Rao, G., McNaughton, B. L., and Barnes, C. A. (1997). Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus, 7, 549-58.
131. Rothstein, J. D., Tsai, G., Kuncl, R. W., et al. (1990). Abnormal excitatory amino acid metabolism in amyotrophic lateral sclerosis. Ann Neurol, 28, 18-25.
132. Rothstein, J. D., Jin, L., Dykes-Hoberg, M., and Kuncl, R. W. (1993). Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc Natl Acad Sci U S A, 90, 6591-5.
133. Rothstein, J. D., Dykes-Hoberg, M., Pardo, C. A., et al. (1996). Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron, 16, 675-86.
134. Rowland, L. P., and Shneider, N. A. (2001). Amyotrophic lateral sclerosis. N Engl J Med, 344, 1688-700.
135. Sadek, H. A., Szweda, P.A., and Szweda, L. I. (2004). Modulation of mitochondrial complex I activity by reversible Ca2+ and NADH mediated superoxide anion dependent inhibition. Biochemistry, 43, 8494-502.
136. Sagar, H. J., and Oxbury, J. M. (1987). Hippocampal neuron loss in temporal lobe epilepsy: correlation with early childhood convulsions. Ann Neurol, 22, 334-40.
137. Sayre, L. M., Smith, M. A., and Perry, G. (2001). Chemistry and biochemistry of oxidative stress in neurodegenerative disease. Curr Med Chem, 8, 721-38.
138. Scheff, S. W., and Price, D. A. (2003). Synaptic pathology in Alzheimer's disease: a review of ultrastructural studies. Neurobiol Aging, 24, 1029-46.
139. Scheff, S. W., Price, D. A., Schmitt, F. A., and Mufson, E. J. (2006). Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment. Neurobiol Aging, 27, 1372-84.
140. Schmidt-Kastner, R., and Freund, T. F. (1991). Selective vulnerability of the hippocampus in brain ischemia. Neuroscience, 40, 599-636.
141. Scholz, W. (1953). Selective neuronal necrosis and its topistic patterns in hypoxemia and olegemia. J Neuropathol Exp Neurol, 12, 249-61.
142. Scholz, W., and Hager, H. (Eds.) (1956). Epilepsie. Berlin: Springer.
143. Schwarcz, R., and Meldrum, B. (1985). Excitatory aminoacid antagonists provide a therapeutic approach to neurological disorders. Lancet, 2, 140-3.
144. Scott, H. L., Pow, D. V., Tannenberg, A. E., and Dodd, P. R. (2002). Aberrant expression of the glutamate transporter excitatory amino acid transporter 1 (EAAT1) in Alzheimer's disease. J Neurosci, 22, RC206.
145. Sharma, H. S., Miclescu, A., and Wiklund, L. (2011). Cardiac arrest-induced regional blood-brain barrier breakdown, edema formation and brain pathology: a light and electron microscopic study on a new model for neurodegeneration and neuroprotection in porcine brain. J Neural Transm, 118(1), 87-114.
146. Siesjo, B. K. (1988). Mechanisms of ischemic brain damage. Crit Care Med, 16, 954-63.
147. Simic, G., Kostovic, I., Winblad, B., and Bogdanovic, N. (1997). Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J Comp Neurol, 379, 482-94.
148. Smith, D. E., Rapp, P. R., McKay, H. M., Roberts, J. A., and Tuszynski, M. H. (2004). Memory impairment in aged primates is associated with focal death of cortical neurons and atrophy of subcortical neurons. J Neurosci, 24, 4373-81.
149. Spargo, E., Everall, I. P., and Lantos, P. L. (1993). Neuronal loss in the hippocampus in Huntington's disease: a comparison with HIV infection. J Neurol Neurosurg Psychiatry, 56, 487-91.
150. Spielmeyer, W. (1927). Die Pathogenese des epileptisches Krampfes. Histopathologischer Teil. (Pathogenesis of the epileptic seizure. Histopathological part). Ztschr Neurol Psychiat, 109, 501-19.
151. Spielmeyer, W. (1931). The significance of local factors for electivity in central nervous system disease processes. Medicine, 10, 243-56.
152. Squire, L. R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev, 99, 195-231.
153. Squire, L. R., Ojemann, J. G., Miezin, F. M., Petersen, S. E., Videen, T. O., and Raichle, M. E. (1992). Activation of the hippocampus in normal humans: a functional anatomical study of memory. Proc Natl Acad Sci U S A, 89, 1837-41.
154. Stanika, R. I., Winters, C. A., Pivovarova, N. B., and Andrews, S. B. (2010). Differential NMDA receptor-dependent calcium loading and mitochondrial dysfunction in CA1 vs. CA3 hippocampal neurons. Neurobiol Dis, 37, 403-11.
155. Szatkowski, M., and Attwell, D. (1994). Triggering and execution of neuronal death in brain ischaemia: two phases of glutamate release by different mechanisms. Trends Neurosci, 17, 359-65.
156. Tanaka, K., Watase, K., Manabe, T., et al. (1997). Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science, 276, 1699-702.
157. Terry, R. D., and Katzman, R (2001). Life span and synapses: will there be a primary senile dementia? Neurobiol Aging, 22, 347-8; discussion 353-44.
158. Terry, R. D., DeTeresa, R., and Hansen, L. A. (1987). Neocortical cell counts in normal human adult aging. Ann Neurol, 21, 530-9.
159. Thiels, E., Urban, N. N., Gonzalez-Burgos, G. R., et al. (2000). Impairment of long-term potentiation and associative memory in mice that overexpress extracellular superoxide dismutase. J Neurosci, 20, 7631-9.
160. Torres-Munoz, J. E., Van Waveren, C., Keegan, M. G., Bookman, R. J., and Petito, C. K. (2004). Gene expression profiles in microdissected neurons from human hippocampal subregions. Brain Res, Mol Brain Res, 127, 105-14.
161. Turrens, J. F. (1997). Superoxide production by the mitochondrial respiratory chain. Biosci Rep, 17, 3-8.
162. Uttl, B., and Graf, P. (1993). Episodic spatial memory in adulthood. Psychol Aging, 8, 257-73.
163. Vaishnavi, S. N., Vlassenko, A. G., Rundle, M. M., Snyder, A. Z., Mintun, M. A., and Raichle, M. E. (2010). Regional aerobic glycolysis in the human brain. Proc Natl Acad Sci U S A, 107, 17757-62.
164. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T., Mazur, M., and Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol, 39, 44-84.
165. Valtschanoff, J. G., Weinberg, R. J., Kharazia, V. N., Nakane, M., and Schmidt, H. H. (1993a). Neurons in rat hippocampus that synthesize nitric oxide. J Comp Neurol, 331, 111-21.
166. Valtschanoff, J. G., Weinberg, R. J., Kharazia, V. N., Schmidt, H. H., Nakane, M., and Rustioni, A. (1993b). Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA. Neurosci Lett, 157, 157-61.
167. van Muiswinkel, F. L., de Vos, R. A., Bol, J. G., et al. (2004). Expression of NAD(P)H:quinone oxidoreductase in the normal and Parkinsonian substantia nigra. Neurobiol Aging, 25, 1253-62.
168. Vlassenko, A. G., Vaishnavi, S. N., Couture, L., et al. (2010). Spatial correlation between brain aerobic glycolysis and amyloid-beta (Abeta) deposition. Proc Natl Acad Sci U S A, 107, 17763-7.
169. Vogt, C., and Vogt, O. (1937). Sitz und Wesen der Krankheiten im Lichte der topistischen Hirnforschung und des Variierens der Tiere. J Psychol Neurol, 47, 237-457.
170. Vogt, O. (1925). Der Begriff der Pathoklise. J Psychol Neurol, 31, 245-55.
171. Wang, X., and Michaelis, E. K. (2010). Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci, 2, 12.
172. Wang, J., Xiong, S., Xie, C., Markesbery, W. R., and Lovell, M. A. (2005a). Increased oxidative damage in nuclear and mitochondrial DNA in Alzheimer's disease. J Neurochem, 93, 953-62.
173. Wang, X., Pal, R., Chen, X. W., Limpeanchob, N., Kumar, K. N., and Michaelis, E. K. (2005b). High intrinsic oxidative stress may underlie selective vulnerability of the hippocampal CA1 region. Brain Res Mol Brain Res, 140, 120-6.
174. Wang, X., Pal, R., Chen, X. W., Kumar, K. N., Kim, O. J., and Michaelis, E. K. (2007). Genome-wide transcriptome profiling of region-specific vulnerability to oxidative stress in the hippocampus. Genomics, 90, 201-12.
175. Wang, X., Zaidi, A., Pal, R., et al. (2009). Genomic and biochemical approaches in the discovery of mechanisms for selective neuronal vulnerability to oxidative stress. BMC Neurosci, 10, 12.
176. Wang, X., Bao, X., Pal, R., Agbas, A., and Michaelis, E. K. (2010a). Transcriptomic responses in mouse brain exposed to chronic excess of the neurotransmitter glutamate. BMC Genomics, 11, 360.
177. Wang, X., Michaelis, M. L., and Michaelis, E. K. (2010b). Functional genomics of brain aging and alzheimer's disease, focus on selective neuronal vulnerability. Curr Genom, 11, 618-33.
178. Weinberger, D. R. (1999). Cell biology of the hippocampal formation in schizophrenia. Biol Psychiatry, 45, 395-402.
179. Wilde, G. J., Pringle, A. K., Wright, P., and Iannotti, F. (1997). Differential vulnerability of the CA1 and CA3 subfields of the hippocampus to superoxide and hydroxyl radicals in vitro. J Neurochem, 69, 883-6.
180. Winkelmann, E. R., Charcansky, A., Faccioni-Heuser, M. C., Netto, C. A., and Achaval, M. (2006). An ultrastructural analysis of cellular death in the CA1 field in the rat hippocampus after transient forebrain ischemia followed by 2, 4 and 10 days of reperfusion. Anat Embryol (Berl), 211, 423-34.
181. Wisniewski, H. M., and Terry, R. D. (1973). Morphology of the aging brain, human and animal. Prog Brain Res, 40, 167-86.
182. Witter, M. P., Groenewegen, H. J., Lopes da Silva, F. H., and Lohman, A. H. (1989). Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol, 33, 161-253.
183. Wu, K., Aoki, C., Elste, A., Rogalski-Wilk, A. A., and Siekevitz, P. (1997). The synthesis of ATP by glycolytic enzymes in the postsynaptic density and the effect of endogenously generated nitric oxide. Proc Natl Acad Sci U S A, 94, 13273-8.
184. Xu, X., Zhan, M., Duan, W., et al. (2007). Gene expression atlas of the mouse central nervous system: impact and interactions of age, energy intake and gender. Genome Biol, 8, R234.
185. Xu, Y., Jack, C. R., Jr., O'Brien, P. C., et al. (2000). Usefulness of MRI measures of entorhinal cortex versus hippocampus in AD. Neurology, 54, 1760-7.
186. Zeier, Z., Madorsky, I., Xu, Y., Ogle, W. O., Notterpek, L., and Foster, T. C. (2011). Gene expression in the hippocampus: regionally specific effects of aging and caloric restriction. Mech Ageing Dev, 132, 8-19.
187. Zeng, L. H., Ouyang, Y., Gazit, V., et al. (2007). Abnormal glutamate homeostasis and impaired synaptic plasticity and learning in a mouse model of tuberous sclerosis complex. Neurobiol Dis, 28, 184-96.
188. Zhu, X., Raina, A. K., Lee, H. G., Casadesus, G., Smith, M. A., and Perry, G. (2004a). Oxidative stress signalling in Alzheimer's disease. Brain Res, 1000, 32-9.
189. Zhu, X., Smith, M. A., Perry, G., and Aliev, G. (2004b). Mitochondrial failures in Alzheimer's disease. Am J Alzheimers Dis Other Demen, 19, 345-52.
190. Zoia, C., Cogliati, T., Tagliabue, E., et al. (2004). Glutamate transporters in platelets: EAAT1 decrease in aging and in Alzheimer's disease. Neurobiol Aging, 25, 149-57.
191. Zoia, C. P., Tagliabue, E., Isella, V., et al. (2005). Fibroblast glutamate transport in aging and in AD: correlations with disease severity. Neurobiol Aging, 26, 825-32.
192. Zola-Morgan, S., Squire, L. R., Rempel, N. L., Clower, R. P., and Amaral, D. G. (1992). Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J Neurosci, 12, 2582-96.