Spatial memory is enhanced in long-living Ames dwarf mice and maintained following kainic acid induced neurodegeneration

Mechanisms of Ageing and Development

Volumn 131, Issue 6, 2010, Pages 422-435

  Sharma, Sunita ^a   Haselton, James ^a   Rakoczy, Sharlene ^a   Branshaw, Stephanie ^a   Brown Borg, Holly M ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Ames dwarf; Barnes maze; Hippocampus; Kainic acid; Spatial memory

Indexed keywords

KAINIC ACID; SOMATOMEDIN C;

AGING; AMES DWARF MICE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; COGNITION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENOTYPE; HIPPOCAMPUS; LATENT PERIOD; LEARNING; MALE; MAZE TEST; MOUSE; MOUSE STRAIN; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SHORT TERM MEMORY; SPATIAL MEMORY; ANIMAL; CHEMICALLY INDUCED; COGNITIVE DEFECT; DEGENERATIVE DISEASE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; LONGEVITY; MEMORY; MUTANT MOUSE STRAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; TOXICITY;

ANIMALS; COGNITION; COGNITION DISORDERS; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR I; KAINIC ACID; LONGEVITY; MALE; MAZE LEARNING; MEMORY; MICE; MICE, MUTANT STRAINS; NEURODEGENERATIVE DISEASES;

ANIMALIA; MUS;

EID: 77955050213     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2010.06.004     Document Type: Article

References (109)

1. Adams M.M., Elizabeth Forbes M., Constance Linville M., Riddle D.R., Sonntag W.E., Brunso-Bechtold J.K. Stability of local brain levels of insulin-like growth factor-I in two well-characterized models of decreased plasma IGF-I. Growth Factors 2009, 27:181-188.
2. Agarwal S., Sohal R.S. Relationship between susceptibility to protein oxidation, aging, and maximum life span potential of different species. Exp. Gerontol. 1996, 31:365-372.
3. Albert, M.S., Funkenstein, H.H., 1992. The effects of age: normal variation and its relation to disease. In: A.A.K., McKhann, G.M., M.W.I. (Eds.), Diseases of the Nervous System: Clinical Neurobiology. Saunders, Philadelphia, pp. 598-611.
4. Aleman A., Verhaar H.J., De Haan E.H., De Vries W.R., Samson M.M., Drent M.L., Van der Veen E.A., Koppeschaar H.P. Insulin-like growth factor-I and cognitive function in healthy older men. J. Clin. Endocrinol. Metab. 1999, 84:471-475.
5. Amador-Noguez D., Yagi K., Venable S., Darlington G. Gene expression profile of long-lived Ames dwarf mice and Little mice. Aging Cell 2004, 3:423-441.
6. Arkhipov V., Kulesskaja N., Lebedev D. Behavioral perseveration and impairment of long-term memory in rats after intrahippocampal injection of kainic acid in subconvulsive dose. Pharmacol. Biochem. Behav. 2008, 88:299-305.
7. Barnes C.A. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 1979, 93:74-104.
8. Barnes C.A. Aging and the physiology of spatial memory. Neurobiol. Aging 1988, 9:563-568.
9. Bartke A., Brown-Borg H., Mattison J., Kinney B., Hauck S., Wright C. Prolonged longevity of hypopituitary dwarf mice. Exp. Gerontol. 2001, 36:21-28.
10. Benkovic S.A., O'Callaghan J.P., Miller D.B. Regional neuropathology following kainic acid intoxication in adult and aged C57BL/6J mice. Brain Res. 2006, 1070:215-231.
11. Bizon J., Prescott S., Nicolle M.M. Intact spatial learning in adult Tg2576 mice. Neurobiol. Aging 2007, 28:440-446.
12. Bluthe R.M., Frenois F., Kelley K.W., Dantzer R. Pentoxifylline and insulin-like growth factor-I (IGF-I) abrogate kainic acid-induced cognitive impairment in mice. J. Neuroimmunol. 2005, 169:50-58.
13. Bokov A.F., Lindsey M.L., Khodr C., Sabia M.R., Richardson A. Long-lived Ames dwarf mice are resistant to chemical stressors. J. Gerontol. A Biol. Sci. Med. Sci. 2009, 64:819-827.
14. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
15. Brown-Borg H.M., Bode A.M., Bartke A. Antioxidative mechanisms and plasma growth hormone levels: potential relationship in the aging process. Endocrine 1999, 11:41-48.
16. Brown-Borg H.M., Borg K.E., Meliska C.J., Bartke A. Dwarf mice and the ageing process. Nature 1996, 384:33.
17. Brown-Borg H.M., Rakoczy S.G. Catalase expression in delayed and premature aging mouse models. Exp. Gerontol. 2000, 35:199-212.
18. Brown-Borg H.M., Rakoczy S.G. Growth hormone administration to long-living dwarf mice alters multiple components of the antioxidative defense system. Mech. Ageing Dev. 2003, 124:1013-1024.
19. Brown-Borg H.M., Rakoczy S.G. Glutathione metabolism in long-living Ames dwarf mice. Exp. Gerontol. 2005, 40:115-120.
20. Brown-Borg H.M., Rakoczy S.G., Sharma S., Bartke A. Long-living growth hormone receptor knockout mice: potential mechanisms of altered stress resistance. Exp. Gerontol. 2008.
21. Brown-Borg H.M., Rakoczy S.G., Uthus E.O. Growth hormone alters components of the glutathione metabolic pathway in Ames dwarf mice. Ann. N. Y. Acad. Sci. 2004, 1019:317-320.
22. Brown-Borg H.M., Rakoczy S.G., Uthus E.O. Growth hormone alters methionine and glutathione metabolism in Ames dwarf mice. Mech. Ageing Dev. 2005, 126:389-398.
23. Brown-Croyts L.M., Caton P.W., Radecki D.T., McPherson S.L. Phenobarbital pre-treatment prevents kainic acid-induced impairments in acquisition learning. Life Sci. 2000, 67:643-650.
24. Bruce A.J., Baudry M. Oxygen free radicals in rat limbic structures after kainate-induced seizures. Free Radic. Biol. Med. 1995, 18:993-1002.
25. Chen Z., Ljunggren H.G., Bogdanovic N., Nennesmo I., Winblad B., Zhu J. Excitotoxic neurodegeneration induced by intranasal administration of kainic acid in C57BL/6 mice. Brain Res. 2002, 931:135-145.
26. Cherry K.E., Park D.C. Individual difference and contextual variables influence spatial memory in younger and older adults. Psychol. Aging 1993, 8:517-526.
27. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
28. Connor D.J., Langlais P.J., Thal L.J. Behavioral impairments after lesions of the nucleus basalis by ibotenic acid and quisqualic acid. Brain Res. 1991, 555:84-90.
29. Coyle J.T., Biziere K., Schwarcz R. Neurotoxicity of excitatory amino acids in the neural retina. Kainic Acid as a Tool in Neurobiology 1978, 177-188. Raven, New York, NY. E.G. McGeer, J.W. Olney, P.L. McGeer (Eds.).
30. Cronin J., Dudek F.E. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 1988, 474:181-184.
31. Deacon R.M., Bannerman D.M., Kirby B.P., Croucher A., Rawlins J.N. Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery. Behav. Brain Res. 2002, 133:57-68.
32. Dik M.G., Pluijm S.M., Jonker C., Deeg D.J., Lomecky M.Z., Lips P. Insulin-like growth factor I (IGF-I) and cognitive decline in older persons. Neurobiol. Aging 2003, 24:573-581.
33. Dubey A., Forster M.J., Lal H., Sohal R.S. Effect of age and caloric intake on protein oxidation in different brain regions and on behavioral functions of the mouse. Arch. Biochem. Biophys. 1996, 333:189-197.
34. Erickson C.A., Barnes C.A. The neurobiology of memory changes in normal aging. Exp. Gerontol. 2003, 38:61-69.
35. Evans G.W., Brennan P.L., Skorpanich M.A., Held D. Cognitive mapping and elderly adults: verbal and location memory for urban landmarks. J. Gerontol. 1984, 39:452-457.
36. Forster M.J., Dubey A., Dawson K.M., Stutts W.A., Lal H., Sohal R.S. Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:4765-4769.
37. Frick K.M., Baxter M.G., Markowska A.L., Olton D.S., Price D.L. Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging 1995, 16:149-160.
38. Gallagher M., Nicolle M.M. Animal models of normal aging: relationship between cognitive decline and markers in hippocampal circuitry. Behav. Brain Res. 1993, 57:155-162.
39. Gayoso M.J., Primo C., al-Majdalawi A., Fernandez J.M., Garrosa M., Iniguez C. Brain lesions and water-maze learning deficits after systemic administration of kainic acid to adult rats. Brain Res. 1994, 653:92-100.
40. Geinisman Y., de Toledo-Morrell L., Morrell F. Loss of perforated synapses in the dentate gyrus: morphological substrate of memory deficit in aged rats. Proc. Natl. Acad. Sci. U.S.A. 1986, 83:3027-3031.
41. Harrison F.E., Hosseini A.H., McDonald M.P. Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks. Behav. Brain Res. 2009, 198:247-251.
42. Harrison F.E., Reiserer R.S., Tomarken A.J., McDonald M.P. Spatial and nonspatial escape strategies in the Barnes maze. Learn. Mem. 2006, 13:809-819.
43. Hashimoto K., Watanabe K., Nishimura T., Iyo M., Shirayama Y., Minabe Y. Behavioral changes and expression of heat shock protein hsp-70 mRNA, brain-derived neurotrophic factor mRNA, and cyclooxygenase-2 mRNA in rat brain following seizures induced by systemic administration of kainic acid. Brain Res. 1998, 804:212-223.
44. Heid C.A., Stevens J., Livak K.J., Williams P.M. Real time quantitative PCR. Genome Res. 1996, 6:986-994.
45. Heiman M.L., Tinsley F.C., Mattison J.A., Hauck S., Bartke A. Body composition of prolactin-, growth hormone, and thyrotropin-deficient Ames dwarf mice. Endocrine 2003, 20:149-154.
46. Holmes G.L., Thompson J.L., Marchi T., Feldman D.S. Behavioral effects of kainic acid administration on the immature brain. Epilepsia 1988, 29:721-730.
47. Hu R.Q., Koh S., Torgerson T., Cole A.J. Neuronal stress and injury in C57/BL mice after systemic kainic acid administration. Brain Res. 1998, 810:229-240.
48. Jarrard L.E. On the role of the hippocampus in learning and memory in the rat. Behav. Neural Biol. 1993, 60:9-26.
49. Kesner R.P. Subregional analysis of mnemonic functions of the prefrontal cortex in the rat. Psychobiology 2000, 28:219-228.
50. Kim H., Bing G., Jhoo W., Ko K.H., Kim W.K., Suh J.H., Kim S.J., Kato K., Hong J.S. Changes of hippocampal Cu/Zn-superoxide dismutase after kainate treatment in the rat. Brain Res. 2000, 853:215-226.
51. Kim H.C., Bing G., Jhoo W.K., Kim W.K., Shin E.J., Park E.S., Choi Y.S., Lee D.W., Shin C.Y., Ryu J.R., Ko K.H. Oxidative damage causes formation of lipofuscin-like substances in the hippocampus of the senescence-accelerated mouse after kainate treatment. Behav. Brain Res. 2002, 131:211-220.
52. Kim H.C., Bing G., Jhoo W.K., Ko K.H., Kim W.K., Lee D.C., Shin E.J., Hong J.S. Dextromethorphan modulates the AP-1 DNA-binding activity induced by kainic acid. Brain Res. 1999, 824:125-132.
53. Kim H.C., Jhoo W.K., Kim W.K., Suh J.H., Shin E.J., Kato K.K.H.K. An immunocytochemical study of mitochondrial manganese-superoxide dismutase in the rat hippocampus after kainate administration. Neurosci. Lett. 2000, 281:65-68.
54. Kinney B.A., Coschigano K.T., Kopchick J.J., Steger R.W., Bartke A. Evidence that age-induced decline in memory retention is delayed in growth hormone resistant GH-R-KO (Laron) mice. Physiol. Behav. 2001, 72:653-660.
55. Kinney B.A., Meliska C.J., Steger R.W., Bartke A. Evidence that Ames dwarf mice age differently from their normal siblings in behavioral and learning and memory parameters. Horm. Behav. 2001, 39:277-284.
56. Kinney-Forshee B.A., Kinney N.E., Steger R.W., Bartke A. Could a deficiency in growth hormone signaling be beneficial to the aging brain?. Physiol. Behav. 2004, 80:589-594.
57. Kirasic K.C., Bernicki M.R. Acquisition of spatial knowledge under conditions of temporospatial discontinuity in young and elderly adults. Psychol. Res. 1990, 52:76-79.
58. Kraft A.D., Lee J.M., Johnson D.A., Kan Y.W., Johnson J.A. Neuronal sensitivity to kainic acid is dependent on the Nrf2-mediated actions of the antioxidant response element. J. Neurochem. 2006, 98:1852-1865.
59. Liang L.P., Beaudoin M.E., Fritz M.J., Fulton R., Patel M. Kainate-induced seizures, oxidative stress and neuronal loss in aging rats. Neuroscience 2007, 147:1114-1118.
60. Liu F., Schafer D.P., McCullough L.D. TTC, FluoroJade B and NeuN staining confirm evolving phases of infarction induced by middle cerebral artery occlusion. J. Neurosci. Methods 2009, 179:1-8.
61. Louilot A., Taghzouti K., Simon H., Le Moal M. Limbic system, basal ganglia, and dopaminergic neurons. Executive and regulatory neurons and their role in the organization of behavior. Brain Behav. Evol. 1989, 33:157-161.
62. Lupberger J., Kreuzer K.A., Baskaynak G., Peters U.R., le Coutre P., Schmidt C.A. Quantitative analysis of beta-actin, beta-2-microglobulin and porphobilinogen deaminase mRNA and their comparison as control transcripts for RT-PCR. Mol. Cell Probes 2002, 16:25-30.
63. Magnusson K.R., Scruggs B., Aniya J., Wright K.C., Ontl T., Xing Y., Bai L. Age-related deficits in mice performing working memory tasks in a water maze. Behav. Neurosci. 2003, 117:485-495.
64. Mattison J.A., Wright C., Bronson R.T., Roth G.S., Ingram D.T., Bartke A. Studies of aging in Ames dwarf mice: effects of caloric restriction. J. Am. Aging Assoc. 2000, 23:9-16.
65. Mazarati A., Lu X., Shinmei S., Badie-Mahdavi H., Bartfai T. Patterns of seizures, hippocampal injury and neurogenesis in three models of status epilepticus in galanin receptor type 1 (GalR1) knockout mice. Neuroscience 2004, 128:431-441.
66. McGeer P.L., McGeer E.G. Kainic acid: the neurotoxic breakthrough. Crit. Rev. Toxicol. 1982, 10:1-26.
67. Meliska C.J., Burke P.A., Bartke A., Jensen R.A. Inhibitory avoidance and appetitive learning in aged normal mice: comparison with transgenic mice having elevated plasma growth hormone levels. Neurobiol. Learn. Mem. 1997, 68:1-12.
68. Mesulam M.M. Neuroplasticity failure in Alzheimer's disease: bridging the gap between plaques and tangles. Neuron 1999, 24:521-529.
69. Miller D.B., O'Callaghan J.P. Aging, stress and the hippocampus. Ageing Res. Rev. 2005, 4:123-140.
70. Mitruskova B., Orendacova J., Racekova E. FluoroJade-B detection of dying cells in the SVZ and RMS of adult rats after bilateral olfactory bulbectomy. Cell. Mol. Neurobiol. 2005, 25:1255-1264.
71. Moffat S.D., Zonderman A.B., Resnick S.M. Age differences in spatial memory in a virtual environment navigation task. Neurobiol. Aging 2001, 22:787-796.
72. Moore T.E., Richards B., Hood J. Aging and the coding of spatial information. J. Gerontol. 1984, 39:210-212.
73. Morris R.G., Schenk F., Tweedie F., Jarrard L.E. Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning. Eur. J. Neurosci. 1990, 2:1016-1028.
74. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971, 34:171-175.
75. Oswald C.J., Yee B.K., Rawlins J.N., Bannerman D.B., Good M., Honey R.C. The influence of selective lesions to components of the hippocampal system on the orienting [correction of orientating] response, habituation and latent inhibition. Eur. J. Neurosci. 2002, 15:1983-1990.
76. Pompl P.N., Mullan M.J., Bjugstad K., Arendash G.W. Adaptation of the circular platform spatial memory task for mice: use in detecting cognitive impairment in the APP(SW) transgenic mouse model for Alzheimer's disease. J. Neurosci. Methods 1999, 87:87-95.
77. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 1972, 32:281-294.
78. Ramos J.M. Is spatial memory transformed during the consolidation process: effect of reminding. Acta Neurobiol. Exp. (Wars) 2009, 69:545-551.
79. Rapp P.R., Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:9926-9930.
80. Romanick M.A., Rakoczy S.G., Brown-Borg H.M. Long-lived Ames dwarf mouse exhibits increased antioxidant defense in skeletal muscle. Mech. Ageing Dev. 2004, 125:269-281.
81. Schauwecker P.E., Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:4103-4108.
82. Schmued L.C., Albertson C., Slikker W. Fluoro-Jade: a novel fluorochrome for the sensitive and reliable histochemical localization of neuronal degeneration. Brain Res. 1997, 751:37-46.
83. Schmued L.C., Hopkins K.J. Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res. 2000, 874:123-130.
84. Schmued L.C., Hopkins K.J. Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol. Pathol. 2000, 28:91-99.
85. Schmued L.C., Stowers C.C., Scallet A.C., Xu L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 2005, 1035:24-31.
86. Schrag M., Sharma S., Brown-Borg H., Ghribi O. Hippocampus of Ames dwarf mice is resistant to beta-amyloid-induced tau hyperphosphorylation and changes in apoptosis-regulatory protein levels. Hippocampus 2008, 18:239-244.
87. Sharps M.J., Gollin E.S. Memory for object locations in young and elderly adults. J. Gerontol. 1987, 42:336-341.
88. Shin E.J., Jeong J.H., Bing G., Park E.S., Chae J.S., Yen T.P., Kim W.K., Wie M.B., Jung B.D., Kim H.J., Lee S.Y., Kim H.C. Kainate-induced mitochondrial oxidative stress contributes to hippocampal degeneration in senescence-accelerated mice. Cell Signal. 2008, 20:645-658.
89. Sohal R.S., Agarwal S., Candas M., Forster M.J., Lal H. Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mech. Ageing Dev. 1994, 76:215-224.
90. Sperk G. Kainic acid seizures in the rat. Prog. Neurobiol. 1994, 42:1-32.
91. Sperk G., Lassmann H., Baran H., Kish S.J., Seitelberger F., Hornykiewicz O. Kainic acid induced seizures: neurochemical and histopathological changes. Neuroscience 1983, 10:1301-1315.
92. Sperk G., Lassmann H., Baran H., Seitelberger F., Hornykiewicz O. Kainic acid-induced seizures: dose-relationship of behavioural, neurochemical and histopathological changes. Brain Res. 1985, 338:289-295.
93. Sun A.Y., Cheng Y., Bu Q., Oldfield F. The biochemical mechanisms of the excitotoxicity of kainic acid. Free radical formation. Mol. Chem. Neuropathol. 1992, 17:51-63.
94. Sun L.Y., Al-Regaiey K., Masternak M.M., Wang J., Bartke A. Local expression of GH and IGF-1 in the hippocampus of GH-deficient long-lived mice. Neurobiol. Aging 2005, 26:929-937.
95. Sun L.Y., Bartke A. Adult neurogenesis in the hippocampus of long-lived mice during aging. J. Gerontol. A Biol. Sci. Med. Sci. 2007, 62:117-125.
96. Sun L.Y., Evans M.S., Hsieh J., Panici J., Bartke A. Increased neurogenesis in dentate gyrus of long-lived Ames dwarf mice. Endocrinology 2005, 146:1138-1144.
97. Sunyer B., Patil S., Hoger H.G.L. Barnes maze, a useful task to assess spatial reference memory in mice. Nat. Protocol 2007, 198:58-68.
98. Sutherland R.J., McDonald R.J. Hippocampus, amygdala, and memory deficits in rats. Behav. Brain Res. 1990, 37:57-79.
99. Swindell W.R. Gene expression profiling of long-lived dwarf mice: longevity-associated genes and relationships with diet, gender and aging. BMC Genomics 2007, 8:353.
100. Takashima A., Nieuwenhuis I.L., Jensen O., Talamini L.M., Rijpkema M., Fernandez G. Shift from hippocampal to neocortical centered retrieval network with consolidation. J. Neurosci. 2009, 29:10087-10093.
101. Trejo J.L., Carro E., Lopez-Lopez C., Torres-Aleman I. Role of serum insulin-like growth factor I in mammalian brain aging. Growth Horm. IGF Res. 2004, 14(Suppl A):S39-43.
102. van Dam P.S., Aleman A. Insulin-like growth factor-I, cognition and brain aging. Eur. J. Pharmacol. 2004, 490:87-95.
103. Wang Q., Yu S., Simonyi A., Sun G.Y., Sun A.Y. Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol. Neurobiol. 2005, 31:3-16.
104. Watson R.E., Wiegand S.J., Clough R.W., Hoffman G.E. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 1986, 7:155-159.
105. West M.J. Regionally specific loss of neurons in the aging human hippocampus. Neurobiol. Aging 1993, 14:287-293.
106. Wickelgren I. Is hippocampal cell death a myth?. Science 1996, 271:1229-1230.
107. Wilcoxon J.S., Nadolski G.J., Samarut J., Chassande O., Redei E.E. Behavioral inhibition and impaired spatial learning and memory in hypothyroid mice lacking thyroid hormone receptor alpha. Behav. Brain Res. 2007, 177:109-116.
108. Yau J.L., McNair K.M., Noble J., Brownstein D., Hibberd C., Morton N., Mullins J.J., Morris R.G., Cobb S., Seckl J.R. Enhanced hippocampal long-term potentiation and spatial learning in aged 11beta-hydroxysteroid dehydrogenase type 1 knock-out mice. J. Neurosci. 2007, 27:10487-10496.
109. Zhang X.M., Jin T., Quezada H.C., Mix E., Winblad B., Zhu J. Kainic acid-induced microglial activation is attenuated in aged interleukin-18 deficient mice. J. Neuroinflamm. 2010, 7:26.