Age-related increase in amyloid plaque burden is associated with impairment in conditioned fear memory in CRND8 mouse model of amyloidosis

Alzheimer's Research and Therapy

Volumn 4, Issue 3, 2012, Pages

  Hanna, Amanda ^b   Iremonger, Kayleigh ^c   Das, Pritam ^b   Dickson, Dennis ^b   Golde, Todd ^a   Janus, Christopher ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84862237175     PISSN: None     EISSN: 17589193     Source Type: Journal    
DOI: 10.1186/alzrt124     Document Type: Article

References (86)

1. Alzheimer's Disease International: World Alzheimer Report 2009 - Executive Summary. [http://www.alz.co.uk/research/files/WorldAlzheimerReport-ExecutiveSummary.pdf].
2. Delacourte A: Tau pathology and neurodegeneration: an obvious but misunderstood link. J Alzheimers Dis 2008, 14:437-440.
3. Hardy J: The relationship between amyloid and tau. J Mol Neurosci 2003, 20:203-206.
4. Price JL, Davis PB, Morris JC, White DL: The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease. Neurobiol Aging 1991, 12:295-312.
5. Selkoe DJ: Normal and abnormal biology of the β-amyloid precursor protein. Annu Rev Neurosci 1994, 17:489-517.
6. Braak H, Braak E: Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) 1991, 82:239-259.
7. Braak H, Braak E: Pathology of Alzheimer's disease. In Neurodegenerative Diseases. Edited by: Calne DB. Philadelphia: Saunders; 1994:585-613.
8. Braak H, Braak E: Diagnostic criteria for neuropathologic assessment of Alzheimer's disease. Neurobiol Aging 1997, 18:S85-88.
9. Hooper MW, Vogel FS: The limbic system in Alzheimer's disease. Am J Pathol 1976, 85:1-20.
10. Almkvist O, Winblad B: Early diagnosis of Alzheimer dementia based on clinical and biological factors. Eur Arch Psychiatry Clin Neurosci 1999, 249(Suppl 3):3-9.
11. Braak H, Braak E: Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol Aging 1997, 18:351-357.
12. Cairns NJ, Chadwick A, Luthert PJ, Lantos PL: beta-Amyloid protein load is relatively uniform throughout neocortex and hippocampus in elderly Alzheimer's disease patients. Neuroscience Lett 1991, 129:115-118.
13. de la Torre JC: Pathophysiology of neuronal energy crisis in Alzheimer's disease. Neurodegener Dis 2008, 5:126-132.
14. den Heijer T, Geerlings MI, Hoebeek FE, Hofman A, Koudstaal PJ, Breteler MM: Use of hippocampal and amygdalar volumes on magnetic resonance imaging to predict dementia in cognitively intact elderly people. Arch Gen Psychiatry 2006, 63:57-62.
15. Kril JJ, Patel S, Harding AJ, Halliday GM: Neuron loss from the hippocampus of Alzheimer's disease exceeds extracellular neurofibrillary tangle formation. Acta Neuropathol (Berl) 2002, 103:370-376.
16. Sze CI, Troncoso JC, Kawas C, Mouton P, Price DL, Martin LJ: Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J Neuropathol Exp Neurol 1997, 56:933-944.
17. Tapiola T, Pennanen C, Tapiola M, Tervo S, Kivipelto M, Hanninen T, Pihlajamaki M, Laakso MP, Hallikainen M, Hamalainen A, Vanhanen M, Helkala EL, Vanninen R, Nissinen A, Rossi R, Frisoni GB, Soininen H: MRI of hippocampus and entorhinal cortex in mild cognitive impairment: a follow-up study. Neurobiol Aging 2008, 29:31-38.
18. West MJ, Coleman PD, Flood DG, Troncoso JC: Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994, 344:769-772.
19. Ashe KH: Mechanisms of memory loss in Abeta and tau mouse models. Biochem Soc Trans 2005, 33:591-594.
20. Dodart JC, Mathis C, Bales KR, Paul SM: Does my mouse have Alzheimer's disease? Genes, Brain Behav 2002, 1:142-155.
21. Eriksen JL, Janus CG: Plaques, tangles, and memory loss in mouse models of neurodegeneration. Behav Genet 2007, 37:79-100.
22. Price DL, Sisodia SS: Mutant genes in familial Alzheimer's disease and transgenic models. Annu Rev Neurosci 1998, 21:479-505.
23. Seabrook GR, Rosahl TW: Transgenic animals relevant to Alzheimer's disease. Neuropharmacology 1999, 38:1-17.
24. Hanna A, Horne P, Yager D, Eckman C, Eckman E, Janus C: Amyloid beta and impairment in multiple memory systems in older transgenic APP TgCRND8 mice. Genes Brain Behav 2009, 8:676-684.
25. Janus C: Search strategies used by APP transgenic mice during navigation in the Morris water maze. Learn Mem 2004, 11:337-346.
26. Janus C, Pearson J, McLaurin J, Mathews PM, Jiang Y, Schmidt SD, Chishti MA, Horne P, Heslin D, French J, Mount HT, Nixon RA, Mercken M, Bergeron C, Fraser PE, St George-Hyslop P, Westaway D: A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 2000, 408:979-982.
27. Lovasic L, Bauschke H, Janus C: Working memory impairment in a transgenic amyloid precursor protein TgCRND8 mouse model of Alzheimer's disease. Genes Brain Behav 2005, 4:197-208.
28. Janus C, Welzl H, Hanna A, Lovasic L, Lane N, St George-Hyslop P, Westaway D: Impaired conditioned taste aversion learning in APP transgenic mice. Neurobiol Aging 2004, 25:1213-1219.
29. Ambree O, Touma C, Gortz N, Keyvani K, Paulus W, Palme R, Sachser N: Activity changes and marked stereotypic behavior precede Abeta pathology in TgCRND8 Alzheimer mice. Neurobiol Aging 2006, 27:955-964.
30. Dudal S, Krzywkowski P, Paquette J, Morissette C, Lacombe D, Tremblay P, Gervais F: Inflammation occurs early during the Abeta deposition process in TgCRND8 mice. Neurobiol Aging 2004, 25:861-871.
31. Del Vecchio RA, Gold LH, Novick SJ, Wong G, Hyde LA: Increased seizure threshold and severity in young transgenic CRND8 mice. Neurosci Lett 2004, 367:164-167.
32. Fanselow MS: Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 2000, 110:73-81.
33. LeDoux JE, Sakaguchi A, Iwata J, Reis DJ: Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli. Neuroscience 1986, 17:615-627.
34. Chen G, Wang LP, Tsien JZ: Neural population-level memory traces in the mouse hippocampus. PLoS One 2009, 4:e8256.
35. Logue SF, Paylor R, Wehner JM: Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task. Behav Neurosci 1997, 111:104-113.
36. Phillips RG, LeDoux JE: Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992, 106:274-285.
37. Schafe GE, Nader K, Blair HT, LeDoux JE: Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci 2001, 24:540-546.
38. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J, Turner S, Lozza G, Grilli M, Kunicki S, Morissette C, Paquette J, Gervais F, Bergeron C, Fraser PE, Carlson GA, George-Hyslop PS, Westaway D: Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 2001, 276:21562-21570.
39. Selkoe DJ: Alzheimer's Disease: genotypes, phenotypes, and treatments. Science 1997, 275:630-631.
40. Chartier-Harlin M-C, Crawford F, Houlden H, Warren A, Hughes D, Fidani L, Goate A, Rossor M, Roques P, Hardy J, Mullan M: Early-onset Alzheimer's Disease caused by mutations at codon 717 of the β-amyloid precursor protein gene. Nature 1991, 353:844-846.
41. Rogers DC, Fisher EM, Brown SD, Peters J, Hunter AJ, Martin JE: Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 1997, 8:711-713.
42. Rogers DC, Jones DN, Nelson PR, Jones CM, Quilter CA, Robinson TL, Hagan JJ: Use of SHIRPA and discriminant analysis to characterise marked differences in the behavioural phenotype of six inbred mouse strains. Behav Brain Res 1999, 105:207-217.
43. Fanselow MS: Factors governing one-trial contextual conditioning. Anim Learn Behav 1990, 18:264-270.
44. Franklin KBJ, Paxinos G: The Mouse Brain in Stereotaxic Coordinates. 3 edition. New York: Elsevier/Academic Press; 2007.
45. Ruifrok AC, Johnston DA: Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol 2001, 23:291-299.
46. Howell DC: Statistical Methods for Psychology Belmont, California: Duxbury Press; 1992.
47. Siegel S, Castellan JNJ: Nonparametric Statistics for Behavioral Sciences New York: McGraw-Hill Book Company; 1988.
48. Bayer TA, Wirths O: Review on the APP/PS1KI mouse model: intraneuronal Abeta accumulation triggers axonopathy, neuron loss and working memory impairment. Genes Brain Behav 2008, 7(Suppl 1):6-11.
49. Dewachter I, van Dorpe J, Spittaels K, Tesseur I, Van Den Haute C, Moechars D, Van Leuven F: Modeling Alzheimer's disease in transgenic mice: effect of age and of presenilin1 on amyloid biochemistry and pathology in APP/London mice. Exp Gerontol 2000, 35:831-841.
50. Gimenez-Llort L, Blazquez G, Canete T, Johansson B, Oddo S, Tobena A, LaFerla FM, Fernandez-Teruel A: Modeling behavioral and neuronal symptoms of Alzheimer's disease in mice: a role for intraneuronal amyloid. Neurosci Biobehav Rev 2007, 31:125-147.
51. Gotz J, Ittner LM: Animal models of Alzheimer's disease and frontotemporal dementia. Nat Rev Neurosci 2008, 9:532-544.
52. McGowan E, Eriksen J, Hutton M: A decade of modeling Alzheimer's disease in transgenic mice. Trends Genet 2006, 22:281-289.
53. Spires TL, Hyman BT: Transgenic models of Alzheimer's disease: learning from animals. NeuroRx 2005, 2:423-437.
54. Radulovic J, Kammermeier J, Spiess J: Generalization of fear responses in C57BL/6N mice subjected to one-trial foreground contextual fear conditioning. Behav Brain Res 1998, 95:179-189.
55. Gould TJ, Feiro OR: Age-related deficits in the retention of memories for cued fear conditioning are reversed by galantamine treatment. Behav Brain Res 2005, 165:160-171.
56. Chen G, Chen KS, Knox J, Inglis J, Bernard A, Martin SJ, Justice A, McConlogue L, Games D, Freedman SB, Morris RG: A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease. Nature 2000, 408:975-979.
57. Dineley KT, Xia X, Bui D, Sweatt JD, Zheng H: Accelerated plaque accumulation, associative learning deficits, and up-regulation of alpha 7 nicotinic receptor protein in transgenic mice co-expressing mutant human presenilin 1 and amyloid precursor proteins. J Biol Chem 2002, 277:22768-22780.
58. Jacobsen JS, Wu CC, Redwine JM, Comery TA, Arias R, Bowlby M, Martone R, Morrison JH, Pangalos MN, Reinhart PH, Bloom FE: Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 2006, 103:5161-5166.
59. Desmedt A, Garcia R, Jaffard R: An 8-day extensive elemental, but not contextual, fear conditioning potentiates hippocampal-lateral septal synaptic efficacy in mice. Synapse 2003, 49:270-278.
60. Desmedt A, Marighetto A, Garcia R, Jaffard R: The effects of ibotenic hippocampal lesions on discriminative fear conditioning to context in mice: impairment or facilitation depending on the associative value of a phasic explicit cue. Eur J Neurosci 2003, 17:1953-1963.
61. Bach ME, Hawkins RD, Osman M, Kandel ER, Mayford M: Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell 1995, 81:905-915.
62. d'Isa R, Clapcote SJ, Voikar V, Wolfer DP, Giese KP, Brambilla R, Fasano S: Mice lacking Ras-GRF1 show contextual fear conditioning but not spatial memory impairments: convergent evidence from two independently generated mouse mutant lines. Front Behav Neurosci 2011, 5:78.
63. Mizuno K, Giese KP: Hippocampus-dependent memory formation: do memory type-specific mechanisms exist? J Pharmacol Sci 2005, 98:191-197.
64. Corcoran KA, Lu Y, Turner RS, Maren S: Overexpression of hAPPswe impairs rewarded alternation and contextual fear conditioning in a transgenic mouse model of Alzheimer's disease. Learn Mem 2002, 9:243-252.
65. Frankland PW, Josselyn SA, Anagnostaras SG, Kogan JH, Takahashi E, Silva AJ: Consolidation of CS and US representations in associative fear conditioning. Hippocampus 2004, 14:557-569.
66. Terry RD: The pathogenesis of Alzheimer disease: an alternative to the amyloid hypothesis. J Neuropathol Exp Neurol 1996, 55:1023-1025.
67. Masliah E, Terry RD, Mallory M, Alford M, Hansen LA: Diffuse plaques do not accentuate synapse loss in Alzheimer's disease. Am J Pathol 1990, 137:1293-1297.
68. Einstein G, Buranosky R, Crain BJ: Dendritic pathology of granule cells in Alzheimer's disease is unrelated to neuritic plaques. J Neurosci 1994, 14:5077-5088.
69. Hyman BT, Marzloff K, Arriagada PV: The lack of accumulation of senile plaques or amyloid burden in Alzheimer's disease suggests a dynamic balance between amyloid deposition and resolution. J Neuropathol Exp Neurol 1993, 52:594-600.
70. Rentz DM, Locascio JJ, Becker JA, Moran EK, Eng E, Buckner RL, Sperling RA, Johnson KA: Cognition, reserve, and amyloid deposition in normal aging. Ann Neurol 2010, 67:353-364.
71. Naslund J, Haroutunian V, Mohs R, Davis KL, Davies P, Greengard P, Buxbaum JD: Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 2000, 283:1571-1577
72. Bancher C, Braak H, Fischer P, Jellinger KA: Neuropathological staging of Alzheimer lesions and intellectual status in Alzheimer's and Parkinson's disease patients. Neurosci Lett 1993, 162:179-182.
73. Thal DR, Holzer M, Rub U, Waldmann G, Gunzel S, Zedlick D, Schober R: Alzheimer-related tau-pathology in the perforant path target zone and in the hippocampal stratum oriens and radiatum correlates with onset and degree of dementia. Exp Neurol 2000, 163:98-110
74. Cummings BJ, Cotman CW: Image analysis of beta-amyloid load in Alzheimer's disease and relation to dementia severity. Lancet 1995, 346:1524-1528.
75. Kim JJ, Rison RA, Fanselow MS: Effects of amygdala, hippocampus, and periaqueductal gray lesions on short-term and long-term contextual fear. Beh Neurosci 1993, 107:1093-1098.
76. LeDoux JE: Emotion, memory and the brain. Sci Am 1994, 270:50-57
77. LeDoux JE: Emotion circuits in the brain. Annu Rev Neurosci 2000, 23:155-184.
78. Bechara A, Damasio H, Damasio AR, Lee GP: Different contributions of the human amygdala and ventromedial prefrontal cortex to decisionmaking. J Neurosci 1999, 19:5473-5481
79. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR: Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 1995, 269:1115-1118.
80. Buchel C, Dolan RJ: Classical fear conditioning in functional neuroimaging. Curr Opin Neurobiol 2000, 10:219-223.
81. Phelps EA: Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 2004, 14:198-202
82. Squire LR: Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 1992, 99:195-231
83. Squire LR: Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 2004, 82:171-177.
84. Hamann S, Monarch ES, Goldstein FC: Impaired fear conditioning in Alzheimer's disease. Neuropsychologia 2002, 40:1187-1195.
85. Hoefer M, Allison SC, Schauer GF, Neuhaus JM, Hall J, Dang JN, Weiner MW, Miller BL, Rosen HJ: Fear conditioning in frontotemporal lobar degeneration and Alzheimer's disease. Brain 2008, 131:1646-1657
86. de Souza LC, Corlier F, Habert MO, Uspenskaya O, Maroy R, Lamari F, Chupin M, Lehericy S, Colliot O, Hahn-Barma V, Samri D, Dubois B, Bottlaender M, Sarazin M: Similar amyloid-beta burden in posterior cortical atrophy and Alzheimer's disease. Brain 2011, 134:2036-2043