Aβ Deposition in aging is associated with increases in brain activation during successful memory encoding

Cerebral Cortex

Volumn 22, Issue 8, 2012, Pages 1813-1823

  Mormino, Elizabeth C ^a   Brandel, Michael G ^a   Madison, Cindee M ^a   Marks, Shawn ^a   Baker, Suzanne L ^b   Jagust, William J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

aging; Alzheimer's disease; beta amyloid; episodic memory; fMRI; PIB PET

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E;

ADULT; AGED; AGING; ARTICLE; BLOOD SAMPLING; BRAIN REGION; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; EPISODIC MEMORY; FEMALE; GENOTYPE; HUMAN; MALE; MEMORY; MINI MENTAL STATE EXAMINATION; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; OCCIPITAL CORTEX; PARIETAL LOBE; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIORITY JOURNAL; SEMANTIC MEMORY; TASK PERFORMANCE; TEMPORAL CORTEX; VISUAL MEMORY; WORKING MEMORY;

AGED; AGED, 80 AND OVER; AGING; AMYLOID BETA-PEPTIDES; BRAIN; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, EPISODIC; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; YOUNG ADULT;

EID: 84863683381     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr255     Document Type: Article

References (73)

1. Becker JA, Hedden T, Carmasin J, Maye J, Rentz DM, Putcha D, Fischl B, Greve DN, Marshall GA, Salloway S, et al. 2011. Amyloid-beta associated cortical thinning in clinically normal elderly. Ann Neurol. 69:1032-1042.
2. Bennett DA, Schneider JA, Arvanitakis Z, Kelly JF, Aggarwal NT, Shah RC, Wilson RS. 2006. Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology. 66:1837-1844. (Pubitemid 44049813)
3. Bero AW, Yan P, Roh JH, Cirrito JR, Stewart FR, Raichle ME, Lee JM, Holtzman DM. 2011. Neuronal activity regulates the regional vulnerability to amyloid-beta deposition. Nat Neurosci. 14:750-756.
4. Blumenfeld RS, Ranganath C. 2007. Prefrontal cortex and long-term memory encoding: an integrative review of findings from neuropsychology and neuroimaging. Neuroscientist. 13:280-291. (Pubitemid 46801762)
5. Bookheimer SY, Strojwas MH, Cohen MS, Saunders AM, Pericak-Vance MA, Mazziotta JC, Small GW. 2000. Patterns of brain activation in people at risk for Alzheimer's disease. N Engl J Med. 343:450-456. (Pubitemid 30646483)
6. Braak H, Braak E. 1991. Neuropathological stageing of Alzheimerrelated changes. Acta Neuropathol. 82:239-259.
7. Braak H, Del Tredici K. 2011. The pathological process underlying Alzheimer's disease in individuals under thirty. Acta Neuropathol. 121:171-181.
8. Braskie MN, Landau SM, Wilcox CE, Taylor SD, O'Neil JP, Baker SL, Madison CM, Jagust WJ. 2010. Correlations of striatal dopamine synthesis with default network deactivations during working memory in younger adults. Hum Brain Mapp. 32:947-961.
9. Buckner RL, Andrews-Hanna JR, Schacter DL. 2008. The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci. 1124:1-38. (Pubitemid 351506788)
10. Buckner RL, Snyder AZ, Shannon BJ, LaRossa G, Sachs R, Fotenos AF, Sheline YI, Klunk WE, Mathis CA, Morris JC, et al. 2005. Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J Neurosci. 25:7709-7717. (Pubitemid 41208641)
11. Burt C, Thomson GH. 1947. The factorial analysis of human ability [Bk Rev.]. Br J Educ Psychol. 17:40-48.
12. Cabeza R, Anderson ND, Locantore JK, McIntosh AR. 2002. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage. 17:1394-1402. (Pubitemid 35339393)
13. Chetelat G, Villemagne VL, Bourgeat P, Pike KE, Jones G, Ames D, Ellis KA, Szoeke C, Martins RN, O'Keefe GJ, et al. 2010. Relationship between atrophy and beta-amyloid deposition in Alzheimer disease. Ann Neurol. 67:317-324.
14. Cirrito JR, Yamada KA, Finn MB, Sloviter RS, Bales KR, May PC, Schoepp DD, Paul SM, Mennerick S, Holtzman DM. 2005. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron. 48:913-922. (Pubitemid 41814696)
15. Dale AM. 1999. Optimal experimental design for event-related fMRI. Hum Brain Mapp. 8:109-114. (Pubitemid 29480297)
16. Dale AM, Fischl B, Sereno MI. 1999. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 9:179-194. (Pubitemid 29369874)
17. Daselaar SM, Prince SE, Cabeza R. 2004. When less means more: deactivations during encoding that predict subsequent memory. Neuroimage. 23:921-927. (Pubitemid 39446526)
18. de Chastelaine M, Wang TH, Minton B, Muftuler LT, Rugg MD. 2011. The effects of age, memory performance, and callosal integrity on the neural correlates of successful associative encoding. Cereb Cortex. 21:2166-2176.
19. Delis D, Kramer J, Kaplan E, Ober B. 2000. California verbal learning test. San Antonio (TX): The Psychological Corporation.
20. Dickerson BC, Bakkour A, Salat DH, Feczko E, Pacheco J, Greve DN, Grodstein F, Wright CI, Blacker D, Rosas HD, et al. 2009. The cortical signature of Alzheimer's disease: regionally specific cortical thinning relates to symptom severity in very mild to mild AD dementia and is detectable in asymptomatic amyloid-positive individuals. Cereb Cortex. 19:497-510.
21. Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, Rentz DM, Bertram L, Mullin K, Tanzi RE, Blacker D, et al. 2005. Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology. 65:404-411. (Pubitemid 41099803)
22. Duverne S, Motamedinia S, Rugg MD. 2009. The relationship between aging, performance, and the neural correlates of successful memory encoding. Cereb Cortex. 19:733-744.
23. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE. 2009. Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci USA. 106:7209-7214.
24. Fischl B, Liu A, Dale AM. 2001. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging. 20:70-80. (Pubitemid 32293421)
25. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, et al. 2002. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron. 33:341-355. (Pubitemid 34162530)
26. Fletcher PC, Stephenson CM, Carpenter TA, Donovan T, Bullmorel ET. 2003. Regional brain activations predicting subsequent memory success: an event-related fMRI study of the influence of encoding tasks. Cortex. 39:1009-1026. (Pubitemid 37351079)
27. Fotenos AF, Mintun MA, Snyder AZ, Morris JC, Buckner RL. 2008. Brain volume decline in aging: evidence for a relation between socioeconomic status, preclinical Alzheimer disease, and reserve. Arch Neurol. 65:113-120.
28. Gutchess AH, Welsh RC, Hedden T, Bangert A, Minear M, Liu LL, Park DC. 2005. Aging and the neural correlates of successful picture encoding: frontal activations compensate for decreased medialtemporal activity. J Cogn Neurosci. 17:84-96.
29. Hardy J, Selkoe DJ. 2002. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science. 297:353-356. (Pubitemid 34790756)
30. Hedden T, Van Dijk KR, Becker JA, Mehta A, Sperling RA, Johnson KA, Buckner RL. 2009. Disruption of functional connectivity in clinically normal older adults harboring amyloid burden. J Neurosci. 29:12686-12694.
31. Jack CR, Jr., Knopman DS, Jagust WJ, Shaw LM, Aisen PS, Weiner MW, Petersen RC, Trojanowski JQ. 2010. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol. 9:119-128.
32. Kaplan E, Goodglass H, Weintraub S. 1983. Boston naming test. Philadelphia: Lea and Febiger.
33. Kemppainen NM, Aalto S, Karrasch M, Nagren K, Savisto N, Oikonen V, Viitanen M, Parkkola R, Rinne JO. 2008. Cognitive reserve hypothesis: Pittsburgh Compound B and fluorodeoxyglucose positron emission tomography in relation to education in mild Alzheimer's disease. Ann Neurol. 63:112-118. (Pubitemid 351240557)
34. Kok E, Haikonen S, Luoto T, Huhtala H, Goebeler S, Haapasalo H, Karhunen PJ. 2009. Apolipoprotein E-dependent accumulation of Alzheimer disease-related lesions begins in middle age. Ann Neurol. 65:650-657.
35. Kukolja J, Thiel CM, Wilms M, Mirzazade S, Fink GR. 2009. Ageingrelated changes of neural activity associated with spatial contextual memory. Neurobiol Aging. 30:630-645.
36. Lezak M. 1995. Neuropsychological assessment. 2nd ed. New York: Oxford University Press, Inc.
37. Li SC, Brehmer Y, Shing YL, Werkle-Bergner M, Lindenberger U. 2006. Neuromodulation of associative and organizational plasticity across the life span: empirical evidence and neurocomputational modeling. Neurosci Biobehav Rev. 30:775-790. (Pubitemid 44292286)
38. Logan J, Fowler JS, Volkow ND, Wang GJ, Ding YS, Alexoff DL. 1996. Distribution volume ratios without blood sampling from graphical analysis of PET data. J Cereb Blood Flow Metab. 16:834-840. (Pubitemid 26292051)
39. Logan JM, Sanders AL, Snyder AZ, Morris JC, Buckner RL. 2002. Underrecruitment and nonselective recruitment: dissociable neural mechanisms associated with aging. Neuron. 33:827-840. (Pubitemid 34219252)
40. Lopresti BJ, Klunk WE, Mathis CA, Hoge JA, Ziolko SK, Lu X, Meltzer CC, Schimmel K, Tsopelas ND, DeKosky ST, et al. 2005. Simplified quantification of Pittsburgh Compound B amyloid imaging PET studies: a comparative analysis. J Nucl Med. 46:1959-1972. (Pubitemid 46657441)
41. Mathis CA, Wang Y, Holt DP, Huang GF, Debnath ML, Klunk WE. 2003. Synthesis and evaluation of 11C-labeled 6-substituted 2-arylbenzothiazoles as amyloid imaging agents. J Med Chem. 46:2740-2754. (Pubitemid 36702542)
42. Mondadori CR, de Quervain DJ, Buchmann A, Mustovic H, Wollmer MA, Schmidt CF, Boesiger P, Hock C, Nitsch RM, Papassotiropoulos A, et al. 2007. Better memory and neural efficiency in young apolipoprotein E epsilon4 carriers. Cereb Cortex. 17:1934-1947. (Pubitemid 47216511)
43. Morcom AM, Good CD, Frackowiak RS, Rugg MD. 2003. Age effects on the neural correlates of successful memory encoding. Brain. 126:213-229. (Pubitemid 36068571)
44. Mormino EC, Brandel MG, Madison CM, Rabinovici GD, Marks S, Baker SL, Jagust W. 2011. Not quite PIB-positive, not quite PIBnegative: slight PIB elevations in elderly normal control subjects are biologically relevant. Neuroimage. doi: 10.1016/j.neuroimage. 2011.07.098.
45. Mormino EC, Kluth JT, Madison CM, Rabinovici GD, Baker SL, Miller BL, Koeppe RA, Mathis CA, Weiner MW, Jagust WJ. 2009. Episodic memory loss is related to hippocampal-mediated beta-amyloid deposition in elderly subjects. Brain. 132:1310-1323.
46. Mormino EC, Smiljic A, Hayenga AO, Onami S, Greicius MD, Rabinovici GD, Janabi M, Baker SL, Yen IV, Madison CM, et al. 2011. Relationships between beta-amyloid and functional connectivity in different components of the default mode network in aging. Cereb Cortex. doi: 10.1093/cercor/bhr025.
47. Morris JC, Roe CM, Grant EA, Head D, Storandt M, Goate AM, Fagan AM, Holtzman DM, Mintun MA. 2009. Pittsburgh compound B imaging and prediction of progression from cognitive normality to symptomatic Alzheimer disease. Arch Neurol. 66:1469-1475.
48. Morris JC, Roe CM, Xiong C, Fagan AM, Goate AM, Holtzman DM, Mintun MA. 2010. APOE predicts amyloid-beta but not tau Alzheimer pathology in cognitively normal aging. Ann Neurol. 67:122-131.
49. O'Brien JL, O'Keefe KM, LaViolette PS, DeLuca AN, Blacker D, Dickerson BC, Sperling RA. 2010. Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology. 74:1969-1976.
50. Oh H, Mormino EC, Madison C, Hayenga A, Smiljic A, Jagust WJ. 2010. beta-Amyloid affects frontal and posterior brain networks in normal aging. Neuroimage. 54:1887-1895.
51. Park DC, Reuter-Lorenz P. 2009. The adaptive brain: aging and neurocognitive scaffolding. Annu Rev Psychol. 60:173-196.
52. Persson J, Nyberg L, Lind J, Larsson A, Nilsson LG, Ingvar M, Buckner RL. 2006. Structure-function correlates of cognitive decline in aging. Cereb Cortex. 16:907-915. (Pubitemid 43992441)
53. Reber PJ, Siwiec RM, Gitelman DR, Parrish TB, Mesulam MM, Paller KA. 2002. Neural correlates of successful encoding identified using functional magnetic resonance imaging. J Neurosci. 22:9541-9548. (Pubitemid 35356195)
54. Reitan R. 1958. Validity of the Trail Making Test as an indication of organic brain damage. Percept Mot Skills. 8:271-276.
55. Rentz DM, Locascio JJ, Becker JA, Moran EK, Eng E, Buckner RL, Sperling RA, Johnson KA. 2010. Cognition, reserve, and amyloid deposition in normal aging. Ann Neurol. 67:353-364.
56. Rosen AC, Prull MW, O'Hara R, Race EA, Desmond JE, Glover GH, Yesavage JA, Gabrieli JD. 2002. Variable effects of aging on frontal lobe contributions to memory. Neuroreport. 13:2425-2428. (Pubitemid 36143537)
57. Rowe CC, Ellis KA, Rimajova M, Bourgeat P, Pike KE, Jones G, Fripp J, Tochon-Danguy H, Morandeau L, O'Keefe G, et al. 2010. Amyloid imaging results from the Australian Imaging, Biomarkers and Lifestyle (AIBL) study of aging. Neurobiol Aging. 31:1275-1283.
58. Savva GM, Wharton SB, Ince PG, Forster G, Matthews FE, Brayne C. 2009. Age, neuropathology, and dementia. N Engl J Med. 360:2302-2309.
59. Segonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B. 2004. A hybrid approach to the skull stripping problem in MRI. Neuroimage. 22:1060-1075. (Pubitemid 38829195)
60. Selkoe DJ. 2002. Alzheimer's disease is a synaptic failure. Science. 298:789-791. (Pubitemid 35231524)
61. Sheline YI, Raichle ME, Snyder AZ, Morris JC, Head D, Wang S, Mintun MA. 2009. Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol Psychiatry. 67:584-587.
62. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR, Kaye J, Montine TJ, et al. 2011. Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging and the Alzheimer's Association workgroup. Alzheimers Dement. 7:280-292.
63. Sperling RA, Laviolette PS, O'Keefe K, O'Brien J, Rentz DM, Pihlajamaki M, Marshall G, Hyman BT, Selkoe DJ, Hedden T, et al. 2009. Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron. 63:178-188.
64. Stern Y. 2006. Cognitive reserve and Alzheimer disease. Alzheimer Dis Assoc Disord. 20:S69-S74. (Pubitemid 44265854)
65. Storandt M, Mintun MA, Head D, Morris JC. 2009. Cognitive decline and brain volume loss as signatures of cerebral amyloid-beta peptide deposition identified with Pittsburgh compound B: cognitive decline associated with Abeta deposition. Arch Neurol. 66:1476-1481.
66. Thal DR, Rub U, Orantes M, Braak H. 2002. Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology. 58:1791-1800. (Pubitemid 34663580)
67. Trivedi MA, Murphy CM, Goetz C, Shah RC, Gabrieli JD, Whitfield-Gabrieli S, Turner DA, Stebbins GT. 2008. fMRI activation changes during successful episodic memory encoding and recognition in amnestic mild cognitive impairment relative to cognitively healthy older adults. Dement Geriatr Cogn Disord. 26:123-137.
68. Vannini P, Hedden T, Becker JA, Sullivan C, Putcha D, Rentz D, Johnson KA, Sperling RA. 2011. Age and amyloid-related alterations in default network habituation to stimulus repetition. Neurobiol Aging. doi: 10.1016/j. neurobiolaging.2011.01.003.
69. Villemagne VL, Pike KE, Chetelat G, Ellis KA, Mulligan RS, Bourgeat P, Ackermann U, Jones G, Szoeke C, Salvado O, et al. 2011. Longitudinal assessment of Abeta and cognition in aging and Alzheimer disease. Ann Neurol. 69:181-192.
70. Vlassenko AG, Vaishnavi SN, Couture L, Sacco D, Shannon BJ, Mach RH, Morris JC, Raichle ME, Mintun MA. 2011. Spatial correlation between brain aerobic glycolysis and amyloid-beta (Abeta) deposition. Proc Natl Acad Sci USA. 107:17763-17767.
71. Walsh DM, Selkoe DJ. 2007. A beta oligomers-a decade of discovery. J Neurochem. 101:1172-1184.
72. Wechsler D. 1987. Wechsler memory scale-revised. San Antonio (TX): The Psychological Corporation.
73. Zec R. 1986. The stroop color-word test: a paradigm for procedural learning. Arch Clin Neuropsychol. 1:274-275.