Aβ-related hyperactivation in frontoparietal control regions in cognitively normal elderly

Neurobiology of Aging

Volumn 36, Issue 12, 2015, Pages 3247-3254

  Oh, Hwamee ^a   Steffener, Jason ^a   Razlighi, Qolamreza R ^a   Habeck, Christian ^a   Liu, Dan ^a   Gazes, Yunglin ^a   Janicki, Sarah ^a   Stern, Yaakov ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

Aging; Amyloid PET; Amyloid beta deposition; FMRI; Frontoparietal control regions; Working memory

Indexed keywords

AMYLOID BETA PROTEIN;

ADULT; ARTICLE; BRAIN FUNCTION; COGNITION; CONTROLLED STUDY; ENZYME ACTIVATION; EPISODIC MEMORY; FEMALE; FRONTOPARIETAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE PROCESSING; MALE; MENTAL TASK; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RESPONSE TIME; TASK PERFORMANCE; WORKING MEMORY; YOUNG ADULT; AGED; AGING; DIAGNOSTIC IMAGING; FRONTAL LOBE; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL LOBE; PATHOLOGY; PHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY;

ADULT; AGED; AGING; AMYLOID BETA-PEPTIDES; COGNITION; FEMALE; FRONTAL LOBE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PARIETAL LOBE; POSITRON-EMISSION TOMOGRAPHY; YOUNG ADULT;

EID: 84947025545     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.08.016     Document Type: Article

References (76)

1. Archer H.A., Edison P., Brooks D.J., Barnes J., Frost C., Yeatman T., Fox N.C., Rossor M.N. Amyloid load and cerebral atrophy in Alzheimer's disease: an 11C-PIB positron emission tomography study. Ann. Neurol. 2006, 60:145-147.
2. Baddeley A. Working Memory 1986, Oxford University Press, Oxford.
3. Bakker A., Krauss G.L., Albert M.S., Speck C.L., Jones L.R., Stark C.E., Yassa M.A., Bassett S.S., Shelton A.L., Gallagher M. Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 2012, 74:467-474.
4. Becker J.A., Hedden T., Carmasin J., Maye J., Rentz D.M., Putcha D., Fischl B., Greve D.N., Marshall G.A., Salloway S., Marks D., Buckner R.L., Sperling R.A., Johnson K.A. Amyloid-beta associated cortical thinning in clinically normal elderly. Ann. Neurol. 2011, 69:1032-1042.
5. Bennett D.A., Schneider J.A., Arvanitakis Z., Kelly J.F., Aggarwal N.T., Shah R.C., Wilson R.S. Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology 2006, 66:1837-1844.
6. Benzinger T.L., Blazey T., Jack C.R., Koeppe R.A., Su Y., Xiong C., Raichle M.E., Snyder A.Z., Ances B.M., Bateman R.J., Cairns N.J., Fagan A.M., Goate A., Marcus D.S., Aisen P.S., Christensen J.J., Ercole L., Hornbeck R.C., Farrar A.M., Aldea P., Jasielec M.S., Owen C.J., Xie X., Mayeux R., Brickman A., McDade E., Klunk W., Mathis C.A., Ringman J., Thompson P.M., Ghetti B., Saykin A.J., Sperling R.A., Johnson K.A., Salloway S., Correia S., Schofield P.R., Masters C.L., Rowe C., Villemagne V.L., Martins R., Ourselin S., Rossor M.N., Fox N.C., Cash D.M., Weiner M.W., Holtzman D.M., Buckles V.D., Moulder K., Morris J.C. Regional variability of imaging biomarkers in autosomal dominant Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E4502-E4509.
7. Bourgeat P., Chetelat G., Villemagne V.L., Fripp J., Raniga P., Pike K., Acosta O., Szoeke C., Ourselin S., Ames D., Ellis K.A., Martins R.N., Masters C.L., Rowe C.C., Salvado O. Beta-amyloid burden in the temporal neocortex is related to hippocampal atrophy in elderly subjects without dementia. Neurology 2010, 74:121-127.
8. Braak H., Braak E. Demonstration of amyloid deposits and neurofibrillary changes in whole brain sections. Brain Pathol. 1991, 1:213-216.
9. Brett M., Anton J.-L., Valabregue R., Poline J.-B. Region of interest analysis using an SPM toolbox. Neuroimage 2002, 16.
10. Buckner R.L., Snyder A.Z., Shannon B.J., LaRossa G., Sachs R., Fotenos A.F., Sheline Y.I., Klunk W.E., Mathis C.A., Morris J.C., Mintun M.A. Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J. Neurosci. 2005, 25:7709-7717.
11. Buschke H., Fuld P.A. Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology 1974, 24:1019-1025.
12. Cabeza R., Daselaar S.M., Dolcos F., Prince S.E., Budde M., Nyberg L. Task-independent and task-specific age effects on brain activity during working memory, visual attention and episodic retrieval. Cereb. Cortex 2004, 14:364-375.
13. Cappell K.A., Gmeindl L., Reuter-Lorenz P.A. Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load. Cortex 2010, 46:462-473.
14. Celone K.A., Calhoun V.D., Dickerson B.C., Atri A., Chua E.F., Miller S.L., DePeau K., Rentz D.M., Selkoe D.J., Blacker D., Albert M.S., Sperling R.A. Alterations in memory networks in mild cognitive impairment and Alzheimer's disease: an independent component analysis. J. Neurosci. 2006, 26:10222-10231.
15. Chen C.J., Chen C.C., Wu D., Chi N.F., Chen P.C., Liao Y.P., Chiu H.W., Hu C.J. Effects of the apolipoprotein E epsilon4 allele on functional MRI during n-back working memory tasks in healthy middle-aged adults. AJNR Am. J. Neuroradiol. 2013, 34:1197-1202.
16. Chetelat G., Villemagne V.L., Bourgeat P., Pike K.E., Jones G., Ames D., Ellis K.A., Szoeke C., Martins R.N., O'Keefe G.J., Salvado O., Masters C.L., Rowe C.C. Relationship between atrophy and beta-amyloid deposition in Alzheimer disease. Ann. Neurol. 2010, 67:317-324.
17. Chetelat G., Villemagne V.L., Pike K.E., Ellis K.A., Bourgeat P., Jones G., O'Keefe G.J., Salvado O., Szoeke C., Martins R.N., Ames D., Masters C.L., Rowe C.C. Independent contribution of temporal beta-amyloid deposition to memory decline in the pre-dementia phase of Alzheimer's disease. Brain 2011, 134(Pt 3):798-807.
18. Csernansky J.G., Hamstra J., Wang L., McKeel D., Price J.L., Gado M., Morris J.C. Correlations between antemortem hippocampal volume and postmortem neuropathology in AD subjects. Alzheimer Dis. Assoc. Disord. 2004, 18:190-195.
19. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999, 9:179-194.
20. de Leon M.J., George A.E., Stylopoulos L.A., Smith G., Miller D.C. Early marker for Alzheimer's disease: the atrophic hippocampus. Lancet 1989, 2:672-673.
21. D'Esposito M., Postle B.R. The cognitive neuroscience of working memory. Annu. Rev. Psychol. 2015, 66:1-28.
22. D'Esposito M., Postle B.R., Rypma B. Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies. Exp. Brain Res. 2000, 133:3-11.
23. Dickerson B.C., Bakkour A., Salat D.H., Feczko E., Pacheco J., Greve D.N., Grodstein F., Wright C.I., Blacker D., Rosas H.D., Sperling R.A., Atri A., Growdon J.H., Hyman B.T., Morris J.C., Fischl B., Buckner R.L. 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 2009, 19:497-510.
24. Dickerson B.C., Salat D.H., Greve D.N., Chua E.F., Rand-Giovannetti E., Rentz D.M., Bertram L., Mullin K., Tanzi R.E., Blacker D., Albert M.S., Sperling R.A. Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 2005, 65:404-411.
25. Elman J.A., Madison C.M., Baker S.L., Vogel J.W., Marks S.M., Crowley S., O'Neil J.P., Jagust W.J. Effects of beta-amyloid on resting state functional connectivity within and between networks reflect known patterns of regional vulnerability. Cereb. Cortex 2014, [Epub ahead of print].
26. Engler H., Forsberg A., Almkvist O., Blomquist G., Larsson E., Savitcheva I., Wall A., Ringheim A., Langstrom B., Nordberg A. Two-year follow-up of amyloid deposition in patients with Alzheimer's disease. Brain 2006, 129(Pt 11):2856-2866.
27. Filippini N., MacIntosh B.J., Hough M.G., Goodwin G.M., Frisoni G.B., Smith S.M., Matthews P.M., Beckmann C.F., Mackay C.E. Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7209-7214.
28. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., van der Kouwe A., Killiany R., Kennedy D., Klaveness S., Montillo A., Makris N., Rosen B., Dale A.M. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002, 33:341-355.
29. Fjell A.M., Walhovd K.B., Fennema-Notestine C., McEvoy L.K., Hagler D.J., Holland D., Blennow K., Brewer J.B., Dale A.M. Brain atrophy in healthy aging is related to CSF levels of Abeta1-42. Cereb. Cortex 2010, 20:2069-2079.
30. Forsberg A., Engler H., Almkvist O., Blomquist G., Hagman G., Wall A., Ringheim A., Langstrom B., Nordberg A. PET imaging of amyloid deposition in patients with mild cognitive impairment. Neurobiol. Aging 2008, 29:1456-1465.
31. Golden C.J. Stroop Color and Word Test 1978, Stolting, Chicago, IL.
32. Grimmer T., Henriksen G., Wester H.J., Forstl H., Klunk W.E., Mathis C.A., Kurz A., Drzezga A. Clinical severity of Alzheimer's disease is associated with PIB uptake in PET. Neurobiol. Aging 2009, 30:1902-1909.
33. Grober E., Sliwinski L. Development and validation of a model for estimating premorbid verbal intelligence in the elderly. J. Clin. Exp. Neuropsychol. 1991, 13:933-949.
34. Habeck C., Rakitin B.C., Moeller J., Scarmeas N., Zarahn E., Brown T., Stern Y. An event-related fMRI study of the neural networks underlying the encoding, maintenance, and retrieval phase in a delayed-match-to-sample task. Brain Res. Cogn. Brain Res. 2005, 23:207-220.
35. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
36. Hedden T., Oh H., Younger A.P., Patel T.A. Meta-analysis of amyloid-cognition relations in cognitively normal older adults. Neurology 2013, 80:1341-1348.
37. Hedden T., Van Dijk K.R., Becker J.A., Mehta A., Sperling R.A., Johnson K.A., Buckner R.L. Disruption of functional connectivity in clinically normal older adults harboring amyloid burden. J. Neurosci. 2009, 29:12686-12694.
38. Huijbers W., Mormino E.C., Wigman S.E., Ward A.M., Vannini P., McLaren D.G., Becker J.A., Schultz A.P., Hedden T., Johnson K.A., Sperling R.A. Amyloid deposition is linked to aberrant entorhinal activity among cognitively normal older adults. J. Neurosci. 2014, 34:5200-5210.
39. Jack C.R., Lowe V.J., Senjem M.L., Weigand S.D., Kemp B.J., Shiung M.M., Knopman D.S., Boeve B.F., Klunk W.E., Mathis C.A., Petersen R.C. 11C PiB and structural MRI provide complementary information in imaging of Alzheimer's disease and amnestic mild cognitive impairment. Brain 2008, 131:665-680.
40. Jack C.R., Lowe V.J., Weigand S.D., Wiste H.J., Senjem M.L., Knopman D.S., Shiung M.M., Gunter J.L., Boeve B.F., Kemp B.J., Weiner M., Petersen R.C. Serial PIB and MRI in normal, mild cognitive impairment and Alzheimer's disease: implications for sequence of pathological events in Alzheimer's disease. Brain 2009, 132:1355-1365.
41. Kemppainen N.M., Aalto S., Wilson I.A., Nagren K., Helin S., Bruck A., Oikonen V., Kailajarvi M., Scheinin M., Viitanen M., Parkkola R., Rinne J.O. PET amyloid ligand [11C]PIB uptake is increased in mild cognitive impairment. Neurology 2007, 68:1603-1606.
42. Koechlin E., Ody C., Kouneiher F. The architecture of cognitive control in the human prefrontal cortex. Science 2003, 302:1181-1185.
43. Landau S.M., Breault C., Joshi A.D., Pontecorvo M., Mathis C.A., Jagust W.J., Mintun M.A. Amyloid-beta imaging with Pittsburgh compound B and florbetapir: comparing radiotracers and quantification methods. J. Nucl. Med. 2013, 54:70-77. Alzheimer's Disease Neuroimaging Initiative.
44. Landau S.M., Fero A., Baker S.L., Koeppe R., Mintun M., Chen K., Reiman E.M., Jagust W.J. Measurement of longitudinal beta-amyloid change with 18F-Florbetapir PET and standardized uptake value ratios. J. Nucl. Med. 2015, 56:567-574.
45. Mattis S. Dementia Rating Scale (DRS) 1988, Psychological Assessment Resources, Odessa, FL.
46. Miller E.K., Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 2001, 24:167-202.
47. Mintun M.A., Larossa G.N., Sheline Y.I., Dence C.S., Lee S.Y., Mach R.H., Klunk W.E., Mathis C.A., DeKosky S.T., Morris J.C. [11C]PIB in a nondemented population: potential antecedent marker of Alzheimer disease. Neurology 2006, 67:446-452.
48. Monsell S.E., Mock C., Hassenstab J., Roe C.M., Cairns N.J., Morris J.C., Kukull W. Neuropsychological changes in asymptomatic persons with Alzheimer disease neuropathology. Neurology 2014, 83:434-440.
49. Mormino E.C., Brandel M.G., Madison C.M., Marks S., Baker S.L., Jagust W.J. Abeta deposition in aging is associated with increases in brain activation during successful memory encoding. Cereb. Cortex 2012, 22:1813-1823.
50. Mormino E.C., Kluth J.T., Madison C.M., Rabinovici G.D., Baker S.L., Miller B.L., Koeppe R.A., Mathis C.A., Weiner M.W., Jagust W.J. Episodic memory loss is related to hippocampal-mediated beta-amyloid deposition in elderly subjects. Brain 2009, 132:1310-1323.
51. Mormino E.C., Smiljic A., Hayenga A.O., Onami S.H., Greicius M.D., Rabinovici G.D., Janabi M., Baker S.L., Yen I.V., Madison C.M., Miller B.L., Jagust W.J. Relationships between beta-amyloid and functional connectivity in different components of the default mode network in aging. Cereb. Cortex 2011, 21:2399-2407.
52. Niendam T.A., Laird A.R., Ray K.L., Dean Y.M., Glahn D.C., Carter C.S. Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn. Affect. Behav. Neurosci. 2012, 12:241-268.
53. Oh H., Jagust W.J. Frontotemporal network connectivity during memory encoding is increased with aging and disrupted by beta-amyloid. J. Neurosci. 2013, 33:18425-18437.
54. Oh H., Madison C., Villeneuve S., Markley C., Jagust W.J. Association of gray matter atrophy with age, beta-amyloid, and cognition in aging. Cereb. Cortex 2014, 24:1609-1618.
55. Oh H., Mormino E.C., Madison C., Hayenga A., Smiljic A., Jagust W.J. Beta-amyloid affects frontal and posterior brain networks in normal aging. Neuroimage 2011, 54:1887-1895.
56. Pike K.E., Savage G., Villemagne V.L., Ng S., Moss S.A., Maruff P., Mathis C.A., Klunk W.E., Masters C.L., Rowe C.C. Beta-amyloid imaging and memory in non-demented individuals: evidence for preclinical Alzheimer's disease. Brain 2007, 130:2837-2844.
57. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N. Engl. J. Med. 2010, 362:329-344.
58. Quiroz Y.T., Budson A.E., Celone K., Ruiz A., Newmark R., Castrillon G., Lopera F., Stern C.E. Hippocampal hyperactivation in presymptomatic familial Alzheimer's disease. Ann. Neurol. 2010, 68:865-875.
59. Reitan R. Manual for Administration of Neuropsychological Test Batteries for Adults and Children 1978, Reitan Neuropsychology Laboratories, Inc, Tucson, AZ.
60. Reuter-Lorenz P.A., Cappell K. Neurocognitive aging and the compensation hypothesis. Curr. Dir. Psychol. Sci. 2008, 18:177-182.
61. Salami A., Eriksson J., Nyberg L. Opposing effects of aging on large-scale brain systems for memory encoding and cognitive control. J. Neurosci. 2012, 32:10749-10757.
62. Sambataro F., Safrin M., Lemaitre H.S., Steele S.U., Das S.B., Callicott J.H., Weinberger D.R., Mattay V.S. Normal aging modulates prefrontoparietal networks underlying multiple memory processes. Eur. J. Neurosci. 2012, 36:3559-3567.
63. Selkoe D.J. Folding proteins in fatal ways. Nature 2003, 426:900-904.
64. Smith E.E., Jonides J. Storage and executive processes in the frontal lobes. Science 1999, 283:1657-1661.
65. Snodgrass J.G., Corwin J. Pragmatics of measuring recognition memory: applications to dementia and amnesia. J. Exp. Psychol. Gen. 1988, 117:34-50.
66. Sperling R.A., Laviolette P.S., O'Keefe K., O'Brien J., Rentz D.M., Pihlajamaki M., Marshall G., Hyman B.T., Selkoe D.J., Hedden T., Buckner R.L., Becker J.A., Johnson K.A. Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 2009, 63:178-188.
67. Spreng R.N., Turner G.R. Structural covariance of the default network in healthy and pathological aging. J. Neurosci. 2013, 33:15226-15234.
68. Stern Y. Cognitive reserve and Alzheimer disease. Alzheimer Dis. Assoc. Disord. 2006, 20:112-117.
69. St-Laurent M., Abdi H., Burianova H., Grady C.L. Influence of aging on the neural correlates of autobiographical, episodic, and semantic memory retrieval. J. Cogn. Neurosci. 2011, 23:4150-4163.
70. Storandt M., Mintun M.A., Head D., Morris J.C. 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. 2009, 66:1476-1481.
71. Tosun D., Schuff N., Mathis C.A., Jagust W., Weiner M.W. Spatial patterns of brain amyloid-beta burden and atrophy rate associations in mild cognitive impairment. Brain 2011, 134(Pt 4):1077-1088.
72. Villemagne V.L., Burnham S., Bourgeat P., Brown B., Ellis K.A., Salvado O., Szoeke C., Macaulay S.L., Martins R., Maruff P., Ames D., Rowe C.C., Masters C.L., Australian Imaging B., Lifestyle Research G. Amyloid beta deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study. Lancet Neurol. 2013, 12:357-367.
73. Wechsler D. Wechsler Adult Intelligence Scale-III 1997, Psychological Corporation, San Antonio, TX.
74. Wishart H.A., Saykin A.J., Rabin L.A., Santulli R.B., Flashman L.A., Guerin S.J., Mamourian A.C., Belloni D.R., Rhodes C.H., McAllister T.W. Increased brain activation during working memory in cognitively intact adults with the APOE epsilon4 allele. Am. J. Psychiatry 2006, 163:1603-1610.
75. Wolk D.A., Price J.C., Saxton J.A., Snitz B.E., James J.A., Lopez O.L., Aizenstein H.J., Cohen A.D., Weissfeld L.A., Mathis C.A., Klunk W.E., De-Kosky S.T. Amyloid imaging in mild cognitive impairment subtypes. Ann. Neurol. 2009, 65:557-568.
76. Zarahn E., Rakitin B., Abela D., Flynn J., Stern Y. Age-related changes in brain activation during a delayed item recognition task. Neurobiol. Aging 2007, 28:784-798.