Amyloid Deposition Is Associated with Impaired Default Network Function in Older Persons without Dementia

Neuron

Volumn 63, Issue 2, 2009, Pages 178-188

  Sperling, Reisa A ^a   LaViolette, Peter S ^a   O'Keefe, Kelly ^a   O'Brien, Jacqueline ^a   Rentz, Dorene M ^a   Pihlajamaki, Maija ^a   Marshall, Gad ^a   Hyman, Bradley T ^a   Selkoe, Dennis J ^a   Hedden, Trey ^a,b   Buckner, Randy L ^a,b,c   Becker, J Alex ^a   Johnson, Keith A ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

HUMDISEASE; MOLNEURO; SYSNEURO

Indexed keywords

AMYLOID BETA PROTEIN;

ADULT; AGE; AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IN VIVO STUDY; MALE; PRIORITY JOURNAL;

ADULT; AGED; AGED, 80 AND OVER; AMYLOID BETA-PROTEIN; COGNITION; DEMENTIA; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MICROSCOPY, ELECTRON; NERVE NET; NEURONS;

EID: 67650875899     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2009.07.003     Document Type: Article

References (73)

1. Aizenstein H.J., Nebes R.D., Saxton J.A., Price J.C., Mathis C.A., Tsopelas N.D., Ziolko S.K., James J.A., Snitz B.E., Houck P.R., et al. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch. Neurol. 65 (2008) 1509-1517
2. Andrews-Hanna J.R., Snyder A.Z., Vincent J.L., Lustig C., Head D., Raichle M.E., and Buckner R.L. Disruption of large-scale brain systems in advanced aging. Neuron 56 (2007) 924-935
3. Arriagada P.V., Marzloff K., and Hyman B.T. Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease. Neurology 42 (1992) 1681-1688
4. Bai F., Zhang Z., Yu H., Shi Y., Yuan Y., Zhu W., Zhang X., and Qian Y. Default-mode network activity distinguishes amnestic type mild cognitive impairment from healthy aging: a combined structural and resting-state functional MRI study. Neurosci. Lett. 438 (2008) 111-115
5. Baig S., Wilcock G.K., and Love S. Loss of perineuronal net N-acetylgalactosamine in Alzheimer's disease. Acta Neuropathol. (Berl.) 110 (2005) 393-401
6. Bennett D., Schneider J., Arvanitakis Z., Kelly J., Aggarwal N., Shah R., and Wilson R. Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology 66 (2006) 1837-1844
7. Bondi M.W., Houston W.S., Eyler L.T., and Brown G.G. fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease. Neurology 64 (2005) 501-508
8. Bookheimer S.Y., Strojwas M.H., Cohen M.S., Saunders A.M., Pericak-Vance M.A., Mazziotta J.C., and Small G.W. Patterns of brain activation in people at risk for Alzheimer's disease. N. Engl. J. Med. 343 (2000) 450-456
9. 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., and Mintun M.A. Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J. Neurosci. 25 (2005) 7709-7717
10. Buckner R.L., Andrews-Hanna J.R., and Schacter D.L. The brain's default network: Anatomy, function, and relevance to disease. Ann. N Y Acad. Sci. 1124 (2008) 1-38
11. Buckner R.L., Sepulcre J., Talukdar T., Krienen F., Liu H., Hedden T., Andrews-Hanna J., Sperling R.A., and Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: Mapping, assessment of stability, and relation to Alzheimer's disease. J. Neurosci. 29 (2009) 1860-1873
12. Busche M.A., Eichhoff G., Adelsberger H., Abramowski D., Wiederhold K.H., Haass C., Staufenbiel M., Konnerth A., and Garaschuk O. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321 (2008) 1686-1689
13. 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., et al. Alterations in memory networks in mild cognitive impairment and Alzheimer's disease: an independent component analysis. J. Neurosci. 26 (2006) 10222-10231
14. Chua E.F., Schacter D.L., Rand-Giovannetti E., and Sperling R.A. Understanding metamemory: neural correlates of the cognitive process and subjective level of confidence in recognition memory. Neuroimage 29 (2006) 1150-1160
15. Cirrito J.R., Yamada K.A., Finn M.B., Sloviter R.S., Bales K.R., May P.C., Schoepp D.D., Paul S.M., Mennerick S., and Holtzman D.M. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 48 (2005) 913-922
16. Daselaar S.M., Veltman D.J., Rombouts S.A., Raaijmakers J.G., and Jonker C. Neuroanatomical correlates of episodic encoding and retrieval in young and elderly subjects. Brain 126 (2003) 43-56
17. Daselaar S.M., Prince S.E., and Cabeza R. When less means more: deactivations during encoding that predict subsequent memory. Neuroimage 23 (2004) 921-927
18. Dickerson B.C., Salat D.H., Bates J.F., Atiya M., Killiany R.J., Greve D.N., Dale A.M., Stern C.E., Blacker D., Albert M.S., and Sperling R.A. Medial temporal lobe function and structure in mild cognitive impairment. Ann. Neurol. 56 (2004) 27-35
19. Dickerson B.C., Salat D., Greve D., Chua E., Rand-Giovannetti E., Rentz D., Bertram L., Mullin K., Tanzi R., Blacker D., et al. Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 65 (2005) 404-411
20. 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., et al. 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 (2009) 497-510
21. Duverne S., Motamedinia S., and Rugg M.D. The relationship between aging, performance, and the neural correlates of successful memory encoding. Cereb. Cortex 19 (2008) 733-744
22. Fischl B., van der Kouwe A., Destrieux C., Halgren E., Segonne F., Salat D.H., Busa E., Seidman L.J., Goldstein J., Kennedy D., et al. Automatically parcellating the human cerebral cortex. Cereb. Cortex 14 (2004) 11-22
23. Fotenos A.F., Mintun M.A., Snyder A.Z., Morris J.C., and Buckner R.L. Brain volume decline in aging: evidence for a relation between socioeconomic status, preclinical Alzheimer disease, and reserve. Arch. Neurol. 65 (2008) 113-120
24. Fransson P., and Marrelec G. The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis. Neuroimage 42 (2008) 1178-1184
25. Freire L., and Mangin J.F. Motion correction algorithms may create spurious brain activations in the absence of subject motion. Neuroimage 14 (2001) 709-722
26. Gomperts S.N., Rentz D.M., Moran E., Becker J.A., Locascio J.J., Klunk W.E., Mathis C.A., Elmaleh D.R., Shoup T., Fischman A.J., et al. Imaging amyloid deposition in Lewy body diseases. Neurology 71 (2008) 903-910
27. Greicius M.D., Srivastava G., Reiss A.L., and Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. USA 101 (2004) 4637-4642
28. Greicius M.D., Supekar K., Menon V., and Dougherty R.F. Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb. Cortex 19 (2009) 72-78
29. Hagmann P., Cammoun L., Gigandet X., Meuli R., Honey C.J., Wedeen V.J., and Sporns O. Mapping the structural core of human cerebral cortex. PLoS Biol. 6 (2008) e159
30. Hyman B.T., Van Hoesen G.W., Damasio A.R., and Barnes C.L. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225 (1984) 1168-1170
31. Hyman B.T., Marzloff K., Wenniger J.J., Dawson T.M., Bredt D.S., and Snyder S.H. Relative sparing of nitric oxide synthase-containing neurons in the hippocampal formation in Alzheimer's disease. Ann. Neurol. 32 (1992) 818-820
32. Jagust W., Gitcho A., Sun F., Kuczynski B., Mungas D., and Haan M. Brain imaging evidence of preclinical Alzheimer's disease in normal aging. Ann. Neurol. 59 (2006) 673-681
33. Johnson K.A., and Albert M.S. Perfusion abnormalities in prodromal AD. Neurobiol. Aging 21 (2000) 289-292
34. Johnson K.A., Jones K., Holman B.L., Becker J.A., Spiers P.A., Satlin A., and Albert M.S. Preclinical prediction of Alzheimer's disease using SPECT. Neurology 50 (1998) 1563-1571
35. Johnson N.A., Jahng G.H., Weiner M.W., Miller B.L., Chui H.C., Jagust W.J., Gorno-Tempini M.L., and Schuff N. Pattern of cerebral hypoperfusion in Alzheimer disease and mild cognitive impairment measured with arterial spin-labeling MR imaging: initial experience. Radiology 234 (2005) 851-859
36. Johnson K.A., Gregas M., Becker J.A., Kinnecom C., Salat D.H., Moran E.K., Smith E.E., Rosand J., Rentz D.M., Klunk W.E., et al. Imaging of amyloid burden and distribution in cerebral amyloid angiopathy. Ann. Neurol. 62 (2007) 229-234
37. Kircher T.T., Weis S., Freymann K., Erb M., Jessen F., Grodd W., Heun R., and Leube D.T. Hippocampal activation in patients with mild cognitive impairment is necessary for successful memory encoding. J. Neurol. Neurosurg. Psychiatry 78 (2007) 812-818
38. Klunk W.E., Engler H., Nordberg A., Wang Y., Blomqvist G., Holt D.P., Bergstrom M., Savitcheva I., Huang G.F., Estrada S., et al. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann. Neurol. 55 (2004) 306-319
39. Lustig C., Snyder A.Z., Bhakta M., O'Brien K.C., McAvoy M., Raichle M.E., Morris J.C., and Buckner R.L. Functional deactivations: change with age and dementia of the Alzheimer type. Proc. Natl. Acad. Sci. USA 100 (2003) 14504-14509
40. Mathis C.A., Bacskai B.J., Kajdasz S.T., McLellan M.E., Frosch M.P., Hyman B.T., Holt D.P., Wang Y., Huang G.F., Debnath M.L., and Klunk W.E. A lipophilic thioflavin-T derivative for positron emission tomography (PET) imaging of amyloid in brain. Bioorg. Med. Chem. Lett. 12 (2002) 295-298
41. McKhann G., Drachman D., Folstein M., Katzman R., Price D., and Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34 (1984) 939-944
42. Meyer-Luehmann M., Spires-Jones T.L., Prada C., Garcia-Alloza M., de Calignon A., Rozkalne A., Koenigsknecht-Talboo J., Holtzman D.M., Bacskai B.J., and Hyman B.T. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 451 (2008) 720-724
43. Miller S.L., Fenstermacher E., Bates J., Blacker D., Sperling R.A., and Dickerson B.C. Hippocampal activation in adults with mild cognitive impairment predicts subsequent cognitive decline. J. Neurol. Neurosurg. Psychiatry 79 (2007) 365-630
44. Miller S.L., Celone K., DePeau K., Diamond E., Dickerson B.C., Rentz D., Pihlajamaki M., and Sperling R.A. Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation. Proc. Natl. Acad. Sci. USA 105 (2008) 2181-2186
45. Miller S.L., Fenstermacher E., Bates J., Blacker D., Sperling R.A., and Dickerson B.C. Hippocampal activation in adults with mild cognitive impairment predicts subsequent cognitive decline. J. Neurol. Neurosurg. Psychiatry 79 (2008) 630-635
46. Minoshima S., Giordani B., Berent S., Frey K.A., Foster N.L., and Kuhl D.E. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann. Neurol. 42 (1997) 85-94
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., and Morris J.C. [11C]PIB in a nondemented population: potential antecedent marker of Alzheimer disease. Neurology 67 (2006) 446-452
48. 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., and Jagust W.J. Episodic memory loss is related to hippocampal-mediated {beta}-amyloid deposition in elderly subjects. Brain 132 (2008) 1310-1323
49. Morris J.C., Storandt M., McKeel Jr. D.W., Rubin E.H., Price J.L., Grant E.A., and Berg L. Cerebral amyloid deposition and diffuse plaques in "normal" aging: Evidence for presymptomatic and very mild Alzheimer's disease. Neurology 46 (1996) 707-719
50. Morris J.C., Weintraub S., Chui H.C., Cummings J., Decarli C., Ferris S., Foster N.L., Galasko D., Graff-Radford N., Peskind E.R., et al. The Uniform Data Set (UDS): clinical and cognitive variables and descriptive data from Alzheimer Disease Centers. Alzheimer Dis. Assoc. Disord. 20 (2006) 210-216
51. Otten L.J., and Rugg M.D. Task-dependency of the neural correlates of episodic encoding as measured by fMRI. Cereb. Cortex 11 (2001) 1150-1160
52. Palop J.J., Chin J., Roberson E.D., Wang J., Thwin M.T., Bien-Ly N., Yoo J., Ho K.O., Yu G.Q., Kreitzer A., et al. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55 (2007) 697-711
53. Persson J., Lind J., Larsson A., Ingvar M., Sleegers K., Van Broeckhoven C., Adolfsson R., Nilsson L.G., and Nyberg L. Altered deactivation in individuals with genetic risk for Alzheimer's disease. Neuropsychologia 46 (2008) 1679-1687
54. Petersen R.C. Mild cognitive impairment as a diagnostic entity. J. Intern. Med. 256 (2004) 183-194
55. Petersen R.C., Doody R., Kurz A., Mohs R.C., Morris J.C., Rabins P.V., Ritchie K., Rossor M., Thal L., and Winblad B. Current concepts in mild cognitive impairment. Arch. Neurol. 58 (2001) 1985-1992
56. Petrella J.R., Prince S.E., Wang L., Hellegers C., and Doraiswamy P.M. Prognostic value of posteromedial cortex deactivation in mild cognitive impairment. PLoS ONE 2 (2007) e1104
57. Pihlajamaki M., Depeau K.M., Blacker D., and Sperling R.A. Impaired medial temporal repetition suppression is related to failure of parietal deactivation in Alzheimer disease. Am. J. Geriatr. Psychiatry 16 (2008) 283-292
58. Pihlajamaki M., O'Keefe K., Bertram L., Tanzi R., Dickerson B., Blacker D., Albert M., and Sperling R. Evidence of altered posteromedial cortical fMRI activity in subjects at risk for Alzheimer disease. Alzheimer Dis. Assoc. Disord. (2009) 10.1097/WAD.0b013e3181a785c9 in press. Published online June 30, 2009
59. Pike K.E., Savage G., Villemagne V.L., Ng S., Moss S.A., Maruff P., Mathis C.A., Klunk W.E., Masters C.L., and Rowe C.C. Beta-amyloid imaging and memory in non-demented individuals: evidence for preclinical Alzheimer's disease. Brain 130 (2007) 2837-2844
60. Price J.C., Klunk W.E., Lopresti B.J., Lu X., Hoge J.A., Ziolko S.K., Holt D.P., Meltzer C.C., DeKosky S.T., and Mathis C.A. Kinetic modeling of amyloid binding in humans using PET imaging and Pittsburgh Compound-B. J. Cereb. Blood Flow Metab. 25 (2005) 1528-1547
61. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., and Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. USA 98 (2001) 676-682
62. Reiman E.M., Caselli R.J., Chen K., Alexander G.E., Bandy D., and Frost J. Declining brain activity in cognitively normal apolipoprotein E varepsilon 4 heterozygotes: A foundation for using positron emission tomography to efficiently test treatments to prevent Alzheimer's disease. Proc. Natl. Acad. Sci. USA 98 (2001) 3334-3339
63. Rombouts S.A., Barkhof F., Goekoop R., Stam C.J., and Scheltens P. Altered resting state networks in mild cognitive impairment and mild Alzheimer's disease: an fMRI study. Hum. Brain Mapp. 26 (2005) 231-239
64. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14 (2008) 837-842
65. Shulman G.L., Fiez J.A., Corbetta M., Buckner R.L., Miezin F.M., Raichle M.E., and Petersen S.E. Common blood flow changes across visual tasks: Decreases in cerebral cortex. J. Cogn. Neurosci. 9 (1997) 648-663
66. Sojkova J., Beason-Held L., Zhou Y., An Y., Kraut M.A., Ye W., Ferrucci L., Mathis C.A., Klunk W.E., Wong D.F., and Resnick S.M. Longitudinal cerebral blood flow and amyloid deposition: an emerging pattern?. J. Nucl. Med. 49 (2008) 1465-1471
67. Sorg C., Riedl V., Muhlau M., Calhoun V.D., Eichele T., Laer L., Drzezga A., Forstl H., Kurz A., Zimmer C., and Wohlschlager A.M. Selective changes of resting-state networks in individuals at risk for Alzheimer's disease. Proc. Natl. Acad. Sci. USA 104 (2007) 18760-18765
68. Sperling R., Chua E., Cocchiarella A., Rand-Giovannetti E., Poldrack R., Schacter D.L., and Albert M. Putting names to faces: successful encoding of associative memories activates the anterior hippocampal formation. Neuroimage 20 (2003) 1400-1410
69. Svoboda E., McKinnon M.C., and Levine B. The functional neuroanatomy of autobiographical memory: a meta-analysis. Neuropsychologia 44 (2006) 2189-2208
70. Vincent J.L., Snyder A.Z., Fox M.D., Shannon B.J., Andrews J.R., Raichle M.E., and Buckner R.L. Coherent spontaneous activity identifies a hippocampal-parietal memory network. J. Neurophysiol. 96 (2006) 3517-3531
71. Vul E., Harris C., Winkielman P., and Pashler H. Puzzlingly high correlations in fMRI studies of emotion. Personality and Social Cognition 3 (2009) 274-290
72. Wagner A.D., Shannon B.J., Kahn I., and Buckner R.L. Parietal lobe contributions to episodic memory retrieval. Trends Cogn. Sci. 9 (2005) 445-453
73. Walsh D.M., and Selkoe D.J. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44 (2004) 181-193