Disrupted intrinsic networks link amyloid-β pathology and impaired cognition in prodromal Alzheimer's disease

Cerebral Cortex

Volumn 25, Issue 12, 2015, Pages 4678-4688

  Koch, Kathrin ^a,b   Myers, Nicholas E ^a,b,c   Göttler, Jens ^a,b   Pasquini, Lorenzo ^a,b   Grimmer, Timo ^a   Förster, Stefan ^a,b   Manoliu, Andrei ^a,b   Neitzel, Julia ^a,b,d   Kurz, Alexander ^a   Förstl, Hans ^a   Riedl, Valentin ^a,b   Wohlschläger, Afra M ^a,b   Drzezga, Alexander ^e   Sorg, Christian ^a,b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF MUNICH   (Germany)

^e Klinik und Poliklinik für Nuklearmedizin   (Germany)

Author keywords

Amyloid plaques; Impaired cognition; Intrinsic connectivity networks; PiB PET; Prodromal Alzheimer's disease; resting state fMRI; Task fMRI

Indexed keywords

AMYLOID BETA PROTEIN; PITTSBURGH COMPOUND B; 2-(4'-(METHYLAMINO)PHENYL)-6-HYDROXYBENZOTHIAZOLE; ANILINE DERIVATIVE; THIAZOLE DERIVATIVE;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; ATTENTION; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DEFAULT MODE NETWORK; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INTRINSIC CONNECTIVITY NETWORK; MALE; MEMORY; MULTIMODAL IMAGING; NERVE CELL NETWORK; PARIETAL CORTEX; POSITRON EMISSION TOMOGRAPHY; POSTERIOR PARIETAL CORTEX; PRIORITY JOURNAL; PRODROMAL SYMPTOM; REST; STRUCTURAL EQUATION MODELING; TASK PERFORMANCE; BRAIN MAPPING; METABOLISM; MIDDLE AGED; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANILINE COMPOUNDS; ATTENTION; BRAIN MAPPING; COGNITION; COGNITIVE DYSFUNCTION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; POSITRON-EMISSION TOMOGRAPHY; THIAZOLES;

EID: 84954518029     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu151     Document Type: Article

References (63)

1. Agosta F, Pievani M, Geroldi C, Copetti M, Frisoni GB, Filippi M. 2012. Resting state fMRI in Alzheimer's disease: beyond the default mode network. Neurobiol Aging. 33:1564-1578.
2. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC et al. 2011. The diagnosis of mild cognitive impairment due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement. 7:270-279.
3. Allen EA, Erhardt EB, Damaraju E, Gruner W, Segall JM, Silva RF, Havlicek M, Rachakonda S, Fries J, Kalyanam R et al. 2011. A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci. 5:2.
4. Baron RM, Kenny DA. 1986. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 51:1173-1182.
5. Barulli D, Stern Y. 2013. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci. 17:502-509.
6. Berkes P, Orbán G, Lengyel M, Fiser J. 2011. Spontaneous cortical activity reveals hallmarks of an optimal internal model of the environment. Science. 331:83-87.
7. Braak H, Braak E, Bohl J. 1993. Staging of Alzheimer-related cortical destruction. Eur Neurol. 33:403-408.
8. Brett M, Anton J-L, Valabregue R, Poline J-B. 2002. Region of interest analysis using an SPM toolbox [abstract]. Presented at the 8th International Conference on Functional Mapping of the Human Brain, 2-6 June 2002, Sendai, Japan. Available on CD-ROM in NeuroImage. 16(2).
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.
10. Buckner RL, Sepulcre J, Talukdar T, Krienen FM, Liu H, Hedden T, Andrews-Hanna JR, Sperling RA, Johnson KA. 2009. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J Neurosci. 29:1860-1873.
11. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, Staufenbiel M, Konnerth A, Garaschuk O. 2008. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science. 321:1686-1689.
12. Calhoun VD, Adali T, Pearlson GD, Pekar JJ. 2001. Spatial and temporal independent component analysis of functional MRI data containing a pair of task-related waveforms. Hum Brain Mapp. 13:43-53.
13. Calhoun VD, Kiehl KA, Pearlson GD. 2008. Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Hum Brain Mapp. 29:828-838.
14. Celone KA, Calhoun VD, Dickerson BC, Atri A, Chua EF, Miller SL, DePeau K, Rentz DM, Selkoe DJ, Blacker D et al. 2006. Alterations in memory networks in mild cognitive impairment and Alzheimer's disease: an independent component analysis. J Neurosci. 2640:10222-10231.
15. Corbetta M, Shulman GL. 2002. Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 3:215-229.
16. Damoiseaux JS, Rombouts SARB, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF. 2006. Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci. 103:13848-13853.
17. Dannhauser TM, Walker Z, Stevens T, Lee L, Seal M. 2005. The functional anatomy of divided attention in amnestic mild cognitive impairment. Brain. 128:1418-1427.
18. Dickerson BC, Salat DH, Bates JF, Atiya M, Killiany RJ, Greve DN, Dale AM, Stern CE, Blacker D, Albert MS et al. 2004. Medial temporal lobe function and structure in mild cognitive impairment. Ann Neurol. 56:27-35.
19. Dosenbach NUF, Fair DA, Cohen AL, Schlaggar BL, Petersen SE. 2008. A dual-networks architecture of top-down control. Trends Cogn Sci. 12:99-105.
20. Drzezga A, Becker JA, Van Dijk KR, Sreenivasan A, Talukdar T, Sullivan C, Schultz AP, Sepulcre J, Putcha D, Greve D et al. 2011. Neuronal dysfunction and disconnection of cortical hubs in non-demented subjects with elevated amyloid burden. Brain. 134: 1635-1646.
21. Dubois B, Feldman HH, Jacova C, DeKosky ST, Barberger-Gateau P, Cummings J, Delacourte A, Galasko D, Gauthier S, Jicha G et al. 2007. Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS-ADRDA criteria. Lancet Neurol. 6:734-746.
22. Eichele T, Debener S, Calhoun VD, Specht K, Engel AK, Hugdahl K, von Cramon DY, Ullsperger M. 2008. Prediction of human errors by maladaptive changes in event-related brain networks. Proc Natl Acad Sci. 105:6173-6178.
23. Engler H, Forsberg A, Almkvist O, Blomquist G, Larsson E, Savitcheva I, Wall A, Ringheim A, Långström B, Nordberg A. 2006. Two-year follow-up of amyloid deposition in patients with Alzheimer's disease. Brain. 129:2856-2866.
24. Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, Hall K, Hasegawa K, Hendrie H, Huang Y et al. 2005. Global prevalence of dementia: a Delphi consensus study. Lancet. 366:2112-2117.
25. Fox MD, Raichle ME. 2007. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci. 8:700-711.
26. Gauthier S, Reisberg B, Zaudig M, Petersen RC, Ritchie K, Broich K, Belleville S, Brodaty H, Bennett D, Chertkow H et al. 2006. Mild cognitive impairment. Lancet. 367:1262-1270.
27. Gitelman DR, Nobre AC, Parrish TB, LaBar KS, Kim Y-H, Meyer JR, Mesulam MM. 1999. A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. Brain. 122:1093-1106.
28. Greicius MD, Srivastava G, Reiss AL, Menon V. 2004. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci. 101:4637-4642.
29. Grimmer T, Henriksen G, Wester HJ, Förstl H, Klunk WE, Mathis CA, Kurz A, Drzezga A. 2009. Clinical severity of Alzheimer's disease is associated with PIB uptake in PET. Neurobiol Aging. 30:1902-1909.
30. Hansson O, Zetterberg H, Buchhave P, Londos E, Blennow K, Minthon L. 2006. Association between CSF biomarkers and incipient Alzheimer's disease in patients with mild cognitive impairment: a follow-up study. Lancet Neurol. 5:228-234.
31. Hedden T, Van Dijk KRA, 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.
32. Ikonomovic MD, Klunk WE, Abrahamson EE, Wuu J, Mathis CA, Scheff SW, Mufson EJ, DeKosky ST. 2011. Precuneus amyloid burden is associated with reduced cholinergic activity in Alzheimer disease. Neurology. 77:39-47.
33. Karrasch M, Sinervä E, Grönholm P, Rinne J, Laine M. 2005. CERAD test performances in amnestic mild cognitive impairment and Alzheimer's disease. Acta Neurol Scand. 111:172-179.
34. Laird AR, Fox PM, Eickhoff SB, Turner JA, Ray KL, McKay DR, Glahn DC, Beckmann CF, Smith SM, Fox PT. 2011. Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci. 23: 4022-4037.
35. Lewis CM, Baldassarre A, Committeri G, Romani GL, Corbetta M. 2009. Learning sculpts the spontaneous activity of the resting human brain. Proc Natl Acad Sci USA. 106:17558-17563.
36. Li R, Wu X, Fleisher AS, Reiman EM, Chen K, Yao L. 2011. Attention-related networks in Alzheimer's disease: a resting functional MRI study. Hum Brain Mapp. 33:1076-1088.
37. Lustig C, Buckner RL. 2004. Preserved neural correlates of priming in old age and dementia. Neuron. 42:865-875.
38. Mandal PK. 2012. Predictive biomarkers for Alzheimer's disease using state-of-the-art brain imaging techniques. J Alzheimer's Dis. 31: S1-S3.
39. 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. 21:2399-2407.
40. Morris JC. 1993. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology. 43:2412-2414.
41. Morris JC, Heyman A, Mohs RC, Hughes JP. 1989. The consortium to establish a registry for Alzheimer's disease (CERAD): I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology. 39:1159-1165.
42. 18F-FDG PET diagnosis of mild cognitive impairment, Alzheimer's disease, and other dementias. J Nucl Med. 49:390-398.
43. Myers N, Pasquini L, Göttler J, Grimmer T, Koch K, Ortner M, Neitzel J, Mühlau M, Förster S, Kurz A et al. 2014. Within-patient correspondence of amyloid-β and intrinsic network connectivity in Alzheimer's disease. Brain. doi:10.1093/brain/awu103.
44. Nelson PT, Abner EL, Scheff SW, Schmitt FA, Kryscio RJ, Jicha GA, Smith CD, Patel E, Markesbery WR. 2009. Alzheimer's-type neuro-pathology in the precuneus is not increased relative to other areas of neocortex across a range of cognitive impairment. Neurosci Lett. 450:336-339.
45. Neufang S, Akhrif A, Riedl V, Förstl H, Kurz A. 2011. Disconnection of frontal and parietal areas contributes to impaired attention in very early Alzheimer's disease. J Alzheimer's Dis. 25:309-321.
46. Nobre AC, Sebestyen GN, Gitelman DR, Mesulam MM, Frackowiak RS, Frith CD. 1997. Functional localization of the system for visuospatial attention using positron emission tomography. Brain. 120:515-533.
47. Palop JJ, Mucke L. 2010. Amyloid-β-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci. 13:812-818.
48. Perez SE, He B, Nadeem M, Wuu J, Scheff SW, Abrahamson EE, Ikono-movic MD, Mufson EJ. 2014. Resilience of precuneus neurotrophic signaling pathways despite amyloid pathology in prodromal Alzheimer's disease. Biol Psychiatry. doi:10.1016/j.biopsych.2013. 12.016.
49. Petrella JR, Wang L, Krishnan S, Slavin MJ, Prince SE, Tran TTT, Dorais-wamy PM. 2007. Cortical deactivation in mild cognitive impairment: high-field-strength functional MR imaging. Radiology. 245:224-235.
50. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. 2012. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage. 59:2142-2154.
51. Raichle ME. 2011. The restless brain. Brain Connectivity. 1:3-12.
52. Riedl V, Valet M, Wöller A, Sorg C, Vogel D, Sprenger T, Boecker H, Wohlschläger AM, Tölle TR. 2011. Repeated pain induces adaptations of intrinsic brain activity to reflect past and predict future pain. NeuroImage. 57:206-213.
53. Rombouts SARB, Barkhof F, Goekoop R, Stam CJ, Scheltens P. 2005. Altered resting state networks in mild cognitive impairment and mild Alzheimer's disease: an fMRI study. Hum Brain Mapp. 26:231-239.
54. Scheff SW, Price DA, Schmitt FA, Roberts KN, Ikonomovic MD, Mufson EJ. 2013. Synapse stability in the precuneus early in the progression of Alzheimer's disease. J Alzheimers Dis. 35:599-609.
55. Schlösser RGM, Koch K, Wagner G. 2007. Assessing the state space of the brain with fMRI: an integrative view of current methods. Phar-macopsychiatry. 40:85-92.
56. Selkoe DJ. 2002. Alzheimer's disease is a synaptic failure. Science. 298:789-791.
57. Sheline YI, Raichle ME, Snyder AZ, Morrise JC, Head D, Wang S, Mintun MA. 2010. Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol Psychiatry. 67:584-587.
58. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR et al. 2009. Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci. 106:13040-13045.
59. Sorg C, Riedl V, Mühlau M, Calhoun VD, Eichele T, Laer L, Drzezga A, Förstl H, Kurz A, Zimmer C et al. 2007. Selective changes of resting-state networks in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci. 104:18760-18765.
60. Sorg C, Riedl V, Perneczky R, Kurz A, Wohlschläger AM. 2009. Impact of Alzheimer's disease on the functional connectivity of spontaneous brain activity. Curr Alzheimer Res. 6:541-553.
61. Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, LaViolette PS, Vitolo OV, Hedden T, Becker JA, Rentz DM, Selkoe DJ et al. 2010. Functional alterations in memory networks in early Alzheimer's disease. Neuro Mol Med. 12:27-43.
62. 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.
63. Van Dijk KRA, Sabuncu MR, Buckner RL. 2012. The influence of head motion on intrinsic functional connectivity MRI. NeuroImage. 59:431-438.