Functional connectivity and graph theory in preclinical Alzheimer's disease

Neurobiology of Aging

Volumn 35, Issue 4, 2014, Pages 757-768

  Brier, Matthew R ^a   Thomas, Jewell B ^a   Fagan, Anne M ^a,b   Hassenstab, Jason ^a,b   Holtzman, David M ^a,b   Benzinger, Tammie L ^a,b   Morris, John C ^a,b   Ances, Beau M ^a,b,c  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

Alzheimer's disease; Biomarker; Functional connectivity; Graph theory; Resting state

Indexed keywords

ADULT; AGED; AGING; ALZHEIMER DISEASE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CEREBROSPINAL FLUID ANALYSIS; CLINICAL ASSESSMENT; COGNITIVE DEFECT; CONNECTOME; CONTROLLED STUDY; DISEASE MARKER; DISEASE SEVERITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAPH THEORY; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; IMAGE QUALITY; MAJOR CLINICAL STUDY; MALE; MATHEMATICAL AND STATISTICAL PROCEDURES; MIDDLE AGED; NERVOUS SYSTEM PARAMETERS; PRIORITY JOURNAL; VERY ELDERLY;

ALZHEIMER'S DISEASE; BIOMARKER; FUNCTIONAL CONNECTIVITY; GRAPH THEORY; RESTING-STATE;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; BRAIN; BRAIN MAPPING; COGNITION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; SEVERITY OF ILLNESS INDEX; TAU PROTEINS;

EID: 84891371277     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.10.081     Document Type: Article

References (59)

1. Achard S., Bullmore E. Efficiency and cost of economical brain functional networks. PLoS Comput. Biol. 2007, 3:e17.
2. Bai F., Shu N., Yuan Y., Shi Y., Yu H., Wu D., Wang J., Xia M., He Y., Zhang Z. Topologically convergent and divergent structural connectivity patterns between patients with remitted geriatric depression and amnestic mild cognitive impairment. J.Neurosci. 2012, 32:4307-4318.
3. Beckmann C.F., DeLuca M., Devlin J.T., Smith S.M. Investigations into resting-state connectivity using independent component analysis. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2005, 360:1001-1013.
4. Berg L., McKeel D.W., Miller J., et al. Clinicopathologic Studies in Cognitively Healthy Aging and Alzheimer Disease: Relation of Histologic Markers to Dementia Severity, Age, Sex, and Apolipoprotein E Genotype. Arch Neurol. 1998, 55:326-335. 10.1001/archneur.55.3.326.
5. Bero A.W., Yan P., Roh J.H., Cirrito J.R., Stewart F.R., Raichle M.E., Lee J.M., Holtzman D.M. Neuronal activity regulates the regional vulnerability to amyloid-B deposition. Nautre Neuroscience 2011, 14:750-756.
6. Bero A.W., Bauer A.Q., Stewart F.R., White B.R., Cirrito J.R., Raichle M.E., Culver J.P., Holtzman D.M. Bidirectional relationship between functional connectivity and amyloid- deposition in mouse brain. J.Neurosci. 2012, 32:4334-4340.
7. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
8. Blennow K., de Leon M.J., Zetterberg H. Alzheimer's disease. Lancet 2006, 368:387-403.
9. Braak H., Thal D.R., Ghebremedhin E., Del Tredici K. Stages of the pathologic process in Alzheimer disease: age categories from 1 to 100 years. J.Neuropathol. Exp. Neurol. 2011, 70:960-969.
10. Brier M.R., Thomas J.B., Snyder A.Z., Benzinger T.L., Zhang D., Raichle M.E., Holtzman D.M., Morris J.C., Ances B.M. Loss of intranetwork and internetwork resting state functional connections with Alzheimer's disease progression. J.Neurosci. 2012, 32:8890-8899.
11. Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., Andrews-Hanna J.R., Sperling R.A., Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. J.Neurosci. 2009, 29:1860-1873.
12. Ciftçi K. Minimum spanning tree reflects the alterations of the default mode network during Alzheimer's disease. Ann. Biomed. Eng. 2011, 39:1493-1504.
13. Dosenbach N.U.F., Nardos B., Cohen A.L., Fair D.A., Power J.D., Church J.A., Nelson S.M., Wig G.S., Vogel A.C., Lessov-Schlaggar C.N., Barnes K.A., Dubis J.W., Feczko E., Coalson R.S., Pruett J.R., Barch D.M., Petersen S.E., Schlaggar B.L. Prediction of individual brain maturity using fMRI. Science 2010, 329:1358-1361.
14. Duchek J.M., Balota D.A., Thomas J.B., Snyder A.Z., Rich P., Benzinger T.L., Fagan A.M., Holtzman D.M., Morris J.C., Ances B.M. Relationship between Stroop performance and resting state functional connectivity in cognitively normal older adults. Neuropsychology 2013, 27:516-528.
15. Erdos P, Rényi A. 1959. On random graphs. Publicationes Mathematicae Debrecen 6, 290-297.
16. Fagan A.M., Mintun M.A., Mach R.H., Lee S.-Y., Dence C.S., Shah A.R., LaRossa G.N., Spinner M.L., Klunk W.E., Mathis C.A., DeKosky S.T., Morris J.C., Holtzman D.M. Inverse relation between invivo amyloid imaging load and cerebrospinal fluid Abeta42 in humans. Ann. Neurol. 2006, 59:512-519.
17. Folstein M.F., Folstein S.E., McHugh P.R. "Mini-mental state." A practical method for grading the cognitive state of patients for the clinician. J.Psychiatr. Res. 1975, 12:189-198.
18. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A 2005, 102:9673-9678.
19. Fox M.D., Zhang D., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. J.Neurophysiol. 2009, 101:3270-3283.
20. Greicius M.D., Srivastava G., Reiss A.L., Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U.S.A 2004, 101:4637-4642.
21. Hedden T., Van Dijk K.R.A., 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.
22. Hlinka J., Paluš M., Vejmelka M., Mantini D., Corbetta M. Functional connectivity in resting-state fMRI: is linear correlation sufficient?. Neuroimage 2011, 54:2218-2225.
23. Holtzman D.M., Morris J.C., Goate A.M. Alzheimer's disease: the challenge of the second century. Sci. Transl Med. 2011, 3:77sr1.
24. Humphries M.D., Gurney K. Network "small-world-ness": a quantitative method for determining canonical network equivalence. PLoS ONE 2008, 3:e0002051.
25. Jack C.R., Knopman D.S., Weigand S.D., Wiste H.J., Vemuri P., Lowe V., Kantarci K., Gunter J.L., Senjem M.L., Ivnik R.J., Roberts R.O., Rocca W.A., Boeve B.F., Petersen R.C. An operational approach to National Institute on Aging-Alzheimer's Association criteria for preclinical Alzheimer disease. Ann. Neurol. 2012, 71:765-775.
26. Jack C.R., Vemuri P., Wiste H.J., Weigand S.D., Aisen P.S., Trojanowski J.Q., Shaw L.M., Bernstein M.A., Petersen R.C., Weiner M.W., Knopman D.S., for the Alzheimer's Disease Neuroimaging Initiative Evidence for ordering of Alzheimer disease biomarkers. Arch. Neurol. 2011, 68:1526-1535.
27. Kaiser M. Atutorial in connectome analysis: topological and spatial features of brain networks. Neuroimage 2011, 57:892-907.
28. Latora V., Marchiori M. Efficient behavior of small-world networks. Phys. Rev. Lett. 2001, 87:198701.
29. Lo C.Y., Wang P.N., Chou K.H., Wang J., He Y., Lin C.P. Diffusion tensor tractography reveals abnormal topological organization in structural cortical networks in Alzheimer's disease. J.Neurosci. 2010, 30:16876-16885.
30. McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease. Neurology 1984, 34:939-944.
31. Meunier D., Achard S., Morcom A., Bullmore E. Age-related changes in modular organization of human brain functional networks. Neuroimage 2009, 44:715-723.
32. Morris J.C. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 1993, 43:2412-2414.
33. Newman M. 2003. The structure and function of complex networks. SIAM review.
34. Newman M.E.J., Girvan M. Finding and evaluating community structure in networks. Phys. Rev. E Stat. Nonlin Soft Matter Phys. 2004, 69:026113.
35. Ojemann J., Buckner R., Corbetta M. Imaging studies of memory and attention. Neurosurg. Clin. N. Am. 1997, 8:307-319.
36. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Petersen S.E. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012, 59:2142-2154.
37. Power J.D., Cohen A.L., Nelson S.M., Wig G.S., Barnes K.A., Church J.A., Vogel A.C., Laumann T.O., Miezin F.M., Schlaggar B.L., Petersen S.E. Functional network organization of the human brain. Neuron 2011, 72:665-678.
38. Price J.L., McKeel D.W., Buckles V.D., Roe C.M., Xiong C., Grundman M., Hansen L.A., Petersen R.C., Parisi J.E., Dickson D.W., Smith C.D., Davis D.G., Schmitt F.A., Markesbery W.R., Kaye J., Kurlan R., Hulette C., Kurland B.F., Higdon R., Kukull W., Morris J.C. Neuropathology of nondemented aging: presumptive evidence for preclinical Alzheimer disease. Neurobiol. Aging 2009, 30:1026-1036.
39. Price J.L., Morris J.C. Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann. Neurol. 1999, 45:358-368.
40. Reitz C., Brayne C., Mayeux R. Epidemiology of Alzheimer disease. Nat. Rev. Neurol. 2011, 7:137-152.
41. Rubinov M., Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage 2010, 52:1059-1069.
42. Salvador R., Suckling J., Coleman M.R., Pickard J.D., Menon D., Bullmore E. Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb. Cortex 2004, 15:1332-1342.
43. Sanz-Arigita E.J., Schoonheim M.M., Damoiseaux J.S., Rombouts S.A.R.B., Maris E., Barkhof F., Scheltens P., Stam C.J. Loss of 'small-world' networks in Alzheimer's disease: graph analysis of FMRI resting-state functional connectivity. PLoS ONE 2010, 5:e13788.
44. Seeley W.W., Crawford R.K., Zhou J., Miller B.L., Greicius M.D. Neurodegenerative diseases target large-scale human brain networks. Neuron 2009, 62:42-52.
45. Sheline Y.I., Raichle M.E., Snyder A.Z., Morris J.C., Head D., Wang S., Mintun M.A. Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol. Psychiatry 2010, 67:584-587.
46. Shulman G., Fiez J., Corbetta M. Common blood flow changes across visual tasks: I. increases in subcortical structures and cerebellum but not in nonvisual cortex. J.Cogn. Neurosci. 1997, 9:624-647.
47. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U.S.A 2009, 106:13040-13045.
48. Sperling R.A., Aisen P.S., Beckett L.A., Bennett D.A., Craft S., Fagan A.M., Iwatsubo T., Jack C.R., Kaye J., Montine T.J., Park D.C., Reiman E.M., Rowe C.C., Siemers E., Stern Y., Yaffe K., Carrillo M.C., Thies B., Morrison-Bogorad M., Wagster M.V., Phelps C.H. Toward defining the preclinical stages of Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's Demen. 2011, 7:280-292.
49. Storandt M., Grant E.A., Miller J.P., Morris J.C. Longitudinal course and neuropathologic outcomes in original vs revised MCI and in pre-MCI. Neurology 2006, 67:467-473.
50. Supekar K., Menon V., Rubin D., Musen M., Greicius M.D. Network analysis of intrinsic functional brain connectivity in Alzheimer's disease. PLoS Comput. Biol. 2008, 4:e1000100.
51. Tarawneh R., D'Angelo G., Macy E., Xiong C., Carter D., Cairns N.J., Fagan A.M., Head D., Mintun M.A., Ladenson J.H., Lee J.-M., Morris J.C., Holtzman D.M. Visinin-like protein-1: diagnostic and prognostic biomarker in Alzheimer disease. Ann. Neurol. 2011, 70:274-285.
52. Tijms B.M., Wink A.M., de Haan W., van der Flier W.M., Stam C.J., Scheltens P., Barkhof F. Alzheimer's disease: connecting findings from graph theoretical studies of brain networks. NBA 2013, 34:1-14.
53. Van Dijk K.R.A., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 2012, 59:431-438.
54. Wang J., Zuo X., Dai Z., Xia M., Zhao Z., Zhao X., Jia J., Han Y., He Y. Disrupted functional brain connectome in individuals at risk for Alzheimer's disease. Biol. Psychiatry 2013, 73:472-481.
55. Wang J., Zuo X., He Y. Graph-based network analysis of resting-state functional MRI. Front. Syst. Neurosci. 2010, 4:16.
56. Wang K., Liang M., Wang L., Tian L., Zhang X., Li K., Jiang T. Altered functional connectivity in early Alzheimer's disease: a resting-state fMRI study. Hum. Brain Mapp. 2007, 28:967-978.
57. Wang L., Brier M.R., Snyder A.Z., Thomas J.B., Fagan A.M., Xiong C., Benzinger T.L., Holtzman D.M., Morris J.C., Ances B.M. Cerebrospinal fluid Aβ42, phosphorylated tau181, and resting-state functional connectivity. JAMA Neurol 2013, 70:1242-1248.
58. Watts D.J., Strogatz S.H. Collective dynamics of "small-world" networks. Nature 1998, 393:440-442.
59. Zhou J., Greicius M.D., Gennatas E.D., Growdon M.E., Jang J.Y., Rabinovici G.D., Kramer J.H., Weiner M., Miller B.L., Seeley W.W. Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 2010, 133:1352-1367.