Modular reorganization of brain resting state networks and its independent validation in Alzheimer's disease patients

Frontiers in Human Neuroscience

Volumn , Issue JUL, 2013, Pages

  Chen, Guangyu ^a   Zhang, Hong Ying ^a   Xie, Chunming ^a,b   Chen, Gang ^a   Zhang, Zhi Jun ^b   Teng, Gao Jun ^b   Li, Shi Jiang ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b SOUTHEAST UNIVERSITY   (China)

Author keywords

Alzheimer's disease; Brain network; Graph theory; Gray matter concentration; MCI; Module analysis; Resting state functional connectivity; Validation

Indexed keywords

AGED; ALZHEIMER DISEASE; ARTICLE; COGNITION; CONTROLLED STUDY; FRONTAL OPERCULUM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLOBUS PALLIDUS; GRAY MATTER; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; INFERIOR FRONTAL GYRUS; INSULA; MAJOR CLINICAL STUDY; MATHEMATICAL ANALYSIS; MILD COGNITIVE IMPAIRMENT; NUCLEAR MAGNETIC RESONANCE SCANNER; PARS TRIANGULARIS; QUANTITATIVE ANALYSIS; RESTING STATE NETWORK; SUPERIOR TEMPORAL GYRUS; TEMPORAL GYRUS;

EID: 84933670894     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00456     Document Type: Article

References (75)

1. Ahnert SE, Garlaschelli D, Fink TM, Caldarelli G (2007) Ensemble approach to the analysis of weighted networks. Phys Rev E Stat Nonlin Soft Matter Phys 76:016101.
2. Alexander-Bloch AF, Gogtay N, Meunier D, Birn R, Clasen L, Lalonde F, Lenroot R, Giedd J, Bullmore ET (2010) Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Front Syst Neurosci 4:147.
3. Allen JS, Emmorey K, Bruss J, Damasio H (2008) Morphology of the insula in relation to hearing status and sign language experience. J Neurosci 28:11900-11905.
4. Babiloni C, Miniussi C, Moretti DV, Vecchio F, Salinari S, Frisoni G, Rossini PM (2004) Cortical networks generating movement-related EEG rhythms in Alzheimer's disease: an EEG coherence study. Behav Neurosci 118:698-706.
5. Balenzuela P, Chernomoretz A, Fraiman D, Cifre I, Sitges C, Montoya P, Chialvo DR (2010) Modular organization of brain resting state networks in chronic back pain patients. Front Neuroinform 4:116.
6. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541.
7. Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, Smith SM, Beckmann CF, Adelstein JS, Buckner RL, Colcombe S, Dogonowski AM, Ernst M, Fair D, Hampson M, Hoptman MJ, Hyde JS, Kiviniemi VJ, Kotter R, Li SJ, Lin CP, Lowe MJ, Mackay C, Madden DJ, Madsen KH, Margulies DS, Mayberg HS, McMahon K, Monk CS, Mostofsky SH, Nagel BJ, Pekar JJ, Peltier SJ, Petersen SE, Riedl V, Rombouts SA, Rypma B, Schlaggar BL, Schmidt S, Seidler RD, Siegle GJ, Sorg C, Teng GJ, Veijola J, Villringer A, Walter M, Wang L, Weng XC, Whitfield-Gabrieli S, Williamson P, Windischberger C, Zang YF, Zhang HY, Castellanos FX, Milham MP (2010) Toward discovery science of human brain function. Proc Natl Acad Sci U S A 107:4734-4739.
8. Bonthius DJ, Solodkin A, Van Hoesen GW (2005) Pathology of the insular cortex in Alzheimer disease depends on cortical architecture. J Neuropathol Exp Neurol 64:910-922.
9. 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.
10. Chang C, Glover GH (2010) Time-frequency dynamics of resting-state brain connectivity measured with fMRI. Neuroimage 50:81-98.
11. Chen G, Ward BD, Xie C, Li W, Wu Z, Jones JL, Franczak M, Antuono P, Li SJ (2011a) Classification of Alzheimer disease, mild cognitive impairment, and normal cognitive status with large-scale network analysis based on resting-state functional MR imaging. Radiology 259:213-221.
12. Chen G, Xie C, Li SJ (2011b) Negative functional connectivity and its dependence on the shortest path length of positive network in the resting-state human brain. Brain connectivity 1:195-206.
13. Chen ZJ, He Y, Rosa-Neto P, Germann J, Evans AC (2008) Revealing modular architecture of human brain structural networks by using cortical thickness from MRI. Cereb Cortex 18:2374-2381.
14. Clauset A, Newman ME, Moore C (2004) Finding community structure in very large networks. Phys Rev E Stat Nonlin Soft Matter Phys 70:066111.
15. Dai Z, Yan C, Wang Z, Wang J, Xia M, Li K, He Y (2012) Discriminative analysis of early Alzheimer's disease using multi-modal imaging and multi-level characterization with multi-classifier (M3). Neuroimage 59:2187-2195.
16. de Haan W, van der Flier WM, Koene T, Smits LL, Scheltens P, Stam CJ (2012) Disrupted modular brain dynamics reflect cognitive dysfunction in Alzheimer's disease. Neuroimage 59:3085-3093.
17. Delbeuck X, Van der Linden M, Collette F (2003) Alzheimer's disease as a disconnection syndrome? Neuropsychol Rev 13:79-92.
18. Dickerson BC, Sperling RA (2009) Large-scale functional brain network abnormalities in Alzheimer's disease: insights from functional neuroimaging. Behav Neurol 21:63-75.
19. Duch J. AA (2005) Community detection in complex networks using extremal optimization. Phys Rev E 72.
20. Ewers M, Insel P, Jagust WJ, Shaw L, Trojanowski JJ, Aisen P, Petersen RC, Schuff N, Weiner MW (2012) CSF biomarker and PIB-PET-derived beta-amyloid signature predicts metabolic, gray matter, and cognitive changes in nondemented subjects. Cereb Cortex 22:1993-2004.
21. Fan Y, Resnick SM, Wu X, Davatzikos C (2008) Structural and functional biomarkers of prodromal Alzheimer's disease: a high-dimensional pattern classification study. Neuroimage 41:277-285.
22. Faria AV, Joel SE, Zhang Y, Oishi K, van Zjil PC, Miller MI, Pekar JJ, Mori S (2012) Atlas-based analysis of resting-state functional connectivity: evaluation for reproducibility and multi-modal anatomy-function correlation studies. Neuroimage 61:613-621.
23. Fleisher AS, Sherzai A, Taylor C, Langbaum JB, Chen K, Buxton RB (2009) Resting-state BOLD networks versus task-associated functional MRI for distinguishing Alzheimer's disease risk groups. Neuroimage 47:1678-1690.
24. Geschwind N (1965) Disconnexion syndromes in animals and man. I. Brain 88:237-294.
25. 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 U S A 101:4637-4642.
26. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159.
27. He Y, Chen Z, Evans A (2008) Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. J Neurosci 28:4756-4766.
28. He Y, Wang J, Wang L, Chen ZJ, Yan C, Yang H, Tang H, Zhu C, Gong Q, Zang Y, Evans AC (2009) Uncovering intrinsic modular organization of spontaneous brain activity in humans. PLoS One 4:e5226.
29. Hilgetag CC, Burns GA, O'Neill MA, Scannell JW, Young MP (2000) Anatomical connectivity defines the organization of clusters of cortical areas in the macaque monkey and the cat. Philos Trans R Soc Lond B Biol Sci 355:91-110.
30. Horwitz B, Grady CL, Schlageter NL, Duara R, Rapoport SI (1987) Intercorrelations of regional cerebral glucose metabolic rates in Alzheimer's disease. Brain Res 407:294-306.
31. Johnson KA, Fox NC, Sperling RA, Klunk WE (2012) Brain imaging in Alzheimer disease. Cold Spring Harb Perspect Med 2:a006213.
32. Kelly C, Zuo XN, Gotimer K, Cox CL, Lynch L, Brock D, Imperati D, Garavan H, Rotrosen J, Castellanos FX, Milham MP (2011) Reduced interhemispheric resting state functional connectivity in cocaine addiction. Biol Psychiatry 69:684-692.
33. Khalili-Mahani N, Chang C, van Osch MJ, Veer IM, van Buchem MA, Dahan A, Beckmann CF, van Gerven JM, Rombouts SA (2012) The impact of "physiological correction" on functional connectivity analysis of pharmacological resting state fMRI. Neuroimage.
34. Koch W, Teipel S, Mueller S, Benninghoff J, Wagner M, Bokde AL, Hampel H, Coates U, Reiser M, Meindl T (2012) Diagnostic power of default mode network resting state fMRI in the detection of Alzheimer's disease. Neurobiol Aging 33:466-478.
35. Koch W, Teipel S, Mueller S, Buerger K, Bokde AL, Hampel H, Coates U, Reiser M, Meindl T (2010) Effects of aging on default mode network activity in resting state fMRI: does the method of analysis matter? Neuroimage 51:280-287.
36. Kohannim O, Hua X, Hibar DP, Lee S, Chou YY, Toga AW, Jack CR, Jr., Weiner MW, Thompson PM (2010) Boosting power for clinical trials using classifiers based on multiple biomarkers. Neurobiol Aging 31:1429-1442.
37. Lakmache Y, Lassonde M, Gauthier S, Frigon JY, Lepore F (1998) Interhemispheric disconnection syndrome in Alzheimer's disease. Proc Natl Acad Sci U S A 95:9042-9046.
38. Leicht EA, Newman ME (2008) Community structure in directed networks. Phys Rev Lett 100:118703.
39. Li SJ, Li Z, Wu G, Zhang MJ, Franczak M, Antuono PG (2002) Alzheimer Disease: evaluation of a functional MR imaging index as a marker. Radiology 225:253-259.
40. Locatelli T, Cursi M, Liberati D, Franceschi M, Comi G (1998) EEG coherence in Alzheimer's disease. Electroencephalography and clinical neurophysiology 106:229-237.
41. Lustig C, Snyder AZ, Bhakta M, O'Brien KC, McAvoy M, Raichle ME, Morris JC, Buckner RL (2003) Functional deactivations: change with age and dementia of the Alzheimer type. Proc Natl Acad Sci U S A 100:14504-14509.
42. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR, Jr., Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH (2011) The diagnosis of dementia due to Alzheimer's disease: recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimer's & dementia: the journal of the Alzheimer's Association 7:263-269.
43. Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655-667.
44. Meunier D, Achard S, Morcom A, Bullmore E (2009a) Age-related changes in modular organization of human brain functional networks. Neuroimage 44:715-723.
45. Meunier D, Lambiotte R, Bullmore ET (2010) Modular and hierarchically modular organization of brain networks. Front Neurosci 4:200.
46. Meunier D, Lambiotte R, Fornito A, Ersche KD, Bullmore ET (2009b) Hierarchical modularity in human brain functional networks. Front Neuroinform 3:37.
47. Mezer A, Yovel Y, Pasternak O, Gorfine T, Assaf Y (2009) Cluster analysis of resting-state fMRI time series. Neuroimage 45:1117-1125.
48. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315:531-534.
49. Nettiksimmons J, Harvey D, Brewer J, Carmichael O, DeCarli C, Jack CR, Jr., Petersen R, Shaw LM, Trojanowski JQ, Weiner MW, Beckett L (2010) Subtypes based on cerebrospinal fluid and magnetic resonance imaging markers in normal elderly predict cognitive decline. Neurobiol Aging 31:1419-1428.
50. Newman M. E. J. GM (2004) Finding and evaluating community structure in networks. Phys Rev E 69.
51. Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci U S A 103:8577-8582.
52. Ovadia-Caro S, Nir Y, Soddu A, Ramot M, Hesselmann G, Vanhaudenhuyse A, Dinstein I, Tshibanda JF, Boly M, Harel M, Laureys S, Malach R (2012) Reduction in inter-hemispheric connectivity in disorders of consciousness. PLoS One 7:e37238.
53. Palop JJ, Chin J, Mucke L (2006) A network dysfunction perspective on neurodegenerative diseases. Nature 443:768-773.
54. Pawela CP, Biswal BB, Cho YR, Kao o DS, Li R, Jones SR, Schulte ML, Matloub HS, Hudetz AG, Hyde JS (2008) Resting-state functional connectivity of the rat brain. Magn Reson Med 59:1021-1029.
55. Pawela CP, Biswal BB, Hudetz AG, Li R, Jones SR, Cho YR, Matloub HS, Hyde JS (2010) Interhemispheric neuroplasticity following limb deafferentation detected by resting-state functional connectivity magnetic resonance imaging (fcMRI) and functional magnetic resonance imaging (fMRI). Neuroimage 49:2467-2478.
56. Prvulovic D, Bokde AL, Faltraco F, Hampel H (2011) Functional magnetic resonance imaging as a dynamic candidate biomarker for Alzheimer's disease. Progress in neurobiology 95:557-569.
57. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98:676-682.
58. Royall DR (2008) Insular Alzheimer disease pathology and the psychometric correlates of mortality. Cleve Clin J Med 75 Suppl 2:S97-99.
59. Sanz-Arigita EJ, Schoonheim MM, Damoiseaux JS, Rombouts SA, Maris E, Barkhof F, Scheltens P, Stam CJ (2010) Loss of 'small-world' networks in Alzheimer's disease: graph analysis of FMRI resting-state functional connectivity. PLoS One 5:e13788.
60. Sheline YI, Morris JC, Snyder AZ, Price JL, Yan Z, D'Angelo G, Liu C, Dixit S, Benzinger T, Fagan A, Goate A, Mintun MA (2010a) APOE4 allele disrupts resting state fMRI connectivity in the absence of amyloid plaques or decreased CSF Abeta42. J Neurosci 30:17035-17040.
61. Sheline YI, Raichle ME, Snyder AZ, Morris JC, Head D, Wang S, Mintun MA (2010b) Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol Psychiatry 67:584-587.
62. Sorg C, Riedl V, Perneczky R, Kurz A, Wohlschlager AM (2009) Impact of Alzheimer's disease on the functional connectivity of spontaneous brain activity. Curr Alzheimer Res 6:541-553.
63. Sperling RA, Laviolette PS, O'Keefe K, O'Brien J, Rentz DM, Pihlajamaki M, Marshall G, Hyman BT, Selkoe DJ, Hedden T, Buckner RL, Becker JA, Johnson KA (2009) Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 63:178-188.
64. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273-289.
65. van den Heuvel MP, Hulshoff Pol HE (2010) Specific somatotopic organization of functional connections of the primary motor network during resting state. Hum Brain Mapp 31:631-644.
66. Wada Y, Nanbu Y, Koshino Y, Yamaguchi N, Hashimoto T (1998) Reduced interhemispheric EEG coherence in Alzheimer disease: analysis during rest and photic stimulation. Alzheimer Dis Assoc Disord 12:175-181.
67. Walhovd KB, Fjell AM, Brewer J, McEvoy LK, Fennema-Notestine C, Hagler DJ, Jr., Jennings RG, Karow D, Dale AM (2010) Combining MR imaging, positron-emission tomography, and CSF biomarkers in the diagnosis and prognosis of Alzheimer disease. AJNR Am J Neuroradiol 31:347-354.
68. Westman E, Aguilar C, Muehlboeck JS, Simmons A (2012a) Regional Magnetic Resonance Imaging Measures for Multivariate Analysis in Alzheimer's Disease and Mild Cognitive Impairment. Brain Topogr.
69. Westman E, Muehlboeck JS, Simmons A (2012b) Combining MRI and CSF measures for classification of Alzheimer's disease and prediction of mild cognitive impairment conversion. Neuroimage 62:229-238.
70. Xie C, Bai F, Yu H, Shi Y, Yuan Y, Chen G, Li W, Zhang Z, Li SJ (2012) Abnormal insula functional network is associated with episodic memory decline in amnestic mild cognitive impairment. Neuroimage 63:320-327.
71. Yu Q, Plis SM, Erhardt EB, Allen EA, Sui J, Kiehl KA, Pearlson G, Calhoun VD (2011) Modular Organization of Functional Network Connectivity in Healthy Controls and Patients with Schizophrenia during the Resting State. Front Syst Neurosci 5:103.
72. Zhang HY, Wang SJ, Liu B, Ma ZL, Yang M, Zhang ZJ, Teng GJ (2010) Resting brain connectivity: changes during the progress of Alzheimer disease. Radiology 256:598-606.
73. Zhang HY, Wang SJ, Xing J, Liu B, Ma ZL, Yang M, Zhang ZJ, Teng GJ (2009) Detection of PCC functional connectivity characteristics in resting-state fMRI in mild Alzheimer's disease. Behav Brain Res 197:103-108.
74. Zhang Y, Schuff N, Ching C, Tosun D, Zhan W, Nezamzadeh M, Rosen HJ, Kramer JH, Gorno-Tempini ML, Miller BL, Weiner MW (2011) Joint assessment of structural, perfusion, and diffusion MRI in Alzheimer's disease and frontotemporal dementia. Int J Alzheimers Dis 2011:546871.
75. Zuo XN, Kelly C, Di Martino A, Mennes M, Margulies DS, Bangaru S, Grzadzinski R, Evans AC, Zang YF, Castellanos FX, Milham MP (2010) Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. J Neurosci 30:15034-15043.