Loss of 'Small-World' Networks in Alzheimer's Disease: Graph Analysis of fMRI Resting-State Functional Connectivity

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Sanz Arigita, Ernesto J ^a,b   Schoonheim, Menno M ^a   Damoiseaux, Jessica S ^c   Rombouts, Serge A R B ^d   Maris, Erik ^e   Barkhof, Frederik ^a   Scheltens, Philip ^a   Stam, Cornelis J ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Fundacion CITA Alzheimer   (Spain)

^c STANFORD UNIVERSITY   (United States)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e RADBOUD UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ALZHEIMER DISEASE; ANALYTIC METHOD; ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; CLINICAL ARTICLE; CLUSTER ANALYSIS; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DISEASE SEVERITY; FEMALE; FRONTAL CORTEX; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAPH ANALYSIS; HUMAN; MALE; OCCIPITAL CORTEX; PARIETAL LOBE; POST HOC ANALYSIS; QUANTITATIVE ANALYSIS; ADOLESCENT; ALGORITHM; BIOLOGICAL MODEL; BRAIN; BRAIN MAPPING; METHODOLOGY; MIDDLE AGED; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; REST;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ALGORITHMS; ALZHEIMER DISEASE; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MODELS, NEUROLOGICAL; NERVE NET; REST; YOUNG ADULT;

EID: 78249275549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013788     Document Type: Article

References (71)

1. Delbeuck X, Van der Linden M, Collette F (2003) Alzheimer's disease as a disconnection syndrome? Neuropsychol Rev 13: 79-92.
2. O'Sullivan M, Jones DK, Summers PE, Morris RG, Williams SC, et al. (2001) Evidence for cortical "disconnection" as a mechanism of age-related cognitive decline. Neurology 57: 632-638.
3. Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci U S A 100: 253-258.
4. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, et al. (2001) A default mode of brain function. Proc Natl Acad Sci U S A 98: 676-682.
5. Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18: 193-222.
6. Hopfinger JB, Buonocore MH, Mangun GR (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3: 284-291.
7. Damoiseaux J, Beckmann CF, Sanz Arigita EJ, Stam CJ, Barkhof F, et al. (2008) Reduced resting state activity in the dorsal visuo-spatial attention system in Alzheimer's disease. Neuroimage 41: S144.
8. 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.
9. Wang K, Liang M, Wang L, Tian L, Zhang X, et al. (2007) Altered functional connectivity in early Alzheimer's disease: a resting-state fMRI study. Hum Brain Mapp 28: 967-978.
10. Mason I (2007) Continence care for patients with inflammatory bowel disease. Nurs Stand 22: 43-46.
11. Damoiseaux JS, Beckmann CF, Arigita EJ, Barkhof F, Scheltens P, et al. (2008) Reduced resting-state brain activity in the "default network" in normal aging. Cereb Cortex 18: 1856-1864.
12. Grady CL, Hongwanishkul D, Keightley M, Lee W, Hasher L (2007) The effect of age on memory for emotional faces. Neuropsychology 21: 371-380.
13. Lindeboom J, Weinstein H (2004) Neuropsychology of cognitive ageing, minimal cognitive impairment, Alzheimer's disease, and vascular cognitive impairment. Eur J Pharmacol 490: 83-86.
14. Grady CL, McIntosh AR, Beig S, Keightley ML, Burian H, et al. (2003) Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer's disease. J Neurosci 23: 986-993.
15. Sole-Padulles C, Bartres-Faz D, Junque C, Vendrell P, Rami L, et al. (2009) Brain structure and function related to cognitive reserve variables in normal aging, mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 30: 1114-1124.
16. Woodard JL, Grafton ST, Votaw JR, Green RC, Dobraski ME, et al. (1998) Compensatory recruitment of neural resources during overt rehearsal of word lists in Alzheimer's disease. Neuropsychology 12: 491-504.
17. Supekar K, Menon V, Rubin D, Musen M, Greicius MD (2008) Network analysis of intrinsic functional brain connectivity in Alzheimer's disease. PLoS Comput Biol 4: e1000100.
18. Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens P (2007) Small-world networks and functional connectivity in Alzheimer's disease. Cereb Cortex 17: 92-99.
19. 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.
20. Reijneveld JC, Ponten SC, Berendse HW, Stam CJ (2007) The application of graph theoretical analysis to complex networks in the brain. Clin Neurophysiol 118: 2317-2331.
21. Strogatz SH (2001) Exploring complex networks. Nature 410: 268-276.
22. Stam CJ, Van Dijk BW (2002) Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets. Physica D- Nonlinear Phenomena 163: 236-251.
23. Watts DJ, Strogatz SH (1998) Collective dynamics of 'small-world' networks. Nature 393: 440-442.
24. Hagmann P, Kurant M, Gigandet X, Thiran P, Wedeen VJ, et al. (2007) Mapping human whole-brain structural networks with diffusion MRI. PLoS One 2: e597.
25. Sporns O, Honey CJ, Kotter R (2007) Identification and classification of hubs in brain networks. PLoS One 2: e1049.
26. Stam CJ (2004) Functional connectivity patterns of human magnetoencephalographic recordings: a 'small-world' network? Neurosci Lett 355: 25-28.
27. Stam CJ, Jones BF, Manshanden I, van Cappellen van Walsum AM, Montez T, et al. (2006) Magnetoencephalographic evaluation of resting-state functional connectivity in Alzheimer's disease. Neuroimage 32: 1335-1344.
28. Bassett DS, Bullmore E (2006) Small-world brain networks. Neuroscientist 12: 512-523.
29. Ferri R, Rundo F, Bruni O, Terzano MG, Stam CJ (2007) Small-world network organization of functional connectivity of EEG slow-wave activity during sleep. Clin Neurophysiol 118: 449-456.
30. Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E (2006) A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. Journal of Neuroscience 26: 63-72.
31. Tononi G, Edelman GM (1998) Consciousness and complexity. Science 282: 1846-1851.
32. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, et al. (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103: 13848-13853.
33. Liu Y, Liang M, Zhou Y, He Y, Hao Y, et al. (2008) Disrupted small-world networks in schizophrenia. Brain 131: 945-961.
34. Micheloyannis S, Pachou E, Stam CJ, Breakspear M, Bitsios P, et al. (2006) Small-world networks and disturbed functional connectivity in schizophrenia. Schizophr Res 87: 60-66.
35. Stam CJ, de Haan W, Daffertshofer A, Jones BF, Manshanden I, et al. (2009) Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. Brain 132: 213-224.
36. Wang HY, Cui TG, Hou FF, Ni ZH, Chen XM, et al. (2008) Induction treatment of proliferative lupus nephritis with leflunomide combined with prednisone: a prospective multi-centre observational study. Lupus 17: 638-644.
37. Folstein MF, Folstein SE, McHugh PR (1975) "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12: 189-198.
38. McKhann G, Drachman D, Folstein M, Katzman R, Price D, et al. (1984) 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: 939-944.
39. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am J Roentgenol 149: 351-356.
40. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1: S208-219.
41. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17: 825-841.
42. Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17: 143-155.
43. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, et al. (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15: 273-289.
44. Montez T, Linkenkaer-Hansen K, van Dijk BW, Stam CJ (2006) Synchronization likelihood with explicit time-frequency priors. Neuroimage 33: 1117-1125.
45. Newman ME (2003) Properties of highly clustered networks. Phys Rev E Stat Nonlin Soft Matter Phys 68: 026121.
46. Ponten SC, Bartolomei F, Stam CJ (2007) Small-world networks and epilepsy: graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures. Clin Neurophysiol 118: 918-927.
47. Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296: 910-913.
48. Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164: 177-190.
49. Eguiluz VM, Chialvo DR, Cecchi GA, Baliki M, Apkarian AV (2005) Scale-free brain functional networks. Phys Rev Lett 94: 018102.
50. Kaiser M (2007) Brain architecture: a design for natural computation. Philos Transact A Math Phys Eng Sci 365: 3033-3045.
51. Kaiser M, Hilgetag CC (2006) Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput Biol 2: e95.
52. Lago-Fernandez LF, Huerta R, Corbacho F, Siguenza JA (2000) Fast response and temporal coherent oscillations in small-world networks. Phys Rev Lett 84: 2758-2761.
53. Sporns O, Chialvo DR, Kaiser M, Hilgetag CC (2004) Organization, development and function of complex brain networks. Trends Cogn Sci 8: 418-425.
54. Sporns O, Tononi G, Edelman GM (2000) Theoretical neuroanatomy: relating anatomical and functional connectivity in graphs and cortical connection matrices. Cereb Cortex 10: 127-141.
55. Sorg C, Riedl V, Muhlau M, Calhoun VD, Eichele T, et al. (2007) Selective changes of resting-state networks in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci U S A 104: 18760-18765.
56. Grady CL, Furey ML, Pietrini P, Horwitz B, Rapoport SI (2001) Altered brain functional connectivity and impaired short-term memory in Alzheimer's disease. Brain 124: 739-756.
57. Horwitz B, McIntosh AR, Haxby JV, Furey M, Salerno JA, et al. (1995) Network analysis of PET-mapped visual pathways in Alzheimer type dementia. Neuroreport 6: 2287-2292.
58. Hao J, Li K, Zhang D, Wang W, Yang Y, et al. (2005) Visual attention deficits in Alzheimer's disease: an fMRI study. Neurosci Lett 385: 18-23.
59. He Y, Wang L, Zang Y, Tian L, Zhang X, et al. (2007) Regional coherence changes in the early stages of Alzheimer's disease: a combined structural and resting-state functional MRI study. Neuroimage 35: 488-500.
60. Prvulovic D, Hubl D, Sack AT, Melillo L, Maurer K, et al. (2002) Functional imaging of visuospatial processing in Alzheimer's disease. Neuroimage 17: 1403-1414.
61. Alsop DC, Detre JA, Grossman M (2000) Assessment of cerebral blood flow in Alzheimer's disease by spin-labeled magnetic resonance imaging. Ann Neurol 47: 93-100.
62. Buckner RL, Snyder AZ, Shannon BJ, LaRossa G, Sachs R, et al. (2005) Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J Neurosci 25: 7709-7717.
63. Lustig C, Snyder AZ, Bhakta M, O'Brien KC, McAvoy M, et al. (2003) Functional deactivations: change with age and dementia of the Alzheimer type. Proc Natl Acad Sci U S A 100: 14504-14509.
64. Karas GB, Burton EJ, Rombouts SA, van Schijndel RA, O'Brien JT, et al. (2003) A comprehensive study of gray matter loss in patients with Alzheimer's disease using optimized voxel-based morphometry. Neuroimage 18: 895-907.
65. Fein G, Di Sclafani V, Tanabe J, Cardenas V, Weiner MW, et al. (2000) Hippocampal and cortical atrophy predict dementia in subcortical ischemic vascular disease. Neurology 55: 1626-1635.
66. Block F, Dihne M, Loos M (2005) Inflammation in areas of remote changes following focal brain lesion. Prog Neurobiol 75: 342-365.
67. Villain N, Desgranges B, Viader F, de la Sayette V, Mezenge F, et al. (2008) Relationships between hippocampal atrophy, white matter disruption, and gray matter hypometabolism in Alzheimer's disease. J Neurosci 28: 6174-6181.
68. Honey CJ, Sporns O (2008) Dynamical consequences of lesions in cortical networks. Hum Brain Mapp 29: 802-809.
69. Friston K (2002) Functional integration and inference in the brain. Prog Neurobiol 68: 113-143.
70. de Leeuw FE, Barkhof F, Scheltens P (2004) White matter lesions and hippocampal atrophy in Alzheimer's disease. Neurology 62: 310-312.
71. Whitwell JL, Przybelski SA, Weigand SD, Knopman DS, Boeve BF, et al. (2007) 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer's disease. Brain 130: 1777-1786.