Classifying minimally disabled multiple sclerosis patients from resting state functional connectivity

NeuroImage

Volumn 62, Issue 3, 2012, Pages 2021-2033

  Richiardi, Jonas ^a,b   Gschwind, Markus ^a,c,d   Simioni, Samanta ^c   Annoni, Jean Marie ^a,d,e   Greco, Beatrice ^f   Hagmann, Patric ^b,c   Schluep, Myriam ^c   Vuilleumier, Patrik ^a,d   Van De Ville, Dimitri ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b EPFL   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^e UNIVERSITY OF FRIBOURG   (Switzerland)

^f MERCK SERONO S A   (Switzerland)

Author keywords

Brain decoding; Brain networks; Classification; Functional magnetic resonance imaging; Imaging marker

Indexed keywords

BETA1A INTERFERON; GLATIRAMER; INTERFERON BETA SERINE;

ADULT; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; DISABLED PERSON; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MULTIPLE SCLEROSIS; PATTERN RECOGNITION; PREDICTION; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; SUBCORTEX; TEMPORAL LOBE; WHITE MATTER LESION;

ADULT; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; REST; SENSITIVITY AND SPECIFICITY;

EID: 84863671296     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.05.078     Document Type: Article

References (99)

1. Achard S., Salvador R., Whitcher B., Suckling J., Bullmore E. A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 2006, 26(1):63-72. (Jan.).
2. Alemán-Gómez Y., Melie-García L., Valdés-Hernandez P. IBASPM: toolbox for automatic parcellation of brain structures. Proc. 12th Annual Meeting of the Organization for Human Brain Mapping. Florence, Italy 2006, (June).
3. Ashburner J., Friston K.J. Unified segmentation. NeuroImage 2005, 26(3):839-851. (Jul), (URL http://dx.doi.org/10.1016/j.neuroimage.2005.02.018).
4. Audoin B., Davies G.R., Finisku L., Chard D.T., Thompson A.J., Miller D.H. Localization of grey matter atrophy in early rrms. J. Neurol. 2006, 253(11):1495-1501. (URL http://dx.doi.org/10.1007/s00415-006-0264-2).
5. Barkhof F. The clinico-radiological paradox in multiple sclerosis revisited. Curr. Opin. Neurol. 2002, 15(3):239-245. (URL http://journals.lww.com/co-neurology/Fulltext/2002/06000/ The_clinico_radiological_paradox_in_multiple.3.aspx).
6. Barkhof F., Filippi M. Multiple sclerosis: MRI-the perfect surrogate marker for multiple sclerosis?. Nat. Rev. Neurol. 2009, 5(4):182-183. (Apr.), (URL http://dx.doi.org/10.1038/nrneurol.2009.31).
7. Barkhof F., Calabresi P.A., Miller D.H., Reingold S.C. Imaging outcomes for neuroprotection and repair in multiple sclerosis trials. Nat. Rev. Neurol. 2009, 5(5):256-266. (May), (URL http://dx.doi.org/10.1038/nrneurol.2009.41).
8. Bendfeldt K., Klöppel S., Nichols T.E., Smieskova R., Kuster P., Traud S., Mueller-Lenke N., Naegelin Y., Kappos L., Radue E.-W., Borgwardt S.J. Multivariate pattern classification of gray matter pathology in multiple sclerosis. NeuroImage 2012, 60(1):400-408. (Mar.), (URL http://www.sciencedirect.com/science/article/pii/S1053811911014728).
9. Biswal B., Yetkin F., Haughton V., Hyde J. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34(4):537-541.
10. Bö L., Geurts J., Mörk S., Van Der Valk P. Grey matter pathology in multiple sclerosis. Acta Neurol. Scand. 2006, 113(Suppl. 183):48-50. (URL http://www.scopus.com/inward/record.url?eid=2-s2.0-33645533249&partnerID=40&md5=fb17b7b13f009d3cc7f889e03cda4129).
11. Bonavita S., Gallo A., Sacco R., Corte M.D., Bisecco A., Docimo R., Lavorgna L., Corbo D., Costanzo A.D., Tortora F., Cirillo M., Esposito F., Tedeschi G. Distributed changes in default-mode resting-state connectivity in multiple sclerosis. Mult. Scler. J. 2011, 17(4):411-422. 10.1177/1352458510394609.
12. Buckner R., Andrews-Hanna J., Schacter D. The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 2008, 1124:1-38. (URL http://www.scopus.com/inward/record.url?eid=2-s2.0-41949121294&partnerID=40).
13. 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(6):1860-1873.
14. Budde M.D., Xie M., Cross A.H., Song S.-K. Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. J. Neurosci. 2009, 29(9):2805-2813. (URL http://www.jneurosci.org/content/29/9/2805.abstract).
15. Cader S., Cifelli A., Abu-Omar Y., Palace J., Matthews P.M. Reduced brain functional reserve and altered functional connectivity in patients with multiple sclerosis. Brain 2006, 129(Pt 2):527-537. (Feb), (URL http://dx.doi.org/10.1093/brain/awh670).
16. Chen G., Ward B.D., Xie C., Li W., Wu Z., Jones J.L., Franczak M., Antuono P., Li S.-J. Classification of alzheimer disease, mild cognitive impairment, and normal cognitive status with large-scale network analysis based on resting state functional mr imaging. Radiology 2011, 259(1):213-221. (Apr), (URL http://dx.doi.org/10.1148/radiol.10100734).
17. Ciccarelli O., Toosy A.T., Hickman S.J., Parker G.J.M., Wheeler-Kingshott C.A.M., Miller D.H., Thompson A.J. Optic radiation changes after optic neuritis detected by tractography-based group mapping. Hum. Brain Mapp. 2005, 25(3):308-316. (Jul), (URL http://dx.doi.org/10.1002/hbm.20101).
18. Cifelli A., Matthews P.M. Cerebral plasticity in multiple sclerosis: insights from fMRI. Mult. Scler. 2002, 8(3):193-199. (May).
19. Cifelli A., Arridge M., Jezzard P., Esiri M.M., Palace J., Matthews P.M. Thalamic neurodegeneration in multiple sclerosis. Ann. Neurol. 2002, 52(5):650-653. (URL http://dx.doi.org/10.1002/ana.10326).
20. Compston A., Coles A. Multiple sclerosis. Lancet 2008, 372(9648):1502-1517. (Oct), (URL http://dx.doi.org/10.1016/S0140-6736(08)61620-7).
21. Cover K.S., Vrenken H., Geurts, Jeroen J.G., van Oosten B.W., Jelles B., Polman C.H., Stam C.J., van Dijk B.W. Multiple sclerosis patients show a highly significant decrease in alpha band interhemispheric synchronization measured using MEG. Neuroimage 2006, 29(3):783-788. (Feb). 10.1016/j.neuroimage.2005.08.048.
22. Craddock R.C., Holtzheimer P.E., Hu X.P., Mayberg H.S. Disease state prediction from resting state functional connectivity. Magn. Reson. Med. 2009, 62(6):1619-1628. (Dec), (URL http://dx.doi.org/10.1002/mrm.22159).
23. Dineen R.A., Vilisaar J., Hlinka J., Bradshaw C.M., Morgan P.S., Constantinescu C.S., Auer D.P. Disconnection as a mechanism for cognitive dysfunction in multiple sclerosis. Brain 2009, 132(Pt 1):239-249. (Jan), (URL http://dx.doi.org/10.1093/brain/awn275).
24. Eryilmaz H., Ville D.V.D., Schwartz S., Vuilleumier P. Impact of transient emotions on functional connectivity during subsequent resting state: a wavelet correlation approach. NeuroImage 2011, 54(3):2481-2491. (Feb), (URL http://dx.doi.org/10.1016/j.neuroimage.2010.10.021).
25. Ethofer T., Van De Ville D., Scherer K., Vuilleumier P. Decoding of emotional information in voice-sensitive cortices. Curr. Biol. 2009, 19(12):1028-1033. (June 23).
26. Evangelou N., Esiri M.M., Smith S., Palace J., Matthews P.M. Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis. Ann. Neurol. 2000, 47(3):391-395. (cited By (since 1996) 238. URL http://www.scopus.com/inward/record.url?eid=2-s2.0-0034104079&partnerID=40&md5=0d5927019c4440e8e7abb1c2cad80da8).
27. Filippi M., Agosta F. Imaging biomarkers in multiple sclerosis. J. Magn. Reson. Imaging 2010, 31(4):770-788. (Apr), (URL http://dx.doi.org/10.1002/jmri.22102).
28. Fox M.D., Greicius M. Clinical applications of resting state functional connectivity. Front. Syst. Neurosci. 2010, 4:19. (URL http://dx.doi.org/10.3389/fnsys.2010.00019).
29. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8(9):700-711. (Sep.), (URL http://dx.doi.org/10.1038/nrn2201).
30. Friston K., Williams S., Howard R., Frackowiak R., Turner R. Movement-related effects in fMRI time-series. Magn. Reson. Med. 1996, 35(3):346-355. (URL http://www.scopus.com/inward/record.url?eid=2-s2.0-0030032333&partnerID=40&md5=957aefc7ca5b34ca21ee30ae9774cdb0).
31. Fu L., Matthews P.M., De Stefano N., Worsley K.J., Narayanan S., Francis G.S., Antel J.P., Wolfson C., Arnold D.L. Imaging axonal damage of normal-appearing white matter in multiple sclerosis. Brain 1998, 121(Pt 1):103-113. (Jan).
32. Gean-Marton A., Vezina L., Marton K., Stimac G., Peyster R., Taveras J., Davis K. Abnormal corpus callosum: a sensitive and specific indicator of multiple sclerosis. Radiology 1991, 180(1):215-221. (URL http://www.scopus.com/inward/record.url?eid=2-s2.0-0025878670&partnerID=40&md5=6b8eeff2ea08a4641b244e5f0461710e).
33. Golanov E.V., Reis D.J. Contribution of oxygen-sensitive neurons of the rostral ventrolateral medulla to hypoxic cerebral vasodilatation in the rat. J. Physiol. 1996, 495(Pt 1):201-216. (Aug).
34. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(1):253-258. (Jan.), (URL http://www.pnas.org/content/100/1/253.abstract).
35. Greicius M.D., Srivastava G., Reiss A.L., Menon V. Defaultmode network activity distinguishes alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(13):4637-4642. (Mar), (URL http://dx.doi.org/10.1073/pnas.0308627101).
36. Greicius M.D., Flores B.H., Menon V., Glover G.H., Solvason H.B., Kenna H., Reiss A.L., Schatzberg A.F. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol. Psychiatry 2007, 62(5):429-437. (Sep), (URL http://dx.doi.org/10.1016/j.biopsych.2006.09.020).
37. Greicius M.D., Supekar K., Menon V., Dougherty R.F. Restingstate functional connectivity reflects structural connectivity in the default mode network. Cereb. Cortex 2009, 19(1):72-78. (Jan), (URL http://dx.doi.org/10.1093/cercor/bhn059).
38. Haber S.N., Knutson B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010, 35(1):4-26. (Jan), (URL http://dx.doi.org/10.1038/npp.2009.129).
39. Hawellek D.J., Hipp J.F., Lewis C.M., Corbetta M., Engel A.K. Increased functional connectivity indicates the severity of cognitive impairment in multiple sclerosis. Proc. Natl. Acad.Sci. U. S. A. 2011, 108(47):19066-19071.
40. Helekar S.A., Shin J.C., Mattson B.J., Bartley K., Stosic M., Saldana-King T., Montague P.R., Hutton G.J. Functional brain network changes associated with maintenance of cognitive function in multiple sclerosis. Front. Hum. Neurosci. 2010, 4:219. (URL http://dx.doi.org/10.3389/fnhum.2010.00219).
41. Jacobs L.D., Beck R.W., Simon J.H., Kinkel R.P., Brownscheidle C.M., Murray T.J., Simonian N.A., Slasor P.J., Sandrock A.W. Intramuscular interferon beta-1a therapy initiated during a first demyelinating event in multiple sclerosis. N. Engl. J. Med. 2000, 343(13):898-904. (Sep), (URL http://dx.doi.org/10.1056/NEJM200009283431301).
42. Jafri M.J., Pearlson G.D., Stevens M., Calhoun V.D. A method for functional network connectivity among spatially independent resting state components in schizophrenia. NeuroImage 2008, 39(4):1666-1681. (Feb), (URL http://dx.doi.org/10.1016/j.neuroimage.2007.11.001).
43. Jones D.T., Mateen F.J., Lucchinetti C.F., Jack C.R., Welker K.M. Default mode network disruption secondary to a lesion in the anterior thalamus. Arch. Neurol. 2011, 68(2):242-247. (Feb), (URL http://dx.doi.org/10.1001/archneurol.2010.259).
44. Kamitani Y., Tong F. Decoding the visual and subjective contents of the human brain. Nat. Neurosci. 2005, 8:679-685.
45. Kappos L., Freedman M.S., Polman C.H., Edan G., Hartung H.-P., Miller D.H., Montalbán X., Barkhof F., Radü E.-W., Bauer L., Dahms S., Lanius V., Pohl C., Sandbrink R., B.E.N.E.F.I.T.Study Group Effect of early versus delayed interferon beta-1b treatment on disability after a first clinical event suggestive of multiple sclerosis: a 3-year follow-up analysis of the BENEFIT study. Lancet 2007, 370(9585):389-397. (Aug).
46. Kensinger E.A., Schacter D.L. Neural processes supporting young and older adults' emotional memories. J. Cogn. Neurosci. 2008, 20(7):1161-1173. (URL http://www.mitpressjournals.org/doi/abs/10.1162/jocn.2008. 20080).
47. Kurtzke J.F. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983, 33(11):1444-1452. (Nov).
48. Langs G., Menze B.H., Lashkari D., Golland P. Detecting stable distributed patterns of brain activation using gini contrast. NeuroImage 2011, 56(2):497-507. (URL http://www.sciencedirect.com/science/article/B6WNP-50S8PM9-1/2/40411edede5ff716c2502fe4bff8dc05).
49. Lee M., Reddy H., Johansen-Berg H., Pendlebury S., Jenkinson M., Smith S., Palace J., Matthews P.M. The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis. Ann. Neurol. 2000, 47(5):606-613. (May).
50. Li S.-J., Li Z., Wu G., Zhang M.-J., Franczak M., Antuono P.G. Alzheimer disease: evaluation of a functional MR imaging index as a marker. Radiology 2002, 225(1):253-259. (Oct).
51. Lin X., Tench C.R., Morgan P.S., Niepel G., Constantinescu C.S. importance sampling' in ms: use of diffusion tensor tractography to quantify pathology related to specific impairment. J. Neurol. Sci. 2005, 237(1-2):13-19. (Oct), (URL http://dx.doi.org/10.1016/j.jns.2005.04.019).
52. Liu Y., Liang P., Duan Y., Jia X., Yu C., Zhang M., Wang F., Zhang M., Dong H., Ye J., Butzkueven H., Li K. Brain plasticity in relapsing-remitting multiple sclerosis: evidence from resting state fMRI. J. Neurol. Sci. 2011, 304(1-2):127-131. (Feb), (URL http://dx.doi.org/10.1016/j.jns.2011.01.023).
53. Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 2008, 453(7197):869-878. (Jun), (URL http://dx.doi.org/10.1038/nature06976).
54. Lowe M.J., Mock B.J., Sorenson J.A. Functional connectivity in single and multislice echoplanar imaging using resting state fluctuations. NeuroImage 1998, 7(2):119-132. (Feb.), (URL http://www.sciencedirect.com/science/article/B6WNP-45M2Y15-1G/2/88964e40762eb2eadd8376e575d6e198).
55. Lowe M.J., Beall E.B., Sakaie K.E., Koenig K.A., Stone L., Marrie R.A., Phillips M.D. Resting state sensorimotor functional connectivity in multiple sclerosis inversely correlates with transcallosal motor pathway transverse diffusivity. Hum. Brain Mapp. 2008, 29(7):818-827. (Jul), (URL http://dx.doi.org/10.1002/hbm.20576).
56. Mainero C., Caramia F., Pozzilli C., Pisani A., Pestalozza I., Borriello G., Bozzao L., Pantano P. fMRI evidence of brain reorganization during attention and memory tasks in multiple sclerosis. NeuroImage 2004, 21(3):858-867. (Mar), (URL http://dx.doi.org/10.1016/j.neuroimage.2003.10.004).
57. Manson S.C., Palace J., Frank J.A., Matthews P.M. Loss of interhemispheric inhibition in patients with multiple sclerosis is related to corpus callosum atrophy. Exp. Brain Res. 2006, 174(4):728-733. (Oct), (URL http://dx.doi.org/10.1007/s00221-006-0517-4).
58. Manson S.C., Wegner C., Filippi M., Barkhof F., Beckmann C., Ciccarelli O., Stefano N.D., Enzinger C., Fazekas F., Agosta F., Gass A., Hirsch J., Johansen-Berg H., Kappos L., Korteweg T., Polman C., Mancini L., Manfredonia F., Marino S., Miller D.H., Montalban X., Palace J., Rocca M., Ropele S., Rovira A., Smith S., Thompson A., Thornton J., Yousry T., Frank J.A., Matthews P.M. Impairment of movementassociated brain deactivation in multiple sclerosis: further evidence for a functional pathology of interhemispheric neuronal inhibition. Exp. Brain Res. 2008, 187(1):25-31. (May), (URL http://dx.doi.org/10.1007/s00221-008-1276-1).
59. Mantini D., Perrucci M.G., Gratta C.D., Romani G.L., Corbetta M. Electrophysiological signatures of resting state networks in the human brain. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(32):13170-13175. (Aug), (URL http://dx.doi.org/10.1073/pnas.0700668104).
60. Mesaros S., Rocca M.A., Riccitelli G., Pagani E., Rovaris M., Caputo D., Ghezzi A., Capra R., Bertolotto A., Comi G., Filippi M. Corpus callosum damage and cognitive dysfunction in benign MS. Hum. Brain Mapp. 2009, 30(8):2656-2666. (Aug), (URL http://dx.doi.org/10.1002/hbm.20692).
61. Miller D.H., Thompson A.J., Filippi M. Magnetic resonance studies of abnormalities in the normal appearing white matter and greymatter in multiple sclerosis. J. Neurol. 2003, 250(12):1407-1419. (Dec), (URL http://dx.doi.org/10.1007/s00415-003-0243-9).
62. Minden S.L., Schiffer R.B. Affective disorders in multiple sclerosis. review and recommendations for clinical research. Arch. Neurol. 1990, 47(1):98-104. (Jan).
63. Morgen K., Kadom N., Sawaki L., Tessitore A., Ohayon J., McFarland H., Frank J., Martin R., Cohen L.G. Training-dependent plasticity in patients with multiple sclerosis. Brain 2004, 127(Pt 11). (Nov).
64. Morgen K., Sammer G., Courtney S.M., Wolters T., Melchior H., Blecker C.R., Oschmann P., Kaps M., Vaitl D. Distinct mechanisms of altered brain activation in patients with multiple sclerosis. NeuroImage 2007, 37(3):937-946. (Sep), (URL http://dx.doi.org/10.1016/j.neuroimage.2007.05.045).
65. Mourao-Miranda J., Bokde A.L., Born C., Hampel H., Stetter M. Classifying brain states and determining the discriminating activation patterns: support vector machine on functional MRI data. NeuroImage 2005, 28(4):980-995. (Dec.), (URL http://www.sciencedirect.com/science/article/B6WNP-4HGM79R-1/2/fcb89095569ad4445086c71d6eb5bfff).
66. Muehlhan M., Lueken U., Wittchen H.-U., Kirschbaum C. The scanner as a stressor: evidence from subjective and neuroendocrine stress parameters in the time course of a functional magnetic resonance imaging session. Int. J. Psychophysiol. 2011, 79(2):118-126. (Feb), (URL http://dx.doi.org/10.1016/j.ijpsycho.2010.09.009).
67. Noseworthy J.H., Lucchinetti C., Rodriguez M., Weinshenker B.G. Multiple sclerosis. N. Engl. J. Med. 2000, 343(13):938-952. (Sep.), (URL http://content.nejm.org).
68. Olson I.R., Plotzker A., Ezzyat Y. The enigmatic temporal pole: a review of findings on social and emotional processing. Brain 2007, 130(Pt 7):1718-1731. (Jul), (URL http://dx.doi.org/10.1093/brain/awm052).
69. Pelletier J., Suchet L., Witjas T., Habib M., Guttmann C.R., Salamon G., Lyon-Caen O., Chérif A.A. A longitudinal study of callosal atrophy and interhemispheric dysfunction in relapsing-remitting multiple sclerosis. Arch. Neurol. 2001, 58(1):105-111. Jan.
70. Polman C.H., Reingold S.C., Edan G., Filippi M., Hartung H.-P., Kappos L., Lublin F.D., Metz L.M., McFarland H.F., O'Connor P.W., Sandberg-Wollheim M., Thompson A.J., Weinshenker B.G., Wolinsky J.S. Diagnostic criteria for multiple sclerosis: 2005 revisions to the McDonald criteria. Ann. Neurol. 2005, 58(6):840-846. (URL http://dx.doi.org/10.1002/ana.20703).
71. Polman C.H., Reingold S.C., Banwell B., Clanet M., Cohen J.A., Filippi M., Fujihara K., Havrdova E., Hutchinson M., Kappos L., Lublin F.D., Montalban X., O'Connor P., Sandberg-Wollheim M., Thompson A.J., Waubant E., Weinshenker B., Wolinsky J.S. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann. Neurol. 2011, 69(2):292-302. (Feb), (URL http://dx.doi.org/10.1002/ana.22366).
72. Prinster A., Quarantelli M., Orefice G., Lanzillo R., Brunetti A., Mollica C., Salvatore E., Brescia Morra V., Coppola G., Vacca G., Alfano B., Salvatore M. Grey matter loss in relapsing-remitting multiple sclerosis: a voxel-based morphometry study. NeuroImage 2006, 29:859-867.
73. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(2):676-682. (Jan), (URL http://dx.doi.org/10.1073/pnas.98.2.676).
74. Rashid W., Parkes L., Ingle G., Chard D., Toosy A., Altmann D., Symms M., Tofts P., Thompson A., Miller D. Abnormalities of cerebral perfusion in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 2004, 75(9):1288-1293. (URL http://www.scopus.com/inward/record.url?eid=2-s2.0-4344661629&partnerID=40&md5=f852ccf9dc516189d966445fd6cce419).
75. Ratchford J.N., Calabresi P.A. The diagnosis of MS: white spots and red flags. Neurology 2008, 70(13 Part 2):1071-1072. (URL http://www.neurology.org).
76. Reddy H., Narayanan S., Matthews P.M., Hoge R.D., Pike G.B., Duquette P., Antel J., Arnold D.L. Relating axonal injury to functional recovery in ms. Neurology 2000, 54(1):236-239. (Jan).
77. Reddy H., Narayanan S., Arnoutelis R., Jenkinson M., Antel J., Matthews P.M., Arnold D.L. Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. Brain 2000, 123(Pt11):2314-2320. Nov.
78. Reich D.S., Smith S.A., Gordon-Lipkin E.M., Ozturk A., Caffo B.S., Balcer L.J., Calabresi P.A. Damage to the optic radiation in multiple sclerosis is associated with retinal injury and visual disability. Arch. Neurol. 2009, 66(8):998-1006. (Aug), (URL http://dx.doi.org/10.1001/archneurol.2009 107).
79. Richiardi J., Van De Ville D., Riesen K., Bunke H. Vector space embedding of undirected graphs with fixed-cardinality vertex sequences for classification. Proc. 20th Int. Conf. on Pattern Recognition (ICPR) 2010, 902-905.
80. Richiardi J., Eryilmaz H., Schwartz S., Vuilleumier P., Van De Ville D. Decoding brain states from fMRI connectivity graphs. NeuroImage 2011, 56(2):616-626. (May), (Special Issue on Multivariate Decoding and Brain Reading).
81. Rocca M.A., Filippi M. Functional MRI in multiple sclerosis. J. Neuroimaging 2007, 17(Suppl. 1):36S-41S. (Apr), (URL http://dx.doi.org/10.1111/j.1552-6569.2007.00135.x).
82. Rocca M.A., Pagani E., Absinta M., Valsasina P., Falini A., Scotti G., Comi G., Filippi M. Altered functional and structural connectivities in patients with MS: a 3-T study. Neurology 2007, 69(23):2136-2145. (Dec), (URL http://dx.doi.org/10.1212/01.wnl.0000295504.92020.ca).
83. Rocca M.A., Valsasina P., Absinta M., Riccitelli G., Rodegher M.E., Misci P., Rossi P., Falini A., Comi G., Filippi M. Default-mode network dysfunction and cognitive impairment in progressive MS. Neurology 2010, 74(16):1252-1259. (Apr), (URL http://dx.doi.org/10.1212/WNL.0b013e3181d9ed91).
84. Rolak L.A., Fleming J.O. The differential diagnosis of multiple sclerosis. Neurologist 2007, 13(2):57-72. (March).
85. Roosendaal S.D., Schoonheim M.M., Hulst H.E., Sanz-Arigita E.J., Smith S.M., Geurts J.J.G., Barkhof F. Resting state networks change in clinically isolated syndrome. Brain 2010, 133(Pt 6):1612-1621. (Jun), (URL http://dx.doi.org/10.1093/brain/awq058).
86. Rousseeuw P.J., Driessen K.V. A fast algorithm for the minimum covariance determinant estimator. Technometrics 1998, 41:212-223.
87. Rovira A., Swanton J., Tintore M., Huerga E., Barkhof F., Filippi M., Frederiksen J.L., Langkilde A., Miszkiel K., Polman C., Rovaris M., Sastre-Garriga J., Miller D., Montalban X. A single, early magnetic resonance imaging study in the diagnosis of multiple sclerosis. Arch. Neurol. 2009, 66(5):587-592. (May), (URL http://archneur.ama-assn.org/cgi/content/abstract/66/5/587).
88. 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 2005, 15(9):1332-1342. (Sep), (URL http://dx.doi.org/10.1093/cercor/bhi016).
89. Shirer W.R., Ryali S., Rykhlevskaia E., Menon V., Greicius M.D. Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb. Cortex 2011, 10.1093/cercor/bhr099.
90. Song S.-K., Sun S.-W., Ju W.-K., Lin S.-J., Cross A.H., Neufeld A.H. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage 2003, 20(3):1714-1722. (Nov).
91. Swanton J.K., Rovira A., Tintore M., Altmann D.R., Barkhof F., Filippi M., Huerga E., Miszkiel K.A., Plant G.T., Polman C., Rovaris M., Thompson A.J., Montalban X., Miller D.H. Mri criteria for multiple sclerosis in patients presenting with clinically isolated syndromes: a multicentre retrospective study. Lancet Neurol. 2007, 6(8):677-686. (August), (URL http://dx.doi.org/10.1016/S1474-4422(07)70176-X).
92. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., Bo L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 1998, 338(5):278-285. (Jan.), (URL http://content.nejm.org/cgi/content/abstract/338/5/278).
93. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002, 15:273-289.
94. Vercellino M., Masera S., Lorenzatti M., Condello C., Merola A., Mattioda A., Tribolo A., Capello E., Mancardi G.L., Mutani R., Giordana M.T., Cavalla P. Demyelination, inflammation, and neurodegeneration in multiple sclerosis deep gray matter. J. Neuropathol. Exp. Neurol. 2009, 68(5):489-502. (May), (URL http://dx.doi.org/10.1097/NEN.0b013e3181a19a5a).
95. Weil R.S., Rees G. Decoding the neural correlates of consciousness. Curr. Opin. Neurol. 2010, 23(6):649-655. (Dec), (URL http://dx.doi.org/10.1097/WCO.0b013e32834028c7).
96. Weygandt M., Hackmack K., Pfüller C., Bellmann-Strobl J., Paul F., Zipp F., Haynes J. Mri pattern recognition in multiple sclerosis normalappearing brain areas. PLoS One 2011, 6(6):e21138-e. (Jun.), (URL http://dx.doi.org/10.1371%2Fjournal.pone.0021138).
97. Wylezinska M., Cifelli A., Jezzard P., Palace J., Alecci M., Matthews P.M. Thalamic neurodegeneration in relapsing-remitting multiple sclerosis. Neurology 2003, 60(12):1949-1954. (URL http://www.neurology.org/content/60/12/1949.abstract).
98. Yaldizli O., Glassl S., Sturm D., Papadopoulou A., Gass A., Tettenborn B., Putzki N. Fatigue and progression of corpus callosum atrophy in multiple sclerosis. J. Neurol. 2011, 258(12):2199-2205. (Dec). 10.1007/s00415-011-6091-0.
99. Zhu B., Moore G.R., Zwimpfer T.J., Kastrukoff L.F., Dyer J.K., Steeves J.D., Paty D.W., Cynader M.S. Axonal cytoskeleton changes in experimental optic neuritis. Brain Res. 1999, 824(2):204-217. (Apr).