Clinical and imaging assessment of cognitive dysfunction in multiple sclerosis

The Lancet Neurology

Volumn 14, Issue 3, 2015, Pages 302-317

  Rocca, Maria A ^a,b   Amato, Maria P ^c   De Stefano, Nicola ^d   Enzinger, Christian ^e   Geurts, Jeroen J ^f   Penner, Iris K ^g   Rovira, Alex ^h   Sumowski, James F ⁱ   Valsasina, Paola ^a   Filippi, Massimo ^a,b  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

^d UNIVERSITY OF SIENA   (Italy)

^e MEDICAL UNIVERSITY OF GRAZ   (Austria)

^f VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^g UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^h HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

ⁱ KESSLER FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN CORTEX LESION; COGNITION; COGNITION ASSESSMENT; COGNITIVE DEFECT; COGNITIVE RESERVE; COMORBIDITY; DEPRESSION; FATIGUE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HUMAN; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROPHYSIOLOGICAL RECRUITMENT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REVIEW; WHITE MATTER; WHITE MATTER LESION; COGNITION DISORDERS; CROSS-SECTIONAL STUDY; DIAGNOSTIC IMAGING; LONGITUDINAL STUDY; PROCEDURES; PSYCHOLOGY;

COGNITION DISORDERS; CROSS-SECTIONAL STUDIES; DIAGNOSTIC IMAGING; HUMANS; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MULTIPLE SCLEROSIS; NEUROPSYCHOLOGICAL TESTS;

EID: 84923314421     PISSN: 14744422     EISSN: 14744465     Source Type: Journal    
DOI: 10.1016/S1474-4422(14)70250-9     Document Type: Review

References (146)

1. Charcot J Histologie de le sclerose en plaques. Gaz Hop (Paris) 1868, 141:554-558.
2. Filippi M, Rocca MA, Horsfield MA, et al. Imaging cortical damage and dysfunction in multiple sclerosis. JAMA Neurol 2013, 70:556-564.
3. Filippi M, Rocca MA, Barkhof F, et al. Association between pathological and MRI findings in multiple sclerosis. Lancet Neurol 2012, 11:349-360. the Attendees of the Correlation between Pathological MRI findings in MS workshop.
4. Filippi M, Rocca MA, Benedict RH, et al. The contribution of MRI in assessing cognitive impairment in multiple sclerosis. Neurology 2010, 75:2121-2128.
5. Geurts JJ, Calabrese M, Fisher E, Rudick RA Measurement and clinical effect of grey matter pathology in multiple sclerosis. Lancet Neurol 2012, 11:1082-1092.
6. Lassmann H The pathologic substrate of magnetic resonance alterations in multiple sclerosis. Neuroimaging Clin N Am 2008, 18:563-576.
7. Chiaravalloti ND, DeLuca J Cognitive impairment in multiple sclerosis. Lancet Neurol 2008, 7:1139-1151.
8. Benedict RHB, Fischer JS, Archibald CJ, et al. Minimal neuropsychological assessment of MS patients: a consensus approach. Clin Neuropsychol 2002, 16:381-397.
9. Benedict RHB, Cookfair D, Gavett R, et al. Validity of the minimal assessment of cognitive function in multiple sclerosis (MACFIMS). J Int Neuropsychol Soc 2006, 12:549-558.
10. Benedict RH, Cox D, Thompson LL, Foley F, Weinstock-Guttman B, Munschauer F Reliable screening for neuropsychological impairment in multiple sclerosis. Mult Scler 2004, 10:675-678.
11. Sherman TE, Rapport LJ, Ryan KA Awareness of deficit in multiple sclerosis. J Clin Exp Neuropsychol 2008, 30:301-311.
12. Marrie RA, Goldman M Validity of performance scales for disability assessment in multiple sclerosis. Mult Scler 2007, 13:1176-1182.
13. Benedict RH, Munschauer F, Linn R, et al. Screening for multiple sclerosis cognitive impairment using a self-administered 15-item questionnaire. Mult Scler 2003, 9:95-101.
14. Rao SM A manual for the brief, repeatable battery of neuropsychological tests in multiple sclerosis 1991, National Multiple Sclerosis Society, New York.
15. Strober L, Englert J, Munschauer F, Weinstock-Guttman B, Rao S, Benedict RH Sensitivity of conventional memory tests in multiple sclerosis: comparing the Rao Brief Repeatable Neuropsychological Battery and the Minimal Assessment of Cognitive Function in MS. Mult Scler 2009, 15:1077-1084.
16. Langdon DW, Amato MP, Boringa J, et al. Recommendations for a Brief International Cognitive Assessment for Multiple Sclerosis (BICAMS). Mult Scler 2012, 18:891-898.
17. Smith A Symbol digit modalities test: manual 1982, Western Psychological Services, Los Angeles, CA.
18. Delis DC, Kramer JH, Kaplan E, Ober BA California verbal learning test manual: second edition, adult version 2000, Psychological Corporation, San Antonio, TX.
19. Benedict RHB Brief visuospatial memory test - revised: professional manual 1997, Psychological Assessment Resources, Inc, Odessa, FL.
20. Amato MP, Portaccio E, Goretti B, et al. Relevance of cognitive deterioration in early relapsing-remitting MS: a 3-year follow-up study. Mult Scler 2010, 16:1474-1482. the TuSCIMS Study Group.
21. Benedict RH, Amato MP, Boringa J, et al. Brief International Cognitive Assessment for MS (BICAMS): international standards for validation. BMC Neurol 2012, 12:55.
22. Feinstein A Multiple sclerosis and depression. Mult Scler 2011, 17:1276-1281.
23. Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 1989, 46:1121-1123.
24. Morrow SA, Weinstock-Guttman B, Munschauer FE, Hojnacki D, Benedict RH Subjective fatigue is not associated with cognitive impairment in multiple sclerosis: cross-sectional and longitudinal analysis. Mult Scler 2009, 15:998-1005.
25. Andreasen AK, Spliid PE, Andersen H, Jakobsen J Fatigue and processing speed are related in multiple sclerosis. Eur J Neurol 2010, 17:212-218.
26. Simioni S, Ruffieux C, Bruggimann L, Annoni JM, Schluep M Cognition, mood and fatigue in patients in the early stage of multiple sclerosis. Swiss Med Wkly 2007, 137:496-501.
27. Diagnostic and statistical manual of mental disorders 2013, American Psychiatric Association, Arlington, VA. 5th edn.
28. Montgomery SA, Asberg M A new depression scale designed to be sensitive to change. Br J Psychiatry 1979, 134:382-389.
29. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J An inventory for measuring depression. Arch Gen Psychiatry 1961, 4:561-571.
30. Beck AT, Steer RA, Brown GK BDI-Fast screen for medical patients: manual 2000, Psychological Corporation, San Antonio, TX.
31. Benedict RH, Fishman I, McClellan MM, Bakshi R, Weinstock-Guttman B Validity of the Beck Depression Inventory-Fast Screen in multiple sclerosis. Mult Scler 2003, 9:393-396.
32. Penner IK, Raselli C, Stöcklin M, Opwis K, Kappos L, Calabrese P The Fatigue Scale for Motor and Cognitive Functions (FSMC): validation of a new instrument to assess multiple sclerosis-related fatigue. Mult Scler 2009, 15:1509-1517.
33. Rao SM, Leo GJ, Haughton VM, St Aubin-Faubert P, Bernardin L Correlation of magnetic resonance imaging with neuropsychological testing in multiple sclerosis. Neurology 1989, 39:161-166.
34. Swirsky-Sacchetti T, Mitchell DR, Seward J, et al. Neuropsychological and structural brain lesions in multiple sclerosis: a regional analysis. Neurology 1992, 42:1291-1295.
35. Arnett PA, Rao SM, Bernardin L, Grafman J, Yetkin FZ, Lobeck L Relationship between frontal lobe lesions and Wisconsin Card Sorting Test performance in patients with multiple sclerosis. Neurology 1994, 44:420-425.
36. Foong J, Rozewicz L, Quaghebeur G, et al. Executive function in multiple sclerosis. The role of frontal lobe pathology. Brain 1997, 120:15-26.
37. Miki Y, Grossman RI, Udupa JK, et al. Isolated U-fiber involvement in MS: preliminary observations. Neurology 1998, 50:1301-1306.
38. Rovaris M, Filippi M, Falautano M, et al. Relation between MR abnormalities and patterns of cognitive impairment in multiple sclerosis. Neurology 1998, 50:1601-1608.
39. Fulton JC, Grossman RI, Udupa J, et al. MR lesion load and cognitive function in patients with relapsing-remitting multiple sclerosis. AJNR Am J Neuroradiol 1999, 20:1951-1955.
40. Comi G, Rovaris M, Falautano M, et al. A multiparametric MRI study of frontal lobe dementia in multiple sclerosis. J Neurol Sci 1999, 171:135-144.
41. Camp SJ, Stevenson VL, Thompson AJ, et al. Cognitive function in primary progressive and transitional progressive multiple sclerosis: a controlled study with MRI correlates. Brain 1999, 122:1341-1348.
42. Rovaris M, Filippi M, Minicucci L, et al. Cortical/subcortical disease burden and cognitive impairment in patients with multiple sclerosis. AJNR Am J Neuroradiol 2000, 21:402-408.
43. Lazeron RH, Langdon DW, Filippi M, et al. Neuropsychological impairment in multiple sclerosis patients: the role of (juxta)cortical lesion on FLAIR. Mult Scler 2000, 6:280-285.
44. Foong J, Rozewicz L, Chong WK, Thompson AJ, Miller DH, Ron MA A comparison of neuropsychological deficits in primary and secondary progressive multiple sclerosis. J Neurol 2000, 247:97-101.
45. Filippi M, Tortorella C, Rovaris M, et al. Changes in the normal appearing brain tissue and cognitive impairment in multiple sclerosis. J Neurol Neurosurg Psychiatry 2000, 68:157-161.
46. Zivadinov R, De Masi R, Nasuelli D, et al. MRI techniques and cognitive impairment in the early phase of relapsing-remitting multiple sclerosis. Neuroradiology 2001, 43:272-278.
47. Pujol J, Vendrell P, Deus J, et al. The effect of medial frontal and posterior parietal demyelinating lesions on stroop interference. Neuroimage 2001, 13:68-75.
48. Nocentini U, Rossini PM, Carlesimo GA, et al. Patterns of cognitive impairment in secondary progressive stable phase of multiple sclerosis: correlations with MRI findings. Eur Neurol 2001, 45:11-18.
49. Rovaris M, Iannucci G, Falautano M, et al. Cognitive dysfunction in patients with mildly disabling relapsing-remitting multiple sclerosis: an exploratory study with diffusion tensor MR imaging. J Neurol Sci 2002, 195:103-109.
50. Archibald CJ, Wei X, Scott JN, et al. Posterior fossa lesion volume and slowed information processing in multiple sclerosis. Brain 2004, 127:1526-1534.
51. Benedict RHB, Weinstock-Guttman B, Fishman I, Sharma J, Tjoa CW, Bakshi R Prediction of neuropsychological impairment in multiple sclerosis: comparison of conventional magnetic resonance imaging measures of atrophy and lesion burden. Arch Neurol 2004, 61:226-230.
52. Lazeron RH, Boringa JB, Schouten M, et al. Brain atrophy and lesion load as explaining parameters for cognitive impairment in multiple sclerosis. Mult Scler 2005, 11:524-531.
53. Deloire MS, Salort E, Bonnet M, et al. Cognitive impairment as marker of diffuse brain abnormalities in early relapsing remitting multiple sclerosis. J Neurol Neurosurg Psychiatry 2005, 76:519-526.
54. Benedict RH, Bruce JM, Dwyer MG, et al. Neocortical atrophy, third ventricular width, and cognitive dysfunction in multiple sclerosis. Arch Neurol 2006, 63:1301-1306.
55. Lin X, Tench CR, Morgan PS, Constantinescu CS Use of combined conventional and quantitative MRI to quantify pathology related to cognitive impairment in multiple sclerosis. J Neurol Neurosurg Psychiatry 2008, 79:437-441.
56. Sánchez MP, Nieto A, Barroso J, Martín V, Hernández MA Brain atrophy as a marker of cognitive impairment in mildly disabling relapsing-remitting multiple sclerosis. Eur J Neurol 2008, 15:1091-1099.
57. Amato MP, Portaccio E, Stromillo ML, et al. Cognitive assessment and quantitative magnetic resonance metrics can help to identify benign multiple sclerosis. Neurology 2008, 71:632-638.
58. Rovaris M, Riccitelli G, Judica E, et al. Cognitive impairment and structural brain damage in benign multiple sclerosis. Neurology 2008, 71:1521-1526.
59. Tiemann L, Penner IK, Haupts M, Schlegel U, Calabrese P Cognitive decline in multiple sclerosis: impact of topographic lesion distribution on differential cognitive deficit patterns. Mult Scler 2009, 15:1164-1174.
60. Ukkonen M, Vahvelainen T, Hämäläinen P, Dastidar P, Elovaara I Cognitive dysfunction in primary progressive multiple sclerosis: a neuropsychological and MRI study. Mult Scler 2009, 15:1055-1061.
61. Calabrese M, Agosta F, Rinaldi F, et al. Cortical lesions and atrophy associated with cognitive impairment in relapsing-remitting multiple sclerosis. Arch Neurol 2009, 66:1144-1150.
62. Heesen C, Schulz KH, Fiehler J, et al. Correlates of cognitive dysfunction in multiple sclerosis. Brain Behav Immun 2010, 24:1148-1155.
63. Rossi F, Giorgio A, Battaglini M, et al. Relevance of brain lesion location to cognition in relapsing multiple sclerosis. PLoS One 2012, 7:e44826.
64. Hulst HE, Steenwijk MD, Versteeg A, et al. Cognitive impairment in MS: impact of white matter integrity, gray matter volume, and lesions. Neurology 2013, 80:1025-1032.
65. Papadopoulou A, Müller-Lenke N, Naegelin Y, et al. Contribution of cortical and white matter lesions to cognitive impairment in multiple sclerosis. Mult Scler 2013, 19:1290-1296.
66. Hohol MJ, Guttmann CR, Orav J, et al. Serial neuropsychological assessment and magnetic resonance imaging analysis in multiple sclerosis. Arch Neurol 1997, 54:1018-1025.
67. Sperling RA, Guttmann CR, Hohol MJ, et al. Regional magnetic resonance imaging lesion burden and cognitive function in multiple sclerosis: a longitudinal study. Arch Neurol 2001, 58:115-121.
68. Camp SJ, Stevenson VL, Thompson AJ, et al. A longitudinal study of cognition in primary progressive multiple sclerosis. Brain 2005, 128:2891-2898.
69. Bellmann-Strobl J, Wuerfel J, Aktas O, et al. Poor PASAT performance correlates with MRI contrast enhancement in multiple sclerosis. Neurology 2009, 73:1624-1627.
70. Kincses ZT, Ropele S, Jenkinson M, et al. Lesion probability mapping to explain clinical deficits and cognitive performance in multiple sclerosis. Mult Scler 2011, 17:681-689.
71. Vellinga MM, Geurts JJ, Rostrup E, et al. Clinical correlations of brain lesion distribution in multiple sclerosis. J Magn Reson Imaging 2009, 29:768-773.
72. Sepulcre J, Masdeu JC, Pastor MA, et al. Brain pathways of verbal working memory: a lesion-function correlation study. Neuroimage 2009, 47:773-778.
73. Summers M, Swanton J, Fernando K, et al. Cognitive impairment in multiple sclerosis can be predicted by imaging early in the disease. J Neurol Neurosurg Psychiatry 2008, 79:955-958.
74. Summers M, Fisniku L, Anderson V, Miller D, Cipolotti L, Ron M Cognitive impairment in relapsing-remitting multiple sclerosis can be predicted by imaging performed several years earlier. Mult Scler 2008, 14:197-204.
75. Penny S, Khaleeli Z, Cipolotti L, Thompson A, Ron M Early imaging predicts later cognitive impairment in primary progressive multiple sclerosis. Neurology 2010, 74:545-552.
76. Mesaros S, Rocca MA, Riccitelli G, et al. Corpus callosum damage and cognitive dysfunction in benign MS. Hum Brain Mapp 2009, 30:2656-2666.
77. Fink F, Eling P, Rischkau E, et al. The association between California Verbal Learning Test performance and fibre impairment in multiple sclerosis: evidence from diffusion tensor imaging. Mult Scler 2010, 16:332-341.
78. Van Hecke W, Nagels G, Leemans A, Vandervliet E, Sijbers J, Parizel PM Correlation of cognitive dysfunction and diffusion tensor MRI measures in patients with mild and moderate multiple sclerosis. J Magn Reson Imaging 2010, 31:1492-1498.
79. Roca M, Torralva T, Meli F, et al. Cognitive deficits in multiple sclerosis correlate with changes in fronto-subcortical tracts. Mult Scler 2008, 14:364-369.
80. Khaleeli Z, Cercignani M, Audoin B, Ciccarelli O, Miller DH, Thompson AJ Localized grey matter damage in early primary progressive multiple sclerosis contributes to disability. Neuroimage 2007, 37:253-261.
81. Dineen RA, Vilisaar J, Hlinka J, et al. Disconnection as a mechanism for cognitive dysfunction in multiple sclerosis. Brain 2009, 132:239-249.
82. Roosendaal SD, Geurts JJ, Vrenken H, et al. Regional DTI differences in multiple sclerosis patients. Neuroimage 2009, 44:1397-1403.
83. Mesaros S, Rocca MA, Kacar K, et al. Diffusion tensor MRI tractography and cognitive impairment in multiple sclerosis. Neurology 2012, 78:969-975.
84. Kutzelnigg A, Lucchinetti CF, Stadelmann C, et al. Cortical demyelination and diffuse white matter injury in multiple sclerosis. Brain 2005, 128:2705-2712.
85. Seewann A, Enzinger C, Filippi M, et al. MRI characteristics of atypical idiopathic inflammatory demyelinating lesions of the brain: a review of reported findings. J Neurol 2008, 255:1-10. the MAGNIMS network.
86. Roosendaal SD, Moraal B, Vrenken H, et al. In vivo MR imaging of hippocampal lesions in multiple sclerosis. J Magn Reson Imaging 2008, 27:726-731.
87. Calabrese M, Poretto V, Favaretto A, et al. Cortical lesion load associates with progression of disability in multiple sclerosis. Brain 2012, 135:2952-2961.
88. Geurts JJ, Roosendaal SD, Calabrese M, et al. Consensus recommendations for MS cortical lesion scoring using double inversion recovery MRI. Neurology 2011, 76:418-424. the MAGNIMS Study Group.
89. Nelson F, Poonawalla AH, Hou P, Huang F, Wolinsky JS, Narayana PA Improved identification of intracortical lesions in multiple sclerosis with phase-sensitive inversion recovery in combination with fast double inversion recovery MR imaging. AJNR Am J Neuroradiol 2007, 28:1645-1649.
90. Nelson F, Poonawalla A, Hou P, Wolinsky JS, Narayana PA 3D MPRAGE improves classification of cortical lesions in multiple sclerosis. Mult Scler 2008, 14:1214-1219.
91. Mainero C, Benner T, Radding A, et al. In vivo imaging of cortical pathology in multiple sclerosis using ultra-high field MRI. Neurology 2009, 73:941-948.
92. Nelson F, Datta S, Garcia N, et al. Intracortical lesions by 3T magnetic resonance imaging and correlation with cognitive impairment in multiple sclerosis. Mult Scler 2011, 17:1122-1129.
93. Nielsen AS, Kinkel RP, Madigan N, Tinelli E, Benner T, Mainero C Contribution of cortical lesion subtypes at 7T MRI to physical and cognitive performance in MS. Neurology 2013, 81:641-649.
94. Riccitelli G, Rocca MA, Pagani E, et al. Cognitive impairment in multiple sclerosis is associated to different patterns of gray matter atrophy according to clinical phenotype. Hum Brain Mapp 2011, 32:1535-1543.
95. Houtchens MK, Benedict RH, Killiany R, et al. Thalamic atrophy and cognition in multiple sclerosis. Neurology 2007, 69:1213-1223.
96. Minagar A, Barnett MH, Benedict RH, et al. The thalamus and multiple sclerosis: modern views on pathologic, imaging, and clinical aspects. Neurology 2013, 80:210-219.
97. Muhlert N, Atzori M, De Vita E, et al. Memory in multiple sclerosis is linked to glutamate concentration in grey matter regions. J Neurol Neurosurg Psychiatry 2014, 85:833-839.
98. Batista S, Zivadinov R, Hoogs M, et al. Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J Neurol 2012, 259:139-146.
99. Sicotte NL, Kern KC, Giesser BS, et al. Regional hippocampal atrophy in multiple sclerosis. Brain 2008, 131:1134-1141.
100. Sanfilipo MP, Benedict RH, Weinstock-Guttman B, Bakshi R Gray and white matter brain atrophy and neuropsychological impairment in multiple sclerosis. Neurology 2006, 66:685-692.
101. Llufriu S, Martinez-Heras E, Fortea J, et al. Cognitive functions in multiple sclerosis: impact of gray matter integrity. Mult Scler 2014, 20:424-432.
102. Filippi M, Preziosa P, Copetti M, et al. Gray matter damage predicts the accumulation of disability 13 years later in MS. Neurology 2013, 81:1759-1767.
103. Battaglini M, Giorgio A, Stromillo ML, et al. Voxel-wise assessment of progression of regional brain atrophy in relapsing-remitting multiple sclerosis. J Neurol Sci 2009, 282:55-60.
104. Bendfeldt K, Kuster P, Traud S, et al. Association of regional gray matter volume loss and progression of white matter lesions in multiple sclerosis - A longitudinal voxel-based morphometry study. Neuroimage 2009, 45:60-67.
105. He Y, Dagher A, Chen Z, et al. Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. Brain 2009, 132:3366-3379.
106. Audoin B, Ibarrola D, Ranjeva JP, et al. Compensatory cortical activation observed by fMRI during a cognitive task at the earliest stage of MS. Hum Brain Mapp 2003, 20:51-58.
107. Mainero C, Caramia F, Pozzilli C, et al. fMRI evidence of brain reorganization during attention and memory tasks in multiple sclerosis. Neuroimage 2004, 21:858-867.
108. Rocca MA, Valsasina P, Ceccarelli A, et al. Structural and functional MRI correlates of Stroop control in benign MS. Hum Brain Mapp 2009, 30:276-290.
109. Audoin B, Au Duong MV, Ranjeva JP, et al. Magnetic resonance study of the influence of tissue damage and cortical reorganization on PASAT performance at the earliest stage of multiple sclerosis. Hum Brain Mapp 2005, 24:216-228.
110. Penner IK, Rausch M, Kappos L, Opwis K, Radü EW Analysis of impairment related functional architecture in MS patients during performance of different attention tasks. J Neurol 2003, 250:461-472.
111. Rocca MA, Riccitelli G, Rodegher M, et al. Functional MR imaging correlates of neuropsychological impairment in primary-progressive multiple sclerosis. AJNR Am J Neuroradiol 2010, 31:1240-1246.
112. Rocca MA, Agosta F, Colombo B, et al. fMRI changes in relapsing-remitting multiple sclerosis patients complaining of fatigue after IFNbeta-1a injection. Hum Brain Mapp 2007, 28:373-382.
113. Raichle ME, Snyder AZ A default mode of brain function: a brief history of an evolving idea. Neuroimage 2007, 37:1083-1090. discussion 1097-99.
114. Rocca MA, Valsasina P, Absinta M, et al. Default-mode network dysfunction and cognitive impairment in progressive MS. Neurology 2010, 74:1252-1259.
115. Bonavita S, Gallo A, Sacco R, et al. Distributed changes in default-mode resting-state connectivity in multiple sclerosis. Mult Scler 2011, 17:411-422.
116. Loitfelder M, Filippi M, Rocca M, et al. Abnormalities of resting state functional connectivity are related to sustained attention deficits in MS. PLoS One 2012, 7:e42862.
117. Hawellek DJ, Hipp JF, Lewis CM, Corbetta M, Engel AK Increased functional connectivity indicates the severity of cognitive impairment in multiple sclerosis. Proc Natl Acad Sci USA 2011, 108:19066-19071.
118. Faivre A, Rico A, Zaaraoui W, et al. Assessing brain connectivity at rest is clinically relevant in early multiple sclerosis. Mult Scler 2012, 18:1251-1258.
119. Rocca MA, Valsasina P, Hulst HE, et al. Functional correlates of cognitive dysfunction in multiple sclerosis: A multicenter fMRI Study. Hum Brain Mapp 2014, 35:5799-5814. the The MAGNIMS fMRI Study Group.
120. Cader S, Cifelli A, Abu-Omar Y, Palace J, Matthews PM Reduced brain functional reserve and altered functional connectivity in patients with multiple sclerosis. Brain 2006, 129:527-537.
121. Loitfelder M, Fazekas F, Petrovic K, et al. Reorganization in cognitive networks with progression of multiple sclerosis: insights from fMRI. Neurology 2011, 76:526-533.
122. Tortorella C, Romano R, Direnzo V, et al. Load-dependent dysfunction of the putamen during attentional processing in patients with clinically isolated syndrome suggestive of multiple sclerosis. Mult Scler 2013, 19:1153-1160.
123. Amann M, Dössegger LS, Penner IK, et al. Altered functional adaptation to attention and working memory tasks with increasing complexity in relapsing-remitting multiple sclerosis patients. Hum Brain Mapp 2011, 32:1704-1719.
124. Audoin B, Reuter F, Duong MV, et al. Efficiency of cognitive control recruitment in the very early stage of multiple sclerosis: a one-year fMRI follow-up study. Mult Scler 2008, 14:786-792.
125. Loitfelder M, Fazekas F, Koschutnig K, et al. Brain activity changes in cognitive networks in relapsing-remitting multiple sclerosis - insights from a longitudinal FMRI study. PLoS One 2014, 9:e93715.
126. Parry AM, Scott RB, Palace J, Smith S, Matthews PM Potentially adaptive functional changes in cognitive processing for patients with multiple sclerosis and their acute modulation by rivastigmine. Brain 2003, 126:2750-2760.
127. Cader S, Palace J, Matthews PM Cholinergic agonism alters cognitive processing and enhances brain functional connectivity in patients with multiple sclerosis. J Psychopharmacol 2009, 23:686-696.
128. Filippi M, Riccitelli G, Mattioli F, et al. Multiple sclerosis: effects of cognitive rehabilitation on structural and functional MR imaging measures--an explorative study. Radiology 2012, 262:932-940.
129. Sastre-Garriga J, Alonso J, Renom M, et al. A functional magnetic resonance proof of concept pilot trial of cognitive rehabilitation in multiple sclerosis. Mult Scler 2011, 17:457-467.
130. Cerasa A, Gioia MC, Valentino P, et al. Computer-assisted cognitive rehabilitation of attention deficits for multiple sclerosis: a randomized trial with fMRI correlates. Neurorehabil Neural Repair 2013, 27:284-295.
131. Roosendaal SD, Schoonheim MM, Hulst HE, et al. Resting state networks change in clinically isolated syndrome. Brain 2010, 133:1612-1621.
132. Rocca MA, Valsasina P, Martinelli V, et al. Large-scale neuronal network dysfunction in relapsing-remitting multiple sclerosis. Neurology 2012, 79:1449-1457.
133. Schoonheim MM, Hulst HE, Landi D, et al. Gender-related differences in functional connectivity in multiple sclerosis. Mult Scler 2012, 18:164-173.
134. Stern Y Cognitive reserve in ageing and Alzheimer's disease. Lancet Neurol 2012, 11:1006-1012.
135. Sumowski JF, Leavitt VM Cognitive reserve in multiple sclerosis. Mult Scler 2013, 19:1122-1127.
136. Sumowski JF, Rocca MA, Leavitt VM, et al. Brain reserve and cognitive reserve in multiple sclerosis: what you've got and how you use it. Neurology 2013, 80:2186-2193.
137. Sumowski JF, Wylie GR, Chiaravalloti N, DeLuca J Intellectual enrichment lessens the effect of brain atrophy on learning and memory in multiple sclerosis. Neurology 2010, 74:1942-1945.
138. Pinter D, Sumowski J, DeLuca J, et al. Higher education moderates the effect of T2 lesion load and third ventricle width on cognition in multiple sclerosis. PLoS One 2014, 9:e87567.
139. Amato MP, Razzolini L, Goretti B, et al. Cognitive reserve and cortical atrophy in multiple sclerosis: a longitudinal study. Neurology 2013, 80:1728-1733.
140. Sumowski JF, Wylie GR, Deluca J, Chiaravalloti N Intellectual enrichment is linked to cerebral efficiency in multiple sclerosis: functional magnetic resonance imaging evidence for cognitive reserve. Brain 2010, 133:362-374.
141. Benedict RH, Morrow SA, Weinstock Guttman B, Cookfair D, Schretlen DJ Cognitive reserve moderates decline in information processing speed in multiple sclerosis patients. J Int Neuropsychol Soc 2010, 16:829-835.
142. Sumowski JF, Rocca MA, Leavitt VM, et al. Brain reserve and cognitive reserve protect against cognitive decline over 4.5 years in MS. Neurology 2014, 82:1776-1783.
143. Schwartz CE, Snook E, Quaranto B, Benedict RH, Vollmer T Cognitive reserve and patient-reported outcomes in multiple sclerosis. Mult Scler 2013, 19:87-105.
144. Mahncke HW, Connor BB, Appelman J, et al. Memory enhancement in healthy older adults using a brain plasticity-based training program: a randomized, controlled study. Proc Natl Acad Sci USA 2006, 103:12523-12528.
145. Mattioli F, Stampatori C, Zanotti D, Parrinello G, Capra R Efficacy and specificity of intensive cognitive rehabilitation of attention and executive functions in multiple sclerosis. J Neurol Sci 2010, 288:101-105.
146. Amato MP, Goretti B, Viterbo RG, et al. Computer-assisted rehabilitation of attention in patients with multiple sclerosis: results of a randomized, double-blind trial. Mult Scler 2014, 20:91-98.