Multi-task functional MRI in multiple sclerosis patients without clinical disability

NeuroImage

Volumn 59, Issue 1, 2012, Pages 573-581

  Colorado, René A ^a   Shukla, Karan ^a   Zhou, Yuxiang ^a   Wolinsky, Jerry S ^a   Narayana, Ponnada A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Anterior cingulate cortex; Cognitive control; Cortical reorganization; Dorsolateral prefrontal cortex; Functional magnetic resonance imaging; Multiple sclerosis

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISABILITY; EXPANDED DISABILITY STATUS SCALE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND MOVEMENT; HANDEDNESS; HUMAN; MALE; MENTAL PERFORMANCE; MULTIPLE SCLEROSIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; WORKING MEMORY;

ADULT; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; PSYCHOMOTOR PERFORMANCE;

EID: 80054106752     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.07.065     Document Type: Article

References (77)

1. Adler R.J. The Geometry of Random Fields 1981, John Wiley & Sons, Chichester.
2. Au Duong M.V., Boulanouar K., Audoin B., Treseras S., Ibarrola D., Malikova I., Confort-Gouny S., Celsis P., Pelletier J., Cozzone P.J., Ranjeva J.P. Modulation of effective connectivity inside the working memory network in patients at the earliest stage of multiple sclerosis. NeuroImage 2005, 24:533-538.
3. Audoin B., Ibarrola D., Ranjeva J.P., Confort-Gouny S., Malikova I., Ali-Chérif A., Pelletier J., Cozzone P. Compensatory cortical activation observed by fMRI during a cognitive task at the earliest stage of MS. Hum. Brain Mapp. 2003, 20:51-58.
4. Audoin B., Reuter F., Duong M.V., Malikova I., Confort-Gouny S., Cherif A.A., Cozzone P.J., Pelletier J., Ranjeva J.P. 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.
5. Bobholz J.A., Rao S.M., Lobeck L., Elsinger C., Gleason A., Kanz J., Durgerian S., Maas E. fMRI study of episodic memory in relapsing-remitting MS: correlation with T2 lesion volume. Neurology 2006, 67:1640-1645.
6. Botvinick M., Nystrom L.E., Fissell K., Carter C.S., Cohen J.D. Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 1999, 402:179-181.
7. Botvinick M.M., Braver T.S., Barch D.M., Carter C.S., Cohen J.D. Conflict monitoring and cognitive control. Psychol. Rev. 2001, 108:624-652.
8. 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, 129:527-537.
9. Carter C.S., van Veen V. Anterior cingulate cortex and conflict detection: an update of theory and data. Cogn. Affect. Behav. Neurosci. 2007, 7:367-379.
10. Chiaravalloti N.D., DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol. 2008, 7:1139-1151.
11. Collins L., Holmes C., Peters T., Evans A. Automatic 3-D model-based neuroanatomical segmentation. Hum. Brain Mapp. 1995, 3:190-208.
12. Datta S., Narayana P.A. Automated brain extraction from T2-weighted magnetic resonance images. J. Magn. Reson. Imaging 2011, 33:822-829.
13. Datta S., Sun X., Shukla K., Narayana P.A. Improved segmentation with high-resolution 3D MR images in MS. 17th Annual Meeting of the Organization on Human Brain Mapping, June 26-30, 2011, Quebec city, Quebec, Canada; Abstract #2386 2011.
14. DeLuca J., Chelune G.J., Tulsky D.S., Lengenfelder J., Chiaravalloti N.D. Is speed of processing or working memory the primary information processing deficit in multiple sclerosis?. J. Clin. Exp. Neuropsychol. 2004, 26:550-562.
15. D'Esposito M., Postle B.R., Ballard D., Lease J. Maintenance versus manipulation of information held in working memory: an event-related fMRI study. Brain Cogn. 1999, 41:66-86.
16. Drobyshevsky A., Baumann S.B., Schneider W. A rapid fMRI task battery for mapping of visual, motor, cognitive, and emotional function. NeuroImage 2006, 31:732-744.
17. Egner T., Hirsch J. Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information. Nat. Neurosci. 2005, 8:1784-1790.
18. Fitzgerald P.B., Srithiran A., Benitez J., Daskalakis Z.Z., Oxley T.J., Kulkarni J., Egan G.F. An fMRI study of prefrontal brain activation during multiple tasks in patients with major depressive disorder. Hum. Brain Mapp. 2008, 29:490-501.
19. Forn C., Barros-Loscertales A., Escudero J., Belloch V., Campos S., Parcet M.A., Avila C. Cortical reorganization during PASAT task in MS patients with preserved working memory functions. NeuroImage 2006, 31:686-691.
20. Friston K.J., Holmes A., Poline J.B., Price C.J., Frith C.D. Detecting activations in PET and fMRI: levels of inference and power. NeuroImage 1996, 4:223-235.
21. Giorgio A., Portaccio E., Stromillo M.L., Marino S., Zipoli V., Battaglini M., Blandino A., Bartolozzi M.L., Siracusa G., Amato M.P., De Stefano N. Cortical functional reorganization and its relationship with brain structural damage in patients with benign multiple sclerosis. Mult. Scler. 2010, 16:1326-1334.
22. Hillary F.G. Neuroimaging of working memory dysfunction and the dilemma with brain reorganization hypotheses. J. Int. Neuropsychol. Soc. 2008, 14:526-534.
23. Hillary F.G., Chiaravalloti N.D., Ricker J.H., Steffener J., Bly B.M., Lange G., Liu W.C., Kalnin A.J., DeLuca J. An investigation of working memory rehearsal in multiple sclerosis using fMRI. J. Clin. Exp. Neuropsychol. 2003, 25:965-978.
24. Hillary F.G., Genova H.M., Chiaravalloti N.D., Rypma B., DeLuca J. Prefrontal modulation of working memory performance in brain injury and disease. Hum. Brain Mapp. 2006, 27:837-847.
25. Kerns J.G., Cohen J.D., MacDonald A.W., Cho R.Y., Stenger V.A., Carter C.S. Anterior cingulate conflict monitoring and adjustments in control. Science 2004, 303:1023-1026.
26. Koch G., Rossi S., Prosperetti C., Codecà C., Monteleone F., Petrosini L., Bernardi G., Centonze D. Improvement of hand dexterity following motor cortex rTMS in multiple sclerosis patients with cerebellar impairment. Mult. Scler. 2008, 14:995-998.
27. 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, 47:606-613.
28. Lenzi D., Conte A., Mainero C., Frasca V., Fubelli F., Totaro P., Caramia F., Inghilleri M., Pozzilli C., Pantano P. Effect of corpus callosum damage on ipsilateral motor activation in patients with multiple sclerosis: a functional and anatomical study. Hum. Brain Mapp. 2007, 28:636-644.
29. Loitfelder M., Fazekas F., Petrovic K., Fuchs S., Ropele S., Wallner-Blazek M., Jehna M., Aspeck E., Khalil M., Schmidt R., Neuper C., Enzinger C. Reorganization in cognitive networks with progression of multiple sclerosis: insights from fMRI. Neurology 2011, 76:526-533.
30. Loubinoux I., Carel C., Alary F., Boulanouar K., Viallard G., Manelfe C., Rascol O., Celsis P., Chollet F. Within-session and between-session reproducibility of cerebral sensorimotor activation: a test-retest effect evidenced with functional magnetic resonance imaging. J. Cereb. Blood Flow Metab. 2001, 21:592-607.
31. 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, 21:858-867.
32. Manson S.C., Wegner C., Filippi M., Barkhof F., Beckmann C., Ciccarelli O., De Stefano N., 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 movement-associated brain deactivation in multiple sclerosis: further evidence for a functional pathology of interhemispheric neuronal inhibition. Exp. Brain Res. 2008, 187:25-31.
33. Mansouri F.A., Tanaka K., Buckley M.J. Conflict-induced behavioural adjustment: a clue to the executive functions of the prefrontal cortex. Nat. Rev. Neurosci. 2009, 10:141-152.
34. Mazziotta J., Toga A., Evans A., Fox P., Lancaster J., Zilles K., Woods R., Paus T., Simpson G., Pike B., Holmes C., Collins L., Thompson P., MacDonald D., Iacoboni M., Schormann T., Amunts K., Palomero-Gallagher N., Geyer S., Parsons L., Narr K., Kabani N., Le Goualher G., Boomsma D., Cannon T., Kawashima R., Mazoyer B. A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2001, 356:1293-1322.
35. McAllister T.W., Saykin A.J., Flashman L.A., Sparling M.B., Johnson S.C., Guerin S.J., Mamourian A.C., Weaver J.B., Yanofsky N. Brain activation during working memory 1month after mild traumatic brain injury: a functional MRI study. Neurology 1999, 53:1300-1308.
36. Meyn H., Kraemer M., de Greiff A., Diehl R.R. Activation of working memory in patients at the earliest stage of multiple sclerosis - an fMRI study. Clin. Neurol. Neurosurg. 2010, 112:490-495.
37. Miller E.K., Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 2001, 24:167-202.
38. Morishima Y., Okuda J., Sakai K. Reactive mechanism of cognitive control system. Cereb. Cortex. 2010, 20:2675-2683.
39. Mostofsky S.H., Schafer J.G., Abrams M.T., Goldberg M.C., Flower A.A., Boyce A., Courtney S.M., Calhoun V.D., Kraut M.A., Denckla M.B., Pekar J.J. fMRI evidence that the neural basis of response inhibition is task-dependent. Brain. Res. Cogn. Brain Res. 2003, 17:419-430.
40. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
41. Owen A.M., McMillan K.M., Laird A.R., Bullmore E. N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum. Brain Mapp. 2005, 25:46-59.
42. Padberg F., George M.S. Repetitive transcranial magnetic stimulation of the prefrontal cortex in depression. Exp. Neurol. 2009, 219:2-13.
43. Pantano P., Iannetti G.D., Caramia F., Mainero C., Di Legge S., Bozzao L., Pozzilli C., Lenzi G.L. Cortical motor reorganization after a single clinical attack of multiple sclerosis. Brain 2002, 125:1607-1615.
44. Pantano P., Mainero C., Iannetti G.D., Caramia F., Di Legge S., Piattella M.C., Pozzilli C., Bozzao L., Lenzi G.L. Contribution of corticospinal tract damage to cortical motor reorganization after a single clinical attack of multiple sclerosis. NeuroImage 2002, 17:1837-1843.
45. Pantano P., Mainero C., Caramia F. Functional brain reorganization in multiple sclerosis: evidence from fMRI studies. J. Neuroimaging 2006, 16:104-114.
46. Pelletier J., Audoin B., Reuter F., Ranjeva J. Plasticity in MS: from functional imaging to rehabilitation. Int. MS. J. 2009, 16:26-31.
47. Penner I.K., Rausch M., Kappos L., Opwis K., Radü E.W. Analysis of impairment related functional architecture in MS patients during performance of different attention tasks. J. Neurol. 2003, 250:461-472.
48. Perlstein W.M., Cole M.A., Demery J.A., Seignourel P.J., Dixit N.K., Larson M.J., Briggs R.W. Parametric manipulation of working memory load in traumatic brain injury: behavioral and neural correlates. J. Int. Neuropsychol. Soc. 2004, 10:724-741.
49. Petrides M. The role of the mid-dorsolateral prefrontal cortex in working memory. Exp. Brain Res. 2000, 133:44-54.
50. 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, 69:292-302.
51. Ramsaransing G., Maurits N., Zwanikken C., De Keyser J. Early prediction of a benign course of multiple sclerosis on clinical grounds: a systematic review. Mult. Scler. 2001, 7:345-347.
52. 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, 54:236-239.
53. 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, 123:2314-2320.
54. Reddy H., Narayanan S., Woolrich M., Mitsumori T., Lapierre Y., Arnold D.L., Matthews P.M. Functional brain reorganization for hand movement in patients with multiple sclerosis: defining distinct effects of injury and disability. Brain 2002, 125:2646-2657.
55. Rico A., Zaaraoui W., Franques J., Attarian S., Reuter F., Malikova I., Confort-Gouny S., Soulier E., Pouget J., Cozzone P.J., Pelletier J., Ranjeva J.P., Audoin B. Motor cortical reorganization is present after a single attack of multiple sclerosis devoid of cortico-spinal dysfunction. MAGMA 2011, 24:77-84.
56. Ridding M.C., Rothwell J.C. Is there a future for therapeutic use of transcranial magnetic stimulation?. Nat. Rev. Neurosci. 2007, 8:559-567.
57. Rocca M.A., Falini A., Colombo B., Scotti G., Comi G., Filippi M. Adaptive functional changes in the cerebral cortex of patients with nondisabling multiple sclerosis correlate with the extent of brain structural damage. Ann. Neurol. 2002, 51:330-339.
58. Rocca M.A., Matthews P.M., Caputo D., Ghezzi A., Falini A., Scotti G., Comi G., Filippi M. Evidence for widespread movement-associated functional MRI changes in patients with PPMS. Neurology 2002, 26:866-872.
59. Rocca M.A., Colombo B., Falini A., Ghezzi A., Martinelli V., Scotti G., Comi G., Filippi M. Cortical adaptation in patients with MS: a cross-sectional functional MRI study of disease phenotypes. Lancet Neurol. 2005, 4:618-626.
60. Roelofs A., van Turennout M., Coles M.G. Anterior cingulate cortex activity can be independent of response conflict in Stroop-like tasks. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:13884-13889.
61. Rombouts S.A., Lazeron R.H., Scheltens P., Uitdehaag B.M., Sprenger M., Valk J., Barkhof F. Visual activation patterns in patients with optic neuritis: an fMRI pilot study. Neurology 1998, 50:1896-1899.
62. Rypma B., D'Esposito M. The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. Proc. Natl. Acad. Sci. USA 1999, 96:6558-6563.
63. Rypma B., Berger J.S., D'Esposito M. The influence of working-memory demand and subject performance on prefrontal cortical activity. J. Cogn. Neurosci. 2002, 14:721-731.
64. Sajja B.R., Datta S., He R., Mehta M., Gupta R.K., Wolinsky J.S., Narayana P.A. Unified approach for multiple sclerosis lesion segmentation on brain MRI. Ann. Biomed. Eng. 2006, 34:142-1151.
65. Schneider W., Noll D.C., Cohen J.D. Functional topographic mapping of the cortical ribbon in human vision with conventional MRI scanners. Nature 1993, 365:150-153.
66. Schoonheim M.M., Geurts J.J., Barkhof F. The limits of functional reorganization in multiple sclerosis. Neurology 2010, 74:1246-1247.
67. Staffen W., Mair A., Zauner H., Unterrainer J., Niederhofer H., Kutzelnigg A., Ritter S., Golaszewski S., Iglseder B., Ladurner G. Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task. Brain 2002, 125:1275-1282.
68. Strasser-Fuchs S., Enzinger C., Ropele S., Wallner M., Fazekas F. Clinically benign multiple sclerosis despite large T2 lesion load: can we explain this paradox?. Mult. Scler. 2008, 14:205-211.
69. Sweet L.H., Rao S.M., Primeau M., Mayer A.R., Cohen R.A. Functional magnetic resonance imaging of working memory among multiple sclerosis patients. J. Neuroimaging 2004, 14:150-157.
70. Sweet L.H., Rao S.M., Primeau M., Durgerian S., Cohen R.A. Functional magnetic resonance imaging response to increased verbal working memory demands among patients with multiple sclerosis. Hum. Brain. Mapp. 2006, 27:28-36.
71. Tanji J., Hoshi E. Role of the lateral prefrontal cortex in executive behavioral control. Physiol. Rev. 2008, 88:37-57.
72. Tao G., Datta S., He R., Nelson F., Wolinsky J.S., Narayana P.A. Deep gray matter atrophy in multiple sclerosis: a tensor based morphometry. J. Neurol. Sci. 2009, 282:39-46.
73. Todd J.J., Marois R. Capacity limit of visual short-term memory in human posterior parietal cortex. Nature 2004, 428:751-754.
74. Wang J., Hier D.B. Motor reorganization in multiple sclerosis. Neurol. Res. 2007, 29:3-8.
75. Werring D.J., Bullmore E.T., Toosy A.T., Miller D.H., Barker G.J., MacManus D.G., Brammer M.J., Giampietro V.P., Brusa A., Brex P.A., Moseley I.F., Plant G.T., McDonald W.I., Thompson A.J. Recovery from optic neuritis is associated with a change in the distribution of cerebral response to visual stimulation: a functional magnetic resonance imaging study. J. Neurol. Neurosurg. Psychiatry 2000, 68:441-449.
76. Wishart H.A., Saykin A.J., McDonald B.C., Mamourian A.C., Flashman L.A., Schuschu K.R., Ryan K.A., Fadul C.E., Kasper L.H. Brain activation patterns associated with working memory in relapsing-remitting MS. Neurology 2004, 62:234-238.
77. Xu Y., Chun M.M. Dissociable neural mechanisms supporting visual short-term memory for objects. Nature 2006, 440:91-95.