A multicentre study of motor functional connectivity changes in patients with multiple sclerosis

European Journal of Neuroscience

Volumn 33, Issue 7, 2011, Pages 1256-1263

  Valsasina, Paola ^a   Rocca, Maria A ^a   Absinta, Martina ^a   Sormani, Maria Pia ^b   Mancini, Laura ^c   De Stefano, Nicola ^d   Rovira, Alex ^e   Gass, Achim ^f   Enzinger, Christian ^g   Barkhof, Frederik ^h   Wegner, Christiane ⁱ   Matthews, Paul M ^i,j   Filippi, Massimo ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF SIENA   (Italy)

^e HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^f UNIVERSITY HOSPITAL BASEL   (Switzerland)

^g MEDICAL UNIVERSITY OF GRAZ   (Austria)

^h VU UNIVERSITY MEDICAL CENTER   (Netherlands)

ⁱ UNIVERSITY OF OXFORD   (United Kingdom)

^j HAMMERSMITH HOSPITAL   (United Kingdom)

more..

Author keywords

Connectivity; Cortical reorganization; Demyelination; Magnetic resonance imaging; Sensorimotor network

Indexed keywords

ADULT; ARTICLE; CEREBELLUM; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMISPHERIC DOMINANCE; HUMAN; INFERIOR FRONTAL GYRUS; INSULA; MAJOR CLINICAL STUDY; MALE; MIDDLE FRONTAL GYRUS; MOTOR PERFORMANCE; MULTICENTER STUDY (TOPIC); MULTIPLE SCLEROSIS; POSTCENTRAL GYRUS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SECONDARY SOMATOSENSORY CORTEX; SENSORIMOTOR CORTEX; SENSORIMOTOR FUNCTION; SUPPLEMENTARY MOTOR AREA; TASK PERFORMANCE; THALAMUS;

ADULT; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTOR ACTIVITY; MULTIPLE SCLEROSIS; NERVE NET; NEURAL PATHWAYS;

EID: 79953277768     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2011.07623.x     Document Type: Article

References (49)

1. Au Duong, M.V., Audoin, B., Boulanouar, K., Ibarrola, D., Malikova, I., Confort-Gouny, S., Celsis, P., Pelletier, J., Cozzone, P.J. & Ranjeva, J.P. (2005a) Altered functional connectivity related to white matter changes inside the working memory network at the very early stage of MS. J. Cereb. Blood Flow Metab., 25, 1245-1253.
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. (2005b) Modulation of effective connectivity inside the working memory network in patients at the earliest stage of multiple sclerosis. Neuroimage, 24, 533-538.
3. Bandettini, P.A., Jesmanowicz, A., Wong, E.C. & Hyde, J.S. (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Magn. Reson. Med., 30, 161-173.
4. Biswal, B., Yetkin, F.Z., Haughton, V.M. & Hyde, J.S. (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med., 34, 537-541.
5. Bosnell, R., Wegner, C., Kincses, Z.T., Korteweg, T., Agosta, F., Ciccarelli, O., De Stefano, N., Gass, A., Hirsch, J., Johansen-Berg, H., Kappos, L., Barkhof, F., Mancini, L., Manfredonia, F., Marino, S., Miller, D.H., Montalban, X., Palace, J., Rocca, M.A., Enzinger, C., Ropele, S., Rovira, A., Smith, S., Thompson, A., Thornton, J., Yousry, T., Whitcher, B., Filippi, M. & Matthews, P.M. (2008) Reproducibility of fMRI in the clinical setting: implications for trial designs. Neuroimage, 42, 603-610.
6. Brett, M., Anton, J.L., Valabregue, R. & Poline, J.B. (2002) Region of interest analysis using an SPM toolbox. 8th International Conference of Functional Mapping of the Human Brain, Sendai, Japan, 16, 2.
7. Cader, S., Cifelli, A., Abu-Omar, Y., Palace, J. & Matthews, P.M. (2006) Reduced brain functional reserve and altered functional connectivity in patients with multiple sclerosis. Brain, 129, 527-537.
8. Calautti, C. & Baron, J.C. (2003) Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke, 34, 1553-1566.
9. Cavada, C. & Goldman-Rakic, P.S. (1989) Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J. Comp. Neurol, 129, 422-445.
10. Ceccarelli, A., Rocca, M.A., Valsasina, P., Rodegher, M., Falini, A., Comi, G. & Filippi, M. (2010) Structural and functional magnetic resonance imaging correlates of motor network dysfunction in primary progressive multiple sclerosis. Eur. J. Neurosci., 31, 1273-1280.
11. Filippi, M., Rocca, M.A., Mezzapesa, D.M., Ghezzi, A., Falini, A., Martinelli, V., Scotti, G. & Comi, G. (2004) Simple and complex movement-associated functional MRI changes in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis. Hum. Brain Mapp., 21, 108-117.
12. Friedman, L., Stern, H., Brown, G.G., Mathalon, D.H., Turner, J., Glover, G.H., Gollub, R.L., Lauriello, J., Lim, K.O., Cannon, T., Greve, D.N., Bockholt, H.J., Belger, A., Mueller, B., Doty, M.J., He, J., Wells, W., Smyth, P., Pieper, S., Kim, S., Kubicki, M., Vangel, M. & Potkin, S.G. (2008) Test-retest and between-site reliability in a multicenter fMRI study. Hum. Brain Mapp., 29, 958-972.
13. Friston, K.J., Frith, C.D., Liddle, P.F. & Frackowiak, R.S. (1993) Functional connectivity: the principal-component analysis of large (PET) data sets. J. Cereb. Blood Flow Metab., 13, 5-14.
14. Friston, K.J., Holmes, A.P., Poline, J.B., Grasby, P.J., Williams, S.C., Frackowiak, R.S. & Turner, R. (1995) Analysis of fMRI time-series revisited. Neuroimage, 2, 45-53.
15. Friston, K.J., Mechelli, A., Turner, R. & Price, C.J. (2000) Nonlinear responses in fMRI: the Balloon model, Volterra kernels, and other hemodynamics. Neuroimage, 12, 466-477.
16. Friston, K.J., Harrison, L. & Penny, W. (2003) Dynamic causal modelling. Neuroimage, 19, 1273-1302.
17. Gountouna, V.E., Job, D.E., McIntosh, A.M., Moorhead, T.W., Lymer, G.K., Whalley, H.C., Hall, J., Waiter, G.D., Brennan, D., McGonigle, D.J., Ahearn, T.S., Cavanagh, J., Condon, B., Hadley, D.M., Marshall, I., Murray, A.D., Steele, J.D., Wardlaw, J.M. & Lawrie, S.M. (2010) Functional magnetic resonance imaging (fMRI) reproducibility and variance components across visits and scanning sites with a finger tapping task. Neuroimage, 49, 552-560.
18. Harrington, D.L., Rao, S.M., Haaland, K.Y., Bobholz, J.A., Mayer, A.R., Binderx, J.R. & Cox, R.W. (2000) Specialized neural systems underlying representations of sequential movements. J. Cogn. Neurosci., 12, 56-77.
19. Horwitz, B., Rumsey, J.M. & Donohue, B.C. (1998) Functional connectivity of the angular gyrus in normal reading and dyslexia. Proc. Natl Acad. Sci. USA, 95, 8939-8944.
20. Kim, S.G., Ashe, J., Hendrich, K., Ellermann, J.M., Merkle, H., Ugurbil, K. & Georgopoulos, A.P. (1993) Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. Science, 261, 615-617.
21. Koski, L. & Paus, T. (2000) Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis. Exp. Brain Res., 133, 55-65.
22. Kurtzke, J.F. (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology, 33, 1444-1452.
23. Long, X.Y., Zuo, X.N., Kiviniemi, V., Yang, Y., Zou, Q.H., Zhu, C.Z., Jiang, T.Z., Yang, H., Gong, Q.Y., Wang, L., Li, K.C., Xie, S. & Zang, Y.F. (2008) Default mode network as revealed with multiple methods for resting-state functional MRI analysis. J. Neurosci. Methods, 171, 349-355.
24. Lowe, M.J., Mock, B.J. & Sorenson, J.A. (1998) Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage, 7, 119-132.
25. Lowe, M.J., Beall, E.B., Sakaie, K.E., Koenig, K.A., Stone, L., Marrie, R.A. & Phillips, M.D. (2008) Resting state sensorimotor functional connectivity in multiple sclerosis inversely correlates with transcallosal motor pathway transverse diffusivity. Hum. Brain Mapp., 29, 818-827.
26. Mainero, C., Pantano, P., Caramia, F. & Pozzilli, C. (2006) Brain reorganization during attention and memory tasks in multiple sclerosis: insights from functional MRI studies. J. Neurol. Sci., 245, 93-98.
27. Mancini, L., Ciccarelli, O., Manfredonia, F., Thornton, J.S., Agosta, F., Barkhof, F., Beckmann, C., De Stefano, N., Enzinger, C., Fazekas, F., Filippi, M., Gass, A., Hirsch, J.G., Johansen-Berg, H., Kappos, L., Korteweg, T., Manson, S.C., Marino, S., Matthews, P.M., Montalban, X., Palace, J., Polman, C., Rocca, M.A., Ropele, S., Rovira, A., Wegner, C., Friston, K.J., Thompson, A. & Yousry, T. (2009) Short-term adaptation to a simple motor task: a physiological process preserved in multiple sclerosis. Neuroimage, 45, 500-511.
28. 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.A., Ropele, S., Rovira, A., Smith, S., Thompson, A., Thornton, J., Yousry, T., Frank, J.A. & Matthews, P.M. (2008) Impairment of movement-associated brain deactivation in multiple sclerosis: further evidence for a functional pathology of interhemispheric neuronal inhibition. Exp. Brain Res., 187, 25-31.
29. Mesulam, M.M. & Mufson, E.J. (1985) The insula of reil in man and monkey: architectonics, connectivity, and function. In Peters, A. & Jones, E.G. (Eds), Cerebral Cortex: Association and Auditory Cortices, Plenum Press, New York, pp. 179-226.
30. Ogawa, S., Lee, T.M., Nayak, A.S. & Glynn, P. (1990) Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn. Reson. Med., 14, 68-78.
31. Penny, W.D., Stephan, K.E., Mechelli, A. & Friston, K.J. (2004) Comparing dynamic causal models. Neuroimage, 22, 1157-1172.
32. Press, W.H., Teukolsky, S.A., Vetterling, W.T. & Flannery, B.P. (Eds). (1992) Numerical Recipes in C, 2nd edn. Cambridge University Press, Cambridge, UK.
33. Reddy, H., Narayanan, S., Woolrich, M., Mitsumori, T., Lapierre, Y., Arnold, D.L. & Matthews, P.M. (2002) Functional brain reorganization for hand movement in patients with multiple sclerosis: defining distinct effects of injury and disability. Brain, 125, 2646-2657.
34. Rocca, M.A. & Filippi, M. (2007) Functional MRI in multiple sclerosis. J. Neuroimaging, 17(Suppl. 1), S36-S41.
35. Rocca, M.A., Falini, A., Colombo, B., Scotti, G., Comi, G. & Filippi, M. (2002) Adaptive functional changes in the cerebral cortex of patients with nondisabling multiple sclerosis correlate with the extent of brain structural damage. Ann. Neurol., 51, 330-339.
36. Rocca, M.A., Colombo, B., Falini, A., Ghezzi, A., Martinelli, V., Scotti, G., Comi, G. & Filippi, M. (2005) Cortical adaptation in patients with MS: a cross-sectional functional MRI study of disease phenotypes. Lancet Neurol., 4, 618-626.
37. Rocca, M.A., Pagani, E., Absinta, M., Valsasina, P., Falini, A., Scotti, G., Comi, G. & Filippi, M. (2007) Altered functional and structural connectivities in patients with MS: a 3-T study. Neurology, 69, 2136-2145.
38. Rocca, M.A., Absinta, M., Valsasina, P., Ciccarelli, O., Marino, S., Rovira, A., Gass, A., Wegner, C., Enzinger, C., Korteweg, T., Sormani, M.P., Mancini, L., Thompson, A.J., De Stefano, N., Montalban, X., Hirsch, J., Kappos, L., Ropele, S., Palace, J., Barkhof, F., Matthews, P.M. & Filippi, M. (2009a) Abnormal connectivity of the sensorimotor network in patients with MS: a multicenter fMRI study. Hum. Brain Mapp., 30, 2412-2425.
39. Rocca, M.A., Valsasina, P., Ceccarelli, A., Absinta, M., Ghezzi, A., Riccitelli, G., Pagani, E., Falini, A., Comi, G., Scotti, G. & Filippi, M. (2009b) Structural and functional MRI correlates of Stroop control in benign MS. Hum. Brain Mapp., 30, 276-290.
40. Rocca, M.A., Valsasina, P., Absinta, M., Riccitelli, G., Rodegher, M.E., Misci, P., Rossi, P., Falini, A., Comi, G. & Filippi, M. (2010) Default-mode network dysfunction and cognitive impairment in progressive MS. Neurology, 74, 1252-1259.
41. Roosendaal, S., Hulst, H., Vrenken, H., Feenstra, H.E., Castelijns, J.A., Pouwels, P.J., Barkhof, F. & Geurts, J.J. (2010) Structural and functional hippocampal changes in multiple sclerosis patients with intact memory function. Radiology, 255, 595-604.
42. Saini, S., De Stefano, N., Smith, S., Guidi, L., Amato, M.P., Federico, A. & Matthews, P.M. (2004) Altered cerebellar functional connectivity mediates potential adaptive plasticity in patients with multiple sclerosis. J. Neurol. Neurosurg. Psychiatry, 75, 840-846.
43. Smith, S.M., Zhang, Y., Jenkinson, M., Chen, J., Matthews, P.M., Federico, A. & De Stefano, N. (2002) Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage, 17, 479-489.
44. Stephan, K.M., Fink, G.R., Passingham, R.E., Silbersweig, D., Ceballos-Baumann, A.O., Frith, C.D. & Frackowiak, R.S. (1995) Functional anatomy of the mental representation of upper extremity movements in healthy subjects. J. Neurophysiol., 73, 373-386.
45. Tomasi, D., Wang, G., Wang, R. & Volkow, N.D. (2008) Connectivity of complex networks: a Monte-Carlo based approach for dynamic causal modelling. Proceedings of the 16th Annual Meeting of the International Society of Magnetic Resonance in Medicine, Toronto, Ontario.
46. Ward, N.S. (2006) Compensatory mechanisms in the aging motor system. Ageing Res. Rev., 5, 239-254.
47. Wegner, C., Filippi, M., Korteweg, T., Beckmann, C., Ciccarelli, O., De Stefano, N., Enzinger, C., Fazekas, F., Agosta, F., Gass, A., Hirsch, J., Johansen-Berg, H., Kappos, L., Barkhof, F., Polman, C., Mancini, L., Manfredonia, F., Marino, S., Miller, D.H., Montalban, X., Palace, J., Rocca, M.A., Ropele, S., Rovira, A., Smith, S., Thompson, A., Thornton, J., Yousry, T. & Matthews, P.M. (2008) Relating functional changes during hand movement to clinical parameters in patients with multiple sclerosis in a multi-centre fMRI study. Eur. J. Neurol., 15, 113-122.
48. Wexler, B.E., Fulbright, R.K., Lacadie, C.M., Skudlarski, P., Kelz, M.B., Constable, R.T. & Gore, J.C. (1997) An fMRI study of the human cortical motor system response to increasing functional demands. Magn. Reson. Imaging, 15, 385-396.
49. Zou, K.H., Greve, D.N., Wang, M., Pieper, S.D., Warfield, S.K., White, N.S., Manandhar, S., Brown, G.C., Vangel, M.G., Kikinis, R. & Wells, W.M. (2005) Reproducibility of functional MR imaging: preliminary results of prospective multi-institutional study performed by Biomedical Informatics Research Network. Radiology, 237, 781-789.