Disturbed function and plasticity in multiple sclerosis as gleaned from functional magnetic resonance imaging

Current Opinion in Neurology

Volumn 16, Issue 3, 2003, Pages 275-282

  Filippi, Massimo ^a   Rocca, Maria A ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Brain plasticity; Disability; Functional magnetic resonance imaging; Multiple sclerosis

Indexed keywords

BRAIN; BRAIN CORTEX; CERVICAL SPINAL CORD; DISEASE COURSE; HUMAN; MULTIPLE SCLEROSIS; NERVE CELL PLASTICITY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; REVIEW; TISSUE INJURY;

CEREBRAL CORTEX; HUMANS; MAGNETIC RESONANCE IMAGING; MULTIPLE SCLEROSIS; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; MULTIPLE SCLEROSIS, RELAPSING-REMITTING; NEURONAL PLASTICITY;

EID: 0037782273     PISSN: 13507540     EISSN: None     Source Type: Journal    
DOI: 10.1097/00019052-200306000-00005     Document Type: Review

References (52)

1. Filippi M, Grossman RI. MRI techniques to monitor MS evolution: the present and the future [review]. Neurology 2002; 58:1147-1153.
2. Ferguson B, Matyszak MK, Esiri MM, Perry VH. Axonal damage in acute multiple sclerosis lesions. Brain 1997; 120:393-399.
3. Trapp BD, Ransohoff R, Rudick R. Axonal pathology in multiple sclerosis: relationship to neurologic disability. Curr Opin Neurol 1999; 12:295-302.
4. Kidd D, Barkhof F, McConnel R, et al. Cortical lesions in multiple sclerosis. Brain 1999; 122:17-26.
5. Brownell B, Hughes JT. The distribution of plaques in the cerebrum in multiple sclerosis. J Neurol Neurosurg Psychiatry 1962; 25:315-320.
6. Peterson JW, Bo L, Mork S, et al. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesion. Ann Neurol 2001; 50:389-400.
7. Ge Y, Grossman RI, Udupa JK, et al. Magnetization transfer ratio histogram analysis of normal-appearing gray matter and normal-appearing white matter in multiple sclerosis. J Comput Assist Tomogr 2002; 26:62-68.
8. Cercignani M, Bozzali M, Iannucci G, et al. Magnetisation transfer ratio and mean diffusivity of normal appearing white and grey matter from patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 2001; 70:311-317.
9. Bozzali M, Cercignani M, Sormani MP, et al. Quantification of brain gray matter damage in different MS phenotypes by use of diffusion tensor MR imaging. AJNR Am J Neuroradiol 2002; 23:985-988.
10. 1H magnetic resonance spectroscopy in mainly cortical gray matter of patients with multiple sclerosis. J Neurol 2002; 249:902-910.
11. Ogawa S, Menon RS, Kim SG, Ugurbil K. On the characteristics of functional magnetic resonance imaging of the brain [review]. Annu Rev Biophys Biomol Struct 1998; 27:447-474.
12. Vanzetta I, Grinvald A. Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. Science 1999; 286:1555-1558.
13. Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS. Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 1993; 30:161-173.
14. Worsley KJ, Friston KJ. Analysis of fMRI time-series revisited - again. NeuroImage 1995; 2:173-181.
15. Clanet M, Berry I, Boulanouar K. Functional imaging in multiple sclerosis. Int MS J 1997; 4:26-32.
16. Lee M, Reddy H, Johansen-Berg H, et al. The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis. Ann Neurol 2000; 47:606-613.
17. Werring DJ, Bullmore ET, Toosy AT, et al. 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.
18. Reddy H, Narayanan S, Matthews PM, et al. Relating axonal injury to functional recovery in MS. Neurology 2000; 54:236-239.
19. Rombouts SA, Lazeron RH, Scheltens P, et al. Visual activation patterns in patients with optic neuritis: an fMRI pilot study. Neurology 1998; 50:1896-1899.
20. Langkilde AR, Frederiksen JL, Rostrup E, Larsson HB. Functional MRI of the visual cortex and visual testing in patients with previous optic neuritis. Eur J Neurol 2002; 9:277-286.
21. Reddy H, Narayanan S, Arnoutelis R, et al. Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. Brain 2000; 123:2314-2320.
22. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med 2000; 343:938-952.
23. Iannucci G, Tortorella C, Rovaris M, et al. Prognostic value of MR and magnetization transfer imaging findings in patients with clinically isolated syndromes suggestive of multiple sclerosis at presentation. AJNR Am J Neuroradiol 2000; 21:1034-1038.
24. Brex PA, Jenkins R, Fox NC, et al. Detection of ventricular enlargement in patients at the earliest clinical stage of MS. Neurology 2000; 54:1689-1691.
25. Filippi M, Inglese M, Rovaris M, et al. Magnetization transfer imaging to monitor the evolution of MS: a 1-year follow-up study. Neurology 2000; 55:940-946.
26. Chard DT, Griffin CM, Parker GJ, et al. Brain atrophy in clinically early relapsing-remitting multiple sclerosis. Brain 2000; 125:327-337.
27. Kapeller P, McLean MA, Griffin CM, et al. Preliminary evidence for neuronal damage in cortical grey matter and normal appearing white matter in short duration relapsing-remitting multiple sclerosis: a quantitative MR spectroscopic imaging study. J Neurol 2001; 248:131-138.
28. Toosy AT, Werring DJ, Bullmore ET, et al. Functional magnetic resonance imaging of the cortical response to photic stimulation in humans following optic neuritis recovery. Neurosci Lett 2002; 330:255-259.
29. Russ MO, Cleff U, Lanfermann H, et al. Functional magnetic resonance imaging in acute unilateral optic neuritis. J Neuroimaging 2002; 12:339-350.
30. Rocca MA, Mezzapesa DM, Falini A, et al. Evidence for axonal pathology and adaptive cortical reorganisation in patients at presentation with clinically isolated syndromes suggestive of MS. NeuroImage (in press).
31. Pantano P, Iannetti GD, Caramia F, et al. Cortical motor reorganization after a single clinical attack of multiple sclerosis. Brain 2002; 125:1607-1615.
32. Pantano P, Mainero C, Iannetti GD, et al. Contribution of corticospinal tract damage to cortical motor reorganization after a single clinical attack of multiple sclerosis. NeuroImage 2002; 17:1837-1843. This study investigates the movement-associated cortical activations from patients with early multiple sclerosis. The presentation of the disease was an episode of optic neuritis (10 patients) or an episode of acute hemiparesis (10 patients). Two different patterns of activation were found. A bilateral activation of the cerebral hemispheres was detected in patients with a previous episode of hemiparesis, whereas an increased activation of the contralateral motor-related areas was seen in patients with a previous episode of optic neuritis. This indicates that cortical motor reorganization in the early phase of multiple sclerosis differs with different clinical presentation. Lesion volumes (measured on T2- and T1-weighted scans) in the corticospinal tracts and time since clinical onset were correlated with the extent of activations in motor areas of both cerebral hemispheres.
33. McDonald WI, Compston A, Edan G, et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol 2001; 50:121-127.
34. Rocca MA, Falini A, Colombo B, et al. 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. This study shows that cortical activation occurs over a rather diffuse sensorimotor network in non-disabled patients with RRMS in comparison with healthy volunteers matched for sex and age. It also suggests that increased recruitment of this cortical network might contribute to a limiting of the functional impact of multiple sclerosis-related injury, as suggested by the strong correlations found between the extent of fMRI activations and the severity of tissue damage, measured using magnetization transfer and diffusion tensor MRI.
35. Filippi M, Rocca MA, Colombo B, et al. Functional magnetic resonance imaging correlates of fatigue in multiple sclerosis. NeuroImage 2002; 15:559-567. In this study, a different movement-related brain pattern of cortical activations was demonstrated in 15 multiple sclerosis patients with fatigue compared with 14 multiple sclerosis patients without fatigue. This suggests that the dysruption of a complex movement-associated cortical/subcortical network might contribute to the genesis of this disabling multiple sclerosis symptom, and that fMRI might be valuable for monitoring symptomatic treatment efficacy.
36. Filippi M, Rocca MA, Minicucci L, et al. Magnetization transfer imaging of patients with definite MS and negative conventional MRI. Neurology 1999; 52:845-848.
37. Rocca MA, Pagani E, Ghezzi A, et al. Functional cortical changes in patients with MS and non-specific conventional MRI scans of the brain. NeuroImage (in press).
38. Liepert J, Dettmers C, Terborg C, Weiller C. Inhibition of ipsilateral motor cortex during phasic generation of low force. Clin Neurophysiol 2001; 112:114-121.
39. Lowe MJ, Phillips MD, Lurito JT, et al. Multiple sclerosis: low-frequency temporal blood oxygen level-dependent fluctuations indicate reduced functional connectivity initial results. Radiology 2002; 224:184-192.
40. Rocca MA, Colombo B, Pagani E, et al. Evidence for cortical functional changes in patients with migraine and white matter abnormalities on conventional and diffusion tensor MRI. Stroke (in press).
41. Reddy H, Narayanan S, Mitsumori T, et al. Functional brain reorganization for hand movement in patients with multiple sclerosis: defining distinct effects of injury and disability. Brain 2002; 125: 2646-2657. This study suggests that brain injury and disability in multiple sclerosis may lead to different patterns of activations with hand movements. Patients with significant motor impairment had increased activation of the primary and secondary somatosensory cortices, bilaterally. In contrast, patients with significant brain injury, measured using proton magnetic resonance spectroscopy, had increased recruitment of the ipsilateral premotor cortex and supplementary motor area, bilaterally.
42. Staffen W, Mair A, Zauner H, et al. Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task. Brain 2002; 125:1276-1282. This is the first study to investigate cognitive functioning in multiple sclerosis patients by using fMRI. It demonstrates an altered brain pattern of cortical activations in 21 patients with relapsing - remitting multiple sclerosis and no neuropsychological impairment during the performance of a simple cognitive task. This suggests a possible compensatory mechanism of cortical reorganization limiting the neuropsychological manifestations of the disease.
43. Thompson AJ, Montalban X, Barkhof F, et al. Diagnostic criteria for primary progressive multiple sclerosis: a position paper. Ann Neurol 2000; 47:831-835.
44. Filippi M, Comi G. Primary progressive multiple sclerosis. Milan: Springer; 2002.
45. Rocca MA, Matthews PM, Caputo D, et al. Evidence for widespread movement-associated functional MRI changes in patients with PPMS. Neurology 2002; 58:866-872.
46. Filippi M, Rocca MA, Falini A, et al. Correlations between structural CNS damage and functional MRI changes in primary progressive MS. NeuroImage 2002; 15:537-546. This study demonstrates widespread movement-associated cortical changes in 26 patients with PPMS with no clinical impairment of the tested limbs. In these patients, moderate to strong correlations were found between relative activations of cortical areas located in a widespread network for sensorimotor and multimodal integration and the severity of structural changes of the NABT (as measured using magnetization transfer and diffusion tensor MRI) and the severity of cervical cord damage (as measured using magnetization transfer MRI). This brings additional evidence for an adaptive role for cortical reorganization in limiting the consequences of multiple sclerosis injury in the brain and cervical cord.
47. Mesulam MM. From sensation to cognition. Brain 1998; 121:1013-1052.
48. Rao SM, Binder JR, Bandettini PA, et al. Functional magnetic resonance imaging of complex human movements. Neurology 1993; 43:2311-2318.
49. Paus T, Petrides M, Evans AC, Meyer E. Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J Neurophysiol 1993; 70:453-469.
50. de Gelder B. Neuroscience. More to seeing than meets the eye. Science 2000; 289:1148-1149.
51. Filippi M, Rocca MA, Mezzapesa DM, et al. The role of spinal cord damage on brain cortical plasticity: a functional magnetic resonance imaging study [abstract]. Mult Scler 2002; 8 (Suppl 1):S98.
52. Filippi M, Rocca MA, Rossi P, et al. Demyelination and cortical reorganization: functional MRI data from a case of subacute combined degeneration. NeuroImage 2003; 18:558-563. This multiparametric MRI study of a patient with an early diagnosis of subacute combined degeneration provides evidence that demyelination alone does not necessarily induce adaptive functional changes of the cerebral cortex.