Preserved brain adaptive properties in patients with benign multiple sclerosis

Objectives: We investigated motor network function in patients with benign multiple sclerosis (BMS) and contrasted the results with those obtained from patients with secondary progressive multiple sclerosis (SPMS) and healthy controls (HC) to elucidate better the factors associated with a favorable clinical evolution in multiple sclerosis (MS). Methods: Diffusion tensor (DT) and fMRI scans during the performance of a simple motor task were prospectively acquired from 17 patients with BMS, 15 patients with SPMS, and 17 HC. Patients with BMS and SPMS were matched for age, gender, and disease duration. DT MRI histograms of the normal-appearing white matter (NAWM) and gray matter (GM) were derived. fMRI analysis was performed using SPM5 (Wellcome Department of Cognitive Neurology, London, UK). Results: Compared with HC, patients with BMS and SPMS had increased activations of the left primary sensorimotor cortex. Patients with SPMS also showed increased activations of the left secondary sensorimotor cortex, left inferior frontal gyrus (IFG), right hippocampus, and several visual areas. Compared with HC and patients with BMS, patients with SPMS had reduced activations of the left supplementary motor area, left putamen, and right cerebellum. Compared with patients with BMS, patients with SPMS had increased activations of the left IFG and right middle occipital gyrus. In patients with MS, fMRI changes were correlated with T2 lesion volumes and DT MRI changes in the NAWM and GM. Conclusions: This study shows that, contrary to what happens in secondary progressive multiple sclerosis, the movement-associated pattern of activations seen in benign multiple sclerosis resembles that of healthy people, and its abnormalities are restricted to the sensorimotor network. The long-term preservation of brain functional adaptive mechanisms in these patients is likely to contribute to their favorable clinical course.

[1]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[2]  M. Filippi,et al.  Is a preserved functional reserve a mechanism limiting clinical impairment in pediatric MS patients? , 2009, Human brain mapping.

[3]  M. Filippi,et al.  Simple and complex movement‐associated functional MRI changes in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis , 2004, Human brain mapping.

[4]  H. Maruyama,et al.  Functional , 2020, Congress of Neurological Surgeons Essent.

[5]  David H. Miller,et al.  Apparent diffusion coefficients in benign and secondary progressive multiple sclerosis by nuclear magnetic resonance , 1996, Magnetic resonance in medicine.

[6]  P M Matthews,et al.  The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis , 2000, Annals of neurology.

[7]  M. Filippi,et al.  Adaptive functional changes in the cerebral cortex of patients with nondisabling multiple sclerosis correlate with the extent of brain structural damage , 2002, Annals of neurology.

[8]  P M Matthews,et al.  Functional brain reorganization for hand movement in patients with multiple sclerosis: defining distinct effects of injury and disability. , 2002, Brain : a journal of neurology.

[9]  Sridar Narayanan,et al.  Axonal Damage in Multiple Sclerosis Patients with High versus Low Expanded Disability Status Scale Score , 2004, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[10]  Massimo Filippi,et al.  Normal-appearing white and grey matter damage in MS , 2007, Journal of Neurology.

[11]  M. Filippi,et al.  Functional cortical changes of the sensorimotor network are associated with clinical recovery in multiple sclerosis , 2008, Human brain mapping.

[12]  G J Barker,et al.  Comparison of multiple sclerosis clinical subgroups using navigated spin echo diffusion-weighted imaging. , 1999, Magnetic resonance imaging.

[13]  Jerry L Prince,et al.  Effects of signal‐to‐noise ratio on the accuracy and reproducibility of diffusion tensor imaging–derived fractional anisotropy, mean diffusivity, and principal eigenvector measurements at 1.5T , 2007, Journal of magnetic resonance imaging : JMRI.

[14]  Giuseppe Scotti,et al.  Evidence for axonal pathology and adaptive cortical reorganization in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis , 2003, NeuroImage.

[15]  P. Matthews,et al.  Normalized Accurate Measurement of Longitudinal Brain Change , 2001, Journal of computer assisted tomography.

[16]  D. Li,et al.  Benign versus chronic progressive multiple sclerosis: Magnetic resonance imaging features , 1989, Annals of neurology.

[17]  J. Kurtzke.  Rating neurologic impairment in multiple sclerosis , 1983, Neurology.

[18]  Giuseppe Scotti,et al.  A functional magnetic resonance imaging study of patients with secondary progressive multiple sclerosis , 2003, NeuroImage.

[19]  P M Matthews,et al.  Evidence for widespread movement-associated functional MRI changes in patients with PPMS , 2002, Neurology.

[20]  M. Filippi,et al.  Correlations between Structural CNS Damage and Functional MRI Changes in Primary Progressive MS , 2002, NeuroImage.

[21]  S. Reingold,et al.  Defining the clinical course of multiple sclerosis , 1996, Neurology.

[22]  M Rovaris,et al.  MRI features of benign multiple sclerosis , 2009, Neurology.

[23]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

[24]  M. Rausch,et al.  Analysis of Impairment Related Functional Architecture in MS Patients during Performance of Different Attention Tasks , 2003, Journal of Neurology.

[25]  M. Filippi,et al.  Cortical adaptation in patients with MS: a cross-sectional functional MRI study of disease phenotypes , 2005, The Lancet Neurology.

[26]  M. Preul.  The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy , 2001 .

[27]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[28]  C. Pozzilli,et al.  Brain reorganization during attention and memory tasks in multiple sclerosis: Insights from functional MRI studies , 2006, Journal of the Neurological Sciences.

[29]  J. Martín,et al.  Patterns of disease activity in multiple sclerosis. , 1990, BMJ.

[30]  M. Filippi,et al.  Functional MR imaging in multiple sclerosis. , 2009, Neuroimaging clinics of North America.

[31]  P. Matthews,et al.  Functional response to active and passive ankle movements with clinical correlations in patients with primary progressive multiple sclerosis , 2006, Journal of Neurology.