Decrease of Mutual Information in Brain Electrical Activity of Patients with Relapsing-Remitting Multiple Sclerosis

The disturbance of cortical communication has been hypothesized as an important factor in the appearance of cognitive impairment in (MS). Cortical communication is quantified here in control subjects and patients with relapsing-remitting multiple sclerosis (RRMS) on the basis of mean coherence in the δ, θ, α, β and γ bands and using mutual information computed between pairs of bipolar EEG signals recorded during resting condition. Each patient received also a cognitive assessment using a battery of neuropsychological tests specific to cognitive deficits in MS. No difference was observed for the coherence indices whereas inter-hemispheric and right hemisphere mutual information is significantly lower in patients with MS than in control subjects. Moreover, inter-hemispheric mutual information decrease significantly with illness duration and right mutual information differentiate cognitively deficient and non-deficient patients. Mutual information allows to quantify the cortical communication in patients with RRMS and is related to clinical characteristics. Cortical communication quantified in a resting state might be a potential marker for the neurological damage induced by RRMS.

[1]  D. Wechsler,et al.  Echelle d'intelligence de Wechsler pour adultes , 2000 .

[2]  J. Bendat,et al.  Measurement and Analysis of Random Data , 1968 .

[3]  V. Haughton,et al.  Correlation of magnetic resonance imaging with neuropsychological testing in multiple sclerosis , 1989, Neurology.

[4]  Sébastien Lê,et al.  FactoMineR: An R Package for Multivariate Analysis , 2008 .

[5]  J. Beaumont,et al.  Modality-specific aspects of sustained and divided attentional performance in multiple sclerosis. , 2005, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[6]  J. Valk,et al.  Functional correlates of callosal atrophy in relapsing-remitting multiple sclerosis patients. A preliminary MRI study , 1998, Journal of Neurology.

[7]  E. Mayer,et al.  Interhemispheric transfer evaluation in multiple sclerosis. , 2000 .

[8]  A. Destée,et al.  Frontal lobe dysfunction in unilateral lenticulostriate infarcts. Prominent role of cortical lesions. , 1992, Archives of neurology.

[9]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[10]  J. Sepulcre,et al.  Abnormalities in brain synchronization are correlated with cognitive impairment in multiple sclerosis , 2009, Multiple sclerosis.

[11]  J. Schoffelen,et al.  Nonparametric statistical testing of coherence differences , 2007, Journal of Neuroscience Methods.

[12]  G Fein,et al.  Common reference coherence data are confounded by power and phase effects. , 1988, Electroencephalography and clinical neurophysiology.

[13]  David Gaffan Widespread Cortical Networks Underlie Memory and Attention , 2005, Science.

[14]  P. Pasqualetti,et al.  Cognitive dysfunction in patients with relapsing-remitting multiple sclerosis , 2006, Multiple sclerosis.

[15]  R. Knobler,et al.  Neuropsychological and structural brain lesions in multiple sclerosis , 1992, Neurology.

[16]  A. Nieto,et al.  Brain atrophy as a marker of cognitive impairment in mildly disabling relapsing–remitting multiple sclerosis , 2008, European journal of neurology.

[17]  Pierre Cazes,et al.  Quelques méthodes d'analyse factorielle d'une série de tableaux de données , 2004, Monde des Util. Anal. Données.

[18]  Marco Rovaris,et al.  Corpus callosum damage and cognitive dysfunction in benign MS , 2009, Human brain mapping.

[19]  Jérôme Pagès,et al.  Multiple factor analysis (AFMULT package) , 1994 .

[20]  L. Leocani,et al.  Movement preparation is affected by tissue damage in multiple sclerosis: Evidence from EEG event-related desynchronization , 2005, Clinical Neurophysiology.

[21]  M. Poncet,et al.  Functional and magnetic resonance imaging correlates of callosal involvement in multiple sclerosis. , 1993, Archives of neurology.

[22]  B. Parmenter,et al.  The association between cognitive impairment and physical disability in multiple sclerosis , 2005, Multiple sclerosis.

[23]  Hirofumi Ochi,et al.  [Cognitive impairment in multiple sclerosis]. , 2014, Brain and nerve = Shinkei kenkyu no shinpo.

[24]  A. Compston,et al.  Recommended diagnostic criteria for multiple sclerosis: Guidelines from the international panel on the diagnosis of multiple sclerosis , 2001, Annals of neurology.

[25]  R. Herndon,et al.  A longitudinal study of brain atrophy in relapsing multiple sclerosis , 1999, Neurology.

[26]  K. Hlavácková-Schindler,et al.  Causality detection based on information-theoretic approaches in time series analysis , 2007 .

[27]  K. Dujardin,et al.  [BCcogSEP: a French test battery evaluating cognitive functions in multiple sclerosis]. , 2004, Revue neurologique (Paris).

[28]  N. Geschwind Disconnexion syndromes in animals and man. II. , 1965, Brain : a journal of neurology.

[29]  T. Neumann-Haefelin,et al.  Ipsilateral silent period: A marker of callosal conduction abnormality in early relapsing–remitting multiple sclerosis? , 2006, Journal of Neurological Sciences.

[30]  J. DeLuca,et al.  Speed of information processing as a key deficit in multiple sclerosis: implications for rehabilitation , 1999, Journal of neurology, neurosurgery, and psychiatry.

[31]  G. Comi,et al.  Intra-voxel and inter-voxel coherence in patients with multiple sclerosis assessed using diffusion tensor MRI , 2002, Journal of Neurology.

[32]  C. Pozzilli,et al.  Anterior Corpus Callosum Atrophy and Verbal Fluency in Multiple Sclerosis , 1991, Cortex.

[33]  D. Gronwall Paced Auditory Serial-Addition Task: A Measure of Recovery from Concussion , 1977, Perceptual and motor skills.

[34]  D. Chard,et al.  Grey matter pathology in clinically early multiple sclerosis: Evidence from magnetic resonance imaging , 2009, Journal of the Neurological Sciences.

[35]  Stephen M. Rao,et al.  Cognitive dysfunction in multiple sclerosis. , 1991, Neurology.

[36]  J. DeLuca,et al.  Is Speed of Processing or Working Memory the Primary Information Processing Deficit in Multiple Sclerosis? , 2004, Journal of clinical and experimental neuropsychology.

[37]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[38]  Marco Rovaris,et al.  Electroencephalographic coherence analysis in multiple sclerosis: correlation with clinical, neuropsychological, and MRI findings , 2000, Journal of neurology, neurosurgery, and psychiatry.

[39]  Hitten P. Zaveri,et al.  On the use of bipolar montages for time-series analysis of intracranial electroencephalograms , 2006, Clinical Neurophysiology.

[40]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[41]  HERMAN BUSCHKE,et al.  Evaluating storage, retention, and retrieval in disordered memory and learning , 1974, Neurology.

[42]  C R Guttmann,et al.  A longitudinal study of callosal atrophy and interhemispheric dysfunction in relapsing-remitting multiple sclerosis. , 2001, Archives of neurology.

[43]  H. McFarland,et al.  Contrast-enhanced MRI lesions during treatment with interferonβ-1b predict increase in T1 black hole volume in patients with relapsing-remitting multiple sclerosis , 2005, Multiple sclerosis.

[44]  Cornelis J. Stam,et al.  Multiple sclerosis patients show a highly significant decrease in alpha band interhemispheric synchronization measured using MEG , 2006, NeuroImage.

[45]  Mara Cercignani,et al.  Exploring the relationship between white matter and gray matter damage in early primary progressive multiple sclerosis: An in vivo study with TBSS and VBM , 2009, Human brain mapping.

[46]  Emilio Portaccio,et al.  Multiple sclerosis-related cognitive changes: A review of cross-sectional and longitudinal studies , 2006, Journal of the Neurological Sciences.

[47]  John R. Terry,et al.  Topographic Organization of Nonlinear Interdependence in Multichannel Human EEG , 2002, NeuroImage.

[48]  M. Sá,et al.  Cognitive Dysfunction in Multiple Sclerosis , 2012, Front. Neur..

[49]  Emily Snook,et al.  Cognitive impairments in relapsing-remitting multiple sclerosis: a meta-analysis , 2008, Multiple sclerosis.

[50]  Hans Petter Langtangen,et al.  Python scripting for computational science , 2004 .

[51]  J Barbizet,et al.  Clinical and psychometrical study of a patient with memory disturbances. , 1968, International journal of neurology.

[52]  Peter A. Calabresi,et al.  Multiparametric magnetic resonance imaging analysis of the corticospinal tract in multiple sclerosis , 2007, NeuroImage.

[53]  J. Guàrdia,et al.  Specificity of frontal dysfunctions in relapsing-remitting multiple sclerosis. , 2007, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[54]  W. L. Benedict,et al.  Multiple Sclerosis , 2007, Journal - Michigan State Medical Society.

[55]  G Cazzato,et al.  A longitudinal study of brain atrophy and cognitive disturbances in the early phase of relapsing-remitting multiple sclerosis , 2001, Journal of neurology, neurosurgery, and psychiatry.

[56]  W. Mcdonald,et al.  The pathophysiology of multiple sclerosis: the mechanisms underlying the production of symptoms and the natural history of the disease. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[57]  D. Tucker,et al.  EEG coherency. I: Statistics, reference electrode, volume conduction, Laplacians, cortical imaging, and interpretation at multiple scales. , 1997, Electroencephalography and clinical neurophysiology.

[58]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[59]  Timothy Edward John Behrens,et al.  Discordant white matter N-acetylasparate and diffusion MRI measures suggest that chronic metabolic dysfunction contributes to axonal pathology in multiple sclerosis , 2007, NeuroImage.

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

[61]  J. Ranjeva,et al.  Onset and underpinnings of white matter atrophy at the very early stage of multiple sclerosis - a two-year longitudinal MRI/MRSI study of corpus callosum , 2007, Multiple sclerosis.

[62]  N. Geschwind Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[63]  J. D. Sèze,et al.  La BCcogSEP : une batterie courte d'évaluation des fonctions cognitives destinées aux patients souffrant de sclérose en plaques , 2004 .

[64]  G. vanRossum,et al.  Interactively testing remote servers using the Python programming language , 1991 .

[65]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .