Visual resting-state network in relapsing-remitting MS with and without previous optic neuritis

Objective: To investigate functional connectivity of the visual resting-state network (V-RSN) in normal-sighted relapsing-remitting multiple sclerosis (RRMS) patients with and without previous optic neuritis (ON). Methods: Thirty normal-sighted RRMS patients, 16 without (nON-MS) and 14 with (ON-MS) previous ON, and 15 age- and sex-matched healthy controls (HCs) underwent a neuro-ophthalmologic evaluation, including automated perimetry and retinal nerve fiber layer (RNFL) measurement, as well as an MRI protocol, including structural and resting-state fMRI (RS-fMRI) sequences. Functional connectivity of the V-RSN was evaluated by independent component analysis (ICA). Regional gray matter atrophy was assessed by voxel-based morphometry (VBM). A correlation analysis was performed between RS-fMRI results and clinical, neuro-ophthalmologic, and structural MRI variables. Results: Compared to HCs, patients with RRMS showed a reduced functional connectivity in the peristriate visual cortex, bilaterally. Compared to nON-MS, ON-MS patients revealed a region of stronger functional connectivity in the extrastriate cortex, at the level of right lateral middle occipital gyrus, as well as a region of reduced functional connectivity at the level of right inferior peristriate cortex. These latter changes correlated with the number of previous ON. All detected V-RSN changes did not colocalize with regional gray matter atrophy. Conclusions: Normal-sighted RRMS patients show a significant functional disconnection in the V-RSN. RRMS patients recovered from a previous ON show a complex reorganization of the V-RSN, including an increased functional connectivity at the level of extrastriate visual areas.

[1]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[2]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[3]  Jeff H. Duyn,et al.  Modulation of spontaneous fMRI activity in human visual cortex by behavioral state , 2009, NeuroImage.

[4]  G J Barker,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 , 2000, Journal of neurology, neurosurgery, and psychiatry.

[5]  V. Calhoun,et al.  Selective changes of resting-state networks in individuals at risk for Alzheimer's disease , 2007, Proceedings of the National Academy of Sciences.

[6]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Aapo Hyvärinen,et al.  Independent component analysis of fMRI group studies by self-organizing clustering , 2005, NeuroImage.

[8]  Ravi S. Menon,et al.  Reduced visual evoked responses in multiple sclerosis patients with optic neuritis: Comparison of functional magnetic resonance imaging and visual evoked potentials , 1999, Multiple sclerosis.

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

[10]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

[11]  H. Quigley,et al.  Visual acuity in optic atrophy: a quantitative clinicopathological analysis , 2005, Graefe's Archive for Clinical and Experimental Ophthalmology.

[12]  S. Reingold,et al.  Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria” , 2005, Annals of neurology.

[13]  M. Filippi,et al.  Extra-Visual Functional and Structural Connection Abnormalities in Leber's Hereditary Optic Neuropathy , 2011, PloS one.

[14]  M. Filippi,et al.  Default-mode network dysfunction and cognitive impairment in progressive MS , 2010, Neurology.

[15]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[16]  O. Gout.  Neuroplasticity predicts outcome of optic neuritis independent of tissue damage , 2010, Annals of neurology.

[17]  F. Barkhof,et al.  Resting state networks change in clinically isolated syndrome. , 2010, Brain : a journal of neurology.

[18]  T. Sejnowski,et al.  Independent component analysis of fMRI data: Examining the assumptions , 1998, Human brain mapping.

[19]  Chunshui Yu,et al.  Whole brain functional connectivity in the early blind. , 2007, Brain : a journal of neurology.

[20]  A Giorgio,et al.  Imaging distribution and frequency of cortical lesions in patients with multiple sclerosis , 2010, Neurology.

[21]  E. Formisano,et al.  Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest , 2004, Human brain mapping.

[22]  Rainer Goebel,et al.  Independent component model of the default-mode brain function: combining individual-level and population-level analyses in resting-state fMRI. , 2008, Magnetic resonance imaging.

[23]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[24]  E. Bullmore,et al.  Functional magnetic resonance imaging of the cortical response to photic stimulation in humans following optic neuritis recovery , 2002, Neuroscience Letters.

[25]  E Rostrup,et al.  Functional MRI of the visual cortex and visual testing in patients with previous optic neuritis , 2002, European journal of neurology.

[26]  Chunshui Yu,et al.  Spontaneous activity associated with primary visual cortex: a resting-state FMRI study. , 2008, Cerebral cortex.

[27]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[28]  A. J. Thompson,et al.  Assessing structure and function of the afferent visual pathway in multiple sclerosis and associated optic neuritis , 2009, Journal of Neurology.

[29]  G. Gigli,et al.  Nerve Fibre Layer Analysis with GDx with a Variable Corneal Compensator in Patients with Multiple Sclerosis , 2007, Ophthalmologica.

[30]  Aapo Hyvärinen,et al.  Fast and robust fixed-point algorithms for independent component analysis , 1999, IEEE Trans. Neural Networks.

[31]  B E Kendall,et al.  The early risk of multiple sclerosis after optic neuritis. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[32]  B. Biswal,et al.  Simultaneous assessment of flow and BOLD signals in resting‐state functional connectivity maps , 1997, NMR in biomedicine.

[33]  F. Esposito,et al.  Distributed changes in default-mode resting-state connectivity in multiple sclerosis , 2011, Multiple sclerosis.

[34]  A. Thompson,et al.  Is the frequency of abnormalities on magnetic resonance imaging in isolated optic neuritis related to the prevalence of multiple sclerosis? A global comparison , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[35]  G. Glover,et al.  Resting-State Functional Connectivity in Major Depression: Abnormally Increased Contributions from Subgenual Cingulate Cortex and Thalamus , 2007, Biological Psychiatry.

[36]  Fabrizio Esposito,et al.  Alcohol increases spontaneous BOLD signal fluctuations in the visual network , 2010, NeuroImage.

[37]  S. Rombouts,et al.  Visual activation patterns in patients with optic neuritis , 1998, Neurology.

[38]  Stephen J. Jones,et al.  Adaptive cortical plasticity in higher visual areas after acute optic neuritis , 2005, Annals of neurology.

[39]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.