Brain connectivity in patients with dystonia during motor tasks

The pathophysiology of dystonia has been related to abnormalities of sensorimotor integration and disorders in basal nuclei, but the role of other brain regions is still unclear. This study aims to investigate alterations of brain connectivity using multivariate electroencephalographic data to provide new insights of the brain connectivity dynamics of dystonia. We recorded electroencephalography (EEG) of patients with right upper limb idiopathic focal dystonia and paired controls during resting state, writing-from-memory, and finger-tapping tasks. We applied power spectrum analyses considering the mu, beta and gamma rhythms of the motor cortex and analyzed brain connectivity networks and microstates. The power spectra results showed that patients had a loss of desynchronization of the beta rhythm during the writing task. We observed differences in the structure of the connective core in beta rhythm, as well as, in the intensity of the patient's hubs observed with basis in path length measures in mu and beta rhythms. Abnormalities were also identified in microstates of default mode networks of patients associated with its performances during motor tasks. The EEG connectivity analyses provided interesting insights about the cortical electrophysiological patterns in dystonia, such as loss of event-related desynchronization, changes in the effective connectivity with similar signature to other neurological diseases, indications of alterations in the default-mode-network. Our findings are consistent with previously described connectivity abnormalities in neuroimaging studies confirming that dystonia is a network disorder.

[1]  Mark Hallett,et al.  Abnormal Reorganization of Functional Cortical Small-World Networks in Focal Hand Dystonia , 2011, PloS one.

[2]  T. Koenig,et al.  Cognitive response control in writer’s cramp , 2001, European journal of neurology.

[3]  Ritesh A. Ramdhani,et al.  Isolated Focal Dystonia as a Disorder of Large‐Scale Functional Networks , 2015, Cerebral cortex.

[4]  Abner Cardoso Rodrigues,et al.  Measures for brain connectivity analysis: nodes centrality and their invariant patterns , 2017, The European Physical Journal Special Topics.

[5]  Florian Castrop,et al.  Multiple changes of functional connectivity between sensorimotor areas in focal hand dystonia , 2014, Journal of Neurology, Neurosurgery & Psychiatry.

[6]  Olaf Sporns,et al.  THE HUMAN CONNECTOME: A COMPLEX NETWORK , 2011, Schizophrenia Research.

[7]  C. Beckmann,et al.  Changes in resting‐state brain networks in writer's cramp , 2012, Human brain mapping.

[8]  J. Wolpaw,et al.  Mu and Beta Rhythm Topographies During Motor Imagery and Actual Movements , 2004, Brain Topography.

[9]  Florian Losch,et al.  Electroencephalographic spectral power in writer's cramp patients: Evidence for motor cortex malfunctioning during the cramp , 2005, NeuroImage.

[10]  David G. Norris,et al.  An Investigation of Functional and Anatomical Connectivity Using Magnetic Resonance Imaging , 2002, NeuroImage.

[11]  Clement Hamani,et al.  Disrupted Nodal and Hub Organization Account for Brain Network Abnormalities in Parkinson’s Disease , 2016, Front. Aging Neurosci..

[12]  J. Doyon,et al.  Increased cortico-striatal connectivity during motor practice contributes to the consolidation of motor memory in writer's cramp patients , 2015, NeuroImage: Clinical.

[13]  M. Hallett,et al.  Phenomenology and classification of dystonia: A consensus update , 2013, Movement disorders : official journal of the Movement Disorder Society.

[14]  G. Pfurtscheller,et al.  Visualization of sensorimotor areas involved in preparation for hand movement based on classification of μ and central β rhythms in single EEG trials in man , 1994, Neuroscience Letters.

[15]  T. Münte,et al.  Increase in Beta-Band Activity during Preparation for Overt Speech in Patients with Parkinson’s Disease , 2017, Front. Hum. Neurosci..

[16]  Li Zhao,et al.  Power Spectrum Estimation of the Welch Method Based on Imagery EEG , 2013 .

[17]  Suzanne T. Witt,et al.  Functional neuroimaging correlates of finger-tapping task variations: An ALE meta-analysis , 2008, NeuroImage.

[18]  M. Hallett,et al.  Surround inhibition in the motor system , 2011, Experimental Brain Research.

[19]  Schreiber,et al.  Measuring information transfer , 2000, Physical review letters.

[20]  S. Lehéricy,et al.  The functional neuroanatomy of dystonia , 2011, Neurobiology of Disease.

[21]  H. Jasper,et al.  Electrocorticograms in man: Effect of voluntary movement upon the electrical activity of the precentral gyrus , 1949 .

[22]  Edson Amaro Júnior,et al.  Connective Core Structures in Cognitive Networks: The Role of Hubs , 2019, Entropy.

[23]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[24]  Thomas Koenig,et al.  EEG microstates as a tool for studying the temporal dynamics of whole-brain neuronal networks: A review , 2017, NeuroImage.

[25]  Jaeseung Jeong EEG dynamics in patients with Alzheimer's disease , 2004, Clinical Neurophysiology.

[26]  C. Stam Modern network science of neurological disorders , 2014, Nature Reviews Neuroscience.

[27]  Yong He,et al.  Diffusion Tensor Tractography Reveals Abnormal Topological Organization in Structural Cortical Networks in Alzheimer's Disease , 2010, The Journal of Neuroscience.

[28]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[29]  G. Ojemann,et al.  Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks , 1999, Clinical Neurophysiology.

[30]  S Fahn,et al.  Tolcapone , 1998, Neurology.

[31]  T. Wilson,et al.  Neuromagnetic Evidence of Abnormal Movement-Related Beta Desynchronization in Parkinson's Disease , 2013, Cerebral cortex.

[32]  Antonio Pisani,et al.  Dystonia as a network disorder: a concept in evolution , 2018, Current opinion in neurology.

[33]  M. Hallett,et al.  Pathophysiology of dystonia. , 2006, Journal of neural transmission. Supplementum.

[34]  A. Aron,et al.  High Working Memory Load Increases Intracortical Inhibition in Primary Motor Cortex and Diminishes the Motor Affordance Effect , 2016, The Journal of Neuroscience.

[35]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[36]  Cornelis J. Stam,et al.  Activity Dependent Degeneration Explains Hub Vulnerability in Alzheimer's Disease , 2012, PLoS Comput. Biol..

[37]  Hans-Christian Jabusch,et al.  Musician's cramp as manifestation of maladaptive brain plasticity: arguments from instrumental differences , 2012, Annals of the New York Academy of Sciences.

[38]  Md. Hedayetul Islam Shovon,et al.  Transfer Entropy and Information Flow Patterns in Functional Brain Networks during Cognitive Activity , 2014, ICONIP.

[39]  Spectral characteristics of the hippocampal LFP during contextual fear conditioning. , 2012, Einstein.

[40]  P. Rossini,et al.  Alpha, beta and gamma electrocorticographic rhythms in somatosensory, motor, premotor and prefrontal cortical areas differ in movement execution and observation in humans , 2016, Clinical Neurophysiology.

[41]  Aart J. Nederveen,et al.  Structural, functional and molecular imaging of the brain in primary focal dystonia—A review , 2011, NeuroImage.

[42]  P. Welch The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

[43]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

[44]  Clemens Brunner,et al.  Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks , 2006, NeuroImage.

[45]  A. Pisani,et al.  Abnormal plasticity in dystonia: Disruption of synaptic homeostasis , 2011, Neurobiology of Disease.