Corticomuscular coherence in acute and chronic stroke

OBJECTIVE Motor recovery after stroke is attributed to neuronal plasticity, however not all post-stroke neuronal changes relate to regaining fine motor control. Corticomuscular coherence (CMC) is a measure allowing to trace neuronal reorganizations which are functionally relevant for motor recovery. Contrary to previous studies which were performed only in chronic stage, we measured CMC in patients with stroke at both acute and chronic stroke stages. METHODS For the detection of CMC we used multichannel EEG and EMG recordings along with an optimization algorithm for the detection of corticomuscular interactions. RESULTS In acute stroke, the CMC amplitude was larger on the unaffected side compared to the affected side and also larger compared to the unaffected side in the chronic period. Additionally, CMC peak frequencies on both sides decreased in the acute compared to the chronic period and to control subjects. In chronic stage, there were no inter-hemispheric or group differences in CMC amplitude or frequency. CONCLUSIONS The changes in CMC parameters in acute stroke could result from a temporary decrease in inhibition, which normalizes in the course of recovery. As all patients showed very good motor recovery, the modulation of CMC amplitude and frequency over time might thus reflect the process of motor recovery. SIGNIFICANCE We demonstrate for the first time the dynamical changes of corticomuscular interaction both at acute and chronic stage of stroke.

[1]  L. Goldstein,et al.  Potential effects of common drugs on stroke recovery. , 1998, Archives of neurology.

[2]  J. Ushiba,et al.  Between-subject variance in the magnitude of corticomuscular coherence during tonic isometric contraction of the tibialis anterior muscle in healthy young adults. , 2011, Journal of neurophysiology.

[3]  S. Jang.  A review of motor recovery mechanisms in patients with stroke. , 2007, NeuroRehabilitation.

[4]  W. Wong,et al.  Cerebral Plasticity After Subcortical Stroke as Revealed by Cortico-Muscular Coherence , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[5]  M. Hallett,et al.  Corticomuscular coherence: a review. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[6]  M Tombini,et al.  Long‐term effects of stroke on neuronal rest activity in rolandic cortical areas , 2006, Journal of neuroscience research.

[7]  Robert Oostenveld,et al.  The five percent electrode system for high-resolution EEG and ERP measurements , 2001, Clinical Neurophysiology.

[8]  I. Módy,et al.  Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. , 2010, Nature.

[9]  E. Olivier,et al.  Coherent oscillations in monkey motor cortex and hand muscle EMG show task‐dependent modulation , 1997, The Journal of physiology.

[10]  Y. Assaf,et al.  Diffusion Tensor Imaging (DTI)-based White Matter Mapping in Brain Research: A Review , 2007, Journal of Molecular Neuroscience.

[11]  Zoran Cvetkovic,et al.  Rectification of the EMG is an unnecessary and inappropriate step in the calculation of Corticomuscular coherence , 2012, Journal of Neuroscience Methods.

[12]  R. Hari,et al.  Synchronous cortical oscillatory activity during motor action , 2003, Current Opinion in Neurobiology.

[13]  Jose Luis Patino,et al.  Beta-range cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output , 2007, NeuroImage.

[14]  N. Takeuchi,et al.  Maladaptive Plasticity for Motor Recovery after Stroke: Mechanisms and Approaches , 2012, Neural plasticity.

[15]  Paul L. Furlong,et al.  The Role of Gabaergic Modulation in Motor Function Related Neuronal Network Activity the Role of Gabaergic Modulation in Motor Function Related Neuronal Network Activity , 2022 .

[16]  C. Nicholas Riddle,et al.  The effect of carbamazepine on human corticomuscular coherence , 2004, NeuroImage.

[17]  N. Dancause.  Vicarious Function of Remote Cortex following Stroke: Recent Evidence from Human and Animal Studies , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[18]  Stuart N. Baker,et al.  Digit displacement, not object compliance, underlies task dependent modulations in human corticomuscular coherence , 2006, NeuroImage.

[19]  Gabriel Curio,et al.  Event-related desynchronization of sensorimotor EEG rhythms in hemiparetic patients with acute stroke , 2011, Neuroscience Letters.

[20]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[21]  A. Kral,et al.  Erratum to “Development of Brainstem-Evoked Responses in Congenital Auditory Deprivation” , 2012, Neural Plasticity.

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

[23]  L. Tomasevic,et al.  The myth of the ‘unaffected’ side after unilateral stroke: Is reorganisation of the non‐infarcted corticospinal system to re-establish balance the price for recovery? , 2012, Experimental Neurology.

[24]  S. Rathore,et al.  Characterization of Incident Stroke Signs and Symptoms: Findings From the Atherosclerosis Risk in Communities Study , 2002, Stroke.

[25]  Ulf Ziemann,et al.  Rapid modulation of GABA in sensorimotor cortex induced by acute deafferentation , 2002, Annals of neurology.

[26]  R. Hari,et al.  Cortical control of human motoneuron firing during isometric contraction. , 1997, Journal of neurophysiology.

[27]  S. Baker,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[28]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[29]  Richard S. J. Frackowiak,et al.  Motor system activation after subcortical stroke depends on corticospinal system integrity. , 2006, Brain : a journal of neurology.

[30]  J. Rothwell,et al.  Arm function after stroke: Neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation , 2006, Clinical Neurophysiology.

[31]  Rüdiger J. Seitz,et al.  Relationship Between Interhemispheric Inhibition and Motor Cortex Excitability in Subacute Stroke Patients , 2008, Neurorehabilitation and neural repair.

[32]  M. Butz,et al.  Changes of cortico-muscular coherence: an early marker of healthy aging? , 2011, AGE.

[33]  G. Fink,et al.  Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches , 2011, Brain : a journal of neurology.

[34]  J. Rothwell,et al.  Stages of Motor Output Reorganization after Hemispheric Stroke Suggested by Longitudinal Studies of Cortical Physiology , 2008, Cerebral cortex.

[35]  Gabriel Curio,et al.  A novel method for reliable and fast extraction of neuronal EEG/MEG oscillations on the basis of spatio-spectral decomposition , 2011, NeuroImage.

[36]  F. Zappasodi,et al.  Developmental Tuning and Decay in Senescence of Oscillations Linking the Corticospinal System , 2010, The Journal of Neuroscience.

[37]  J. Rothwell,et al.  Cortical correlate of the Piper rhythm in humans. , 1998, Journal of neurophysiology.

[38]  S. Baker.  Oscillatory interactions between sensorimotor cortex and the periphery , 2007, Current Opinion in Neurobiology.

[39]  R. Oostenveld,et al.  The α-motoneuron pool as transmitter of rhythmicities in cortical motor drive , 2010, Clinical Neurophysiology.

[40]  R. Lemon,et al.  Human Cortical Muscle Coherence Is Directly Related to Specific Motor Parameters , 2000, The Journal of Neuroscience.

[41]  Paolo Maria Rossini,et al.  Rhythmic brain activity at rest from rolandic areas in acute mono-hemispheric stroke: A magnetoencephalographic study , 2005, NeuroImage.

[42]  Gabriel Curio,et al.  It is not all about phase: Amplitude dynamics in corticomuscular interactions , 2013, NeuroImage.

[43]  Yoshikazu Isomura,et al.  Directional organization of sensorimotor oscillatory activity related to the electromyogram in the monkey , 2009, Clinical Neurophysiology.

[44]  Stuart N Baker,et al.  Manipulation of peripheral neural feedback loops alters human corticomuscular coherence , 2005, The Journal of physiology.

[45]  N. Ward.  Neural plasticity and recovery of function. , 2005, Progress in brain research.

[46]  K H Mauritz,et al.  Multimodal EEG analysis in man suggests impairment-specific changes in movement-related electric brain activity after stroke. , 2000, Brain : a journal of neurology.

[47]  Alan J Thompson,et al.  The relationship between brain activity and peak grip force is modulated by corticospinal system integrity after subcortical stroke , 2007, The European journal of neuroscience.

[48]  Michel Rijntjes,et al.  Mechanisms of recovery in stroke patients with hemiparesis or aphasia: new insights, old questions and the meaning of therapies , 2006, Current opinion in neurology.

[49]  Barak A. Pearlmutter,et al.  Linear Spatial Integration for Single-Trial Detection in Encephalography , 2002, NeuroImage.

[50]  S. Rombouts,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[51]  Hubert Preissl,et al.  Crossed cortico‐spinal motor control after capsular stroke , 2007, The European journal of neuroscience.

[52]  R. Nudo.  Postinfarct Cortical Plasticity and Behavioral Recovery , 2007, Stroke.

[53]  S. Baker,et al.  Renshaw Cell Recurrent Inhibition Improves Physiological Tremor by Reducing Corticomuscular Coupling at 10 Hz , 2009, The Journal of Neuroscience.

[54]  Dario Farina,et al.  Identification of common synaptic inputs to motor neurons from the rectified electromyogram , 2013, The Journal of physiology.

[55]  Mikko Pohja,et al.  On the human sensorimotor-cortex beta rhythm: Sources and modeling , 2005, NeuroImage.

[56]  Gabriel Curio,et al.  Optimal imaging of cortico-muscular coherence through a novel regression technique based on multi-channel EEG and un-rectified EMG , 2011, NeuroImage.

[57]  M. Hallett,et al.  Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. , 2006, Brain : a journal of neurology.

[58]  M. Hornberger,et al.  Longitudinal Plasticity Across the Neural Axis in Acute Stroke , 2013, Neurorehabilitation and neural repair.

[59]  W. Byblow,et al.  Functional potential in chronic stroke patients depends on corticospinal tract integrity. , 2006, Brain : a journal of neurology.

[60]  M Hallett,et al.  Coherence Between Cortical and Muscular Activities After Subcortical Stroke , 2001, Stroke.

[61]  C. Calautti,et al.  Functional Neuroimaging Studies of Motor Recovery After Stroke in Adults: A Review , 2003, Stroke.

[62]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[63]  Stuart N Baker,et al.  The effect of diazepam on motor cortical oscillations and corticomuscular coherence studied in man , 2003, The Journal of physiology.

[64]  G. Pfurtscheller,et al.  On the existence of different types of central beta rhythms below 30 Hz. , 1997, Electroencephalography and clinical neurophysiology.

[65]  Guang H. Yue,et al.  Functional corticomuscular connection during reaching is weakened following stroke , 2009, Clinical Neurophysiology.

[66]  M. Hallett,et al.  Force level modulates human cortical oscillatory activities , 1999, Neuroscience Letters.

[67]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.