Exploring the Evolution of Cortical Excitability Following Acute Stroke

Background. Evolution of changes in intracortical excitability following stroke, particularly in the contralesional hemisphere, is being increasingly recognized in relation to maximizing the potential for functional recovery. Objective. The present study utilized a prospective longitudinal design over a 12-month period from stroke onset, to investigate the evolution of intracortical excitability involving both motor cortices and their relationship to recovery, and whether such changes were influenced by baseline stroke characteristics. Methods. Thirty-one patients with acute unilateral ischemic stroke were recruited from a tertiary hospital stroke unit. Comprehensive clinical assessments and cortical excitability were undertaken at stroke onset using a novel threshold-tracking paired-pulse transcranial magnetic stimulation technique, and repeated at 3-, 6-, and 12-month follow-up in 17 patients who completed the longitudinal assessment. Results. Shortly following stroke, short-interval intracortical inhibition (SICI) was significantly reduced in both lesioned and contralesional hemispheres that correlated with degree of recovery over the subsequent 3 months. Over the follow-up period, ipsilesional SICI remained reduced in all patient groups, while SICI over the contralesional hemisphere remained reduced only in the groups with cortical stroke or more baseline functional impairment. Conclusions. The current study has demonstrated that evolution of intracortical excitability, particularly over the contralesional hemisphere, may vary between patients with differing baseline stroke and clinical characteristics, suggesting that ongoing contralesional network recruitment may be necessary for those patients who have significant disruptions to the integrity of ipsilesional motor pathways. Results from the present series have implications for the development of neuromodulatory brain stimulation protocols to harness and thereby facilitate stroke recovery.

[1]  M. Hornberger,et al.  Botulinum toxin modulates cortical maladaptation in post‐stroke spasticity , 2013, Muscle & nerve.

[2]  M. Kiernan,et al.  Motor Cortex Excitability in Acute Cerebellar Infarct , 2013, The Cerebellum.

[3]  W. Byblow,et al.  Ipsilateral Motor Pathways after Stroke: Implications for Non-Invasive Brain Stimulation , 2013, Front. Hum. Neurosci..

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

[5]  J. Krakauer,et al.  Medial Premotor Cortex Shows a Reduction in Inhibitory Markers and Mediates Recovery in a Mouse Model of Focal Stroke , 2013, Stroke.

[6]  W. Byblow,et al.  Contralesional hemisphere control of the proximal paretic upper limb following stroke. , 2012, Cerebral cortex.

[7]  M. Kiernan,et al.  Cortical dysfunction underlies disability in multiple sclerosis , 2012, Multiple sclerosis.

[8]  M. Kiernan,et al.  Corticomotoneuronal integrity and adaptation in spinal muscular atrophy. , 2012, Archives of neurology.

[9]  M. Chopp,et al.  Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation , 2012, The Lancet Neurology.

[10]  S. Carmichael,et al.  Brain Excitability in StrokeThe Yin and Yang of Stroke Progression , 2012 .

[11]  T. Mittmann,et al.  Functional Consequences of the Disturbances in the GABA-Mediated Inhibition Induced by Injuriesin the Cerebral Cortex , 2011, Neural plasticity.

[12]  Majid H. Mohajerani,et al.  Targeted mini-strokes produce changes in interhemispheric sensory signal processing that are indicative of disinhibition within minutes , 2011, Proceedings of the National Academy of Sciences.

[13]  Gereon R Fink,et al.  The role of the contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal FMRI. , 2011, Cerebral cortex.

[14]  Alvaro Pascual-Leone,et al.  Assessment and Modulation of Neural Plasticity in Rehabilitation With Transcranial Magnetic Stimulation , 2010, PM & R : the journal of injury, function, and rehabilitation.

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

[16]  Min-Kyun Oh,et al.  Effect of Transcranial Direct Current Stimulation on Motor Recovery in Patients with Subacute Stroke , 2010, American journal of physical medicine & rehabilitation.

[17]  K. Ikoma,et al.  Correlation of motor function with transcallosal and intracortical inhibition after stroke. , 2010, Journal of rehabilitation medicine.

[18]  M. Kiernan,et al.  Corticospinal tract dysfunction and development of amyotrophic lateral sclerosis following electrical injury , 2010, Muscle & nerve.

[19]  E. Khedr,et al.  Long‐term effect of repetitive transcranial magnetic stimulation on motor function recovery after acute ischemic stroke , 2010, Acta neurologica Scandinavica.

[20]  David Burke,et al.  The effects of alterations in conditioning stimulus intensity on short interval intracortical inhibition , 2009, Brain Research.

[21]  John W Krakauer,et al.  Early imaging correlates of subsequent motor recovery after stroke , 2009, Annals of neurology.

[22]  Ulf T Eysel,et al.  Excitation and Inhibition Jointly Regulate Cortical Reorganization in Adult Rats , 2008, The Journal of Neuroscience.

[23]  G. Zanette,et al.  Motor Cortical Disinhibition During Early and Late Recovery After Stroke , 2008, Neurorehabilitation and neural repair.

[24]  G. Fink,et al.  Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging , 2008, Annals of neurology.

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

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

[27]  J. Eyre,et al.  Corticospinal tract development and its plasticity after perinatal injury , 2007, Neuroscience & Biobehavioral Reviews.

[28]  I. Módy,et al.  Activation of GABAA Receptors: Views from Outside the Synaptic Cleft , 2007, Neuron.

[29]  N. Ward,et al.  The neural substrates of motor recovery after focal damage to the central nervous system. , 2006, Archives of physical medicine and rehabilitation.

[30]  M. Kiernan,et al.  Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. , 2006, Brain : a journal of neurology.

[31]  Matthew C Kiernan,et al.  Assessment of cortical excitability using threshold tracking techniques , 2006, Muscle & nerve.

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

[33]  Cornelius Weiller,et al.  Motor Strokes: The Lesion Location Determines Motor Excitability Changes , 2005, Stroke.

[34]  Ichiro Watanabe,et al.  Repetitive Transcranial Magnetic Stimulation of Contralesional Primary Motor Cortex Improves Hand Function After Stroke , 2005, Stroke.

[35]  E. Jankowska,et al.  How to Enhance Ipsilateral Actions of Pyramidal Tract Neurons , 2005, The Journal of Neuroscience.

[36]  Sergio P. Rigonatti,et al.  A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients , 2005, Neurology.

[37]  W. Byblow,et al.  The Contribution of Cervical Propriospinal Premotoneurons in Recovering Hemiparetic Stroke Patients , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[38]  A. Słowik,et al.  GABA in ischemic stroke. Proton magnetic resonance study. , 2004, Medical science monitor : international medical journal of experimental and clinical research.

[39]  C. Bütefisch,et al.  Plasticity in the Human Cerebral Cortex: Lessons from the Normal Brain and from Stroke , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[40]  L. Cohen,et al.  Influence of interhemispheric interactions on motor function in chronic stroke , 2004, Annals of neurology.

[41]  Richard S. J. Frackowiak,et al.  Neural correlates of motor recovery after stroke: a longitudinal fMRI study. , 2003, Brain : a journal of neurology.

[42]  P. Pasqualetti,et al.  Interhemispheric Asymmetries of Motor Cortex Excitability in the Postacute Stroke Stage: A Paired-Pulse Transcranial Magnetic Stimulation Study , 2003, Stroke.

[43]  Victor De Pasqua,et al.  Post-stroke reorganization of hand motor area: a 1-year prospective follow-up with focal transcranial magnetic stimulation , 2003, Clinical Neurophysiology.

[44]  CinziaCalautti,et al.  Functional Neuroimaging Studies of Motor Recovery After Stroke in Adults , 2003 .

[45]  Volker Hömberg,et al.  Remote changes in cortical excitability after stroke. , 2003, Brain : a journal of neurology.

[46]  P. Rossini,et al.  Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. , 2002, Brain : a journal of neurology.

[47]  E. Wassermann Variation in the response to transcranial magnetic brain stimulation in the general population , 2002, Clinical Neurophysiology.

[48]  P. Manganotti,et al.  Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke , 2002, Clinical Neurophysiology.

[49]  H. Bostock,et al.  Two phases of intracortical inhibition revealed by transcranial magnetic threshold tracking , 2002, Experimental Brain Research.

[50]  W. Young,et al.  Reemergence of Stroke Deficits With Midazolam Challenge , 2002, Stroke.

[51]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[52]  J. Liepert,et al.  Motor cortex disinhibition of the unaffected hemisphere after acute stroke , 2000, Muscle & nerve.

[53]  G. Abbruzzese,et al.  Motor recovery following stroke: a transcranial magnetic stimulation study , 2000, Clinical Neurophysiology.

[54]  J. Liepert,et al.  Motor cortex disinhibition in acute stroke , 2000, Clinical Neurophysiology.

[55]  T. Neumann-Haefelin,et al.  Periinfarct and Remote Excitability Changes after Transient Middle Cerebral Artery Occlusion , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[56]  P J Delwaide,et al.  Absence of response to early transcranial magnetic stimulation in ischemic stroke patients: prognostic value for hand motor recovery. , 1999, Stroke.

[57]  A Cruz Martínez,et al.  Motor hand recovery after stroke. Prognostic yield of early transcranial magnetic stimulation. , 1999, Electromyography and clinical neurophysiology.

[58]  M. Escudero,et al.  Prognostic value of motor evoked potential obtained by transcranial magnetic brain stimulation in motor function recovery in patients with acute ischemic stroke. , 1998, Stroke.

[59]  K. Zilles,et al.  Immunohistochemical evidence for dysregulation of the GABAergic system ipsilateral to photochemically induced cortical infarcts in rats , 1998, Neuroscience.

[60]  T. Neumann-Haefelin,et al.  Increased long‐term potentiation in the surround of experimentally induced focal cortical infarction , 1998, Annals of neurology.

[61]  B. Rosen,et al.  A functional MRI study of subjects recovered from hemiparetic stroke. , 1997, Stroke.

[62]  P. Delwaide,et al.  Can motor recovery in stroke patients be predicted by early transcranial magnetic stimulation? , 1996, Stroke.

[63]  J. Kleim,et al.  Synaptogenesis and dendritic growth in the cortex opposite unilateral sensorimotor cortex damage in adult rats: a quantitative electron microscopic examination , 1996, Brain Research.

[64]  G. Bernardi,et al.  Cerebral plasticity after stroke as revealed by ipsilateral responses to magnetic stimulation. , 1996, Neuroreport.

[65]  G. Hagemann,et al.  Electrophysiological transcortical diaschisis after cortical photothrombosis in rat brain. , 1996, Stroke.

[66]  R. P. Stroemer,et al.  Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. , 1995, Stroke.

[67]  M. Hallett,et al.  Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. , 1995, Journal of neurophysiology.

[68]  J. Donoghue,et al.  Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  T. Neumann-Haefelin,et al.  Cellular correlates of neuronal hyperexcitability in the vicinity of photochemically induced cortical infarcts in rats in vitro , 1995, Neuroscience Letters.

[70]  T. Olsen,et al.  Outcome and time course of recovery in stroke. Part I: Outcome. The Copenhagen Stroke Study. , 1995, Archives of physical medicine and rehabilitation.

[71]  T. Mittmann,et al.  Lesion-induced transient suppression of inhibitory function in rat neocortex in vitro , 1994, Neuroscience.

[72]  T. Jones,et al.  Use-dependent growth of pyramidal neurons after neocortical damage , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[73]  S. Miller,et al.  Longitudinal study of central motor conduction time following stroke. 1. Natural history of central motor conduction. , 1993, Brain : a journal of neurology.

[74]  S. Miller,et al.  Longitudinal study of central motor conduction time following stroke. 2. Central motor conduction measured within 72 h after stroke as a predictor of functional outcome at 12 months. , 1993, Brain : a journal of neurology.

[75]  Karl J. Friston,et al.  Individual patterns of functional reorganization in the human cerebral cortex after capsular infraction , 1993, Annals of neurology.

[76]  R. Mutani,et al.  Magnetic brain stimulation: the silent period after the motor evoked potential. , 1992, Neurology.

[77]  Theresa A. Jones,et al.  Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage , 1992, Brain Research.

[78]  Richard S. J. Frackowiak,et al.  The functional anatomy of motor recovery after stroke in humans: A study with positron emission tomography , 1991, Annals of neurology.

[79]  R. A. Davidoff The pyramidal tract. , 1990, Neurology.

[80]  Sam Silverman,et al.  THE RHESUS MONKEY , 1982 .

[81]  H. Kuypers,et al.  Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain rhesus monkey. , 1973, Brain : a journal of neurology.

[82]  C. Woolsey,et al.  The Pyramidal Tract , 1957, Neurology.

[83]  Christel Genoud,et al.  GABA receptor subunits in human auditory cortex in normal and stroke cases. , 2009, Acta neurobiologiae experimentalis.

[84]  Sung Ho Jang,et al.  The role of the corticospinal tract in motor recovery in patients with a stroke: a review. , 2009, NeuroRehabilitation.

[85]  M. Johnston,et al.  Plasticity in the developing brain: implications for rehabilitation. , 2009, Developmental disabilities research reviews.

[86]  Sergio P. Rigonatti,et al.  Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. , 2007, Restorative neurology and neuroscience.

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

[88]  M. Hallett,et al.  Cortical motor representation of the ipsilateral hand and arm , 2004, Experimental Brain Research.

[89]  P. Thompson,et al.  Unusual focal dyskinesias: The ears, the shoulders, the back, and the abdomen , 1994, Movement disorders : official journal of the Movement Disorder Society.