Lesion-induced and training-induced brain reorganization.

INTRODUCTION A stroke may modulate motor cortex excitability. We examined if distinct ischemic brain lesions are associated with a specific pattern of excitability changes. We also investigated the effects of a rehabilitative therapy on motor excitability. METHODS In stroke patients, the consequences of a) a lesion in the central somatosensory system, b) a cerebellar lesion and c) a two week period of Constraint-induced movement therapy (CIMT), on motor cortex excitability were studied. Transcranial magnetic stimulation techniques and functional magnetic resonance imaging (fMRI) were employed. RESULTS Patients with a lesion in the primary somatosensory cortex or in the ventroposterolateral nucleus of the thalamus had a decreased intracortical inhibition on the affected side. Patients with lesions in the territory of the superior cerebellar artery had a loss of intracortical facilitation and an increase of intracortical inhibition. Patients with cortical lesions undergoing CIMT had a loss of intracortical inhibition prior to therapy. After CIMT, changes of ICI were stronger in the lesioned than in the non-lesioned hemisphere but could result either in an increase of ICI or a reduction of ICI. In three patients fMRI results showed that cortical activation was less post CIMT as compared to pre-treatment activation. In parallel, ICI was reduced after treatment. CONCLUSIONS Our results suggest that, physiologically, central somatosensory influence on the motor cortex is inhibitory. In contrast, the cerebellum normally exerts a facilitatory influence on the motor cortex. CIMT induces changes of intracortical excitability mainly in the affected hemisphere.

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

[2]  S J Riederer,et al.  Mapping of the central sulcus with functional MR: active versus passive activation tasks. , 1998, AJNR. American journal of neuroradiology.

[3]  S. Ogawa,et al.  Oxygenation‐sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields , 1990, Magnetic resonance in medicine.

[4]  C. Weiller,et al.  Recovery and plasticity imaging in stroke patients , 2001 .

[5]  Richard S. J. Frackowiak,et al.  Neural correlates of outcome after stroke: a cross-sectional fMRI study. , 2003, Brain : a journal of neurology.

[6]  Richard S. J. Frackowiak,et al.  Cortical function in progressive lower motor neuron disorders and amyotrophic lateral sclerosis , 1994, Neurology.

[7]  T. Elbert,et al.  Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation , 1995, Nature.

[8]  R. Nudo,et al.  Neural Substrates for the Effects of Rehabilitative Training on Motor Recovery After Ischemic Infarct , 1996, Science.

[9]  G. Thickbroom,et al.  Transcranial magnetic stimulation mapping of the motor cortex in normal subjects The representation of two intrinsic hand muscles , 1993, Journal of the Neurological Sciences.

[10]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[12]  L. Schöls,et al.  Motor cortex activation by transcranial magnetic stimulation in ataxia patients depends on the genetic defect. , 2002, Brain : a journal of neurology.

[13]  U. Ziemann,et al.  Intracortical inhibition and facilitation in the conventional paired TMS paradigm. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

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

[15]  R. Benecke,et al.  On the origin of the postexcitatory inhibition seen after transcranial magnetic brain stimulation in awake human subjects , 2004, Experimental Brain Research.

[16]  J. Kaas,et al.  Large-scale reorganization at multiple levels of the somatosensory pathway follows therapeutic amputation of the hand in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  F. Chollet,et al.  Within-Session and Between-Session Reproducibility of Cerebral Sensorimotor Activation: A Test–Retest Effect Evidenced with Functional Magnetic Resonance Imaging , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  O. Witte,et al.  Lesion-induced plasticity as a potential mechanism for recovery and rehabilitative training. , 1998, Current opinion in neurology.

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

[20]  S. Wolf,et al.  Forced use of hemiplegic upper extremities to reverse the effect of learned nonuse among chronic stroke and head-injured patients , 1989, Experimental Neurology.

[21]  M. Hallett,et al.  Noninvasive mapping of muscle representations in human motor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[22]  J. Liepert,et al.  Treatment-induced cortical reorganization after stroke in humans. , 2000, Stroke.

[23]  M. Ridding,et al.  Stimulus/response curves as a method of measuring motor cortical excitability in man. , 1997, Electroencephalography and clinical neurophysiology.

[24]  D. J. Felleman,et al.  Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys , 1983, Neuroscience.

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

[26]  M. Cynader,et al.  Somatosensory cortical map changes following digit amputation in adult monkeys , 1984, The Journal of comparative neurology.

[27]  S. Kiebel,et al.  Brain Representation of Active and Passive Movements , 1996, NeuroImage.

[28]  W. James,et al.  Il Cervelletto. Nuovi Studi di Fisiologia Normale e Patologica. , 1893 .

[29]  Mark Hallett,et al.  Constraint-Induced Therapy in Stroke: Magnetic-Stimulation Motor Maps and Cerebral Activation , 2003, Neurorehabilitation and neural repair.

[30]  C. Marsden,et al.  Corticocortical inhibition in human motor cortex. , 1993, The Journal of physiology.

[31]  Jonathan W. Mink,et al.  Cerebellar Output: Multiple Maps and Modes of Control in Movement Coordination , 1992 .

[32]  J. Liepert,et al.  Reduced intracortical facilitation in patients with cerebellar degeneration , 1998, Acta neurologica Scandinavica.

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

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

[35]  B. Bussel,et al.  Longitudinal Study of Motor Recovery After Stroke: Recruitment and Focusing of Brain Activation , 2002, Stroke.

[36]  A Münchau,et al.  Motor excitability in a patient with a somatosensory cortex lesion , 2003, Clinical Neurophysiology.

[37]  A. Palmeri,et al.  Changes of cortical excitability of human motor cortex in spinocerebellar ataxia type 2 A study with paired transcranial magnetic stimulation , 2002, Journal of the Neurological Sciences.

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

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

[40]  Karl J. Friston,et al.  Functional reorganization of the brain in recovery from striatocapsular infarction in man , 1992, Annals of neurology.

[41]  N. Miller,et al.  Technique to improve chronic motor deficit after stroke. , 1993, Archives of physical medicine and rehabilitation.

[42]  B. Rosen,et al.  Motor Recovery and Cortical Reorganization after Constraint-Induced Movement Therapy in Stroke Patients: A Preliminary Study , 2002, Neurorehabilitation and neural repair.