Motor cortex activation is preserved in patients with chronic hemiplegic stroke

Many central nervous system conditions that cause weakness, including many strokes, injure corticospinal tract but leave motor cortex intact. Little is known about the functional properties of surviving cortical regions in this setting, in part because many studies have used probes reliant on the corticospinal tract. We hypothesized that many features of motor cortex function would be preserved when assessed independent of the stroke‐affected corticospinal tract. Functional MRI was used to study 11 patients with chronic hemiplegia after unilateral stroke that spared regions of motor cortex. Activation in stroke‐affected hemisphere was evaluated using 3 probes independent of affected corticospinal tract: passive finger movement, a hand‐related visuomotor stimulus, and tapping by the nonstroke index finger. The site and magnitude of cortical activation were similar when comparing the stroke hemisphere to findings in 19 control subjects. Patients activated each of 8 cortical regions with similar frequency as compared to controls, generally with a smaller activation volume. In some cases, clinical measures correlated with the size or the site of stroke hemisphere activation. The results suggest that, despite stroke producing contralateral hemiplegia, surviving regions of motor cortex actively participate in the same proprioceptive, visuomotor, and bilateral movement control processes seen in control subjects.

[1]  Mark Hallett,et al.  The role of the dorsolateral prefrontal cortex in implicit procedural learning , 2004, Experimental Brain Research.

[2]  Marc H. Schieber,et al.  Neural Coding of Finger and Wrist Movements , 2004, Journal of Computational Neuroscience.

[3]  N. A. Borghese,et al.  Different Brain Correlates for Watching Real and Virtual Hand Actions , 2001, NeuroImage.

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

[5]  T. Parrish,et al.  Impact of cerebrovascular occlusive disease on the hemodynamic response measured with fMRI , 2001, NeuroImage.

[6]  M. Schwab,et al.  Neuronal plasticity and formation of new synaptic contacts follow pyramidal lesions and neutralization of Nogo‐A: A light and electron microscopic study in the pontine nuclei of adult rats , 2001, The Journal of comparative neurology.

[7]  R. Andersen,et al.  The parietal reach region codes the next planned movement in a sequential reach task. , 2001, Journal of neurophysiology.

[8]  J. Ashe,et al.  The Effect of Stimulus–Response Compatibility on Cortical Motor Activation , 2001, NeuroImage.

[9]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[10]  J. Stephen,et al.  Sources on the anterior and posterior banks of the central sulcus identified from magnetic somatosensory evoked responses using Multi‐Start Spatio‐Temporal localization , 2000, Human brain mapping.

[11]  D. G. Albrecht,et al.  Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? , 2000, Nature Neuroscience.

[12]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

[13]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[14]  Fabrizio Pisano,et al.  Quantitative measures of spasticity in post-stroke patients , 2000, Clinical Neurophysiology.

[15]  E Donchin,et al.  Brain-computer interface technology: a review of the first international meeting. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[16]  S. Cramer,et al.  Active versus passive finger movement: Bilateral, overlapping activations , 2000, NeuroImage.

[17]  P M Matthews,et al.  The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis , 2000, Annals of neurology.

[18]  Heidi Johansen-Berg,et al.  Attention to touch modulates activity in both primary and secondary somatosensory areas , 2000, NeuroImage.

[19]  D. Gitelman,et al.  Covert Visual Spatial Orienting and Saccades: Overlapping Neural Systems , 2000, NeuroImage.

[20]  J. Krakauer,et al.  Evolution of cortical activation during recovery from corticospinal tract infarction. , 2000, Stroke.

[21]  B R Rosen,et al.  A pilot study of somatotopic mapping after cortical infarct. , 2000, Stroke.

[22]  P. Cheney,et al.  Cortical motor areas and their properties: implications for neuroprosthetics. , 2000, Progress in brain research.

[23]  R. Johansson,et al.  Cortical activity in precision- versus power-grip tasks: an fMRI study. , 2000, Journal of neurophysiology.

[24]  J. Donoghue,et al.  Gaze Direction Modulates Finger Movement Activation Patterns in Human Cerebral Cortex , 1999, The Journal of Neuroscience.

[25]  S. Embretson,et al.  The stroke impact scale version 2.0. Evaluation of reliability, validity, and sensitivity to change. , 1999, Stroke.

[26]  M Hallett,et al.  Dissociation of the pathways mediating ipsilateral and contralateral motor‐evoked potentials in human hand and arm muscles , 1999, The Journal of physiology.

[27]  Miguel A. L. Nicolelis,et al.  Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex , 1999, Nature Neuroscience.

[28]  Scott T. Grafton,et al.  Role of the posterior parietal cortex in updating reaching movements to a visual target , 1999, Nature Neuroscience.

[29]  G. Rizzolatti,et al.  Resonance behaviors and mirror neurons. , 1999, Archives italiennes de biologie.

[30]  R G Shulman,et al.  Energy on Demand , 1999, Science.

[31]  B R Rosen,et al.  Activation of distinct motor cortex regions during ipsilateral and contralateral finger movements. , 1999, Journal of neurophysiology.

[32]  P. Cavanagh,et al.  Cortical fMRI activation produced by attentive tracking of moving targets. , 1998, Journal of neurophysiology.

[33]  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.

[34]  M Hallett,et al.  Studies of neuroplasticity with transcranial magnetic stimulation. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[35]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[36]  S. Miyauchi,et al.  Attention-regulated activity in human primary visual cortex. , 1998, Journal of neurophysiology.

[37]  Yue Cao,et al.  Pilot study of functional MRI to assess cerebral activation of motor function after poststroke hemiparesis. , 1998, Stroke.

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

[39]  S. Cramer,et al.  Computerized measurement of motor performance after stroke. , 1997, Stroke.

[40]  Roger N. Lemon,et al.  Reorganization of the Executive Motor System after Stroke , 1997 .

[41]  M. Hallett,et al.  Involvement of the ipsilateral motor cortex in finger movements of different complexities , 1997, Annals of neurology.

[42]  Babak Boroojerdi,et al.  Transcallosal inhibition in cortical and subcortical cerebral vascular lesions , 1996, Journal of the Neurological Sciences.

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

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

[45]  D Bourbonnais,et al.  Performance of the 'unaffected' upper extremity of elderly stroke patients. , 1996, Stroke.

[46]  B R Rosen,et al.  Modulation of auditory and visual cortex by selective attention is modality-dependent. , 1996, Neuroreport.

[47]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  J. Liepert,et al.  Changes of cortical motor area size during immobilization. , 1995, Electroencephalography and clinical neurophysiology.

[49]  R. Passingham,et al.  Relation between cerebral activity and force in the motor areas of the human brain. , 1995, Journal of neurophysiology.

[50]  G. Kreutzberg Reaction of the neuronal cell body to axonal damage , 1995 .

[51]  J. Kaas,et al.  Thalamic connections of the primary motor cortex (M1) of owl monkeys , 1994, The Journal of comparative neurology.

[52]  V L Towle,et al.  Functional magnetic resonance studies of the reorganization of the human hand sensorimotor area after unilateral brain injury in the perinatal period. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[53]  J. Tanji The supplementary motor area in the cerebral cortex , 1994, Neuroscience Research.

[54]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[55]  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.

[56]  A. P. Georgopoulos,et al.  Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. , 1993, Science.

[57]  J. Kaas,et al.  Architectionis, somatotopic organization, and ipsilateral cortical connections of the primary motor area (M1) of owl monkeys , 1993, The Journal of comparative neurology.

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

[59]  P. Bovolenta,et al.  Neurite Outgrowth Inhibitors in Gliotic Tissue , 1992, Journal of Neuroimmunology.

[60]  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.

[61]  G. Bruyn Atlas of the Cerebral Sulci, M. Ono, S. Kubik, Chad D. Abernathey (Eds.). Georg Thieme Verlag, Stuttgart, New York (1990), 232, DM 298 , 1990 .

[62]  S. Gandevia,et al.  The distribution of muscular weakness in upper motor neuron lesions affecting the arm. , 1989, Brain : a journal of neurology.

[63]  Marie-Claude Hepp-Reymond,et al.  Responses of motor cortex neurons to visual stimulation in the alert monkey , 1989, Neuroscience Letters.

[64]  Richard D. Jones,et al.  Impairment and recovery of ipsilateral sensory-motor function following unilateral cerebral infarction. , 1989, Brain : a journal of neurology.

[65]  P T Fox,et al.  The effect of carotid artery disease on the cerebrovascular response to physiologic stimulation , 1988, Neurology.

[66]  J. Tanji,et al.  Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. , 1988, Journal of neurophysiology.

[67]  Richard W. Bohannon,et al.  Interrater reliability of a modified Ashworth scale of muscle spasticity. , 1987, Physical therapy.

[68]  E. Fetz,et al.  Sensory and motor responses of precentral cortex cells during comparable passive and active joint movements. , 1980, Journal of neurophysiology.

[69]  F. A. Miles,et al.  Concepts of motor organization. , 1979, Annual review of psychology.

[70]  P. Strick Multiple sources of thalamic input to the primate motor cortex , 1975, Brain Research.

[71]  A. Fugl-Meyer,et al.  The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. , 1975, Scandinavian journal of rehabilitation medicine.

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

[73]  V. Brooks,et al.  Motor mechanisms: the role of the pyramidal system in motor control. , 1971, Annual review of physiology.

[74]  W PENFIELD,et al.  The supplementary motor area of the cerebral cortex; a clinical and experimental study. , 1951, A.M.A. archives of neurology and psychiatry.