Motor and Premotor Cortices in Subcortical Stroke

Background. Although functional imaging and neurophysiological approaches reveal alterations in motor and premotor areas after stroke, insights into neurobiological events underlying these alterations are limited in human studies. Objective. We tested whether cerebral metabolites related to neuronal and glial compartments are altered in the hand representation in bilateral motor and premotor areas and correlated with distal and proximal arm motor impairment in hemiparetic persons. Methods. In 20 participants at >6 months postonset of a subcortical ischemic stroke and 16 age- and sex-matched healthy controls, the concentrations of N-acetylaspartate and myo-inositol were quantified by proton magnetic resonance spectroscopy. Regions of interest identified by functional magnetic resonance imaging included primary (M1), dorsal premotor (PMd), and supplementary (SMA) motor areas. Relationships between metabolite concentrations and distal (hand) and proximal (shoulder/elbow) motor impairment using Fugl-Meyer Upper Extremity (FMUE) subscores were explored. Results. N-Acetylaspartate was lower in M1 (P = .04) and SMA (P = .004) and myo-inositol was higher in M1 (P = .003) and PMd (P = .03) in the injured (ipsilesional) hemisphere after stroke compared with the left hemisphere in controls. N-Acetylaspartate in ipsilesional M1 was positively correlated with hand FMUE subscores (P = .04). Significant positive correlations were also found between N-acetylaspartate in ipsilesional M1, PMd, and SMA and in contralesional M1 and shoulder/elbow FMUE subscores (P = .02, .01, .02, and .02, respectively). Conclusions. Our preliminary results demonstrated that proton magnetic resonance spectroscopy is a sensitive method to quantify relevant neuronal changes in spared motor cortex after stroke and consequently increase our knowledge of the factors leading from these changes to arm motor impairment.

[1]  Kuncheng Li,et al.  Proton magnetic resonance spectroscopy in patients with symptomatic unilateral internal carotid artery / middle cerebral artery stenosis or occlusion , 2011, Journal of magnetic resonance imaging : JMRI.

[2]  L. Cohen,et al.  Primary Motor Cortex in Stroke: A Functional MRI-Guided Proton MR Spectroscopic Study , 2011, Stroke.

[3]  渡辺 俊之 Absolute quantification in proton magnetic resonance spectroscopy is useful to differentiate amnesic mild cognitive impairment from Alzheimer's disease and healthy aging , 2011 .

[4]  Scott Barbay,et al.  Reorganization of motor cortex after controlled cortical impact in rats and implications for functional recovery. , 2010, Journal of neurotrauma.

[5]  R. Seitz,et al.  Role of neuroimaging in promoting long‐term recovery from ischemic stroke , 2010, Journal of magnetic resonance imaging : JMRI.

[6]  T. Jones,et al.  Lesion size‐dependent synaptic and astrocytic responses in cortex contralateral to infarcts in middle‐aged rats , 2010, Synapse.

[7]  Hermann Ackermann,et al.  The role of the unaffected hemisphere in motor recovery after stroke , 2010, Human brain mapping.

[8]  Marco Santello,et al.  Compensatory motor control after stroke: an alternative joint strategy for object-dependent shaping of hand posture. , 2010, Journal of neurophysiology.

[9]  P. Cheney,et al.  Forelimb muscle representations and output properties of motor areas in the mesial wall of rhesus macaques. , 2010, Cerebral cortex.

[10]  S. Oliet,et al.  Long term potentiation depends on release of D-serine from astrocytes , 2009, Nature.

[11]  Marie-Hélène Boudrias,et al.  Output properties and organization of the forelimb representation of motor areas on the lateral aspect of the hemisphere in rhesus macaques. , 2010, Cerebral cortex.

[12]  Yasuo Terao,et al.  Primary motor cortical metaplasticity induced by priming over the supplementary motor area , 2009, The Journal of physiology.

[13]  M. Shibuya Brain angiogenesis in developmental and pathological processes: therapeutic aspects of vascular endothelial growth factor , 2009, The FEBS journal.

[14]  Gereon R. Fink,et al.  Interhemispheric Competition After Stroke: Brain Stimulation to Enhance Recovery of Function of the Affected Hand , 2009, Neurorehabilitation and neural repair.

[15]  Mi Young Lee,et al.  Cortical activation pattern of compensatory movement in stroke patients. , 2009, NeuroRehabilitation.

[16]  T. Neumann-Haefelin,et al.  Combined 1H and 31P MR spectroscopic imaging: impaired energy metabolism in severe carotid stenosis and changes upon treatment , 2009, Magnetic Resonance Materials in Physics, Biology and Medicine.

[17]  M. Bastin,et al.  Changes in NAA and lactate following ischemic stroke , 2008, Neurology.

[18]  A. Priori,et al.  Myoinositol content in the human brain is modified by transcranial direct current stimulation in a matter of minutes: A 1H‐MRS study , 2008, Magnetic resonance in medicine.

[19]  S. Barbay,et al.  Early and late changes in the distal forelimb representation of the supplementary motor area after injury to frontal motor areas in the squirrel monkey. , 2008, Journal of neurophysiology.

[20]  Steven C. Cramer Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery , 2008, Annals of neurology.

[21]  M. Giroud,et al.  Is NAA reduction in normal contralateral cerebral tissue in stroke patients dependent on underlying risk factors? , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[22]  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.

[23]  D. Boussaoud,et al.  Callosal connections of dorsal versus ventral premotor areas in the macaque monkey: a multiple retrograde tracing study , 2005, BMC Neuroscience.

[24]  O. Witte,et al.  Motor improvements after focal cortical ischemia in adult rats are mediated by compensatory mechanisms , 2005, Behavioural Brain Research.

[25]  J. Bloch,et al.  A unilateral section of the corticospinal tract at cervical level in primate does not lead to measurable cell loss in motor cortex. , 2005, Journal of neurotrauma.

[26]  A J Thompson,et al.  Metabolite changes in normal-appearing gray and white matter are linked with disability in early primary progressive multiple sclerosis. , 2005, Archives of neurology.

[27]  J. Rothwell,et al.  Interhemispheric interaction between human dorsal premotor and contralateral primary motor cortex , 2004, The Journal of physiology.

[28]  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.

[29]  Morris H. Baslow,et al.  N-Acetylaspartate in the Vertebrate Brain: Metabolism and Function , 2003, Neurochemical Research.

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

[31]  R. Caminiti,et al.  Callosal connections of dorso‐lateral premotor cortex , 2003, The European journal of neuroscience.

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

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

[34]  Sabine Meunier,et al.  Changes in propriospinally mediated excitation of upper limb motoneurons in stroke patients. , 2003, Brain : a journal of neurology.

[35]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[36]  P Kapeller,et al.  Brain metabolite changes in cortical grey and normal-appearing white matter in clinically early relapsing-remitting multiple sclerosis. , 2002, Brain : a journal of neurology.

[37]  Jullie W Pan,et al.  Regional Cerebral Blood Flow and Magnetic Resonance Spectroscopic Imaging Findings in Diaschisis From Stroke , 2002, Stroke.

[38]  R. Lemon,et al.  Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study. , 2002, Cerebral cortex.

[39]  S. Suga,et al.  Longitudinal Changes of Metabolites in Frontal Lobes After Hemorrhagic Stroke of Basal Ganglia: A Proton Magnetic Resonance Spectroscopy Study , 2001, Stroke.

[40]  S. Provencher Automatic quantitation of localized in vivo 1H spectra with LCModel , 2001, NMR in biomedicine.

[41]  B. Barres,et al.  Control of synapse number by glia. , 2001, Science.

[42]  M. Reding,et al.  Effect of Lesion Location on Upper Limb Motor Recovery After Stroke , 2001, Stroke.

[43]  K. Chang,et al.  Neuronal metabolic changes in the cortical region after subcortical infarction: a proton MR spectroscopy study , 2000, Journal of neurology, neurosurgery, and psychiatry.

[44]  A. Blamire,et al.  Evidence for cellular damage in normal-appearing white matter correlates with injury severity in patients following traumatic brain injury: A magnetic resonance spectroscopy study. , 2000, Brain : a journal of neurology.

[45]  M. Levin,et al.  Compensatory strategies for reaching in stroke. , 2000, Brain : a journal of neurology.

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

[47]  D. Saunders,et al.  MR spectroscopy in stroke. , 2000, British medical bulletin.

[48]  E. Bullmore,et al.  The structural and functional mechanisms of motor recovery: complementary use of diffusion tensor and functional magnetic resonance imaging in a traumatic injury of the internal capsule , 1998, Journal of neurology, neurosurgery, and psychiatry.

[49]  W. Brooks,et al.  Neurometabolite markers of cerebral injury in the antiphospholipid antibody syndrome of systemic lupus erythematosus. , 1998, Stroke.

[50]  R T Constable,et al.  Quantifying and comparing region-of-interest activation patterns in functional brain MR imaging: methodology considerations. , 1998, Magnetic resonance imaging.

[51]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[52]  P. V. van Zijl,et al.  Magnetic Resonance Spectroscopy and Spectroscopic Imaging for the Study of Brain Metabolism a , 1997, Annals of the New York Academy of Sciences.

[53]  W. Mali,et al.  Cerebral Metabolism of Patients with Stenosis of the Internal Carotid Artery before and after Endarterectomy , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[54]  L M Harrison,et al.  Evidence for bilateral innervation of certain homologous motoneurone pools in man. , 1994, The Journal of physiology.

[55]  W. Fries,et al.  Motor recovery following capsular stroke. Role of descending pathways from multiple motor areas. , 1993, Brain : a journal of neurology.

[56]  A. Davison Basic Neurochemistry: Molecular, Cellular, and Medical Aspects , 1989 .

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

[58]  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.

[59]  Lieberman Ar The Axon Reaction: A Review of the Principal Features of Perikaryal Responses to Axon Injury , 1971 .

[60]  A. Lieberman The axon reaction: a review of the principal features of perikaryal responses to axon injury. , 1971, International review of neurobiology.