The role of the contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal FMRI.

Stroke may trigger a number of cellular and molecular events in perilesional and remote brain regions enabling cortical reorganization and recovery of function. We here investigated the pattern and time course of acute stroke-induced changes in motor system activity during motor recovery using functional magnetic resonance imaging. Hand movement-related neural activity was assessed in 11 acute stroke patients scanned 3 times during the first 2 weeks starting within 72 h after symptom onset. A motor recovery score was computed based on the action research arm test and the maximum grip force. Increases of activity in primary motor cortex, premotor cortex (dorsal and ventral), and supplementary motor area in both hemispheres significantly correlated with behavioral recovery. These longitudinal changes depended upon the degree of initial motor impairment: Patients with mild deficits did not differ from healthy subjects. In contrast, patients with severe deficits were characterized by a global reduction of task-related activity, followed by increases in ipsilesional as well as contralesional motor areas. The finding that the gradually increasing activity in contralesional primary motor and premotor cortex correlated with improved functional recovery in severely affected patients indicates early cortical reorganization supporting motor function of the affected hand.

[1]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[2]  P. Duncan,et al.  Measurement of Motor Recovery After Stroke: Outcome Assessment and Sample Size Requirements , 1992, Stroke.

[3]  Katrin Amunts,et al.  White matter fiber tracts of the human brain: Three-dimensional mapping at microscopic resolution, topography and intersubject variability , 2006, NeuroImage.

[4]  Gereon R. Fink,et al.  Human medial intraparietal cortex subserves visuomotor coordinate transformation , 2004, NeuroImage.

[5]  D. Noll,et al.  Bilateral basal ganglia activation associated with sensorimotor adaptation , 2006, Experimental Brain Research.

[6]  K. E. Stephan,et al.  The left parietal cortex and motor intention: An event-related functional magnetic resonance imaging study , 2006, Neuroscience.

[7]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[8]  Alan J Thompson,et al.  The influence of time after stroke on brain activations during a motor task , 2004, Annals of neurology.

[9]  Stephen M. Smith,et al.  Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. , 2002, Brain : a journal of neurology.

[10]  U. Halsband,et al.  Motor learning in man: A review of functional and clinical studies , 2006, Journal of Physiology-Paris.

[11]  J. Rauschecker,et al.  Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans , 1999, Nature Neuroscience.

[12]  Earl K. Miller,et al.  Selective representation of relevant information by neurons in the primate prefrontal cortex , 1998, Nature.

[13]  Ivan Toni,et al.  Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study , 1999, Experimental Brain Research.

[14]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[15]  J. Liepert,et al.  Improvement of dexterity by single session low-frequency repetitive transcranial magnetic stimulation over the contralesional motor cortex in acute stroke: a double-blind placebo-controlled crossover trial. , 2007, Restorative neurology and neuroscience.

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

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

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

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

[20]  François Chollet,et al.  Correlation between cerebral reorganization and motor recovery after subcortical infarcts , 2003, NeuroImage.

[21]  Christian Gerloff,et al.  The Role of Multiple Contralesional Motor Areas for Complex Hand Movements after Internal Capsular Lesion , 2006, The Journal of Neuroscience.

[22]  François Chollet,et al.  A longitudinal fMRI study: in recovering and then in clinically stable sub-cortical stroke patients , 2004, NeuroImage.

[23]  Ferdinand Binkofski,et al.  Modulation of the BOLD-response in early recovery from sensorimotor stroke , 2004, Neurology.

[24]  M. Hommel,et al.  Vicarious function within the human primary motor cortex? A longitudinal fMRI stroke study. , 2005, Brain : a journal of neurology.

[25]  Rick M Dijkhuizen,et al.  Correlation between Brain Reorganization, Ischemic Damage, and Neurologic Status after Transient Focal Cerebral Ischemia in Rats: A Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

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

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

[28]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

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

[30]  C. Weiller,et al.  Dynamics of language reorganization after stroke. , 2006, Brain : a journal of neurology.

[31]  Ruopeng Wang,et al.  Structural damage to the corticospinal tract correlates with bilateral sensorimotor cortex reorganization in stroke patients , 2008, NeuroImage.

[32]  A. Schleicher,et al.  Mapping of Histologically Identified Long Fiber Tracts in Human Cerebral Hemispheres to the MRI Volume of a Reference Brain: Position and Spatial Variability of the Optic Radiation , 1999, NeuroImage.

[33]  M. Rushworth,et al.  Attention Systems and the Organization of the Human Parietal Cortex , 2001, The Journal of Neuroscience.

[34]  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.

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

[36]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[37]  Simon B. Eickhoff,et al.  Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM , 2008, NeuroImage.

[38]  M. Rushworth,et al.  The left parietal and premotor cortices: motor attention and selection , 2003, NeuroImage.

[39]  C. Grefkes,et al.  Central adaptation following heterotopic hand replantation probed by fMRI and effective connectivity analysis , 2008, Experimental Neurology.

[40]  Mathias Hoehn,et al.  Early Prediction of Functional Recovery after Experimental Stroke: Functional Magnetic Resonance Imaging, Electrophysiology, and Behavioral Testing in Rats , 2008, The Journal of Neuroscience.

[41]  L. Cohen,et al.  Reorganization of the human ipsilesional premotor cortex after stroke. , 2004, Brain : a journal of neurology.

[42]  Simon B. Eickhoff,et al.  Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling , 2010, NeuroImage.

[43]  B R Rosen,et al.  Functional magnetic resonance imaging of reorganization in rat brain after stroke , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Yale E. Cohen,et al.  A common reference frame for movement plans in the posterior parietal cortex , 2002, Nature Reviews Neuroscience.

[45]  R. D Seidler,et al.  Feedforward and feedback processes in motor control , 2004, NeuroImage.

[46]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

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

[48]  J. C. Rothwell,et al.  Exploring Theta Burst Stimulation as an intervention to improve motor recovery in chronic stroke , 2007, Clinical Neurophysiology.

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

[50]  P. Matthews,et al.  The role of ipsilateral premotor cortex in hand movement after stroke , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Gereon R Fink,et al.  Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. , 2008, Archives of neurology.

[52]  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.

[53]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[54]  R. Lyle A performance test for assessment of upper limb function in physical rehabilitation treatment and research , 1981, International journal of rehabilitation research. Internationale Zeitschrift fur Rehabilitationsforschung. Revue internationale de recherches de readaptation.

[55]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[57]  G. Kwakkel,et al.  Understanding the pattern of functional recovery after stroke: facts and theories. , 2004, Restorative neurology and neuroscience.

[58]  M. Hallett,et al.  Contribution of the ipsilateral motor cortex to recovery after chronic stroke , 2003, Annals of neurology.

[59]  Mark J Lowe,et al.  Comparison of unilateral and bilateral complex finger tapping‐related activation in premotor and primary motor cortex , 2009, Human brain mapping.

[60]  M. Jüptner,et al.  Arm Training Induced Brain Plasticity in Stroke Studied with Serial Positron Emission Tomography , 2001, NeuroImage.

[61]  N. Yozbatiran,et al.  A Standardized Approach to Performing the Action Research Arm Test , 2008, Neurorehabilitation and neural repair.