Neural correlates of motor impairment during motor imagery and motor execution in sub-cortical stroke

Objective: This study aims at identifying the neural substrates for motor execution (ME) and motor imagery (MI) in patients after stroke and their correlations with functional outcomes. Methods: 10 chronic stroke patients with left sub-cortical lesions and 10 unimpaired subjects were recruited. Their cortical processes were studied when they were asked to perform ME and MI unimanually using their unaffected and affected wrists during fMRI. Results: From correlation results, the supplementary motor area (SMA), its activation volume and congruence in functional neuroanatomy associated with ME and MI using affected wrist positively correlated with motor performance. During ME of the affected wrist, the precuneus, its activation volume and congruence in functional neuroanatomy between patient and unimpaired groups showed a negative correlation, while, in non-primary motor areas, the hemispheric balance of premotor cortex and the congruence in functional neuroanatomy of contralesional inferior parietal lobule between patient and unimpaired groups showed a positive correlation with motor performance. Conclusions: The non-primary motor-related areas were revealed to play a critical role in determining motor outcomes after left sub-cortical stroke, which was demonstrated in the stroke patients. In particular, SMA might be the key neural substrate associated with motor recovery.

[1]  T. Maeshima,et al.  Autonomic response specificity during motor imagery. , 2000, Journal of physiological anthropology and applied human science.

[2]  D. Kimura,et al.  Acquisition of a motor skill after left-hemisphere damage. , 1977, Brain : a journal of neurology.

[3]  Steven L. Small,et al.  Network activation during bimanual movements in humans , 2008, NeuroImage.

[4]  S. Black,et al.  The Fugl-Meyer Assessment of Motor Recovery after Stroke: A Critical Review of Its Measurement Properties , 2002, Neurorehabilitation and neural repair.

[5]  N. Hogan,et al.  Assessing the Motor Status Score: A Scale for the Evaluation of Upper Limb Motor Outcomes in Patients after Stroke , 2002, Neurorehabilitation and neural repair.

[6]  M. Hallett,et al.  Neural correlates of bimanual anti-phase and in-phase movements in Parkinson's disease. , 2010, Brain : a journal of neurology.

[7]  Scott T. Grafton,et al.  Parceling of mesial frontal motor areas during ideation and movement using functional magnetic resonance imaging at 1.5 tesla , 1994, Annals of neurology.

[8]  Julien Doyon,et al.  Functional cerebral reorganization following motor sequence learning through mental practice with motor imagery , 2003, NeuroImage.

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

[10]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. I. The effects of bilateral pyramidal lesions. , 1968, Brain : a journal of neurology.

[11]  C. Richards,et al.  Potential role of mental practice using motor imagery in neurologic rehabilitation. , 2001, Archives of physical medicine and rehabilitation.

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

[13]  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.

[14]  M. Hallett,et al.  A functional MRI study of automatic movements in patients with Parkinson's disease. , 2005, Brain : a journal of neurology.

[15]  T. A. Carpenter,et al.  Motor Imagery After Subcortical Stroke: A Functional Magnetic Resonance Imaging Study , 2009, Stroke.

[16]  S. Page,et al.  A randomized efficacy and feasibility study of imagery in acute stroke , 2001, Clinical rehabilitation.

[17]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[18]  M. Jeannerod,et al.  The timing of mentally represented actions , 1989, Behavioural Brain Research.

[19]  Karl J. Friston,et al.  Attention to Action: Specific Modulation of Corticocortical Interactions in Humans , 2001, NeuroImage.

[20]  T. Kimberley,et al.  Neural Substrates for Motor Imagery in Severe Hemiparesis , 2006, Neurorehabilitation and neural repair.

[21]  Kwok-wing Tang,et al.  Hierarchical coding of characters in the ventral and dorsal visual streams of Chinese language processing , 2009, NeuroImage.

[22]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[23]  Steven C Cramer,et al.  Functional imaging in stroke recovery. , 2004, Stroke.

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

[25]  P. Glees,et al.  Ipsilateral representation in the cerebral cortex; its significance in relation to motor function. , 1952, Lancet.

[26]  André J. Szameitat,et al.  Motor imagery of complex everyday movements. An fMRI study , 2007, NeuroImage.

[27]  Scott H. Johnson,et al.  Imagining the impossible: intact motor representations in hemiplegics , 2000, Neuroreport.

[28]  J. Decety,et al.  Neural mechanisms subserving the perception of human actions , 1999, Trends in Cognitive Sciences.

[29]  R. Iansek,et al.  The role of the supplementary motor area in the control of voluntary movement , 1996 .

[30]  D. G. Lawrence,et al.  The functional organization of the motor system in the monkey. II. The effects of lesions of the descending brain-stem pathways. , 1968, Brain : a journal of neurology.

[31]  S. Swinnen,et al.  The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour , 2005, The European journal of neuroscience.

[32]  Jean-Baptiste Poline,et al.  Motor execution and imagination networks in post-stroke dystonia , 2004, Neuroreport.

[33]  Jeffrey M. Zacks,et al.  Lateral somatotopic organization during imagined and prepared movements. , 2006, Journal of neurophysiology.

[34]  M. Jeannerod,et al.  Mentally simulated movements in virtual reality: does Fitt's law hold in motor imagery? , 1995, Behavioural Brain Research.

[35]  Alan C. Evans,et al.  Motor Learning Produces Parallel Dynamic Functional Changes during the Execution and Imagination of Sequential Foot Movements , 2002, NeuroImage.

[36]  F Merten,et al.  Mental practice of motor skills used in poststroke rehabilitation has own effects on central nervous activation. , 1994, The International journal of neuroscience.

[37]  Gary F Egan,et al.  Motor Impairment and Recovery in the Upper Limb After Stroke: Behavioral and Neuroanatomical Correlates , 2005, Stroke.

[38]  Not Available Not Available.  Subcortical Stroke , 2003, Journal of Neurology.

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

[40]  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.

[41]  S. H. Johnson,et al.  Intact Motor Imagery in Chronic Upper Limb Hemiplegics: Evidence for Activity-Independent Action Representations , 2002, Journal of Cognitive Neuroscience.

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

[43]  J. Chae,et al.  Neuromuscular stimulation for upper extremity motor and functional recovery in acute hemiplegia. , 1998, Stroke.

[44]  Chen,et al.  A functional magnetic resonance imaging study , 2011 .

[45]  Nikolaus Weiskopf,et al.  The Role of Contralesional Dorsal Premotor Cortex after Stroke as Studied with Concurrent TMS-fMRI , 2010, The Journal of Neuroscience.

[46]  G. Tassinari,et al.  Motor representation of the hand in the human cortex: an f-MRI study with a conventional 1.5 T clinical unit , 1998, The Italian Journal of Neurological Sciences.

[47]  Scott H. Johnson-Frey.  Stimulation through simulation? Motor imagery and functional reorganization in hemiplegic stroke patients , 2004, Brain and Cognition.

[48]  Jessica A Turner,et al.  Cerebral and cerebellar sensorimotor plasticity following motor imagery-based mental practice of a sequential movement. , 2004, Journal of rehabilitation research and development.