Motor Imagery After Subcortical Stroke: A Functional Magnetic Resonance Imaging Study

Background and Purpose— In recovered subcortical stroke, the pattern of motor network activation during motor execution can appear normal or not, depending on the task. Whether this applies to other aspects of motor function is unknown. We used functional MRI to assess motor imagery (MI), a promising new approach to improve motor function after stroke, and contrasted it to motor execution. Methods— Twenty well-recovered patients with hemiparetic subcortical stroke (14 males; mean age, 66.5 years) and 17 aged-matched control subjects were studied. Extensive behavioral screening excluded 8 patients and 4 control subjects due to impaired MI abilities. Subjects performed MI and motor execution of a paced finger–thumb opposition sequence using a functional MRI paradigm that monitored compliance. Activation within the primary motor cortex (BA4a and 4p), dorsal premotor, and supplementary motor areas was examined. Results— The pattern of activation during affected-hand motor execution was not different from control subjects. Affected-hand MI activation was also largely similar to control subjects, including involvement of BA4, but with important differences: (1) unlike control subjects and the nonaffected hand, activation in BA4a and dorsal premotor was not lower during MI as compared with motor execution; (2) the hemispheric balance of BA4p activation was significantly less lateralized than control subjects; and (3) ipsilesional BA4p activation positively correlated with motor performance. Conclusions— In well-recovered subcortical stroke, the motor system, including ipsilesional BA4, is activated during MI despite the lesion. It, however, remains disorganized in proportion to residual motor impairment. Thus, components of movement upstream from execution appear differentially affected after stroke and could be targeted by rehabilitation in more severely affected patients.

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

[2]  J. T. Massey,et al.  Mental rotation of the neuronal population vector. , 1989, Science.

[3]  H. Markus,et al.  Estimation of Cerebrovascular Reactivity Using Transcranial Doppler, Including the Use of Breath‐Holding as the Vasodilatory Stimulus , 1992, Stroke.

[4]  M. Jeannerod Mental imagery in the motor context , 1995, Neuropsychologia.

[5]  L. Parsons,et al.  Use of implicit motor imagery for visual shape discrimination as revealed by PET , 1995, Nature.

[6]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[7]  A. Sirigu,et al.  The Mental Representation of Hand Movements After Parietal Cortex Damage , 1996, Science.

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

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

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

[11]  C. Calautti,et al.  Dynamics of Motor Network Overactivation After Striatocapsular Stroke: A Longitudinal PET Study Using a Fixed-Performance Paradigm , 2001, Stroke.

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

[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.  Early consolidation in human primary motor cortex , 2002, Nature.

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

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

[17]  K. Zilles,et al.  Neural activity in human primary motor cortex areas 4a and 4p is modulated differentially by attention to action. , 2002, Journal of neurophysiology.

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

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

[21]  A. Sirigu,et al.  Left and right hand recognition in upper limb amputees. , 2004, Brain : a journal of neurology.

[22]  D Yves von Cramon,et al.  Sequences of Abstract Nonbiological Stimuli Share Ventral Premotor Cortex with Action Observation and Imagery , 2004, The Journal of Neuroscience.

[23]  S. Small,et al.  Fine modulation in network activation during motor execution and motor imagery. , 2004, Cerebral cortex.

[24]  L. Cohen,et al.  Mechanisms underlying recovery of motor function after stroke , 2005, Postgraduate Medical Journal.

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

[26]  P. Brugger,et al.  What disconnection tells about motor imagery: evidence from paraplegic patients. , 2005, Cerebral cortex.

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

[28]  Martin Lotze,et al.  Volition and imagery in neurorehabilitation. , 2006, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[29]  Peter S. Jones,et al.  Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study , 2006, NeuroImage.

[30]  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.

[31]  J. Baron,et al.  Motor Imagery: A Backdoor to the Motor System After Stroke? , 2006, Stroke.

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

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

[34]  Preeti Raghavan,et al.  Impaired anticipatory control of fingertip forces in patients with a pure motor or sensorimotor lacunar syndrome. , 2006, Brain : a journal of neurology.

[35]  Jean-Claude Baron,et al.  Quantification of index tapping regularity after stroke with tri-axial accelerometry , 2006, Brain Research Bulletin.

[36]  S. Page,et al.  Mental Practice in Chronic Stroke: Results of a Randomized, Placebo-Controlled Trial , 2007, Stroke.

[37]  Edward T. Bullmore,et al.  The relationship between motor deficit and hemisphere activation balance after stroke: A 3T fMRI study , 2007, NeuroImage.

[38]  Peter S. Jones,et al.  Mapping the involvement of BA 4a and 4p during Motor Imagery , 2008, NeuroImage.

[39]  Paul E. Summers,et al.  Preservation of motor programs in paraplegics as demonstrated by attempted and imagined foot movements , 2008, NeuroImage.