Ipsilateral motor dysfunction from unilateral stroke: implications for the functional neuroanatomy of hemiparesis

Background: Motor dysfunction in the contralateral hand has been well characterised after stroke. The ipsilateral hand has received less attention, yet may provide valuable insights into the structure of the motor system and the nature of the recovery process. By tracking motor function of both hands beginning in the acute stroke period in patients with cortical versus subcortical lesions, we sought to understand the functional anatomy of the ipsilateral deficit. Methods: We examined 30 patients with first-ever unilateral hemiparetic stroke, 23 with subcortical lesions affecting the corticospinal tract, seven with cortical involvement. Patients performed hand dynamometry and the 9-Hole Peg Test (9HPT) with each hand at 24–48 h, 1 week, 3 months and 1 year after stroke. Linear regression was used to compare the two different motor tasks in each hand. Repeated measures ANOVA was used to compare recovery rates of the two tasks in the first 3 months. Results: Ipsilateral 9HPT scores averaged z = −7.1, −3.6, −2.5 and −2.3 at the four time points whereas grip strength was unaffected. The initial degree of impairment of grip strength in the contralateral hand did not correlate with the degree of impairment of 9HPT in either the contralateral or ipsilateral hand (r = 0.001, p = 0.98), whereas the initial degree of impairment of 9HPT in the contralateral hand correlated with the degree of impairment of 9HPT in the ipsilateral hand (r = 0.79, p = 0.035). The rate of recovery also differed for the two tasks (p = 0.005). Conclusion: Ipsilateral motor deficits are demonstrable immediately after stroke and extend into the subacute and chronic recovery period. Dissociation between grip strength and dexterity support the notion that dexterity and grip strength operate as anatomically and functionally distinct entities. Our findings in patients with subcortical lesions suggest that the model of white matter tract injury needs to be refined to reflect the influence of a subcortical lesion on bi-hemispheral cortical networks, rather than as a simple “severed cable” model of disruption of corticofugal fibres. Our data have implications for both stroke clinical trials and the development of new strategies for therapeutic intervention in stroke recovery.

[1]  F. Chollet,et al.  Impairment and recovery of left motor function in patients with right hemiplegia. , 1997, Journal of neurology, neurosurgery, and psychiatry.

[2]  Subashan Perera,et al.  Impaired Grip Force Modulation in the Ipsilesional Hand after Unilateral Middle Cerebral Artery Stroke , 2005, Neurorehabilitation and neural repair.

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

[4]  P. Rossini,et al.  Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. , 2002, Brain : a journal of neurology.

[5]  W. Zung A SELF-RATING DEPRESSION SCALE. , 1965, Archives of general psychiatry.

[6]  P. Skudlarski,et al.  An fMRI study of the human cortical motor system response to increasing functional demands. , 1997, Magnetic resonance imaging.

[7]  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.

[8]  W. Cumming An anatomical review of the corpus callosum. , 1970, Cortex; a journal devoted to the study of the nervous system and behavior.

[9]  Jens Frahm,et al.  Topography of the human corpus callosum revisited—Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging , 2006, NeuroImage.

[10]  V. Hömberg,et al.  Reorganization of motor output in the non-affected hemisphere after stroke. , 1997, Brain : a journal of neurology.

[11]  Donna S Hoffman,et al.  Deficits in movements of the wrist ipsilateral to a stroke in hemiparetic subjects. , 2004, Journal of neurophysiology.

[12]  Antonis P Stylianou,et al.  Ipsilateral deficits of targeted movements after stroke. , 2003, Archives of physical medicine and rehabilitation.

[13]  John W Krakauer,et al.  Arm function after stroke: from physiology to recovery. , 2005, Seminars in neurology.

[14]  D. Pandya,et al.  The cerebrocerebellar system. , 1997, International review of neurobiology.

[15]  Armin Thron,et al.  Motor representation in patients rapidly recovering after stroke: a functional magnetic resonance imaging and transcranial magnetic stimulation study , 2003, Clinical Neurophysiology.

[16]  A. Prevo,et al.  The long-term outcome of arm function after stroke: results of a follow-up study. , 1999, Disability and rehabilitation.

[17]  H. Luhmann Ischemia and lesion induced imbalances in cortical function , 1996, Progress in Neurobiology.

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

[19]  Christian Gerloff,et al.  Ipsilateral cortical activation during finger sequences of increasing complexity: representation of movement difficulty or memory load? , 2003, Clinical Neurophysiology.

[20]  Paolo Maria Rossini,et al.  Rhythmic brain activity at rest from rolandic areas in acute mono-hemispheric stroke: A magnetoencephalographic study , 2005, NeuroImage.

[21]  Kimatha Oxford Grice,et al.  Adult norms for a commercially available Nine Hole Peg Test for finger dexterity. , 2003, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[22]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[23]  J. Poole,et al.  Functional implications of ipsilesional motor deficits after unilateral stroke. , 2005, Archives of physical medicine and rehabilitation.

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

[25]  Carl-Fredrik Westin,et al.  High-resolution line scan diffusion tensor MR imaging of white matter fiber tract anatomy. , 2002, AJNR. American journal of neuroradiology.

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

[27]  R. Dickstein,et al.  Time-Related Changes in Motor Performance of the Upper Extremity Ipsilateral to the Side of the Lesion in Stroke Survivors , 2001, Neurorehabilitation and neural repair.

[28]  A. Brodal,et al.  Self-observations and neuro-anatomical considerations after a stroke. , 1973, Brain : a journal of neurology.

[29]  H. Gräfin von Einsiedel,et al.  The role of lateral premotor-cerebellar-parietal circuits in motor sequence control: a parametric fMRI study. , 2002, Brain research. Cognitive brain research.

[30]  Harold D. Delaney,et al.  Motor deficits after left or right hemisphere damage due to stroke or tumor , 1981, Neuropsychologia.

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

[32]  J. Yelnik Functional anatomy of the basal ganglia , 2002, Movement disorders : official journal of the Movement Disorder Society.

[33]  Sabrina M. Tom,et al.  The Neural Correlates of Motor Skill Automaticity , 2005, The Journal of Neuroscience.

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

[35]  S. Sasaki,et al.  Dexterous finger movements in primate without monosynaptic corticomotoneuronal excitation. , 2004, Journal of neurophysiology.

[36]  Martin E Schwab,et al.  The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats , 2004, Nature Neuroscience.

[37]  P. Manganotti,et al.  Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke , 2002, Clinical Neurophysiology.

[38]  M. Merello,et al.  [Functional anatomy of the basal ganglia]. , 2000, Revista de neurologia.

[39]  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.

[40]  M. Tuszynski,et al.  Bilateral corticospinal projections arise from each motor cortex in the macaque monkey: A quantitative study , 2004, The Journal of comparative neurology.

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

[42]  Deborah L. Harrington,et al.  Hemispheric control of the initial and corrective components of aiming movements , 1989, Neuropsychologia.

[43]  E. Jankowska,et al.  How Can Corticospinal Tract Neurons Contribute to Ipsilateral Movements? A Question With Implications for Recovery of Motor Functions , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[44]  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.

[45]  Victor De Pasqua,et al.  Post-stroke reorganization of hand motor area: a 1-year prospective follow-up with focal transcranial magnetic stimulation , 2003, Clinical Neurophysiology.

[46]  M. Filippi,et al.  Simple and complex movement‐associated functional MRI changes in patients at presentation with clinically isolated syndromes suggestive of multiple sclerosis , 2004, Human brain mapping.

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

[48]  B. Bussel,et al.  Changes in the execution of a complex manual task after ipsilateral ischemic cerebral hemispheric stroke. , 1996, Archives of physical medicine and rehabilitation.