Contralesional motor deficits after unilateral stroke reflect hemisphere-specific control mechanisms.

We have proposed a model of motor lateralization, in which the left and right hemispheres are specialized for different aspects of motor control: the left hemisphere for predicting and accounting for limb dynamics and the right hemisphere for stabilizing limb position through impedance control mechanisms. Our previous studies, demonstrating different motor deficits in the ipsilesional arm of stroke patients with left or right hemisphere damage, provided a critical test of our model. However, motor deficits after stroke are most prominent on the contralesional side. Post-stroke rehabilitation has also, naturally, focused on improving contralesional arm impairment and function. Understanding whether contralesional motor deficits differ depending on the hemisphere of damage is, therefore, of vital importance for assessing the impact of brain damage on function and also for designing rehabilitation interventions specific to laterality of damage. We, therefore, asked whether motor deficits in the contralesional arm of unilateral stroke patients reflect hemisphere-dependent control mechanisms. Because our model of lateralization predicts that contralesional deficits will differ depending on the hemisphere of damage, this study also served as an essential assessment of our model. Stroke patients with mild to moderate hemiparesis in either the left or right arm because of contralateral stroke and healthy control subjects performed targeted multi-joint reaching movements in different directions. As predicted, our results indicated a double dissociation; although left hemisphere damage was associated with greater errors in trajectory curvature and movement direction, errors in movement extent were greatest after right hemisphere damage. Thus, our results provide the first demonstration of hemisphere specific motor control deficits in the contralesional arm of stroke patients. Our results also suggest that it is critical to consider the differential deficits induced by right or left hemisphere lesions to enhance post-stroke rehabilitation interventions.

[1]  Pratik K Mutha,et al.  Relationship between arm usage and instrumental activities of daily living after unilateral stroke. , 2012, Archives of physical medicine and rehabilitation.

[2]  Robert L Sainburg,et al.  Hemispheric specialization for movement control produces dissociable differences in online corrections after stroke. , 2012, Cerebral cortex.

[3]  A. Roby-Brami,et al.  Influence of the side of brain damage on postural upper-limb control including the scapula in stroke patients , 2012, Experimental Brain Research.

[4]  Robert L Sainburg,et al.  Critical neural substrates for correcting unexpected trajectory errors and learning from them. , 2011, Brain : a journal of neurology.

[5]  Robert L Sainburg,et al.  Left Parietal Regions Are Critical for Adaptive Visuomotor Control , 2011, The Journal of Neuroscience.

[6]  Robert L. Sainburg,et al.  Aging reduces asymmetries in interlimb transfer of visuomotor adaptation , 2011, Experimental Brain Research.

[7]  L Pisella,et al.  Right-hemispheric dominance for visual remapping in humans , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  R. Sainburg,et al.  Motor asymmetry reduction in older adults , 2011, Neuroscience Letters.

[9]  K. Sunnerhagen,et al.  Kinematic Variables Quantifying Upper-Extremity Performance After Stroke During Reaching and Drinking From a Glass , 2011, Neurorehabilitation and neural repair.

[10]  Pratik K Mutha,et al.  Coordination deficits in ideomotor apraxia during visually targeted reaching reflect impaired visuomotor transformations , 2010, Neuropsychologia.

[11]  J. Summers,et al.  Bilateral movement training and stroke motor recovery progress: a structured review and meta-analysis. , 2010, Human movement science.

[12]  L. Hale,et al.  The impact of bilateral therapy on upper limb function after chronic stroke: a systematic review , 2010, Disability and rehabilitation.

[13]  E. Paulesu,et al.  Productive symptoms in right brain damage , 2009, Current opinion in neurology.

[14]  R. Sainburg,et al.  Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy , 2009, Neuropsychologia.

[15]  Robert L. Sainburg,et al.  Dissociation of initial trajectory and final position errors during visuomotor adaptation following unilateral stroke , 2009, Brain Research.

[16]  Neil B Alexander,et al.  The influence of age and physical activity on upper limb proprioceptive ability. , 2009, Journal of aging and physical activity.

[17]  Pratik K. Mutha,et al.  Visual modulation of proprioceptive reflexes during movement , 2008, Brain Research.

[18]  Robert L Sainburg,et al.  Ipsilesional motor deficits following stroke reflect hemispheric specializations for movement control. , 2007, Brain : a journal of neurology.

[19]  A. Milner,et al.  Reaching errors in optic ataxia are linked to eye position rather than head or body position , 2006, Neuropsychologia.

[20]  Stephen H Scott,et al.  Limited transfer of learning between unimanual and bimanual skills within the same limb , 2006, Nature Neuroscience.

[21]  Robert L. Sainburg,et al.  Handedness: Differential Specializations for Control of Trajectory and Position , 2005, Exercise and sport sciences reviews.

[22]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

[23]  Roland R. Lee,et al.  Hemispheric asymmetries for kinematic and positional aspects of reaching. , 2004, Brain : a journal of neurology.

[24]  W. Rymer,et al.  Target-dependent differences between free and constrained arm movements in chronic hemiparesis , 2004, Experimental Brain Research.

[25]  Robert L Sainburg,et al.  Nondominant arm advantages in load compensation during rapid elbow joint movements. , 2003, Journal of neurophysiology.

[26]  S. Cramer,et al.  Motor Cortex Organization After Stroke Is Related to Side of Stroke and Level of Recovery , 2003, Stroke.

[27]  Robert L Sainburg,et al.  Handedness: dominant arm advantages in control of limb dynamics. , 2002, Journal of neurophysiology.

[28]  C B Walter,et al.  Bilateral facilitation of motor control in chronic hemiplegia. , 2002, Acta psychologica.

[29]  D. Reinkensmeyer,et al.  Alterations in reaching after stroke and their relation to movement direction and impairment severity. , 2002, Archives of physical medicine and rehabilitation.

[30]  R. Cabeza Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[31]  J. Callicott,et al.  Neurophysiological correlates of age-related changes in human motor function , 2002, Neurology.

[32]  N. Hogan,et al.  Is robot-aided sensorimotor training in stroke rehabilitation a realistic option? , 2001, Current opinion in neurology.

[33]  I. Apel,et al.  Reaching-lifting-placing task during standing after stroke: Coordination among ground forces, ankle muscle activity, and hand movement. , 2001, Archives of physical medicine and rehabilitation.

[34]  M. Wiesendanger,et al.  Different Ipsilateral Representations for Distal and Proximal Movements in the Sensorimotor Cortex: Activation and Deactivation Patterns , 2001, NeuroImage.

[35]  J. Whitall,et al.  Repetitive Bilateral Arm Training With Rhythmic Auditory Cueing Improves Motor Function in Chronic Hemiparetic Stroke , 2000, Stroke.

[36]  R. Sainburg,et al.  Differences in control of limb dynamics during dominant and nondominant arm reaching. , 2000, Journal of neurophysiology.

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

[38]  Elisabetta Làdavas,et al.  RIGHT HEMISPHERE DAMAGE. , 2000 .

[39]  Laurel J. Buxbaum,et al.  Subtypes of optic ataxia: Reframing the disconnection account , 1997 .

[40]  Scott T. Grafton,et al.  Motor task difficulty and brain activity: investigation of goal-directed reciprocal aiming using positron emission tomography. , 1997, Journal of neurophysiology.

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

[42]  V M Haughton,et al.  Ipsilateral hemisphere activation during motor and sensory tasks. , 1996, AJNR. American journal of neuroradiology.

[43]  M. Levin Interjoint coordination during pointing movements is disrupted in spastic hemiparesis. , 1996, Brain : a journal of neurology.

[44]  A. G. Fisher,et al.  Differences between persons with right or left cerebral vascular accident on the Assessment of Motor and Process Skills. , 1995, Archives of Physical Medicine and Rehabilitation.

[45]  W Z Rymer,et al.  Joint dependent passive stiffness in paretic and contralateral limbs of spastic patients with hemiparetic stroke. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[46]  W. Rymer,et al.  Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. , 1995, Brain : a journal of neurology.

[47]  A. Thilmann,et al.  Voluntary movement at the elbow in spastic hemiparesis , 1994, Annals of neurology.

[48]  Giuseppe Vallar,et al.  Deficits of position sense, unilateral neglect and optokinetic stimulation , 1993, Neuropsychologia.

[49]  S. Kinomura,et al.  Regional cerebral blood flow changes of cortical motor areas and prefrontal areas in humans related to ipsilateral and contralateral hand movement , 1993, Brain Research.

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

[51]  el-Abd Ma,et al.  Impaired activation pattern in antagonistic elbow muscles of patients with spastic hemiparesis: contribution to movement disorder. , 1993, Electromyography and clinical neurophysiology.

[52]  N. Miller,et al.  Technique to improve chronic motor deficit after stroke. , 1993, Archives of physical medicine and rehabilitation.

[53]  D. Harrington,et al.  Hemispheric specialization for motor sequencing: Abnormalities in levels of programming , 1991, Neuropsychologia.

[54]  V. Dietz,et al.  Reflex activity and muscle tone during elbow movements in patients with spastic paresis , 1991, Annals of neurology.

[55]  D. Harrington,et al.  The role of the hemispheres in closed loop movements , 1989, Brain and Cognition.

[56]  D Bourbonnais,et al.  Abnormal spatial patterns of elbow muscle activation in hemiparetic human subjects. , 1989, Brain : a journal of neurology.

[57]  C. Ghez,et al.  Trajectory control in targeted force impulses , 1987, Experimental Brain Research.

[58]  D. Perani,et al.  The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man , 1986, Neuropsychologia.

[59]  K. Haaland,et al.  The different types of limb apraxia errors made by patients with left vs. right hemisphere damage , 1984, Brain and Cognition.

[60]  A. Benton Contributions to Neuropsychological Assessment: A Clinical Manual , 1983 .

[61]  R. Angel,et al.  Impairment of voluntary movement by spasticity , 1979, Annals of neurology.

[62]  V. Barnett,et al.  Applied Linear Statistical Models , 1975 .

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

[64]  M. Albert A simple test of visual neglect , 1973, Neurology.

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

[66]  R. Sainburg Lateralization of Goal-Directed Movement , 2010 .

[67]  C. J. Winstein,et al.  Effects of unilateral brain damage on the control of goal-directed hand movements , 2004, Experimental Brain Research.

[68]  Edward Taub,et al.  Constraint-induced movement therapy for chronic stroke hemiparesis and other disabilities. , 2004, Restorative neurology and neuroscience.

[69]  C Ghez,et al.  Trajectory control in targeted force impulses , 2004, Experimental Brain Research.

[70]  R. Sainburg Evidence for a dynamic-dominance hypothesis of handedness , 2001, Experimental Brain Research.

[71]  W. Rymer,et al.  Deficits in the coordination of multijoint arm movements in patients with hemiparesis: evidence for disturbed control of limb dynamics , 2000, Experimental Brain Research.

[72]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[73]  J. Mattingley Attention, Consciousness, and the Damaged Brain: Insights From Parietal Neglect and Extinction , 1999 .

[74]  B R Rosen,et al.  Activation of distinct motor cortex regions during ipsilateral and contralateral finger movements. , 1999, Journal of neurophysiology.

[75]  E. Renzi,et al.  Imitating gestures. A quantitative approach to ideomotor apraxia. , 1980, Archives of neurology.

[76]  B. Bobath Adult hemiplegia: Evaluation and treatment , 1978 .

[77]  Caroline G. Soule Egg-Laying of Limenitis Disippus , 1888 .