Bilateral Synergy: A Framework for Post-Stroke Rehabilitation.

BACKGROUND Unilateral stroke produces debilitating deficits in voluntary control in the contralesional arm, and significant motor coordination deficits in the ipsilesional arm. In addition, patients tend to avoid bilateral arm patterns and during performance of activities of daily living. Nevertheless, upper extremity physical rehabilitation predominantly focuses on motor training activities with only the paretic arm. This can be limiting because of persistent deficits in the ipsilesional arm, and because of the tendency of patients to avoid spontaneous bilateral arm patterns. PROPOSITION Rehabilitation should focus on bilateral training to advance recovery of function in both arms of stroke patients, as well as to facilitate spontaneous bilateral arm use. This paper reviews the rationale for this approach, citing evidence for significant hemisphere specific bilateral motor deficits in stroke patients, which affect both the contralesional and the ipsilesional arm. The rationale for, and advantages of, training both arms simultaneously through bilateral tasks is reviewed. Although bilateral training has been employed to treat stroke patients previously, this has tended to focus on bimanual 'coupling' as a rationale for performing parallel, but not cooperative bilateral tasks. Bilateral synergy provides a more functional framework for structuring post-stroke upper extremity rehabilitation. CONCLUSION Bilateral synergy may be causally linked to spontaneous bilateral arm use, suggesting that rehabilitation should be focused on bilateral cooperative tasks, such as bilateral object transport. Further research is required to determine whether this approach could be efficacious for patients with hemiparesis, and whether both left and right hemisphere strokes can benefit from such intervention.

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

[2]  André Seyfarth,et al.  Inverse biomimetics: How robots can help to verify concepts concerning sensorimotor control of human arm and leg movements , 2009, Journal of Physiology-Paris.

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

[4]  S. Swinnen Interlimb coordination : neural, dynamical, and cognitive constraints , 1994 .

[5]  Andrzej Przybyla,et al.  Contralesional motor deficits after unilateral stroke reflect hemisphere-specific control mechanisms. , 2013, Brain : a journal of neurology.

[6]  M. Turvey,et al.  Symmetry, broken symmetry, and handedness in bimanual coordination dynamics , 2004, Experimental Brain Research.

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

[8]  E. Vaadia,et al.  Single-unit activity related to bimanual arm movements in the primary and supplementary motor cortices. , 2002, Journal of neurophysiology.

[9]  J. Poole,et al.  Ipsilateral deficits in 1-handed shoe tying after left or right hemisphere stroke. , 2009, Archives of physical medicine and rehabilitation.

[10]  Stephan P Swinnen,et al.  Exploring interlimb constraints during bimanual graphic performance: effects of muscle grouping and direction , 1998, Behavioural Brain Research.

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

[12]  E. Vaadia,et al.  Timing of bimanual movements in human and non-human primates in relation to neuronal activity in primary motor cortex and supplementary motor area , 2002, Experimental Brain Research.

[13]  J. Adair,et al.  Arm Use After Left or Right Hemiparesis Is Influenced by Hand Preference , 2009, Stroke.

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

[15]  Robert L Sainburg,et al.  Differentiating between two models of motor lateralization. , 2008, Journal of neurophysiology.

[16]  Robert T. Knight,et al.  Ipsilesional trajectory control is related to contralesional arm paralysis after left hemisphere damage , 2009, Experimental Brain Research.

[17]  A. G. Feldman,et al.  Bilateral coupling facilitates recovery of rhythmical movements from perturbation in healthy and post-stroke subjects , 2013, Experimental Brain Research.

[18]  Jeffery J. Summers,et al.  Bilateral movement training and stroke rehabilitation: A systematic review and meta-analysis , 2006, Journal of the Neurological Sciences.

[19]  N. Hogan,et al.  Robotics and other devices in the treatment of patients recovering from stroke , 2004, Current neurology and neuroscience reports.

[20]  Robert L. Sainburg,et al.  Lateralization of motor adaptation reveals independence in control of trajectory and steady-state position , 2007, Experimental Brain Research.

[21]  W. Byblow,et al.  Neurophysiological and behavioural adaptations to a bilateral training intervention in individuals following stroke , 2004, Clinical rehabilitation.

[22]  Romeo Chua,et al.  Discrete vs. continuous visual control of manual aiming , 1991 .

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

[24]  Y. Samson,et al.  Movement‐ and task‐related activations of motor cortical areas: A positron emission tomographic study , 1994, Annals of neurology.

[25]  Alvaro Pascual-Leone,et al.  Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions , 2003, NeuroImage.

[26]  Ian Q Whishaw,et al.  A Novel Skilled-Reaching Impairment in Paw Supination on the “Good” Side of the Hemi-Parkinson Rat Improved with Rehabilitation , 2003, The Journal of Neuroscience.

[27]  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.

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

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

[30]  D. Elliott,et al.  Asymmetries in the Preparation and Control of Manual Aiming Movements , 1993 .

[31]  S. Wolf,et al.  Forced use of hemiplegic upper extremities to reverse the effect of learned nonuse among chronic stroke and head-injured patients , 1989, Experimental Neurology.

[32]  J. Krakauer Motor learning: its relevance to stroke recovery and neurorehabilitation. , 2006, Current opinion in neurology.

[33]  J. Krakauer,et al.  Motor learning principles for neurorehabilitation. , 2013, Handbook of clinical neurology.

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

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

[36]  J. Dewald,et al.  Impact of gravity loading on post‐stroke reaching and its relationship to weakness , 2007, Muscle & nerve.

[37]  E. Taub,et al.  The learned nonuse phenomenon: implications for rehabilitation. , 2006, Europa medicophysica.

[38]  S. Page,et al.  Modified constraint-induced therapy and botulinum toxin A: a promising combination. , 2003, American journal of physical medicine & rehabilitation.

[39]  Robert L. Sainburg,et al.  Dynamic dominance varies with handedness: reduced interlimb asymmetries in left-handers , 2012, Experimental Brain Research.

[40]  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.

[41]  Gregor Schöner,et al.  The uncontrolled manifold concept: identifying control variables for a functional task , 1999, Experimental Brain Research.

[42]  K. Haaland,et al.  Functional significance of ipsilesional motor deficits after unilateral stroke. , 2008, Archives of physical medicine and rehabilitation.

[43]  R. Sainburg,et al.  Dynamic Dominance Persists During Unsupported Reaching , 2012, Journal of motor behavior.

[44]  Visuomotor learning generalizes between bilateral and unilateral conditions despite varying degrees of bilateral interference. , 2010, Journal of neurophysiology.

[45]  J. Hermsdörfer,et al.  Prehension With the Ipsilesional Hand After Unilateral Brain Damage , 1999, Cortex.

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

[47]  Gregor Schöner,et al.  Goal-equivalent joint coordination in pointing: affect of vision and arm dominance. , 2002, Motor control.

[48]  J. Krakauer,et al.  Getting Neurorehabilitation Right , 2012, Neurorehabilitation and neural repair.

[49]  Gregor Schöner,et al.  Identifying the control structure of multijoint coordination during pistol shooting , 2000, Experimental Brain Research.

[50]  Yuming Lei,et al.  Substantial Generalization of Sensorimotor Learning from Bilateral to Unilateral Movement Conditions , 2013, PloS one.

[51]  J. Tanji,et al.  Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. , 1988, Journal of neurophysiology.

[52]  Maria Wyke,et al.  Effect of brain lesions on the rapidity of arm movement , 1967, Neurology.

[53]  M. Latash,et al.  Structure of motor variability in marginally redundant multifinger force production tasks , 2001, Experimental Brain Research.

[54]  Jeffery J. Summers,et al.  Bilateral and unilateral movement training on upper limb function in chronic stroke patients: A TMS study , 2007, Journal of the Neurological Sciences.

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

[56]  M Wiesendanger,et al.  Temporal coordination in bimanual actions. , 1994, Canadian journal of physiology and pharmacology.

[57]  M. Wyke,et al.  Laterality Differences for Speed but Not for Control in Sequential Finger Tapping , 1988, Perceptual and motor skills.

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

[59]  Marco Santello,et al.  Compensatory motor control after stroke: an alternative joint strategy for object-dependent shaping of hand posture. , 2010, Journal of neurophysiology.

[60]  Pratik K. Mutha,et al.  The Effects of Brain Lateralization on Motor Control and Adaptation , 2012, Journal of motor behavior.

[61]  Pratik K. Mutha,et al.  Rethinking Motor Lateralization: Specialized but Complementary Mechanisms for Motor Control of Each Arm , 2013, PloS one.

[62]  R. Ivry,et al.  Bimanual cross-talk during reaching movements is primarily related to response selection, not the specification of motor parameters , 2003, Psychological research.

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

[64]  C. Brinkman,et al.  Lesions in supplementary motor area interfere with a monkey's performance of a bimanual coordination task , 1981, Neuroscience Letters.

[65]  R Salmelin,et al.  Bilateral activation of the human somatomotor cortex by distal hand movements. , 1995, Electroencephalography and clinical neurophysiology.

[66]  J. Hermsdörfer,et al.  Effects of unilateral brain damage on grip selection, coordination, and kinematics of ipsilesional prehension , 1999, Experimental Brain Research.

[67]  R. Ivry,et al.  Independent on‐line control of the two hands during bimanual reaching , 2004, The European journal of neuroscience.

[68]  C. Winstein,et al.  The co-ordination of bimanual rapid aiming movements following stroke , 2005, Clinical rehabilitation.

[69]  Romeo Chua,et al.  Asymmetries in the spatial localization of transformed targets , 1992, Brain and Cognition.

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

[71]  Jill Whitall,et al.  Bilateral and Unilateral Arm Training Improve Motor Function Through Differing Neuroplastic Mechanisms , 2011, Neurorehabilitation and neural repair.

[72]  S. Wolf,et al.  An application of upper-extremity constraint-induced movement therapy in a patient with subacute stroke. , 1999, Physical therapy.

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

[74]  M. Wyke,et al.  The effects of brain lesions on the performance of bilateral arm movements. , 1971, Neuropsychologia.

[75]  R. Ivry,et al.  Moving to Directly Cued Locations Abolishes Spatial Interference During Bimanual Actions , 2001, Psychological science.

[76]  S. Telera,et al.  Ipsilateral motor activation in patients with cerebral gliomas , 1998, Neurology.

[77]  S. Wolf,et al.  Repetitive Task Practice: A Critical Review of Constraint-Induced Movement Therapy in Stroke , 2002, The neurologist.

[78]  M. D. Ellis,et al.  Mechanisms And Rehabilitation Of Discoordination Following Stroke Using A Cortical Imaging Method , 2005, 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference.

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

[80]  D. Arciniegas,et al.  Constraint-induced movement therapy after stroke: efficacy for patients with minimal upper-extremity motor ability. , 2005, Archives of physical medicine and rehabilitation.

[81]  J. Brust Lesions of the supplementary motor area. , 1996, Advances in neurology.

[82]  A. Luft,et al.  Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial. , 2004, JAMA.

[83]  Robert L Sainburg,et al.  Does motor lateralization have implications for stroke rehabilitation? , 2006, Journal of rehabilitation research and development.

[84]  W Z Rymer,et al.  Reorganization of flexion reflexes in the upper extremity of hemiparetic subjects , 1999, Muscle & nerve.

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

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

[87]  D Goodman,et al.  On the nature of human interlimb coordination. , 1979, Science.

[88]  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.

[89]  A Yamadori,et al.  Comparison of ipsilateral activation between right and left handers: a functional MR imaging study , 1998, Neuroreport.

[90]  J. Whitall,et al.  Bilateral arm training: why and who benefits? , 2008, NeuroRehabilitation.

[91]  Relationship between arm usage and instrumental activities of daily living after unilateral stroke. , 2012, Archives of physical medicine and rehabilitation.

[92]  Stefan Panzer,et al.  Increasingly complex bimanual multi-frequency coordination patterns are equally easy to perform with on-line relative velocity feedback , 2011, Experimental Brain Research.

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

[94]  M. Latash,et al.  Motor Control Strategies Revealed in the Structure of Motor Variability , 2002, Exercise and sport sciences reviews.

[95]  R. H. Jebsen,et al.  Function of "normal" hand in stroke patients. , 1971, Archives of physical medicine and rehabilitation.

[96]  Richard G. Carson,et al.  Manual Asymmetries in the Preparation and Control of Goal-Directed Movements , 2001, Brain and Cognition.

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

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