A Neuroanatomical Framework for Upper Limb Synergies after Stroke

Muscle synergies describe common patterns of co- or reciprocal activation that occur during movement. After stroke, these synergies change, often in stereotypical ways. The mechanism underlying this change reflects damage to key motor pathways as a result of the stroke lesion, and the subsequent reorganization along the neuroaxis, which may be further detrimental or restorative to motor function. The time course of abnormal synergy formation seems to lag spontaneous recovery that occurs in the initial weeks after stroke. In healthy individuals, motor cortical activity, descending via the corticospinal tract (CST) is the predominant driver of voluntary behavior. When the CST is damaged after stroke, other descending pathways may be up-regulated to compensate. The contribution of these pathways may emerge as new synergies take shape at the chronic stage after stroke, as a result of plasticity along the neuroaxis. The location of the stroke lesion and properties of the secondary descending pathways and their regulation are then critical for shaping the synergies in the remaining motor behavior. A consideration of the integrity of remaining descending motor pathways may aid in the design of new rehabilitation therapies.

[1]  W. Byblow,et al.  Cathodal transcranial direct current stimulation of the primary motor cortex improves selective muscle activation in the ipsilateral arm. , 2011, Journal of neurophysiology.

[2]  G. Kwakkel,et al.  Understanding the pattern of functional recovery after stroke: facts and theories. , 2004, Restorative neurology and neuroscience.

[3]  Andrei I Holodny,et al.  Diffusion-tensor MR tractography of somatotopic organization of corticospinal tracts in the internal capsule: initial anatomic results in contradistinction to prior reports. , 2005, Radiology.

[4]  M. Schieber,et al.  How somatotopic is the motor cortex hand area? , 1993, Science.

[5]  R. Malinow,et al.  Negative learning bias is associated with risk aversion in a genetic animal model of depression , 2014, Front. Hum. Neurosci..

[6]  Sook-Lei Liew,et al.  Non-invasive brain stimulation in neurorehabilitation: local and distant effects for motor recovery , 2014, Front. Hum. Neurosci..

[7]  H. Hislop,et al.  Movement therapy in hemiplegia : a neurophysiological approach , 1970 .

[8]  C. Wolfe,et al.  The impact of stroke. , 2000, British medical bulletin.

[9]  E. Bizzi,et al.  Stability of muscle synergies for voluntary actions after cortical stroke in humans , 2009, Proceedings of the National Academy of Sciences.

[10]  W. Rymer,et al.  Alterations in upper limb muscle synergy structure in chronic stroke survivors. , 2013, Journal of neurophysiology.

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

[12]  E. G. Jones,et al.  Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: a correlative anatomic and physiological study. , 1991, Journal of neurophysiology.

[13]  W. Rymer,et al.  Abnormal corticomotor excitability assessed in biceps brachii preceding pronator contraction post-stroke , 2008, Clinical Neurophysiology.

[14]  J. Stinear,et al.  Suppression of motor evoked potentials in biceps brachii preceding pronator contraction , 2007, Experimental Brain Research.

[15]  Andrea d'Avella,et al.  Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. , 2006, Journal of neurophysiology.

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

[17]  Gert Kwakkel,et al.  Early Prediction of Outcome of Activities of Daily Living After Stroke: A Systematic Review , 2011, Stroke.

[18]  Angelo M. Sabatini,et al.  Identification of neuromuscular synergies in natural upper-arm movements , 2002, Biological Cybernetics.

[19]  Silvestro Micera,et al.  Effects of early and intensive neuro-rehabilitative treatment on muscle synergies in acute post-stroke patients: a pilot study , 2013, Journal of NeuroEngineering and Rehabilitation.

[20]  Panayiota Poirazi,et al.  Computational modeling of the effects of amyloid-beta on release probability at hippocampal synapses , 2013, Front. Comput. Neurosci..

[21]  C. Stinear,et al.  Prediction of recovery of motor function after stroke , 2010, The Lancet Neurology.

[22]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  R. Lemon.  Descending pathways in motor control. , 2008, Annual review of neuroscience.

[24]  Julius P. A. Dewald,et al.  Ipsilateral versus contralateral cortical motor projections to a shoulder adductor in chronic hemiparetic stroke: implications for the expression of arm synergies , 2008, Experimental Brain Research.

[25]  Gary W Thickbroom,et al.  Long-term changes in motor cortical organisation after recovery from subcortical stroke 1 1 Published on the World Wide Web on 1 December 2000. , 2001, Brain Research.

[26]  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.

[27]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Christian Ethier,et al.  On the functional organization and operational principles of the motor cortex , 2013, Front. Neural Circuits.

[29]  J. Krakauer,et al.  Neurorehabilitation and Neural Repair Inter-individual Variability in the Capacity for Motor Recovery after Ischemic Stroke Neurorehabilitation and Neural Repair Additional Services and Information for Inter-individual Variability in the Capacity for Motor Recovery after Ischemic Stroke , 2022 .

[30]  Christian Ethier,et al.  The comparable size and overlapping nature of upper limb distal and proximal muscle representations in the human motor cortex , 2006, The European journal of neuroscience.

[31]  J. Krakauer,et al.  Prediction of motor recovery using initial impairment and fMRI 48 h poststroke. , 2011, Cerebral cortex.

[32]  E. Mohammadi,et al.  Barriers and facilitators related to the implementation of a physiological track and trigger system: A systematic review of the qualitative evidence , 2017, International journal for quality in health care : journal of the International Society for Quality in Health Care.

[33]  Simon A. Overduin,et al.  Microstimulation Activates a Handful of Muscle Synergies , 2012, Neuron.

[34]  E. Bizzi,et al.  Article history: , 2005 .

[35]  Martha Flanders,et al.  Muscular and postural synergies of the human hand. , 2004, Journal of neurophysiology.

[36]  Niels Birbaumer,et al.  Cortex Integrity Relevance in Muscle Synergies in Severe Chronic Stroke , 2014, Front. Hum. Neurosci..

[37]  Matthew C. Tresch,et al.  The number and choice of muscles impact the results of muscle synergy analyses , 2013, Front. Comput. Neurosci..

[38]  John P Scholz,et al.  Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. , 2003, Brain : a journal of neurology.

[39]  T. Twitchell.  The restoration of motor function following hemiplegia in man. , 1951, Brain : a journal of neurology.

[40]  W. Byblow,et al.  Ipsilateral Motor Pathways after Stroke: Implications for Non-Invasive Brain Stimulation , 2013, Front. Hum. Neurosci..

[41]  R. E. Lrvine.  Movement Therapy in Hemiplegia: A Neurophysiological Approach , 1972 .

[42]  E. Bizzi,et al.  Responses to spinal microstimulation in the chronically spinalized rat and their relationship to spinal systems activated by low threshold cutaneous stimulation , 1999, Experimental Brain Research.

[43]  E. Bizzi,et al.  Muscle synergy patterns as physiological markers of motor cortical damage , 2012, Proceedings of the National Academy of Sciences.

[44]  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.

[45]  W PENFIELD,et al.  Mechanisms of voluntary movement. , 1954, Brain : a journal of neurology.

[46]  B Hyland,et al.  Cortical cell assemblies: a possible mechanism for motor programs. , 1994, Journal of motor behavior.

[47]  L. Cohen,et al.  Influence of interhemispheric interactions on motor function in chronic stroke , 2004, Annals of neurology.

[48]  L. Miller,et al.  Primary motor cortical neurons encode functional muscle synergies , 2002, Experimental Brain Research.

[49]  Francesco Lacquaniti,et al.  Control of Fast-Reaching Movements by Muscle Synergy Combinations , 2006, The Journal of Neuroscience.

[50]  D Goodman,et al.  On the coordination of two-handed movements. , 1979, Journal of experimental psychology. Human perception and performance.

[51]  W. Byblow,et al.  Contralesional hemisphere control of the proximal paretic upper limb following stroke. , 2012, Cerebral cortex.

[52]  Matthew Petoe,et al.  The PREP algorithm predicts potential for upper limb recovery after stroke. , 2012, Brain : a journal of neurology.