Spasticity may obscure motor learning ability after stroke.

Previous motor learning studies based on adapting movements of the hemiparetic arm in stroke subjects have not accounted for spasticity occurring in specific joint ranges (spasticity zones), resulting in equivocal conclusions about learning capacity. We compared the ability of participants with stroke to rapidly adapt elbow extension movements to changing external load conditions outside and inside spasticity zones. Participants with stroke ( n = 12, aged 57.8 ± 9.6 yr) and healthy age-matched controls ( n = 8, 63.5 ± 9.1 yr) made rapid 40°-50° horizontal elbow extension movements from an initial (3°) to a final (6°) target. Sixteen blocks (6-10 trials/block) consisting of alternating loaded (30% maximal voluntary contraction) and nonloaded trials were made in one (controls) or two sessions (stroke; 1 wk apart). For the stroke group, the tonic stretch reflex threshold angle at which elbow flexors began to be activated during passive elbow extension was used to identify the beginning of the spasticity zone. The task was repeated in joint ranges that did or did not include the spasticity zone. Error correction strategies were identified by the angular positions before correction and compared between groups and sessions. Changes in load condition from no load to load and vice versa resulted in undershoot and overshoot errors, respectively. Stroke subjects corrected errors in 1-4 trials compared with 1-2 trials in controls. When movements did not include the spasticity zone, there was an immediate decrease in the number of trials needed to restore accuracy, suggesting that the capacity to learn may be preserved after stroke but masked by the presence of spasticity. NEW & NOTEWORTHY When arm movements were made outside, instead of inside, the range affected by spasticity, there was an immediate decrease in the number of trials needed to restore accuracy in response to a change in the external load. This suggests that motor learning processes may be preserved in patients with stroke but masked by the presence of spasticity in specific joint ranges. This has important implications for designing rehabilitation interventions predicated on motor learning principles.

[1]  Anatol G. Feldman,et al.  Stretch-reflex threshold modulation during active elbow movements in post-stroke survivors with spasticity , 2017, Clinical Neurophysiology.

[2]  D. Mclellan.  C0-contraction and stretch reflexes in spasticity during treatment with baclofen. , 1977, Journal of neurology, neurosurgery, and psychiatry.

[3]  John W Krakauer,et al.  Motor Learning in Stroke , 2017, Neurorehabilitation and neural repair.

[4]  L. Buxbaum,et al.  Visuo-motor gain adaptation and generalization following left hemisphere stroke , 2011, Neuroscience Letters.

[5]  Stanley P. Azen,et al.  Effect of a Task-Oriented Rehabilitation Program on Upper Extremity Recovery Following Motor Stroke: The ICARE Randomized Clinical Trial. , 2016, JAMA.

[6]  Alain Ptito,et al.  Error correction strategies for motor behavior after unilateral brain damage: short-term motor learning processes , 2002, Neuropsychologia.

[7]  G. Weniger,et al.  Implicit and explicit memory after focal thalamic lesions , 2001, Neurology.

[8]  J. Scholz,et al.  Relationship of diminished interjoint coordination after stroke to hand path consistency , 2015, Experimental Brain Research.

[9]  S. Wolf,et al.  Can the Wolf Motor Function Test be Streamlined? , 2009, Neurorehabilitation and neural repair.

[10]  A. G. Feldman,et al.  Stretch reflex spatial threshold measure discriminates between spasticity and rigidity , 2013, Clinical Neurophysiology.

[11]  Katharina Stibrant Sunnerhagen,et al.  Upper-Limb Spasticity During the First Year After Stroke: Stroke Arm Longitudinal Study at the University of Gothenburg , 2014, American journal of physical medicine & rehabilitation.

[12]  Mindy F Levin,et al.  Spatial zones for muscle coactivation and the control of postural stability , 1997, Brain Research.

[13]  Gregory M. Szilagyi,et al.  Lesion Characteristics of Individuals With Upper Limb Spasticity After Stroke , 2016, Neurorehabilitation and neural repair.

[14]  Anatol G. Feldman,et al.  Referent control of action and perception , 2015, Springer New York.

[15]  Anatol G. Feldman,et al.  Referent control of action and perception: Challenging conventional theories in behavioral neuroscience , 2015 .

[16]  A. G. Feldman.  Once More on the Equilibrium-Point Hypothesis (λ Model) for Motor Control , 1986 .

[17]  Mindy F Levin,et al.  Tonic Stretch Reflex Threshold as a Measure of Ankle Plantar-Flexor Spasticity After Stroke , 2015, Physical Therapy.

[18]  A. G. Feldman,et al.  The influence of different descending systems on the tonic stretch reflex in the cat. , 1972, Experimental neurology.

[19]  F. V. Wright,et al.  The Bobath (NDT) concept in adult neurological rehabilitation: what is the state of the knowledge? A scoping review. Part I: conceptual perspectives , 2015, Disability and rehabilitation.

[20]  S. Holm.  A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[21]  Nicol Korner-Bitensky,et al.  Evaluating Unilateral Spatial Neglect Post Stroke: Working Your Way Through the Maze of Assessment Choices , 2004, Topics in stroke rehabilitation.

[22]  Hermanus J. Hermens,et al.  The recommendations for sensors and sensor placement procedures for surface electromyography , 1999 .

[23]  Janice J Eng,et al.  Paretic Upper-Limb Strength Best Explains Arm Activity in People With Stroke , 2007, Physical Therapy.

[24]  M. Latash.  Control of human movement , 1993 .

[25]  P. Matthews.  The dependence of tension upon extension in the stretch reflex of the soleus muscle of the decerebrate cat , 1959, The Journal of physiology.

[26]  Ping Zhou,et al.  Activation deficit correlates with weakness in chronic stroke: Evidence from evoked and voluntary EMG recordings , 2014, Clinical Neurophysiology.

[27]  G. Kwakkel,et al.  What Is the Evidence for Physical Therapy Poststroke? A Systematic Review and Meta-Analysis , 2014, PloS one.

[28]  David J. Reinkensmeyer,et al.  Hemiparetic stroke impairs anticipatory control of arm movement , 2003, Experimental Brain Research.

[29]  M. Levin,et al.  Regulation of stretch reflex threshold in elbow flexors in children with cerebral palsy: a new measure of spasticity , 2000, Developmental medicine and child neurology.

[30]  Anatol G. Feldman,et al.  Spasticity measurement based on tonic stretch reflex threshold in stroke using a portable device , 2008, Clinical Neurophysiology.

[31]  P. Stratford,et al.  Measuring Physical Impairment and Disability With the Chedoke‐McMaster Stroke Assessment , 1993, Stroke.

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

[33]  R. Teasell,et al.  The Rehabilitation of Patients Recovering from Brainstem Strokes: Case Studies and Clinical Considerations , 2007, Topics in stroke rehabilitation.

[34]  R. Lieber,et al.  Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material , 2003, Muscle & nerve.

[35]  Mindy F. Levin,et al.  Sensorimotor deficits in patients with central nervous system lesions: Explanations based on the λ model of motor control , 2000 .

[36]  Charles Capaday,et al.  The effects of baclofen on the stretch reflex parameters of the cat , 2004, Experimental Brain Research.

[37]  James W. Lance,et al.  The control of muscle tone, reflexes, and movement , 1980, Neurology.

[38]  L. Boyd,et al.  Implicit sequence‐specific motor learning after subcortical stroke is associated with increased prefrontal brain activations: An fMRI Study , 2011, Human brain mapping.

[39]  M. Levin,et al.  Compensatory Versus Noncompensatory Shoulder Movements Used for Reaching in Stroke , 2016, Neurorehabilitation and neural repair.

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

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

[42]  Anatol G. Feldman,et al.  Threshold control of arm posture and movement adaptation to load , 2006, Experimental Brain Research.

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

[44]  Vengateswaran J Ravichandran,et al.  Contributions of altered stretch reflex coordination to arm impairments following stroke. , 2010, Journal of neurophysiology.

[45]  Ethan R. Buch,et al.  Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation , 2009, Proceedings of the National Academy of Sciences.

[46]  Manin H. Konijnenbelt,et al.  Relationship among shoulder proprioception, kinematics, and pain after stroke. , 2009, Archives of physical medicine and rehabilitation.

[47]  P. Fitts.  The information capacity of the human motor system in controlling the amplitude of movement. , 1954, Journal of experimental psychology.

[48]  E. Asmussen,et al.  Body Temperature and Capacity for Work , 1945 .

[49]  Mindy F. Levin,et al.  Are H and stretch reflexes in hemiparesis reproducible and correlated with spasticity? , 1993, Journal of Neurology.

[50]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[51]  C. Winstein,et al.  Neurorehabilitation and Neural Repair Cerebellar Stroke Impairs Temporal but Not Spatial Accuracy during Implicit Motor Learning Neurorehabilitation and Neural Repair Additional Services and Information For , 2022 .

[52]  S. Sahrmann,et al.  The relationship of voluntary movement of spasticity in the upper motor neuron syndrome , 1977, Transactions of the American Neurological Association.

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

[54]  D. Guigou,et al.  [On rehabilitation]. , 1963, Acta pediatrica espanola.

[55]  D Burke,et al.  Spasticity as an adaptation to pyramidal tract injury. , 1988, Advances in neurology.

[56]  I. Hsueh,et al.  Psychometric properties of the sensory scale of the Fugl-Meyer Assessment in stroke patients , 2004, Clinical rehabilitation.

[57]  James Gordon,et al.  Short-Duration and Intensive Training Improves Long-Term Reaching Performance in Individuals With Chronic Stroke , 2016, Neurorehabilitation and neural repair.

[58]  Lara A Boyd,et al.  Preserved motor learning after stroke is related to the degree of proprioceptive deficit , 2009, Behavioral and Brain Functions.

[59]  T Sinkjaer,et al.  Passive, intrinsic and reflex-mediated stiffness in the ankle extensors of hemiparetic patients. , 1994, Brain : a journal of neurology.

[60]  M. Levin,et al.  Deficits in the coordination of agonist and antagonist muscles in stroke patients: implications for normal motor control , 2000, Brain Research.

[61]  Lara A. Boyd,et al.  Learning Implicitly: Effects of Task and Severity After Stroke , 2007, Neurorehabilitation and neural repair.

[62]  A. G. Feldman,et al.  Arm–Trunk Coordination for Beyond-the-Reach Movements in Adults With Stroke , 2014, Neurorehabilitation and neural repair.

[63]  Pierre A. Mathieu,et al.  Relationship between stretch reflex thresholds and voluntary arm muscle activation in patients with spasticity , 2007, Experimental Brain Research.

[64]  M. Levin,et al.  Upper Limb Obstacle Avoidance Behavior in Individuals With Stroke , 2017, Neurorehabilitation and neural repair.

[65]  Anatol G. Feldman,et al.  The role of stretch reflex threshold regulation in normal and impaired motor control , 1994, Brain Research.

[66]  P. Neilson,et al.  Spasticity and muscle contracture following stroke. , 1996, Brain : a journal of neurology.