Non‐paretic leg movements can facilitate cortical drive to the paretic leg in individuals post stroke with severe motor impairment: Implications for motor priming

Cross‐education, a phenomenon where unilateral strength (or skill) training enhances strength (or skill) in the contralateral untrained limb, has been well studied in able‐bodied individuals. Cross‐education effect accompanies bilateral changes of corticomotor activity in the motor cortex (M1). Recent reports demonstrated greater cross‐education effect in stroke survivors compared to healthy individuals, however, corticomotor responses to cross‐education in stroke remains unclear. This study aimed to determine the effects of non‐paretic leg movements on corticomotor excitability (CME) and reaction time of the paretic leg in severely impaired stroke survivors. Seventeen post stroke individuals with severe leg motor impairment (Fugl‐Meyer lower extremity score less than 21 and absence of motor evoked potential in the paretic leg) performed three 20‐min motor trainings using their non‐paretic ankle: skill (targeted dynamic movements), strength (isometric resistance) and sham (sub‐threshold electrical nerve stimulation). During training, verbal instructions were given to the participants to limit their movement to the non‐paretic leg and this was confirmed with visual observation of the paretic leg. Transcranial magnetic stimulation measured CME of the contralateral pathways from the non‐lesioned M1 to the non‐paretic tibialis anterior (TA) muscle, ipsilateral pathways to the paretic TA and transcallosal inhibition (TCI) from the non‐lesioned to lesioned M1. Paretic ankle reaction time was measured using a reaction time paradigm. All outcomes were measured before, immediately post, 30‐min post and 60‐min post priming. CME of the non‐paretic TA increased after skill (.08 ± .10 mV) and strength (.06 ± .05 mV) training (p < .01). Ipsilateral CME of the paretic TA (.02 ± .01 mV) and TCI (.01 ± .01 s, ipsilateral silent period; more inhibition to the lesioned M1) increased after skill (p < .05) but not strength training. Reaction time of the paretic ankle improved after skill and strength training (−.11 ± .2 and −.13 ± .20 s, respectively; p < .05) and was sustained at 60 min. No changes were observed during the sham condition. Our findings may inform future studies for using non‐paretic leg movements as a priming modality, especially for those who are contraindicated to other priming paradigms (e.g., brain stimulation) or unable to perform paretic leg movements. Conclusion: Non‐paretic leg movements can be used as a priming modality, especially for those who are contraindicated to other priming paradigms (e.g., brain stimulation) or unable to perform paretic leg movements.

[1]  S. Madhavan,et al.  Effects of Cross-Education on Neural Adaptations Following Non-Paretic Limb Training in Stroke: A Scoping Review with Implications for Neurorehabilitation , 2022, Journal of motor behavior.

[2]  A. Gharabaghi,et al.  Ipsilateral corticospinal maps correspond to severe poststroke motor impairment , 2022, Brain Stimulation.

[3]  S. Jaberzadeh,et al.  Comparison of transcallosal inhibition between hemispheres and its relationship with motor behavior in patients with severe upper extremity impairment after subacute stroke. , 2022, Journal of stroke and cerebrovascular diseases : the official journal of National Stroke Association.

[4]  S. Madhavan,et al.  Feasibility and Acceptability of Game-Based Cortical Priming and Functional Lower Limb Training in a Remotely Supervised Home Setting for Chronic Stroke: A Case Series , 2022, Frontiers in Rehabilitation Sciences.

[5]  S. Madhavan,et al.  Reliability of transcallosal inhibition measurements for the lower limb motor cortex in stroke , 2020, Neuroscience Letters.

[6]  S. Rossi,et al.  Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert Guidelines , 2020, Clinical Neurophysiology.

[7]  D. Corcos,et al.  Cortical priming strategies for gait training after stroke: a controlled, stratified trial , 2020, Journal of NeuroEngineering and Rehabilitation.

[8]  B. Hordacre,et al.  Implication of the ipsilateral motor network in unilateral voluntary muscle contraction: the cross-activation phenomenon. , 2020, Journal of neurophysiology.

[9]  S. Madhavan,et al.  Differential corticomotor mechanisms of ankle motor control in post stroke individuals with and without motor evoked potentials , 2020, Brain Research.

[10]  Dai Zhang,et al.  Effects of high-frequency repetitive transcranial magnetic stimulation over the contralesional motor cortex on motor recovery in severe hemiplegic stroke: A randomized clinical trial , 2020, Brain Stimulation.

[11]  P. Battista,et al.  Sex Differences in Long-Term Mortality and Functional Outcome After Rehabilitation in Patients With Severe Stroke , 2020, Frontiers in Neurology.

[12]  Francesca N. Delling,et al.  Heart Disease and Stroke Statistics—2020 Update: A Report From the American Heart Association , 2020, Circulation.

[13]  Balamurugan Janakiraman,et al.  Effectiveness of treadmill assisted gait training in stroke survivors: A systematic review and meta-analysis , 2019, Global Epidemiology.

[14]  S. Ng,et al.  Cutoff Score of the Lower-Extremity Motor Subscale of Fugl-Meyer Assessment in Chronic Stroke Survivors: A Cross-Sectional Study. , 2019, Archives of physical medicine and rehabilitation.

[15]  C. Blake,et al.  Unilateral Strength Training and Mirror Therapy in Patients With Chronic Stroke , 2019, American journal of physical medicine & rehabilitation.

[16]  E. Christou,et al.  Motor planning perturbation: muscle activation and reaction time. , 2018, Journal of neurophysiology.

[17]  Lara A. Green,et al.  The effect of unilateral training on contralateral limb strength in young, older, and patient populations: a meta-analysis of cross education , 2018, Physical Therapy Reviews.

[18]  E. Zehr,et al.  Unilateral wrist extension training after stroke improves strength and neural plasticity in both arms , 2018, Experimental Brain Research.

[19]  Timo Rantalainen,et al.  The ipsilateral corticospinal responses to cross-education are dependent upon the motor-training intervention , 2018, Experimental Brain Research.

[20]  W. Byblow,et al.  Revisiting interhemispheric imbalance in chronic stroke: A tDCS study , 2018, Clinical Neurophysiology.

[21]  L. Boyd,et al.  Interhemispheric Pathways Are Important for Motor Outcome in Individuals with Chronic and Severe Upper Limb Impairment Post Stroke , 2017, Neural plasticity.

[22]  T. Rantalainen,et al.  The corticospinal responses of metronome-paced, but not self-paced strength training are similar to motor skill training , 2017, European Journal of Applied Physiology.

[23]  Z. Dvir,et al.  Cross-education of muscular strength following unilateral resistance training: a meta-analysis , 2017, European Journal of Applied Physiology.

[24]  J. Mehrholz,et al.  Treadmill training and body weight support for walking after stroke. , 2017, The Cochrane database of systematic reviews.

[25]  F. Dierick,et al.  Hemorrhagic versus ischemic stroke: Who can best benefit from blended conventional physiotherapy with robotic-assisted gait therapy? , 2017, PloS one.

[26]  M. Stoykov,et al.  Movement-Based Priming: Clinical Applications and Neural Mechanisms , 2017, Journal of motor behavior.

[27]  B. Hordacre,et al.  Minimum number of trials required for within- and between-session reliability of TMS measures of corticospinal excitability , 2016, Neuroscience.

[28]  A. Dromerick,et al.  Role of contralesional hemisphere in paretic arm reaching in patients with severe arm paresis due to stroke: A preliminary report , 2016, Neuroscience Letters.

[29]  S. Madhavan,et al.  Effects of anodal tDCS of the lower limb M1 on ankle reaction time in young adults , 2016, Experimental Brain Research.

[30]  S. Madhavan,et al.  Effects of anodal tDCS of the lower limb M1 on ankle reaction time in young adults , 2015, Experimental Brain Research.

[31]  T. Rantalainen,et al.  Motor cortex excitability is not differentially modulated following skill and strength training , 2015, Neuroscience.

[32]  R. Perna,et al.  Rehabilitation Outcomes: Ischemic versus Hemorrhagic Strokes , 2015, Behavioural neurology.

[33]  F. Ehsani,et al.  The comparison of cross–education effect in young and elderly females from unilateral training of the elbow flexors , 2014, Medical journal of the Islamic Republic of Iran.

[34]  C. Lindsell,et al.  Randomized controlled trial , 2016 .

[35]  W. Byblow,et al.  Bilateral Priming Accelerates Recovery of Upper Limb Function After Stroke: A Randomized Controlled Trial , 2014, Stroke.

[36]  Richard G. Carson,et al.  Neural pathways mediating cross education of motor function , 2013, Front. Hum. Neurosci..

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

[38]  A. Pearce,et al.  Corticomotor plasticity following unilateral strength training , 2012, Muscle & nerve.

[39]  R. Seidler,et al.  Task-dependent effects of interhemispheric inhibition on motor control , 2012, Behavioural Brain Research.

[40]  Mark Hallett,et al.  Interhemispheric plasticity in humans. , 2011, Medicine and science in sports and exercise.

[41]  V. Santilli,et al.  Reliability of TMS-related measures of tibialis anterior muscle in patients with chronic stroke and healthy subjects , 2011, Journal of the Neurological Sciences.

[42]  M. Stokes,et al.  Strength training of one limb increases corticomotor excitability projecting to the contralateral homologous limb. , 2011, Motor control.

[43]  J. Stinear,et al.  A paradox: after stroke, the non‐lesioned lower limb motor cortex may be maladaptive , 2010, The European journal of neuroscience.

[44]  Gereon R. Fink,et al.  Interhemispheric Competition After Stroke: Brain Stimulation to Enhance Recovery of Function of the Affected Hand , 2009, Neurorehabilitation and neural repair.

[45]  Leonardo G. Cohen,et al.  Mechanisms Underlying Functional Changes in the Primary Motor Cortex Ipsilateral to an Active Hand , 2008, The Journal of Neuroscience.

[46]  W. Byblow,et al.  Priming the motor system enhances the effects of upper limb therapy in chronic stroke. , 2008, Brain : a journal of neurology.

[47]  J. Kleim,et al.  Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. , 2006, Journal of applied physiology.

[48]  N. Fong,et al.  Total direct cost, length of hospital stay, institutional discharges and their determinants from rehabilitation settings in stroke patients , 2006, Acta neurologica Scandinavica.

[49]  A. Pollock,et al.  Treadmill training and body weight support for walking after stroke. , 2005, The Cochrane database of systematic reviews.

[50]  Pamela W Duncan,et al.  Sex Differences in Stroke Recovery , 2005, Preventing chronic disease.

[51]  Stephan Riek,et al.  The sites of neural adaptation induced by resistance training in humans , 2002, The Journal of physiology.

[52]  P Bawa,et al.  Responses of ankle extensor and flexor motoneurons to transcranial magnetic stimulation. , 2002, Journal of neurophysiology.

[53]  Jing Z. Liu,et al.  Relationship between muscle output and functional MRI-measured brain activation , 2001, Experimental Brain Research.

[54]  J. Nielsen,et al.  Transcranial magnetic stimulation and stretch reflexes in the tibialis anterior muscle during human walking , 2001, The Journal of physiology.

[55]  Sandra M. Woolley,et al.  Characteristics of Gait in Hemiplegia , 2001, Topics in stroke rehabilitation.

[56]  G. Murray,et al.  Medical complications after stroke: a multicenter study. , 2000, Stroke.

[57]  Babak Boroojerdi,et al.  Transcallosal inhibition in cortical and subcortical cerebral vascular lesions , 1996, Journal of the Neurological Sciences.

[58]  B. Meyer,et al.  Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. , 1995, Brain : a journal of neurology.

[59]  M. Cornwall,et al.  The Influence of Tibialis Anterior Muscle Activity on Rearfoot Motion during Walking , 1994, Foot & ankle international.

[60]  T. Komiyama,et al.  EMG-Reaction Time of the Biceps Brachii in Bilateral Simultaneous Motions , 1986, Perceptual and motor skills.

[61]  J. Avela,et al.  Ipsilateral corticomotor responses are confined to the homologous muscle following cross-education of muscular strength. , 2018, Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme.

[62]  T. Olsen,et al.  Recovery of walking function in stroke patients: the Copenhagen Stroke Study. , 1995, Archives of physical medicine and rehabilitation.

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