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Force control improvements in chronic stroke: bimanual coordination and motor synergy evidence after coupled bimanual movement training

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Abstract

Bimanual movement disorders are common dysfunctions post stroke. This stroke study investigated bimanual force control capabilities to determine the effect of coupled bimanual movement training on bimanual coordination and motor synergy. Stroke participants (N = 11) completed three bimanual force control tasks at 5, 25, and 50 % of maximum voluntary contraction before and after coupled bimanual movement training. Root mean square error (RMSE), approximate entropy, correlation, and bimanual motor synergy were analyzed in two-way completely within-subjects ANOVAs (Test Session × Force Level: 2 × 3). Multiple linear regression analysis determined the relationship between RMSE and other force control measures. The analyses revealed three important findings: (1) RMSE decreased from baseline to posttest (2) negative correlation (e.g., error compensation) and bimanual motor synergy increased at 25 and 50 % after rehabilitation, and (3) increased bimanual motor synergy was strongly associated with decreased RMSE after training. The findings indicate that coupled bimanual movement training improved force control performance, bimanual coordination, and motor synergies. Indeed, the present findings extend bimanual motor synergies as a meaningful indicator for estimating task performance improvements. Finally, bimanual force control is a valid outcome measure in quantifying progress toward motor recovery post stroke.

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Abbreviations

UCM:

Uncontrolled manifold

MVC:

Maximal voluntary contraction

RMSE:

Root mean square error

ApEn:

Approximate entropy

References

  • Bertrand AM, Mercier C, Shun PL, Bourbonnais D, Desrosiers J (2004) Effects of weakness on symmetrical bilateral grip force exertion in subjects with hemiparesis. J Neurophysiol 91:1579–1585

    Article  PubMed  Google Scholar 

  • Calautti C, Naccarato M, Jones PS, Sharma N, Day DD, Carpenter AT, Bullmore ET, Warburton EA, Baron JC (2007) The relationship between motor deficit and hemisphere activation balance after stroke: a 3T fMRI study. Neuroimage 34:322–331

    Article  PubMed  Google Scholar 

  • Carson RG (2005) Neural pathways mediating bilateral interactions between the upper limbs. Brain Res Rev 49:641–662

    Article  CAS  PubMed  Google Scholar 

  • Cauraugh JH (2004) Coupled rehabilitation protocols and neural plasticity: upper extremity improvements in chronic hemiparesis. Restor Neurol Neurosci 22:337–347

    PubMed  Google Scholar 

  • Cauraugh JH, Kim S (2002) Two coupled motor recovery protocols are better than one: electromyogram-triggered neuromuscular stimulation and bilateral movements. Stroke 33:1589–1594

    Article  PubMed  Google Scholar 

  • Cauraugh JH, Summers JJ (2005) Neural plasticity and bilateral movements: a rehabilitation approach for chronic stroke. Prog Neurobiol 75:309–320

    Article  PubMed  Google Scholar 

  • Cauraugh JH, Coombes SA, Lodha N, Naik SK, Summers JJ (2009) Upper extremity improvements in chronic stroke: coupled bilateral load training. Restor Neurol Neurosci 27:17–25

    PubMed Central  PubMed  Google Scholar 

  • Cauraugh JH, Lodha N, Naik SK, Summers JJ (2010) Bilateral movement training and stroke motor recovery progress: a structured review and meta-analysis. Hum Mov Sci 29:853–870

    Article  PubMed Central  PubMed  Google Scholar 

  • Cauraugh JH, Naik SK, Lodha N, Coombes SA, Summers JJ (2011) Long-term rehabilitation for chronic stroke arm movements: a randomized controlled trial. Clin Rehabil 25:1086–1096

    Article  PubMed  Google Scholar 

  • Davis NJ (2007) Memory and coordination in bimanual isometric finger force production. Exp Brain Res 182:137–142

    Article  PubMed  Google Scholar 

  • Diedrichsen J, Hazeltine E, Nurss WK, Ivry RB (2003) The role of the corpus callosum in the coupling of bimanual isometric force pulses. J Neurophysiol 90:2409–2418

    Article  PubMed  Google Scholar 

  • Doucet BM, Lam A, Griffin L (2012) Neuromuscular electrical stimulation for skeletal muscle function. Yale J Biol Med 85:201–215

    PubMed Central  PubMed  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  • Harris-Love ML, McCombe Waller S, Whitall J (2005) Exploiting interlimb coupling to improve paretic arm reaching performance in people with chronic stroke. Arch Phys Med Rehabil 86:2131–2137

    Article  PubMed  Google Scholar 

  • Heffernan KS, Sosnoff JJ, Ofori E, Jae SY, Baynard T, Collier SR, Goulopoulou S, Figueroa A, Woods JA, Pitetti KH, Fernhall B (2009) Complexity of force output during static exercise in individuals with down syndrome. J Appl Physiol 106:1227–1233

    Article  PubMed  Google Scholar 

  • Hidaka Y, Han CE, Wolf SL, Winstein CJ, Schweighofer N (2012) Use it and improve it or lose it: interactions between arm function and use in humans post-stroke. PLoS Comput Biol 8:e1002343

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu X, Newell KM (2011a) Adaptation to bimanual asymmetric weights in isometric force coordination. Neurosci Lett 490:121–125

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Newell KM (2011b) Modeling constraints to redundancy in bimanual force coordination. J Neurophysiol 105:2169–2180

    Article  PubMed  Google Scholar 

  • Hu X, Loncharich M, Newell KM (2011) Visual information interacts with neuromuscular factors in the coordination of bimanual isometric force. Exp Brain Res 209:129–138

    Article  PubMed  Google Scholar 

  • Jorgensen L, Jacobsen BK (2001) Changes in muscle mass, fat mass, and bone mineral content in the legs after stroke: a 1 year prospective study. Bone 28:655–659

    Article  CAS  PubMed  Google Scholar 

  • Kilbreath SL, Crosbie J, Canning CG, Lee MJ (2006) Inter-limb coordination in bimanual reach-to-grasp following stroke. Disabil Rehabil 28:1435–1443

    Article  CAS  PubMed  Google Scholar 

  • Landau WM, Sahrmann SA (2002) Preservation of directly stimulated muscle strength in hemiplegia due to stroke. Arch Neurol 59:1453–1457

    PubMed  Google Scholar 

  • Latash ML (2008) Synergy. Oxford University Press, New York

    Book  Google Scholar 

  • Latash ML (2010a) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322

    Google Scholar 

  • Latash ML (2010b) Stages in learning motor synergies: a view based on the equilibrium-point hypothesis. Hum Mov Sci 29:642–654

    Article  PubMed Central  PubMed  Google Scholar 

  • Latash ML (2012) The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res 217:1–5

    Article  PubMed Central  PubMed  Google Scholar 

  • Latash ML, Anson JG (2006) Synergies in health and disease: relations to adaptive changes in motor coordination. Phys Ther 86:1151–1160

    PubMed  Google Scholar 

  • Lodha N, Naik SK, Coombes SA, Cauraugh JH (2010) Force control and degree of motor impairments in chronic stroke. Clin Neurophysiol 121:1952–1961

    Article  PubMed  Google Scholar 

  • Lodha N, Coombes SA, Cauraugh JH (2012) Bimanual isometric force control: asymmetry and coordination evidence post stroke. Clin Neurophysiol 123:787–795

    Article  PubMed  Google Scholar 

  • Lukacs M (2005) Electrophysiological signs of changes in motor units after ischaemic stroke. Clin Neurophysiol 116:1566–1570

    Article  PubMed  Google Scholar 

  • Marshall MM, Armstrong TJ (2004) Observational assessment of forceful exertion and the perceived force demands of daily activities. J Occup Rehabil 14:281–294

    Article  PubMed  Google Scholar 

  • Montgomery DC, Peck EA (1982) Introduction to linear regression analysis. Wiley, New York

    Google Scholar 

  • Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409

    Article  PubMed  Google Scholar 

  • Nowak DA (2008) The impact of stroke on the performance of grasping: usefulness of kinetic and kinematic motion analysis. Neurosci Biobehav Rev 32:1439–1450

    Article  PubMed  Google Scholar 

  • Pincus SM (1991) Approximate entropy as a measure of system complexity. Proc Natl Acad Sci USA 88:2297–2301

    Article  CAS  PubMed  Google Scholar 

  • Pincus SM, Goldberger AL (1994) Physiological time-series analysis: what does regularity quantify? Am J Physiol 266:H1643–H1656

    CAS  PubMed  Google Scholar 

  • Ranganathan R, Newell KM (2008) Motor synergies: feedback and error compensation within and between trials. Exp Brain Res 186:561–570

    Article  PubMed  Google Scholar 

  • Sarabon N, Markovic G, Mikulic P, Latash ML (2013) Bilateral synergies in foot force production tasks. Exp Brain Res 227:121–130

    Article  PubMed  Google Scholar 

  • Scholz JP, Kang N, Patterson D, Latash ML (2003) Uncontrolled manifold analysis of single trials during multi-finger force production by persons with and without down syndrome. Exp Brain Res 153:45–58

    Article  PubMed  Google Scholar 

  • Slifkin AB, Newell KM (1999) Noise, information transmission, and force variability. J Exp Psychol Hum Percept Perform 25:837–851

    Article  CAS  PubMed  Google Scholar 

  • Stinear JW, Byblow WD (2004) Rhythmic bilateral movement training modulates corticomotor excitability and enhances upper limb motricity post stroke: a pilot study. J Clin Neurophysiol 21:124–131

    Article  PubMed  Google Scholar 

  • Stinear CM, Barber PA, Coxon JP, Fleming MK, Byblow WD (2008) Priming the motor system enhances the effects of upper limb therapy in chronic stroke. Brain 131:1381–1390

    Article  PubMed  Google Scholar 

  • Torre K, Hammami N, Metrot J, van Dokkum L, Coroian F, Mottet D, Amri M, Laffont I (2013) Somatosensory-related limitations for bimanual coordination after stroke. Neurorehabil Neural Repair 27:507–515

    Article  PubMed  Google Scholar 

  • Vaillancourt DE, Slifkin AB, Newell KM (2001) Regularity of force tremor in Parkinson’s disease. Clin Neurophysiol 112:1594–1603

    Article  CAS  PubMed  Google Scholar 

  • Wu YH, Pazin N, Zatsiorsky VM, Latash ML (2013) Improving finger coordination in young and elderly persons. Exp Brain Res 226:273–283

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

Funding from the American Heart Association is gratefully acknowledged in supporting this research with a Grant to JHC (#00093013). The authors thank the reviewers for their valuable suggestions on an earlier version of this manuscript.

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Correspondence to James H. Cauraugh.

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Kang, N., Cauraugh, J.H. Force control improvements in chronic stroke: bimanual coordination and motor synergy evidence after coupled bimanual movement training. Exp Brain Res 232, 503–513 (2014). https://doi.org/10.1007/s00221-013-3758-z

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  • DOI: https://doi.org/10.1007/s00221-013-3758-z

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