Skip to main content
Top
Published in: Experimental Brain Research 2/2014

01-02-2014 | Research Article

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

Authors: Nyeonju Kang, James H. Cauraugh

Published in: Experimental Brain Research | Issue 2/2014

Login to get access

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.
Literature
go back to reference 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 91:1579–1585PubMedCrossRef 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 91:1579–1585PubMedCrossRef
go back to reference 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 34:322–331PubMedCrossRef 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 34:322–331PubMedCrossRef
go back to reference Carson RG (2005) Neural pathways mediating bilateral interactions between the upper limbs. Brain Res Rev 49:641–662PubMedCrossRef Carson RG (2005) Neural pathways mediating bilateral interactions between the upper limbs. Brain Res Rev 49:641–662PubMedCrossRef
go back to reference Cauraugh JH (2004) Coupled rehabilitation protocols and neural plasticity: upper extremity improvements in chronic hemiparesis. Restor Neurol Neurosci 22:337–347PubMed Cauraugh JH (2004) Coupled rehabilitation protocols and neural plasticity: upper extremity improvements in chronic hemiparesis. Restor Neurol Neurosci 22:337–347PubMed
go back to reference Cauraugh JH, Kim S (2002) Two coupled motor recovery protocols are better than one: electromyogram-triggered neuromuscular stimulation and bilateral movements. Stroke 33:1589–1594PubMedCrossRef Cauraugh JH, Kim S (2002) Two coupled motor recovery protocols are better than one: electromyogram-triggered neuromuscular stimulation and bilateral movements. Stroke 33:1589–1594PubMedCrossRef
go back to reference Cauraugh JH, Summers JJ (2005) Neural plasticity and bilateral movements: a rehabilitation approach for chronic stroke. Prog Neurobiol 75:309–320PubMedCrossRef Cauraugh JH, Summers JJ (2005) Neural plasticity and bilateral movements: a rehabilitation approach for chronic stroke. Prog Neurobiol 75:309–320PubMedCrossRef
go back to reference Cauraugh JH, Coombes SA, Lodha N, Naik SK, Summers JJ (2009) Upper extremity improvements in chronic stroke: coupled bilateral load training. Restor Neurol Neurosci 27:17–25PubMedCentralPubMed Cauraugh JH, Coombes SA, Lodha N, Naik SK, Summers JJ (2009) Upper extremity improvements in chronic stroke: coupled bilateral load training. Restor Neurol Neurosci 27:17–25PubMedCentralPubMed
go back to reference 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 29:853–870PubMedCentralPubMedCrossRef 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 29:853–870PubMedCentralPubMedCrossRef
go back to reference 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 25:1086–1096PubMedCrossRef 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 25:1086–1096PubMedCrossRef
go back to reference Davis NJ (2007) Memory and coordination in bimanual isometric finger force production. Exp Brain Res 182:137–142PubMedCrossRef Davis NJ (2007) Memory and coordination in bimanual isometric finger force production. Exp Brain Res 182:137–142PubMedCrossRef
go back to reference 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 90:2409–2418PubMedCrossRef 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 90:2409–2418PubMedCrossRef
go back to reference Doucet BM, Lam A, Griffin L (2012) Neuromuscular electrical stimulation for skeletal muscle function. Yale J Biol Med 85:201–215PubMedCentralPubMed Doucet BM, Lam A, Griffin L (2012) Neuromuscular electrical stimulation for skeletal muscle function. Yale J Biol Med 85:201–215PubMedCentralPubMed
go back to reference 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 12:189–198PubMedCrossRef 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 12:189–198PubMedCrossRef
go back to reference 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 86:2131–2137PubMedCrossRef 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 86:2131–2137PubMedCrossRef
go back to reference 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 106:1227–1233PubMedCrossRef 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 106:1227–1233PubMedCrossRef
go back to reference 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:e1002343PubMedCentralPubMedCrossRef 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:e1002343PubMedCentralPubMedCrossRef
go back to reference Hu X, Newell KM (2011a) Adaptation to bimanual asymmetric weights in isometric force coordination. Neurosci Lett 490:121–125PubMedCrossRef Hu X, Newell KM (2011a) Adaptation to bimanual asymmetric weights in isometric force coordination. Neurosci Lett 490:121–125PubMedCrossRef
go back to reference Hu X, Newell KM (2011b) Modeling constraints to redundancy in bimanual force coordination. J Neurophysiol 105:2169–2180PubMedCrossRef Hu X, Newell KM (2011b) Modeling constraints to redundancy in bimanual force coordination. J Neurophysiol 105:2169–2180PubMedCrossRef
go back to reference Hu X, Loncharich M, Newell KM (2011) Visual information interacts with neuromuscular factors in the coordination of bimanual isometric force. Exp Brain Res 209:129–138PubMedCrossRef Hu X, Loncharich M, Newell KM (2011) Visual information interacts with neuromuscular factors in the coordination of bimanual isometric force. Exp Brain Res 209:129–138PubMedCrossRef
go back to reference 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 28:655–659PubMedCrossRef 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 28:655–659PubMedCrossRef
go back to reference Kilbreath SL, Crosbie J, Canning CG, Lee MJ (2006) Inter-limb coordination in bimanual reach-to-grasp following stroke. Disabil Rehabil 28:1435–1443PubMedCrossRef Kilbreath SL, Crosbie J, Canning CG, Lee MJ (2006) Inter-limb coordination in bimanual reach-to-grasp following stroke. Disabil Rehabil 28:1435–1443PubMedCrossRef
go back to reference Landau WM, Sahrmann SA (2002) Preservation of directly stimulated muscle strength in hemiplegia due to stroke. Arch Neurol 59:1453–1457PubMed Landau WM, Sahrmann SA (2002) Preservation of directly stimulated muscle strength in hemiplegia due to stroke. Arch Neurol 59:1453–1457PubMed
go back to reference Latash ML (2010a) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322 Latash ML (2010a) Motor synergies and the equilibrium-point hypothesis. Mot Control 14:294–322
go back to reference Latash ML, Anson JG (2006) Synergies in health and disease: relations to adaptive changes in motor coordination. Phys Ther 86:1151–1160PubMed Latash ML, Anson JG (2006) Synergies in health and disease: relations to adaptive changes in motor coordination. Phys Ther 86:1151–1160PubMed
go back to reference Lodha N, Naik SK, Coombes SA, Cauraugh JH (2010) Force control and degree of motor impairments in chronic stroke. Clin Neurophysiol 121:1952–1961PubMedCrossRef Lodha N, Naik SK, Coombes SA, Cauraugh JH (2010) Force control and degree of motor impairments in chronic stroke. Clin Neurophysiol 121:1952–1961PubMedCrossRef
go back to reference Lodha N, Coombes SA, Cauraugh JH (2012) Bimanual isometric force control: asymmetry and coordination evidence post stroke. Clin Neurophysiol 123:787–795PubMedCrossRef Lodha N, Coombes SA, Cauraugh JH (2012) Bimanual isometric force control: asymmetry and coordination evidence post stroke. Clin Neurophysiol 123:787–795PubMedCrossRef
go back to reference Lukacs M (2005) Electrophysiological signs of changes in motor units after ischaemic stroke. Clin Neurophysiol 116:1566–1570PubMedCrossRef Lukacs M (2005) Electrophysiological signs of changes in motor units after ischaemic stroke. Clin Neurophysiol 116:1566–1570PubMedCrossRef
go back to reference Marshall MM, Armstrong TJ (2004) Observational assessment of forceful exertion and the perceived force demands of daily activities. J Occup Rehabil 14:281–294PubMedCrossRef Marshall MM, Armstrong TJ (2004) Observational assessment of forceful exertion and the perceived force demands of daily activities. J Occup Rehabil 14:281–294PubMedCrossRef
go back to reference Montgomery DC, Peck EA (1982) Introduction to linear regression analysis. Wiley, New York Montgomery DC, Peck EA (1982) Introduction to linear regression analysis. Wiley, New York
go back to reference Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409PubMedCrossRef Murase N, Duque J, Mazzocchio R, Cohen LG (2004) Influence of interhemispheric interactions on motor function in chronic stroke. Ann Neurol 55:400–409PubMedCrossRef
go back to reference Nowak DA (2008) The impact of stroke on the performance of grasping: usefulness of kinetic and kinematic motion analysis. Neurosci Biobehav Rev 32:1439–1450PubMedCrossRef Nowak DA (2008) The impact of stroke on the performance of grasping: usefulness of kinetic and kinematic motion analysis. Neurosci Biobehav Rev 32:1439–1450PubMedCrossRef
go back to reference Pincus SM (1991) Approximate entropy as a measure of system complexity. Proc Natl Acad Sci USA 88:2297–2301PubMedCrossRef Pincus SM (1991) Approximate entropy as a measure of system complexity. Proc Natl Acad Sci USA 88:2297–2301PubMedCrossRef
go back to reference Pincus SM, Goldberger AL (1994) Physiological time-series analysis: what does regularity quantify? Am J Physiol 266:H1643–H1656PubMed Pincus SM, Goldberger AL (1994) Physiological time-series analysis: what does regularity quantify? Am J Physiol 266:H1643–H1656PubMed
go back to reference Ranganathan R, Newell KM (2008) Motor synergies: feedback and error compensation within and between trials. Exp Brain Res 186:561–570PubMedCrossRef Ranganathan R, Newell KM (2008) Motor synergies: feedback and error compensation within and between trials. Exp Brain Res 186:561–570PubMedCrossRef
go back to reference Sarabon N, Markovic G, Mikulic P, Latash ML (2013) Bilateral synergies in foot force production tasks. Exp Brain Res 227:121–130PubMedCrossRef Sarabon N, Markovic G, Mikulic P, Latash ML (2013) Bilateral synergies in foot force production tasks. Exp Brain Res 227:121–130PubMedCrossRef
go back to reference 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 153:45–58PubMedCrossRef 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 153:45–58PubMedCrossRef
go back to reference Slifkin AB, Newell KM (1999) Noise, information transmission, and force variability. J Exp Psychol Hum Percept Perform 25:837–851PubMedCrossRef Slifkin AB, Newell KM (1999) Noise, information transmission, and force variability. J Exp Psychol Hum Percept Perform 25:837–851PubMedCrossRef
go back to reference 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 21:124–131PubMedCrossRef 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 21:124–131PubMedCrossRef
go back to reference 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 131:1381–1390PubMedCrossRef 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 131:1381–1390PubMedCrossRef
go back to reference 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 27:507–515PubMedCrossRef 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 27:507–515PubMedCrossRef
go back to reference Vaillancourt DE, Slifkin AB, Newell KM (2001) Regularity of force tremor in Parkinson’s disease. Clin Neurophysiol 112:1594–1603PubMedCrossRef Vaillancourt DE, Slifkin AB, Newell KM (2001) Regularity of force tremor in Parkinson’s disease. Clin Neurophysiol 112:1594–1603PubMedCrossRef
go back to reference Wu YH, Pazin N, Zatsiorsky VM, Latash ML (2013) Improving finger coordination in young and elderly persons. Exp Brain Res 226:273–283PubMedCrossRef Wu YH, Pazin N, Zatsiorsky VM, Latash ML (2013) Improving finger coordination in young and elderly persons. Exp Brain Res 226:273–283PubMedCrossRef
Metadata
Title
Force control improvements in chronic stroke: bimanual coordination and motor synergy evidence after coupled bimanual movement training
Authors
Nyeonju Kang
James H. Cauraugh
Publication date
01-02-2014
Publisher
Springer Berlin Heidelberg
Published in
Experimental Brain Research / Issue 2/2014
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-013-3758-z

Other articles of this Issue 2/2014

Experimental Brain Research 2/2014 Go to the issue