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01-08-2016 | Research Article

Deficits in motor abilities for multi-finger force control in hemiparetic stroke survivors

Authors: Yushin Kim, Woo-Sub Kim, Kyung Koh, BumChul Yoon, Diane L. Damiano, Jae Kun Shim

Published in: Experimental Brain Research | Issue 8/2016

Abstract

The ability to control redundant motor effectors is one of hallmarks in human motor control, and the topic has been studied extensively over several decades since the initial inquiries proposed by Nicholi Bernstein. However, our understanding of the influence of stroke on the control of redundant motor systems is very limited. This study aimed to investigate the effect of stroke-related constraints on multi-finger force control abilities in a visuomotor task. Impaired (IH) and less-impaired hands (LH) of 19 hemiparetic stroke survivors and 19 age-matched control subjects were examined. Each hand repeatedly produced isometric forces to match a target force of 5 N shown on a computer screen using all four fingers. The hierarchical variability decomposition (HVD) model was used to separate force-matching errors (motor performance) into task-relevant measures (accuracy, steadiness, and reproducibility). Task-irrelevant sources of variability in individual finger force profiles within and between trials (flexibility and multiformity) were also quantified. The IH in the stroke survivors showed deficits in motor performance attributed mainly to lower accuracy and reproducibility as compared to control hands (p < 0.05). The LH in stroke survivors showed lower reproducibility and both hands in stroke also had higher multiformity than the control hands (p < 0.05). The findings from our HVD model suggest that accuracy, reproducibility, and multiformity were mainly impaired during force-matching task in the stroke survivors. The specific motor deficits identified through the HVD model with the new conceptual framework may be considered as critical factors for scientific investigation on stroke and evidence-based rehabilitation of this population.

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Ada L, Canning CG, Low SL (2003) Stroke patients have selective muscle weakness in shortened range. Brain 126:724–731. doi:10.1093/brain/awg06 CrossRefPubMed

Ansari NN, Naghdi S, Arab TK, Jalaie S (2008) The interrater and intrarater reliability of the Modified Ashworth Scale in the assessment of muscle spasticity: limb and muscle group effect. NeuroRehabilitation 23:231–237PubMed

Bagce HF, Saleh S, Adamovich SV, Tunik E (2012) Visuomotor gain distortion alters online motor performance and enhances primary motor cortex excitability in patients with stroke. Neuromodulation 15:361–366. doi:10.1111/j.1525-1403.2012.00467.x CrossRefPubMedPubMedCentral

Bohannon RW (2007) Muscle strength and muscle training after stroke. J Rehabil Med 39:14–20. doi:10.2340/16501977-0018 CrossRefPubMed

Broeks JG, Lankhorst GJ, Rumping K, Prevo AJ (1999) The long-term outcome of arm function after stroke: results of a follow-up study. Disabil Rehabil 21:357–364CrossRefPubMed

Butler AJ, Kahn S, Wolf SL, Weiss P (2005) Finger extensor variability in TMS parameters among chronic stroke patients. J Neuroeng Rehabil 2:10. doi:10.1186/1743-0003-2-10 CrossRefPubMedPubMedCentral

Carey JR, Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey L, Rundquist P, Ugurbil K (2002) Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125:773–788CrossRefPubMed

Chang SH, Francisco GE, Zhou P, Rymer WZ, Li S (2013) Spasticity, weakness, force variability, and sustained spontaneous motor unit discharges of resting spastic–paretic biceps brachii muscles in chronic stroke. Muscle Nerve 48:85–92. doi:10.1002/mus.23699 CrossRefPubMedPubMedCentral

Duncan PW, Lai SM, Keighley J (2000) Defining post-stroke recovery: implications for design and interpretation of drug trials. Neuropharmacology 39:835–841CrossRefPubMed

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 12:189–198CrossRefPubMed

Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S (1975) The post-stroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 7:13–31PubMed

Holmstrom L, de Manzano O, Vollmer B, Forsman L, Valero-Cuevas FJ, Ullen F, Forssberg H (2011) Dissociation of brain areas associated with force production and stabilization during manipulation of unstable objects. Exp Brain Res 215:359–367. doi:10.1007/s00221-011-2903-9 CrossRefPubMedPubMedCentral

Kang N, Cauraugh JH (2014) Bimanual force variability and chronic stroke: asymmetrical hand control. PLoS One 9:e101817. doi:10.1371/journal.pone.0101817 CrossRefPubMedPubMedCentral

Kantak SS, Mummidisetty CK, Stinear JW (2012) Primary motor and premotor cortex in implicit sequence learning-evidence for competition between implicit and explicit human motor memory systems. Eur J Neurosci 36:2710–2715. doi:10.1111/j.1460-9568.2012.08175.x CrossRefPubMed

Karol S, Kim YS, Huang J, Kim YH, Koh K, Yoon BC, Shim JK (2011) Multi-finger pressing synergies change with the level of extra degrees of freedom. Exp Brain Res 208:359–367. doi:10.1007/s00221-010-2486-x CrossRefPubMed

Kim Y, Kim WS, Yoon B (2014) The effect of stroke on motor selectivity for force control in single- and multi-finger force production tasks. NeuroRehabilitation 34:429–435. doi:10.3233/Nre-141050 PubMed

Kim Y, Kim WS, Shim JK, Suh DW, Kim T, Yoon B (2015) Difference of motor overflow depending on the impaired or unimpaired hand in stroke patients. Hum Mov Sci 39:154–162. doi:10.1016/j.humov.2014.11.007 CrossRefPubMed

Koh K, Kwon HJ, Yoon BC et al (2015) The role of tactile sensation in online and offline hierarchical control of multi-finger force synergy. Exp Brain Res 233:2539–2548. doi:10.1007/s00221-015-4325-6 CrossRefPubMed

Kurillo G, Zupan A, Bajd T (2004) Force tracking system for the assessment of grip force control in patients with neuromuscular diseases. Clin Biomech 19:1014–1021. doi:10.1016/j.clinbiomech.2004.07.003 CrossRef

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

Latash ML (2012) The bliss (not the problem) of motor abundance (not redundancy). Exp Brain Res 217:1–5. doi:10.1007/s00221-012-3000-4 CrossRefPubMedPubMedCentral

Latash ML, Shim JK, Shinohara M, Zatsiorsky VM (2006) Changes in finger coordination and hand function with advanced age. In: Latash ML, Lestienne F (eds) Motor control and learning. Springer, New York, NY, pp 141–159CrossRef

Latash ML, Levin MF, Scholz JP, Schoner G (2010) Motor control theories and their applications. Med Lith 46:382–392

Li S, Latash ML, Yue GH, Siemionow V, Sahgal V (2003) The effects of stroke and age on finger interaction in multi-finger force production tasks. Clin Neurophysiol 114:1646–1655. doi:10.1016/S1388-2457(03)00164-0 CrossRefPubMed

Lindberg PG, Roche N, Robertson J, Roby-Brami A, Bussel B, Maier MA (2012) Affected and unaffected quantitative aspects of grip force control in hemiparetic patients after stroke. Brain Res 1452:96–107. doi:10.1016/j.brainres.2012.03.007 CrossRefPubMed

Lodha N, Naik SK, Coombes SA, Cauraugh JH (2010) Force control and degree of motor impairments in chronic stroke. Clin Neurophysiol 121:1952–1961. doi:10.1016/j.clinph.2010.04.005 CrossRefPubMed

Lodha N, Coombes SA, Cauraugh JH (2012) Bimanual isometric force control: asymmetry and coordination evidence post stroke. Clin Neurophysiol 123:787–795. doi:10.1016/j.clinph.2011.08.014 CrossRefPubMed

Louis ED, Gillman A, Boschung S, Hess CW, Yu Q, Pullman SL (2012) High width variability during spiral drawing: further evidence of cerebellar dysfunction in essential tremor. Cerebellum 11:872–879. doi:10.1007/s12311-011-0352-4 CrossRefPubMed

Lukacs M (2005) Electrophysiological signs of changes in motor units after ischaemic stroke. Clin Neurophysiol 116:1566–1570. doi:10.1016/j.clinph.2005.04.005 CrossRefPubMed

Massy-Westropp NM, Gill TK, Taylor AW, Bohannon RW, Hill CL (2011) Hand Grip Strength: age and gender stratified normative data in a population-based study. BMC Res Notes 4:127. doi:10.1186/1756-0500-4-127 CrossRefPubMedPubMedCentral

Mathiowetz V, Volland G, Kashman N, Weber K (1985) Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther 39:386–391CrossRefPubMed

Matsuoka Y, Brewer BR, Klatzky RL (2007) Using visual feedback distortion to alter coordinated pinching patterns for robotic rehabilitation. J Neuroeng Rehabil 4:17. doi:10.1186/1743-0003-4-17 CrossRefPubMedPubMedCentral

Miller LC, Dewald JP (2012) Involuntary paretic wrist/finger flexion forces and EMG increase with shoulder abduction load in individuals with chronic stroke. Clin Neurophysiol 123:1216–1225. doi:10.1016/j.clinph.2012.01.009 CrossRefPubMedPubMedCentral

Naik SK, Patten C, Lodha N, Coombes SA, Cauraugh JH (2011) Force control deficits in chronic stroke: grip formation and release phases. Exp Brain Res 211:1–15. doi:10.1007/s00221-011-2637-8 CrossRefPubMed

Newell KM, Carlton LG (1988) Force variability in isometric responses. J Exp Psychol Hum Percept Perform 14:37–44CrossRefPubMed

Oliveira MA, Rodrigues AM, Caballero RM, Petersen RD, Shim JK (2008) Strength and isometric torque control in individuals with Parkinson’s disease. Exp Brain Res 184:445–450. doi:10.1007/s00221-007-1212-9 CrossRefPubMed

Platz T, Pinkowski C, van Wijck F, Kim IH, di Bella P, Johnson G (2005) Reliability and validity of arm function assessment with standardized guidelines for the Fugl-Meyer Test, Action Research Arm Test and Box and Block Test: a multicentre study. Clin Rehabil 19:404–411CrossRefPubMed

Raghavan P (2007) The nature of hand motor impairment after stroke and its treatment. Curr Treat Options Cardiovasc Med 9:221–228CrossRefPubMed

Reisman DS, Scholz JP (2003) Aspects of joint coordination are preserved during pointing in persons with post-stroke hemiparesis. Brain 126:2510–2527. doi:10.1093/brain/awg246 CrossRefPubMed

Reisman DS, Scholz JP (2006) Workspace location influences joint coordination during reaching in post-stroke hemiparesis. Exp Brain Res 170:265–276. doi:10.1007/s00221-005-0209-5 CrossRefPubMed

Scholz JP, Schoner G (1999) The uncontrolled manifold concept: identifying control variables for a functional task. Exp Brain Res 126:289–306CrossRefPubMed

Scholz JP, Reisman D, Schoner G (2001) Effects of varying task constraints on solutions to joint coordination in a sit-to-stand task. Exp Brain Res 141:485–500. doi:10.1007/s002210100878 CrossRefPubMed

Scholz JP, Danion F, Latash ML, Schoner G (2002) Understanding finger coordination through analysis of the structure of force variability. Biol Cybern 86:29–39. doi:10.1007/s004220100279 CrossRefPubMed

Shim JK, Latash ML, Zatsiorsky VM (2003) The human central nervous system needs time to organize task-specific covariation of finger forces. Neurosci Lett 353:72–74. doi:10.1016/j.neulet.2003.08.079 CrossRefPubMed

Shim JK, Lay BS, Zatsiorsky VM, Latash ML (2004) Age-related changes in finger coordination in static prehension tasks. J Appl Physiol 97:213–224. doi:10.1152/japplphysiol.00045.2004 CrossRefPubMedPubMedCentral

Shim JK, Olafsdottir H, Zatsiorsky VM, Latash ML (2005) The emergence and disappearance of multi-digit synergies during force-production tasks. Exp Brain Res 164:260–270. doi:10.1007/s00221-005-2248-3 CrossRefPubMedPubMedCentral

Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5:1226–1235. doi:10.1038/nn963 CrossRefPubMed

Vaillancourt DE, Thulborn KR, Corcos DM (2003) Neural basis for the processes that underlie visually guided and internally guided force control in humans. J Neurophysiol 90:3330–3340. doi:10.1152/jn.00394.2003 CrossRefPubMed

Vaillancourt DE, Mayka MA, Corcos DM (2006) Intermittent visuomotor processing in the human cerebellum, parietal cortex, and premotor cortex. J Neurophysiol 95:922–931. doi:10.1152/jn.00718.2005 CrossRefPubMed

Verrel J (2010) Distributional properties and variance-stabilizing transformations for measures of uncontrolled manifold effects. J Neurosci Methods 191:166–170. doi:10.1016/j.jneumeth.2010.06.016 CrossRefPubMed

Williams LS, Weinberger M, Harris LE, Clark DO, Biller J (1999) Development of a stroke-specific quality of life scale. Stroke 30:1362–1369CrossRefPubMed

Title: Deficits in motor abilities for multi-finger force control in hemiparetic stroke survivors
Authors: Yushin Kim
Woo-Sub Kim
Kyung Koh
BumChul Yoon
Diane L. Damiano
Jae Kun Shim
Publication date: 01-08-2016
Publisher: Springer Berlin Heidelberg
Published in: Experimental Brain Research / Issue 8/2016
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-016-4644-2

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Deficits in motor abilities for multi-finger force control in hemiparetic stroke survivors

Abstract

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Abstract

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