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Variability, frequency composition, and temporal regularity of submaximal isometric elbow flexion force in subacute stroke

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Abstract

We compared variability, frequency composition, and temporal regularity of submaximal isometric elbow flexion force at 10, 20, 35, and 50 % of peak torque between 34 stroke subjects (5–48 days post-onset, both arms) and 24 age-matched controls (dominant arm), and related the findings in the paretic arm to motor impairment. Force variability was quantified by the coefficient of variation (CV), frequency composition by the median frequency and relative power in 0–3-, 4–6-, and 8–12-Hz bands, and regularity by the sample entropy (SampEn). The paretic elbow flexors showed significantly increased CV and relative power in 0–3-Hz band, decreased power in 4–6- and 8–12-Hz bands, and decreased SampEn compared to both the non-paretic and control elbow flexors (P ≤ 0.0002), with no differences between the latter two (P ≥ 0.012). With increasing contraction intensity, the relative power in different frequency bands was insufficiently modulated and SampEn excessively decreased in the paretic elbow flexors. Also, CV in the paretic elbow flexors was non-linearly related to the relative power in different frequency bands and SampEn across contraction intensities (rectangular hyperbolic fit, 0.21 ≤ R 2 ≤ 0.55, P ≤ 0.006), whereas no force parameter correlated with arm motor impairment. These results largely extend our previous findings in the paretic knee extensors to the elbow flexors in subacute stroke, except that here force variability was increased only in the paretic elbow flexors and modulation of force regularity with increasing contraction intensity showed the opposite, decreasing pattern, which was considerably exaggerated in the paretic muscles.

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References

  • Abbruzzese G, Assini A, Buccolieri A, Schieppati M, Trompetto C (1999) Comparison of intracortical inhibition and facilitation in distal and proximal arm muscles in humans. J Physiol 514:895–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allum JH, Dietz V, Freund HJ (1978) Neuronal mechanisms underlying physiological tremor. J Neurophysiol 41:557–571

    CAS  PubMed  Google Scholar 

  • Arsian OE (2001) Neuroanatomical basis of clinical neurology. CRC Press, New York, p 363

    Book  Google Scholar 

  • Augustine JR (2008) Human neuroantomy. Academic Press, San Diego, p 268

    Google Scholar 

  • Bohannon RW (2009) Body weight-normalized knee extension strength explains sit-to-stand independence: a validation study. J Strength Cond Res 23:309–311

    Article  PubMed  Google Scholar 

  • Bohannon RW, Smith MB (1987a) Assessment of strength deficits in eight paretic upper extremity muscle groups of stroke patients with hemiplegia. Phys Ther 67:522–525

    CAS  PubMed  Google Scholar 

  • Bohannon RW, Smith MB (1987b) Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 67:206–207

    CAS  PubMed  Google Scholar 

  • Boissy P, Bourbonnais D, Carlotti MM, Gravel D, Arsenault BA (1999) Maximal grip force in chronic stroke subjects and its relationship to global upper extremity function. Clin Rehabil 13:354–362

    Article  CAS  PubMed  Google Scholar 

  • Brouwer B, Hopkins-Rosseel DH (1997) Motor cortical mapping of proximal upper extremity muscles following spinal cord injury. Spinal Cord 35:205–212

    Article  CAS  PubMed  Google Scholar 

  • Campanini I, Merlo A, Farina D (2009) Motor unit discharge pattern and conduction velocity in patients with upper motor neuron syndrome. J Electromyogr Kinesiol 19:22–29

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Chin L, Yue P, Feng JJ, Seow CY (2006) Mathematical simulation of muscle cross-bridge cycle and force-velocity relationship. Biophys J 91:3653–3663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chow JW, Stokic DS (2011) Force control of quadriceps muscle is bilaterally impaired in subacute stroke. J Appl Physiol 111:1290–1295

    Article  PubMed  Google Scholar 

  • Chow JW, Stokic DS (2013) Impaired force steadiness is associated with changes in force frequency composition in subacute stroke. Neuroscience 242:69–77

    Article  CAS  PubMed  Google Scholar 

  • Chow JW, Stokic DS (2014) Variability, frequency composition, and complexity of submaximal isometric knee extension force from subacute to chronic stroke. Neuroscience 273:189–198

    Article  CAS  PubMed  Google Scholar 

  • Colebatch JG, Gandevia SC, Spira PJ (1986) Voluntary muscle strength in hemiparesis: distribution of weakness at the elbow. J Neurol Neurosurg Psychiatry 49:1019–1024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalton BH, Jakobi JM, Allman BL, Rice CL (2010) Differential age-related changes in motor unit properties between elbow flexors and extensors. Acta Physiol (Oxf) 200:45–55

    CAS  Google Scholar 

  • De Luca CJ, Hostage EC (2010) Relationship between firing rate and recruitment threshold of motoneurons in voluntary isometric contractions. J Neurophysiol 104:1034–1046

    Article  PubMed  PubMed Central  Google Scholar 

  • De Luca CJ, Kline JC (2012) Influence of proprioceptive feedback on the firing rate and recruitment of motoneurons. J Neural Eng 9:016007

    Article  PubMed  Google Scholar 

  • Deutsch KM, Newell KM (2004) Changes in the structure of children’s isometric force variability with practice. J Exp Child Psychol 88:319–333

    Article  PubMed  Google Scholar 

  • Dewhurst S, Graven-Nielsen T, De Vito G, Farina D (2007) Muscle temperature has a different effect on force fluctuations in young and older women. Clin Neurophysiol 118:762–769

    Article  PubMed  Google Scholar 

  • Edgerton VR, Smith JL, Simpson DR (1975) Muscle fibre type populations of human leg muscles. Histochem J 7:259–266

    Article  CAS  PubMed  Google Scholar 

  • 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 7:13–31

    CAS  PubMed  Google Scholar 

  • Gemperline JJ, Allen S, Walk D, Rymer WZ (1995) Characteristics of motor unit discharge in subjects with hemiparesis. Muscle Nerve 18:1101–1114

    Article  CAS  PubMed  Google Scholar 

  • Gladstone DJ, Danells CJ, Black SE (2002) The fugl-meyer assessment of motor recovery after stroke: a critical review of its measurement properties. Neurorehabil Neural Repair 16:232–240

    Article  PubMed  Google Scholar 

  • Gydikov A, Kosarov D (1974) Some features of different motor units in human biceps brachii. Pflug Arch 347:75–88

    Article  CAS  Google Scholar 

  • Hara Y, Masakado Y, Chino N (2004) The physiological functional loss of single thenar motor units in the stroke patients: when does it occur? Does it progress? Clin Neurophysiol 115:97–103

    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  PubMed Central  Google Scholar 

  • Hurd WJ, Morrey BF, Kaufman KR (2011) The effects of anthropometric scaling parameters on normalized muscle strength in uninjured baseball pitchers. J Sport Rehabil 20:311–320

    Article  PubMed  Google Scholar 

  • Jennekens FG, Tomlinson BE, Walton JN (1971) Data on the distribution of fibre types in five human limb muscles. An autopsy study. J Neurol Sci 14:245–257

    Article  CAS  PubMed  Google Scholar 

  • Jørgensen HS, Nakayama H, Raaschou HO, Vive-Larsen J, Støier M, Olsen TS (1995) Outcome and time course of recovery in stroke. Part II: time course of recovery. The Copenhagen Stroke Study. Arch Phys Med Rehabil 76:406–412

    Article  PubMed  Google Scholar 

  • Kallenberg LA, Hermens HJ (2009) Motor unit properties of biceps brachii in chronic stroke patients assessed with high-density surface EMG. Muscle Nerve 39:177–185

    Article  PubMed  Google Scholar 

  • Khan S, Leung E, Jay WM (2008) Stroke and visual rehabilitation. Top Stroke Rehabil 15:27–36

    Article  PubMed  Google Scholar 

  • Kitago T, Liang J, Huang VS, Hayes S, Simon P, Tenteromano L, Lazar RM, Marshall RS, Mazzoni P, Lennihan L, Krakauer JW (2013) Improvement after constraint-induced movement therapy: recovery of normal motor control or task-specific compensation? Neurorehabil Neural Repair 27:99–109

    Article  PubMed  Google Scholar 

  • Kouzaki M, Shinohara M, Masani K, Fukunaga T (2004) Force fluctuations are modulated by alternate muscle activity of knee extensor synergists during low-level sustained contraction. J Appl Physiol 97:2121–2131

    Article  PubMed  Google Scholar 

  • Kukulka CG, Clamann HP (1981) Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions. Brain Res 219:45–55

    Article  CAS  PubMed  Google Scholar 

  • Lake DE, Richman JS, Griffin MP, Moorman JR (2002) Sample entropy analysis of neonatal heart rate variability. Am J Physiol Regul Integr Comp Physiol 283:R789–R797

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Li X, Wang YC, Suresh NL, Rymer WZ, Zhou P (2011) Motor unit number reductions in paretic muscles of stroke survivors. IEEE Trans Inf Technol Biomed 15:505–512

    Article  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, Misra G, Coombes SA, Christou EA, Cauraugh JH (2013) Increased force variability in chronic stroke: contributions of force modulation below 1 Hz. PLoS One 8:e83468

    Article  PubMed  PubMed Central  Google Scholar 

  • Luft AR, Smith GV, Forrester L, Whitall J, Macko RF, Hauser TK, Goldberg AP, Hanley DF (2002) Comparing brain activation associated with isolated upper and lower limb movement across corresponding joints. Hum Brain Mapp 17:131–140

    Article  PubMed  Google Scholar 

  • Lukacs M, Vecsei L, Beniczky S (2008) Large motor units are selectively affected following a stroke. Clin Neurophysiol 119:2555–2558

    Article  CAS  PubMed  Google Scholar 

  • McIntosh C (2003) Stroke revisited: visual problems following stroke and their effect on rehabilitation. Br Orthopt J 60:10–14

    Google Scholar 

  • Mercier C, Bourbonnais D (2004) Relative shoulder flexor and handgrip strength is related to upper limb function after stroke. Clin Rehabil 18:215–221

    Article  PubMed  Google Scholar 

  • Moritz CT, Barry BK, Pascoe MA, Enoka RM (2005) Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J Neurophysiol 93:2449–2459

    Article  PubMed  Google Scholar 

  • Muceli S, Farina D, Kirkesola G, Katch F, Falla D (2011) Reduced force steadiness in women with neck pain and the effect of short term vibration. J Electromyogr Kinesiol 21:283–290

    Article  PubMed  Google Scholar 

  • Prodoehl J, Vaillancourt DE (2010) Effects of visual gain on force control at the elbow and ankle. Exp Brain Res 200:67–79

    Article  PubMed  Google Scholar 

  • Richman JS, Moorman JR (2000) Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol 278:H2039–H2049

    CAS  PubMed  Google Scholar 

  • Robertson JV, Roche N, Roby-Brami A (2012) Influence of the side of brain damage on postural upper-limb control including the scapula in stroke patients. Exp Brain Res 218:141–155

    Article  PubMed  Google Scholar 

  • Roh J, Rymer WZ, Beer RF (2015) Evidence for altered upper extremity muscle synergies in chronic stroke survivors with mild and moderate impairment. Front Hum Neurosci 9:1–14

    Article  Google Scholar 

  • Roos MR, Rice CL, Connelly DM, Vandervoort AA (1999) Quadriceps muscle strength, contractile properties, and motor unit firing rates in young and old men. Muscle Nerve 22:1094–1103

    Article  CAS  PubMed  Google Scholar 

  • Rowe F, Brand D, Jackson CA, Price A, Walker L, Harrison S, Eccleston C, Scott C, Akerman N, Dodridge C, Howard C, Shipman T, Sperring U, MacDiarmid S, Freeman C (2009) Visual impairment following stroke: do stroke patients require vision assessment? Age Ageing 38:188–193

    Article  PubMed  Google Scholar 

  • Schiffman JM, Luchies CW, Piscitelle L, Hasselquist L, Gregorczyk KN (2006) Discrete bandwidth visual feedback increases structure of output as compared to continuous visual feedback in isometric force control tasks. Clin Biomech 21:1042–1050

    Article  Google Scholar 

  • Seki K, Narusawa M (1996) Firing rate modulation of human motor units in different muscles during isometric contraction with various forces. Brain Res 719:1–7

    Article  CAS  PubMed  Google Scholar 

  • Simmons RW, Nguyen TT, Levy SS, Thomas JD, Mattson SN, Riley EP (2012) Children with heavy prenatal alcohol exposure exhibit deficits when regulating isometric force. Alcohol Clin Exp Res 36:302–309

    Article  CAS  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 

  • Slifkin AB, Newell KM (2000) Variability and noise in continuous force production. J Mot Behav 32:141–150

    Article  CAS  PubMed  Google Scholar 

  • Slifkin AB, Vaillancourt DE, Newell KM (2000) Intermittency in the control of continuous force production. J Neurophysiol 84:1708–1718

    CAS  PubMed  Google Scholar 

  • Sosnoff JJ, Newell KM (2007) Are visual feedback delays responsible for aging-related increases in force variability? Exp Aging Res 33:399–415

    Article  PubMed  Google Scholar 

  • Sosnoff JJ, Deutsch KM, Newell KM (2007) Does muscular weakness account for younger children’s enhanced force variability? Dev Psychobiol 49:399–405

    Article  PubMed  Google Scholar 

  • Stokic DS, McKay WB, Scott L, Sherwood AM, Dimitrijevic MR (1997) Intracortical inhibition of lower limb motor-evoked potentials after paired transcranial magnetic stimulation. Exp Brain Res 117:437–443

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M, Omori Y, Sugimura S, Miyamoto M, Sugimura Y, Kirimoto H, Yamada S (2011) Predicting recovery of bilateral upper extremity muscle strength after stroke. J Rehabil Med 43:935–943

    Article  PubMed  Google Scholar 

  • Taylor AM, Christou EA, Enoka RM (2003) Multiple features of motor-unit activity influence force fluctuations during isometric contractions. J Neurophysiol 90:1350–1361

    Article  PubMed  Google Scholar 

  • Tracy BL, Mehoudar PD, Ortega JD (2007) The amplitude of force variability is correlated in the knee extensor and elbow flexor muscles. Exp Brain Res 76:448–464

    Article  Google Scholar 

  • Vaillancourt DE, Newell KM (2003) Aging and the time and frequency structure of force output variability. J Appl Physiol 94:903–912

    Article  PubMed  Google Scholar 

  • Vaillancourt DE, Slifkin AB, Newell KM (2001a) Visual control of isometric force in Parkinson’s disease. Neuropsychologia 39:1410–1418

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Verheyden G, Nieuwboer A, De Wit L, Thijs V, Dobbelaere J, Devos H, Severijns D, Vanbeveren S, De Weerdt W (2008) Time course of trunk, arm, leg, and functional recovery after ischemic stroke. Neurorehabil Neural Repair 22:173–179

    Article  PubMed  Google Scholar 

  • Watanabe RN, Kohn AF (2015) Fast oscillatory commands from the motor cortex can be decoded by the spinal cord for force control. J Neurosci 35:13687–13697

    Article  CAS  PubMed  Google Scholar 

  • Yan K, Fang J, Shahani BT (1998) Motor unit discharge behaviors in stroke patients. Muscle Nerve 21:1502–1506

    Article  CAS  PubMed  Google Scholar 

  • Ye Y, Ma L, Yan T, Liu H, Wei X, Song R (2014) Kinetic measurements of hand motor impairments after mild to moderate stroke using grip control tasks. J Neuroeng Rehabil 11:84

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the Wilson Research Foundation, Jackson, MS, USA. We are grateful to Robert Hirko, Heather Maloney, Jennifer Sivak, and L. Anthony Smith for their assistance with this study.

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  1. Center for Neuroscience and Neurological Recovery, Methodist Rehabilitation Center, 1350 East Woodrow Wilson Drive, Jackson, MS, 39216, USA

    John W. Chow & Dobrivoje S. Stokic

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Correspondence to John W. Chow.

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Chow, J.W., Stokic, D.S. Variability, frequency composition, and temporal regularity of submaximal isometric elbow flexion force in subacute stroke. Exp Brain Res 234, 3145–3155 (2016). https://doi.org/10.1007/s00221-016-4712-7

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