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The modulation of force steadiness by electrical nerve stimulation applied to the wrist extensors differs for young and older adults

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Abstract

Purpose

We compared the modulation of force steadiness by different types of electrical nerve stimulation in young (n = 13, 25 ± 4 years) and older (n = 12, 78 ± 5 years) adults.

Methods

The protocol involved four types of isometric contractions with the wrist-extensor muscles at 10% of the maximal force. Three of the contractions involved electrical nerve stimulation that comprised two forms of neuromuscular electrical stimulation (NMES) to evoke muscle contractions and a voluntary contraction with superimposed transcutaneous electrical nerve stimulation (TENS) at an intensity less than motor threshold.

Results

The coefficient of variation (CV) for force during voluntary wrist extension was less (P = 0.03) for young (1.82 ± 0.43%) than older adults (2.80 ± 1.08%). The CV for force did not differ between age groups during the three types of electrical nerve stimulation but was reduced relative to the value observed during voluntary wrist extension for older adults. In contrast, the CV for force increased during the voluntary contraction with superimposed TENS for young adults but not for older adults. Moreover, there were significant negative correlations in older adults between the CV for force during the voluntary contraction and its decrease with electrical nerve stimulation.

Conclusion

Differences in the CV for force between the evoked and voluntary contractions for the two age groups suggest that the variance in common synaptic input to motor neurons during steady voluntary contractions with the wrist extensors is greater for older adults than young adults.

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Abbreviations

ANOVA:

Analysis of variance

CV:

Coefficient of variation

MVC:

Maximal voluntary contraction

NMES:

Neuromuscular electrical stimulation

TENS:

Transcutaneous electrical nerve stimulation

References

  • Adams GR, Harris RT, Woodard D, Dudley GA (1993) Mapping of electrical muscle stimulation using MRI. J Appl Physiol 74:532–537

    Article  CAS  PubMed  Google Scholar 

  • Arpin DJ, Davies BL, Kurz MJ (2016) Multiple sclerosis influences the precision of the ankle plantarflexion muscular force production. Gait Posture 45:170–174

    Article  PubMed  Google Scholar 

  • Baldwin ERL, Klakowicz PM, Collins DF (2006) Wide-pulse width, high-frequency neuromuscular electrical stimulation: implications for functional electrical stimulation. J Appl Physiol 101:228–240

    Article  PubMed  Google Scholar 

  • Baudry S (2016) Aging changes the contribution of spinal and corticospinal pathways to control balance. Exerc Sport Sci Rev 44:104–109

    Article  PubMed  Google Scholar 

  • Baweja HS, Kennedy DM, Vu J, Vaillancourt DE, Christou EA (2010) Greater amount of visual feedback decreases force variability by reducing force oscillations from 0 to 1 and 3–7 Hz. Eur J Appl Physiol 108:935–943

    Article  PubMed  Google Scholar 

  • Baweja HS, Kwon M, Christou EA (2012) Magnified visual feedback exacerbates positional variability in older adults due to altered modulation of the primary agonist muscle. Exp Brain Res 222:355–364

    Article  PubMed  PubMed Central  Google Scholar 

  • Bergquist AJ, Clair JM, Lagerquist O, Mang CS, Okuma Y, Collins DF (2011) Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol 111:2409–2226

    Article  CAS  PubMed  Google Scholar 

  • Bilodeau M, Keen DA, Sweeney PJ, Shields RW, Enoka RM (2000) Strength training can improve steadiness in persons with essential tremor. Muscle Nerve 23:771–778

    Article  CAS  PubMed  Google Scholar 

  • Buckmire AJ, Lockwood DR, Doane CJ, Fuglevand AJ (2018) Distributed stimulation increases force elicited with functional electrical stimulation. J Neural Eng 15:026001

    Article  PubMed  PubMed Central  Google Scholar 

  • Carville SF, Perry MC, Rutherford OM, Smith IC, Newham DJ (2006) Steadiness of quadriceps contractions in young and older adults with and without a history of falling. Eur J Appl Physiol 100:527–533

    Article  PubMed  Google Scholar 

  • Chipchase LS, Schabrun SM, Hodges PW (2011) Corticospinal excitability is dependent on the parameters of peripheral electric stimulation: a preliminary study. Arch Phys Med Rehabil 92:1423–1430

    Article  PubMed  Google Scholar 

  • Clair-Auger JM, Collins DF, Dewald JPA (2012) The effects of wide pulse neuromuscular electrical stimulation on elbow flexion torque in individuals with chronic hemiparetic stroke. Clin Neurophysiol 123:2247–2255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins DF, Burke D, Gandevia SC (2002) Sustained contractions produced by plateau-like behaviour in human motoneurones. J Physiol 538:289–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Nunzio AM, Yavuz US, Martinez-Valdes E, Farina D. Falla D (2018) Electro-tactile stimulation of the posterior neck induces body anteropulsion during upright stance. Exp Brain Res 236:1471–1478

    Article  PubMed  PubMed Central  Google Scholar 

  • Dean JC, Yates LM, Collins DF (2007) Turning on the central contribution to contractions evoked by neuromuscular electrical stimulation. J Appl Physiol 103:170–176

    Article  CAS  PubMed  Google Scholar 

  • Farina D, Negro F (2015) Common synaptic input to motor neurons, motor unit synchronization, and force control. Exerc Sport Sci Rev 43:23–33

    Article  PubMed  Google Scholar 

  • Farina D, Negro F, Muceli S, Enoka RM (2016) Principles of motor unit physiology evolve with advances in technology. Physiology 31:83–94

    Article  PubMed  Google Scholar 

  • Feeney DF, Meyer FG, Noone N, Enoka RM (2017) A latent low-dimensional common input drives a pool of motor neurons: a probabilistic latent state-space model. J Neurophysiol 118:2238–2250

    Article  PubMed  PubMed Central  Google Scholar 

  • Feeney DF, Mani D, Enoka RM (2018) Variability in common synaptic input to motor neurons modulates both force steadiness and pegboard time in young and older adults. J Physiol 596:3793–3806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galganski ME, Fuglevand AJ, Enoka RM (1993) Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. J Neurophysiol 69:2108–2115

    Article  CAS  PubMed  Google Scholar 

  • Gomes-Osman J, Tibbett JA, Poe BP, Field-Fote EC (2017) Priming for improved hand strength in persons with chronic tetraplegia: a comparison of priming-augmented functional task practice, priming alone, and conventional exercise training. Front Neurol 242:1–13

    Google Scholar 

  • Gueugneau N, Grosprêtre S, Stapley P, Lepers R (2017) High-frequency neuromuscular electrical stimulation modulates interhemispheric inhibition in healthy humans. J Neurophysiol 117:467–475

    Article  PubMed  Google Scholar 

  • Hultman E, Sjöholm H, Jäderholm-Ek I, Krynicki J (1983) Evaluation of methods for electrical stimulation of human skeletal muscle in situ. Pflügers Archiv 398:139–141

    Article  CAS  PubMed  Google Scholar 

  • Hyngstrom AS, Kuhnen HR, Kirking KM, Hunter SK (2014) Functional implications of impaired control of submaximal hip flexion following stroke. Muscle Nerve 49:225–232

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones KE, Hamilton AF, Wolpert DM (2002) Sources of signal-dependent noise during isometric force production. J Neurophysiol 88:1533–1544

    Article  PubMed  Google Scholar 

  • Kobayashi H, Koyama Y, Enoka RM, Suzuki S (2014) A unique form of light-load training improves steadiness and performance on some functional tasks in older adults. Scand J Med Sci Sports 24:98–110

    Article  CAS  PubMed  Google Scholar 

  • Kouzaki M, Kimura T, Yoshitake Y, Hayashi T, Moritani T (2012) Subthreshold electrical stimulation reduces motor unit discharge variability and decreases the force fluctuations of plantar flexion. Neurosci Lett 513:146–150

    Article  CAS  PubMed  Google Scholar 

  • Lagerquist O, Collins DF (2010) Influence of stimulus pulse width on M-waves, H-reflexes, and torque during tetanic low-intensity neuromuscular stimulation. Muscle Nerve 42:886–893

    Article  PubMed  Google Scholar 

  • Lagerquist O, Walsh LD, Blouin JS, Collins DF, Gandevia SC (2009) Effect of a peripheral nerve block on torque produced by repetitive electrical stimulation. J Appl Physiol 107:161–167

    Article  PubMed  Google Scholar 

  • Laidlaw DH, Kornatz KW, Keen DA, Suzuki S, Enoka RM (1999) Strength training improves the steadiness of slow lengthening contractions performed by old adults. J Appl Physiol 87:1786–1795

    Article  CAS  PubMed  Google Scholar 

  • Laidlaw DH, Bilodeau M, Enoka RM (2000) Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve 23:600–612

    Article  CAS  PubMed  Google Scholar 

  • Lodha N, Christou EA (2017) Low-frequency oscillations and control of motor output. Front Physiol 8:1–9

    Article  Google Scholar 

  • Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110:223–234

    Article  PubMed  Google Scholar 

  • Magladery JW, McDougal DB Jr (1950) Electrophysiological studies of nerve and reflex activity in normal man. I. Identification of certain reflexes in the electromyogram and the conduction velocity of peripheral nerve fibers. Bull Johns Hopkins Hosp 86:265–290

    CAS  PubMed  Google Scholar 

  • Moon H, Kim C, Kwon M, Chen YT, Onushko T, Lodha N, Christou EA (2014) Force control is related to low-frequency oscillations in force and surface EMG. PLoS One 9:e109202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran F, Leonard T, Hawthrone S, Hughes CM, McCrum-Gardner E, Johnson MI, Rakel BA, Sluka KA, Walsh DM (2011) Hypoalgesia in response to transcutaneous electrical nerve stimulation (TENS) depends on stimulation intensity. J Pain 12:929–935

    Article  PubMed  Google Scholar 

  • Negro F, Holobar A, Farina D (2009) Fluctuations in isometric muscle force can be described by one linear projection of low-frequency components of motor unit discharge rates. J Physiol 587:5925–5938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Negro F, Yavuz US, Farina (2016) The human motor neuron pools receive a dominant slow-varying common synaptic input. J Physiol 594:5491–5505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okuma Y, Bergquist AJ, Hong M, Chan KM, Collins DF (2013) Electrical stimulation site influences the spatial distribution of motor units recruited in tibialis anterior. Clin Neurophysiol 124:2257–2263

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Pantaleao MA, Laurino MF, Gallego NL, Cabral CM, Rakel B, Vance C, Sluka KA, Walsh DM, Liebano RE (2011) Adjusting pulse amplitude during transcutaneous electrical nerve stimulation (TENS) application produces greater hypoalgesia. J Pain 12:581–590

    Article  PubMed  Google Scholar 

  • Park SH, Casamento-Moran A, Yacoubi B, Christou EA (2017a) Voluntary reduction of force variability via modulation of low-frequency oscillations. Exp Brain Res 235:2717–2727

    Article  PubMed  Google Scholar 

  • Park SH, Kwon M, Christou EA (2017b) Motor output oscillations with magnification of visual feedback in older adults. Neurosci Lett 24:647–648

    Google Scholar 

  • Proske U, Gandevia SC (2012) The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force. Physiol Rev 92:1651–1697

    Article  CAS  PubMed  Google Scholar 

  • Puksa L, Stålberg E, Falck B (2003) Reference values of F wave parameters in healthy subjects. Clin Neurophysiol 114:1079–1090

    Article  PubMed  Google Scholar 

  • Radhakrishnan R, Sluka KA (2005) Deep tissue afferents, but not cutaneous afferents, mediate transcutaneous electrical nerve stimulation-induced antihyperalgesia. J Pain 6:673–680

    Article  PubMed  Google Scholar 

  • Salonikidis K, Amiridis IG, Oxyzoglou N, de Villareal ES, Zafeiridis A, Kellis E (2009) Force variability during isometric wrist flexion in highly skilled and sedentary individuals. Eur J Appl Physiol 107:715–722

    Article  PubMed  PubMed Central  Google Scholar 

  • Schieppati M (1987) The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28:345–376

    Article  CAS  PubMed  Google Scholar 

  • Schmidt MW, Hinder MR, Summers JJ, Garry MI (2011) Long-lasting contralateral motor cortex excitability is increased by unilateral hand movement that triggers electrical stimulation of opposite homologous muscles. Neurorehabilit Neural Repair 25:521–530

    Article  Google Scholar 

  • Sluka KA, Walsh D (2003) Transcutaneous electrical nerve stimulation: basic science mechanisms and clinical effectiveness. J Pain 4:109–121

    Article  PubMed  Google Scholar 

  • Thompson CK, Lewek MD, Jayaraman A, Hornby TG (2011) Central excitability contributes to supramaximal volitional contractions in human incomplete spinal cord injury. J Physiol 589:3739–3752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson CK, Negro F, Johnson MD, Holmes MR, McPherson LM, Powers RK, Farina D, Heckman CJ (2018) Robust and accurate decoding of motoneuron behavior and prediction of the resulting force output. J Physiol 596:2643–2659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tracy BL, Enoka RM (2002) Older adults are less steady during submaximal isometric contractions with the knee extensor muscles. J Appl Physiol 92:1004–1012

    Article  PubMed  Google Scholar 

  • Vanderthommen M, Duchateau J (2007) Electrical stimulation as a modality to improve performance of the neuromuscular system. Exerc Sport Sci Rev 35:180–185

    Article  PubMed  Google Scholar 

  • Veldman MP, Gondin J, Place N, Maffiuletti N (2016) Effects of neuromuscular electrical stimulation training on endurance performance. Front Physiol 7:1–5

    Article  Google Scholar 

  • Walker ER, Hyngstrom AS, Schmit BD (2014) Sensory electrical stimulation improves foot placement during targeted stepping post-stroke. Exp Brain Res 232:1137–1143

    Article  PubMed  PubMed Central  Google Scholar 

  • Wegrzyk J, Fouré A, Vilmen C, Ghattas B, Maffiuletti NA, Mattei JP, Place N, Bendahan D, Gondin J (2015) Extra forces induced by wide-pulse, high-frequency electrical stimulation: occurrence, magnitude, variability and underlying mechanisms. Clin Neurophysiol 126:1400–1412

    Article  PubMed  Google Scholar 

  • Yu D, Yin H, Han T, Jiang H, Cao X (2016) Intramuscular innervations of lower leg skeletal muscles: applications in their clinical use in functional muscular transfer. Surg Radiol Anat 38:675–685

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank Melissa Mazzo and Ryan Price for drawing Fig. 1, and Professors Evangelos Christou and Allison Hyngstrom for providing comments on a draft of the manuscript.

Funding

This work was supported by the Rocky Mountain American College of Sports Medicine Research Grant awarded to Diba Mani and the American Society of Biomechanics Graduate Student Grant-In-Aid awarded to Daniel Feeney.

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Correspondence to Diba Mani.

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The authors have declared that no financial conflict of interests exists.

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Communicated by Nicolas Place.

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Mani, D., Feeney, D.F. & Enoka, R.M. The modulation of force steadiness by electrical nerve stimulation applied to the wrist extensors differs for young and older adults. Eur J Appl Physiol 119, 301–310 (2019). https://doi.org/10.1007/s00421-018-4025-6

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