Top

European Journal of Applied Physiology

Published in:

01-01-2017 | Original Article

Changes in the electromechanical delay components during a fatiguing stimulation in human skeletal muscle: an EMG, MMG and force combined approach

Authors: Emiliano Cè, Susanna Rampichini, Elena Monti, Massimo Venturelli, Eloisa Limonta, Fabio Esposito

Published in: European Journal of Applied Physiology | Issue 1/2017

Abstract

Purpose

Peripheral fatigue involves electrochemical and mechanical mechanisms. An electromyographic, mechanomyographic and force combined approach may permit a kinetic evaluation of the changes at the synaptic, skeletal muscle fiber, and muscle–tendon unit level during a fatiguing stimulation.

Methods

Surface electromyogram, mechanomyogram, force and stimulation current were detected from the gastrocnemius medialis muscle in twenty male participants during a fatiguing stimulation (twelve blocks of 35 Hz stimulations, duty cycle 9 s on/1 s off, duration 120 s). The total electromechanical delay and its three components (between stimulation current and electromyogram, synaptic component; between electromyogram and mechanomyogram signal onset, muscle fiber electrochemical component, and between mechanomyogram and force signal onset, mechanical component) were calculated. Interday reliability and sensitivity were determined.

Results

After fatigue, peak force decreased by 48% (P < 0.05) and the total electromechanical delay and its synaptic, electrochemical and mechanical components lengthened from 25.8 ± 0.9, 1.47 ± 0.04, 11.2 ± 0.6, and 13.1 ± 1.3 ms to 29.0 ± 1.6, 1.56 ± 0.05, 12.4 ± 0.9, and 17.2 ± 0.6 ms, respectively (P < 0.05). During fatigue, the total electromechanical delay and the mechanical component increased significantly after the 40th second, and then remained stable. The synaptic and electrochemical components lengthened significantly after the 20th and 30th second, respectively. Interday reliability was high to very high, with an adequate level of sensitivity.

Conclusions

The kinetic evaluation of the delays during the fatiguing stimulation highlighted different onsets and kinetics, with the events at synaptic level being the first to reveal a significant elongation, followed by those at the intra-fiber level. The mechanical events, which were the most affected by fatigue, were the last to lengthen.

Allen DG, Westerblad H, Lee JA, Lannergren J (1992) Role of excitation-contraction coupling in muscle fatigue. Sports Med 13(2):116–126CrossRefPubMed

Amann M, Venturelli M, Ives SJ, McDaniel J, Layec G, Rossman MJ (1985) Richardson RS (2013) Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output. J Appl Physiol 115(3):355–364CrossRef

Amann M, Sidhu SK, Weavil JC, Mangum TS, Venturelli M (2015) Autonomic responses to exercise: group III/IV muscle afferents and fatigue. Auton Neurosci 188:19–23CrossRefPubMed

Ament W, Verkerke GJ (2009) Exercise and fatigue. Sports Med 39(5):389–422CrossRefPubMed

Barry DT (1992) Vibrations and sounds from evoked muscle twitches. Electromyogr Clin Neurophysiol 32(1–2):35–40PubMed

Beck TW, Housh TJ, Cramer JT, Weir JP, Johnson G, Coburn JW, Malek MH, Mielke M (2005) Mechanomyographic amplitude and frequency responses during dynamic muscle actions: a comprehensive review. Biomed Eng Online 4:67CrossRefPubMedPubMedCentral

Bigland-Ritchie B, Woods JJ (1984) Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7(9):691–699CrossRefPubMed

Botter A, Lanfranco F, Merletti R, Minetto MA (2009) Myoelectric fatigue profiles of three knee extensor muscles. Int J Sports Med 30(6):408–417CrossRefPubMed

Cavanagh PR, Komi PV (1979) Electromechanical delay in human skeletal muscle under concentric and eccentric contractions. Eur J Appl Physiol Occup Physiol 42(3):159–163CrossRefPubMed

Cè E, Rampichini S, Agnello L, Limonta E, Veicsteinas A, Esposito F (2013) Effects of temperature and fatigue on the electromechanical delay components. Muscle Nerve 47(4):566–576CrossRefPubMed

Cè E, Rampichini S, Limonta E, Esposito F (2014a) Fatigue effects on the electromechanical delay components during the relaxation phase after isometric contraction. Acta Physiol 11(1):82–96CrossRef

Cè E, Rampichini S, Venturelli M, Limonta E, Veicsteinas A, Esposito F (2014b) Electromechanical delay components during relaxation after voluntary contraction: reliability and effects of fatigue. Muscle Nerve 51(6):907–915CrossRef

Cè E, Rampichini S, Esposito F (2015) Novel insights into skeletal muscle function by mechanomyography: from the laboratory to the field. Sport Sci Health 11:1–28CrossRef

Clausen TO, Overgaard K, Nielsen OB (2004) Evidence that the Na⁺–K⁺ leak/pump ratio contributes to the difference in endurance between fast- and slow-twitch muscles. Acta Physiol Scand 180(2):209–216CrossRefPubMed

de Ruiter CJ, Jones DA, Sargeant AJ, de Haan A (1999) Temperature effect on the rates of isometric force development and relaxation in the fresh and fatigued human adductor pollicis muscle. Exp Physiol 84(6):1137–1150CrossRefPubMed

Debold EP (2012) Recent insights into the molecular basis of muscular fatigue. Med Sci Sports Exerc 44(8):1440–1452CrossRefPubMed

Donoghue D, Stokes EK (2009) How much change is true change? The minimum detectable change of the Berg Balance Scale in elderly people. J Rehab Med 41(5):343–346CrossRef

Edwards JN, Cully TR, Shannon TR, Stephenson DG, Launikonis BS (2012) Longitudinal and transversal propagation of excitation along the tubular system of rat fast-twitch muscle fibers studied by high speed confocal microscopy. J Physiol 590(Pt 3):475–492CrossRefPubMed

Esposito F, Orizio C, Veicsteinas A (1998) Electromyogram and mechanomyogram changes in fresh and fatigued muscle during sustained contraction in men. Eur J Appl Physiol Occup Physiol 78(6):494–501CrossRefPubMed

Esposito F, Ce E, Gobbo M, Veicsteinas A, Orizio C (2005) Surface EMG and mechanomyogram disclose isokinetic training effects on quadriceps muscle in elderly people. Eur J Appl Physiol 94(5–6):549–557CrossRefPubMed

Esposito F, Ce E, Rampichini S, Veicsteinas A (2009) Acute passive stretching in a previously fatigued muscle: electrical and mechanical response during tetanic stimulation. J Sports Sci 27(12):1347–1357CrossRefPubMed

Esposito F, Limonta E, Ce E (2011) Passive stretching effects on electromechanical delay and time course of recovery in human skeletal muscle: new insights from an electromyographic and mechanomyographic combined approach. Eur J Appl Physiol 111(3):485–495CrossRefPubMed

Esposito F, Cè E, Rampichini S, Limonta E, Venturelli M, Monti E, Bet L, Fossati B, Meola G (2016) Electromechanical delay components during skeletal muscle contraction and relaxation in patients with myotonic dystrophy type 1. Neuromuscul Disord 26(1):60–72CrossRefPubMed

Fitts RH (2008) The cross-bridge cycle and skeletal muscle fatigue. J Appl Physiol 104(2):551–558CrossRefPubMed

Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81(4):1725–1789PubMed

Gobbo M, Gaffurini P, Bissolotti L, Esposito F, Orizio C (2011) Transcutaneous neuromuscular electrical stimulation: influence of electrode positioning and stimulus amplitude settings on muscle response. Eur J Appl Physiol 111(10):2451–2459CrossRefPubMed

Hermens H, Freiks B, Merletti R, Stegeman D, Blok J, Rau G, Disselhorst-Klug C, Hagg G (1999) Eurpoean recommendations for surface electromyography. RRD, The Netherlands

Hug F, Gallot T, Catheline S, Nordez A (2011) Electromechanical delay in biceps brachii assessed by ultrafast ultrasonography. Muscle Nerve 43(3):441–443CrossRefPubMed

Jaskolski A, Andrzejewska R, Marusiak J, Kisiel-Sajewicz K, Jaskolska A (2007) Similar response of agonist and antagonist muscles after eccentric exercise revealed by electromyography and mechanomyography. J Electromyogr Kinesiol 17(5):568–577CrossRefPubMed

Juel C (1988) Muscle action-potential propagation velocity changes during activity. Muscle Nerve 11(7):714–719CrossRefPubMed

Lacourpaille L, Hug F, Nordez A (2013a) Influence of passive muscle tension on electromechanical delay in humans. PLoS One 8(1):e53159CrossRefPubMedPubMedCentral

Lacourpaille L, Nordez A, Hug F (2013b) Influence of stimulus intensity on electromechanical delay and its mechanisms. J Electromyogr Kinesiol 23(1):51–55CrossRefPubMed

Lacourpaille L, Hug F, Guevel A, Pereon Y, Magot A, Hogrel JY, Nordez A (2014) New insights on contraction efficiency in patients with Duchenne muscular dystrophy. J Appl Physiol 117(6):658–662CrossRefPubMedPubMedCentral

Lamb GD (2002) Excitation-contraction coupling and fatigue mechanisms in skeletal muscle: studies with mechanically skinned fibers. J Muscle Res Cell Motil 23(1):81–91CrossRefPubMed

Merton PA, Pampiglione G (1950) Strength and fatigue. Nature 166(4221):527CrossRefPubMed

Muraoka T, Muramatsu T, Fukunaga T, Kanehisa H (2004) Influence of tendon slack on electromechanical delay in the human medial gastrocnemius in vivo. J Appl Physiol 96(2):540–544CrossRefPubMed

Nordez A, Cathelin S, Hug F (2009a) A novel method for measuring electromechanical delay on the vastus medialis obliquus and vastus lateralis. Ultrasound Med Biol 35(5):878CrossRefPubMed

Nordez A, Gallot T, Catheline S, Guevel A, Cornu C, Hug F (2009b) Electromechanical delay revisited using very high frame rate ultrasound. J Appl Physiol 106(6):1970–1975CrossRefPubMed

O’Keeffe DT, Lyons GM, Donnelly AE, Byrne CA (2001) Stimulus artifact removal using a software-based two-stage peak detection algorithm. J Neurosci Methods 109:137–145CrossRefPubMed

Orizio C, Gobbo M, Diemont B, Esposito F, Veicsteinas A (2003) The surface mechanomyogram as a tool to describe the influence of fatigue on biceps brachii motor unit activation strategy. Historical basis and novel evidence. Eur J Appl Physiol 90(3–4):326–336CrossRefPubMed

Rampichini S, Cè E, Limonta E, Esposito F (2014) Effects of fatigue on the electromechanical delay components in gastrocnemius medialis muscle. Eur J Appl Physiol 114(3):639–651CrossRefPubMed

Sasaki K, Sasaki T, Ishii N (2011) Acceleration and force reveal different mechanisms of electromechanical delay. Med Sci Sports Exerc 43(7):1200–1206CrossRefPubMed

Selvin D, Renaud JM (2015) Changes in myoplasmic Ca²⁺ during fatigue differ between FDB fibers, between glibenclamide-exposed and Kir6.2^−/− fibers and are further modulated by verapamil. Physiol Rep 3(3):e12303

Sidhu SK, Weavil JC, Venturelli M, Garten RS, Rossman MJ, Richardson RS, Gmelch BS, Morgan DE, Amann M (2014) Spinal mu-opioid receptor-sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle. J Physiol 592(22):5011–5024CrossRefPubMedPubMedCentral

Sieck GC, Prakash YS (1995) Fatigue at the neuromuscular junction. Branch point vs. presynaptic vs. postsynaptic mechanisms. Adv Exp Med Biol 384:83–100CrossRefPubMed

Taylor DC, Brooks DE, Ryan JB (1997) Viscoelastic characteristics of muscle: passive stretching versus muscular contractions. Med Sci Sports Exerc 29(12):1619–1624CrossRefPubMed

Yavuz SU, Sendemir-Urkmez A, Turker KS (2010) Effect of gender, age, fatigue and contraction level on electromechanical delay. Clin Neurophysiol 121(10):1700–1706CrossRefPubMed

Zhang LQ, Rymer WZ (2001) Reflex and intrinsic changes induced by fatigue of human elbow extensor muscles. J Neurophysiol 86(3):1086–1094PubMed

Title: Changes in the electromechanical delay components during a fatiguing stimulation in human skeletal muscle: an EMG, MMG and force combined approach
Authors: Emiliano Cè
Susanna Rampichini
Elena Monti
Massimo Venturelli
Eloisa Limonta
Fabio Esposito
Publication date: 01-01-2017
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Applied Physiology / Issue 1/2017
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-016-3502-z

At a glance: The STEP trials

Springer Medicine

Changes in the electromechanical delay components during a fatiguing stimulation in human skeletal muscle: an EMG, MMG and force combined approach

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2017

An acute session of roller massage prolongs voluntary torque development and diminishes evoked pain

Changes in stiffness of the dorsal scapular muscles before and after computer work: a comparison between individuals with and without neck and shoulder complaints

Separate and combined effects of exposure to heat stress and mental fatigue on endurance exercise capacity in the heat

Shear wave elastography reveals different degrees of passive and active stiffness of the neck extensor muscles

Aging effect on muscle synergies in stepping forth during a forward perturbation

Relationships between lower body strength and the energy cost of treadmill walking in a cohort of healthy older adults: a cross-sectional analysis