Passive muscle stretching impairs rapid force production and neuromuscular function in human plantar flexors
Abstract
Purpose
We examined the effect of muscle stretching on the ability to produce rapid torque and the mechanisms underpinning the changes.
Methods
Eighteen men performed three conditions: (1) continuous stretch (1 set of 5 min), (2) intermittent stretch (5 sets of 1 min with 15-s inter-stretch interval), and (3) control. Isometric plantar flexor rate of torque development was measured during explosive maximal voluntary contractions (MVC) in the intervals 0–100 ms (RTDV100) and 0–200 ms (RTDV200), and in electrically evoked 0.5-s tetanic contractions (20 Hz, 20 Hz preceded by a doublet and 80 Hz). The rate of EMG rise, electromechanical delay during MVC (EMDV) and during a single twitch contraction (EMDtwitch) were assessed.
Results
RTDV200 was decreased (P < 0.05) immediately after continuous (− 15%) and intermittent stretch (− 30%) with no differences between protocols. The rate of torque development during tetanic stimulations was reduced (P < 0.05) immediately after continuous (− 8%) and intermittent stretch (− 10%), when averaged across stimulation frequencies. Lateral gastrocnemius rate of EMG rise was reduced after intermittent stretch (− 27%), and changes in triceps surae rate of EMG rise were correlated with changes in RTDV200 after both continuous (r = 0.64) and intermittent stretch (r = 0.65). EMDV increased immediately (31%) and 15 min (17%) after intermittent stretch and was correlated with changes in RTDV200 (r = − 0.56). EMDtwitch increased immediately after continuous (4%), and immediately (5.4%), 15 min (6.3%), and 30 min after (6.4%) intermittent stretch (P < 0.05).
Conclusions
Reductions in the rate of torque development immediately after stretching were associated with both neural and mechanical mechanisms.
Keywords
Rate of force development Explosive force Flexibility Force transmissionAbbreviations
- ANOVA
Analysis of variance
- CI
Confidence interval
- EMD
Electromechanical delay
- EMDtwitch
Electromechanical delay during the electrically evoked twitch
- EMDV
Electromechanical delay during voluntary contraction
- EMG
Electromyogram
- LG
Lateral gastrocnemius
- Mmax
Maximal compound action potential amplitude
- MVC
Maximal voluntary contraction
- PICs
Persistent inward currents
- RER
Rate of electromyogram rise
- RFD
Rate of force development
- RTD
Rate of torque development
- RTDI
Involuntary rate of torque development
- RTDV
Voluntary rate of torque development
- SOL
Soleus
- VFT
Variable-frequency train of stimulation
Notes
Author contributions
GST and AJB conceived and designed the study. GST and LS conducted the experiments. GST analyzed the data, and drafted the first version of the manuscript. GST, LB, KN, and AJB critically revised the manuscript. All authors read and approved the manuscript.
Funding
This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
Compliance with ethical standards
Conflict of interest
No conflicts of interest, financial or otherwise, are declared by the author(s).
References
- Aagaard P, Simonsen EB, Andersen JL et al (2002) Increased rate of force development and neural drive of human skeletal muscle following resistance training. J Appl Physiol 93:1318–1326. https://doi.org/10.1152/japplphysiol.00283.2002 CrossRefPubMedGoogle Scholar
- Abbate F, Bruton JD, De Haan A, Westerblad H (2002) Prolonged force increase following a high-frequency burst is not due to a sustained elevation of [Ca2+]i. Am J Physiol Physiol 283:C42–C47. https://doi.org/10.1152/ajpcell.00416.2001 CrossRefGoogle Scholar
- Bakdash JZ, Marusich LR (2017) Repeated measures correlation. Front Psychol 8:1–13. https://doi.org/10.3389/fpsyg.2017.00456 CrossRefGoogle Scholar
- Bakker AJ, Cully TR, Wingate CD et al (2017) Doublet stimulation increases Ca2+ binding to troponin C to ensure rapid force development in skeletal muscle. J Gen Physiol 149:323–334. https://doi.org/10.1085/jgp.201611727 CrossRefPubMedPubMedCentralGoogle Scholar
- Balog EM (2010) Excitation-contraction coupling and minor triadic proteins in low-frequency fatigue. Exerc Sport Sci Rev 38:135–142. https://doi.org/10.1097/JES.0b013e3181e3734d CrossRefPubMedPubMedCentralGoogle Scholar
- Behm DG, Blazevich AJ, Kay AD, McHugh M (2016) Acute effects of muscle stretching on physical performance, range of motion, and injury incidence in healthy active individuals: a systematic review. Appl Physiol Nutr Metab 41:1–11. https://doi.org/10.1139/apnm-2015-0235 CrossRefPubMedGoogle Scholar
- Bergquist AJ, Clair JM, Collins DF (2011) Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: triceps surae. J Appl Physiol 110:627–637. https://doi.org/10.1152/japplphysiol.01103.2010 CrossRefPubMedGoogle Scholar
- Binder-Macleod S, Kesar T (2005) Catchlike property of skeletal muscle: recent findings and clinical implications. Muscle Nerve 31:681–693. https://doi.org/10.1002/mus.20290 CrossRefPubMedGoogle Scholar
- Blazevich AJ, Cannavan D, Waugh CM et al (2012) Neuromuscular factors influencing the maximum stretch limit of the human plantar flexors. J Appl Physiol 113:1446–1455. https://doi.org/10.1152/japplphysiol.00882.2012 CrossRefPubMedGoogle Scholar
- Cavanagh PR, Komi PV (1979) Eletromechanical delay in human skeletal muscle under concentric and eccentric contractions. Eur J Appl Physiol 163:159–163CrossRefGoogle Scholar
- Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. L. Erlbaum Associates, Hillsdale, N.JGoogle Scholar
- Costa PB, Ryan ED, Herda TJ et al (2010) Acute effects of passive stretching on the electromechanical delay and evoked twitch properties: a gender comparison. J Appl Biomech 28:645–654. https://doi.org/10.1123/jab.28.6.645 CrossRefGoogle Scholar
- 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 84:1137–1150CrossRefGoogle Scholar
- Desmedt BJE, Godaux E (1977) Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle. J Physiol 264:673–693CrossRefGoogle Scholar
- Duchateau J, Baudry S (2014) Maximal discharge rate of motor units determines the maximal rate of force development during ballistic contractions in human. Front Hum Neurosci 8:9–11. https://doi.org/10.3389/fnhum.2014.00234 CrossRefGoogle Scholar
- Esposito F, Limonta E, Cè 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 111:485–495. https://doi.org/10.1007/s00421-010-1659-4 CrossRefPubMedGoogle Scholar
- Heckman CJ, Enoka RM (2012) Motor unit. Compr Physiol 2:2629–2682. https://doi.org/10.1002/cphy.c100087 CrossRefPubMedGoogle Scholar
- Jenkins NDM, Buckner SL, Cochrane KC et al (2014) Age-related differences in rates of torque development and rise in EMG are eliminated by normalization. Exp Gerontol 57:18–28. https://doi.org/10.1016/j.exger.2014.04.015 CrossRefPubMedGoogle Scholar
- Kay AD, Blazevich AJ (2009) Moderate-duration static stretch reduces active and passive plantar flexor moment but not Achilles tendon stiffness or active muscle length. J Appl Physiol 106:1249–1256. https://doi.org/10.1152/japplphysiol.91476.2008 CrossRefPubMedGoogle Scholar
- Kennedy DS, Fitzpatrick SC, Gandevia SC, Taylor JL (2015) Fatigue-related firing of muscle nociceptors reduces voluntary activation of ipsilateral but not contralateral lower limb muscles. J Appl Physiol 118:408–418. https://doi.org/10.1152/japplphysiol.00375.2014 CrossRefPubMedGoogle Scholar
- Klass M, Baudry S, Duchateau J (2008) Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions. J Appl Physiol 104:739–746. https://doi.org/10.1152/japplphysiol.00550.2007 CrossRefPubMedGoogle Scholar
- Kudina LP, Andreeva RE (2010) Repetitive doublet Wring of motor units: evidence for plateau potentials in human motoneurons? Exp Brain Res 204:79–90. https://doi.org/10.1007/s00221-010-2298-z CrossRefPubMedGoogle Scholar
- Lanza MB, Balshaw TB, Folland JP (2017) MMAX normalisation of voluntary EMG removes the confounding influences of electrode location and body fat. Med Sci Sport Exerc 49:779. https://doi.org/10.1249/01.mss.0000519076.74034.cb CrossRefGoogle Scholar
- Maffiuletti NA, Aagaard P, Blazevich AJ et al (2016) Rate of force development: physiological and methodological considerations. Eur J Appl Physiol. https://doi.org/10.1007/s00421-016-3346-6 CrossRefPubMedPubMedCentralGoogle Scholar
- Martin V, Millet GY, Martin A et al (2004) Assessment of low-frequency fatigue with two methods of electrical stimulation. J Appl Physiol 97:1923–1929. https://doi.org/10.1152/japplphysiol.00376.2004 CrossRefPubMedGoogle Scholar
- Morse CI, Degens H, Seynnes OR et al (2008) The acute effect of stretching on the passive stiffness of the human gastrocnemius muscle tendon unit. J Physiol 586:97–106. https://doi.org/10.1113/jphysiol.2007.140434 CrossRefPubMedGoogle Scholar
- Nielsen BG (2009) Calcium and the role of motoneuronal doublets in skeletal muscle control. Eur Biophys J 38:159–173. https://doi.org/10.1007/s00249-008-0364-2 CrossRefPubMedGoogle Scholar
- Nordez A, Gallot T, Catheline S et al (2009) Electromechanical delay revisited using very high frame rate ultrasound. J Appl Physiol 106:1970–1975. https://doi.org/10.1152/japplphysiol.00221.2009 CrossRefPubMedGoogle Scholar
- Rodriguez-Falces J, Place N (2018) Determinants, analysis and interpretation of the muscle compound action potential (M wave) in humans: implications for the study of muscle fatigue. Eur J Appl Physiol 118:501–521. https://doi.org/10.1007/s00421-017-3788-5 CrossRefPubMedGoogle Scholar
- Simic L, Sarabon N, Markovic G (2013) Does pre-exercise static stretching inhibit maximal muscular performance? A meta-analytical review. Scand J Med Sci Sport 23:131–148. https://doi.org/10.1111/j.1600-0838.2012.01444.x CrossRefGoogle Scholar
- Trajano GS, Nosaka K, Seitz L, Blazevich AJ (2014a) Intermittent stretch reduces force and central drive more than continuous stretch. Med Sci Sports Exerc 46:902–910. https://doi.org/10.1249/MSS.0000000000000185 CrossRefPubMedGoogle Scholar
- Trajano GS, Seitz LB, Nosaka K, Blazevich AJ (2014b) Can passive stretch inhibit motoneuron facilitation in the human plantar flexors? J Appl Physiol 117:1486–1492. https://doi.org/10.1152/japplphysiol.00809.2014 CrossRefPubMedGoogle Scholar
- Trajano GS, Nosaka K, Blazevich AJ (2017) Neurophysiological mechanisms underpinning stretch-induced force loss. Sport Med 47:1531–1541. https://doi.org/10.1007/s40279-017-0682-6 CrossRefGoogle Scholar
- Un CP, Lin KH, Shiang TY et al (2013) Comparative and reliability studies of neuromechanical leg muscle performances of volleyball athletes in different divisions. Eur J Appl Physiol 113:457–466. https://doi.org/10.1007/s00421-012-2454-1 CrossRefPubMedGoogle Scholar
- van Cutsem M, Duchateau J, Hainaut K (1998) Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans. J Physiol 1:295–305CrossRefGoogle Scholar
- Waugh CM, Korff T, Fath F, Blazevich AJ (2013) Rapid force production in children and adults. Med Sci Sport Exerc 45:762–771. https://doi.org/10.1249/mss.0b013e31827a67ba CrossRefGoogle Scholar
- Zhou S, Lawson DL, Morrison WE, Fairweather I (1995) Electromechanical delay in isometric muscle contractions evoked by voluntary, reflex and electrical stimulation. Eur J Appl Physiol Occup Physiol 70:138–145. https://doi.org/10.1007/BF00361541 CrossRefPubMedGoogle Scholar