Skip to main content
Top
Published in: European Journal of Applied Physiology 6/2020

01-06-2020 | Fatigue | Original Article

Fatigue-related modulation of low-frequency common drive to motor units

Authors: Ing-Shiou Hwang, Yen-Ting Lin, Chien-Chun Huang, Yi-Ching Chen

Published in: European Journal of Applied Physiology | Issue 6/2020

Login to get access

Abstract

Purpose

This study investigated fatigue-related modulation of common neural inputs to motor units (MUs) under 5 Hz, which determines force precision control.

Methods

Twenty-seven adults performed a sequence of fatiguing contractions. The participants were assessed with a static isometric index abduction at 20% maximal voluntary contraction in the pre-test and post-test. Discharge characteristics of MUs of the first dorsal interosseous muscle were analyzed with decomposed EMG signals.

Results

Along with increases in the mean (58.40 ± 11.76 ms → 62.55 ± 10.83 ms, P = 0.029) and coefficient of variation (0.204 ± .014 → 0.215 ± 0.017, P = 0.002) in inter-spike intervals, the fatiguing contraction caused reductions in the mean frequency (16.84 ± 3.31 Hz → 15.59 ± 3.21 Hz, P = 0.027) and spectral dispersions (67.54 ± 4.49 → 62.64 ± 6.76 Hz, P = 0.007) of common neural drive, as estimated with smoothed cumulative motor unit spike trains (SCMUSTs). Stabilogram diffusion analysis of SCMUSTs revealed significant fatigue-related reductions in the long-term effective diffusion coefficient (1.91 ± 0.77 Hz2/s → 1.61 ± 0.61 Hz2/s, P = 0.020) and long-term scaling exponent (0.480 ± 0.013 Hz2/s → 0.471 ± 0.017 Hz2/s, P = 0.014). After fatiguing contraction, mutual information of force fluctuations and SCMUSTs was augmented roughly by 12.95% (P = 0.041).

Conclusions

Muscular fatigue could compress and shift the low-frequency common drive to MUs toward lower spectral bands, thereby enhancing transmission of twitch forces through the muscle–tendon complex with a low-pass filter property. The fatigue-induced changes involve increased closed-loop control of the common modulation of MU discharge rates.
Literature
go back to reference Adam A, De Luca CJ (2003) Recruitment order of motor units in human vastus lateralis muscle is maintained during fatiguing contractions. J Neurophysiol 90:2919–2927PubMed Adam A, De Luca CJ (2003) Recruitment order of motor units in human vastus lateralis muscle is maintained during fatiguing contractions. J Neurophysiol 90:2919–2927PubMed
go back to reference Adam A, De Luca CJ, Erim Z (1998) Hand dominance and motor unit firing behavior. J Neurophysiol 80:1373–1382PubMed Adam A, De Luca CJ, Erim Z (1998) Hand dominance and motor unit firing behavior. J Neurophysiol 80:1373–1382PubMed
go back to reference Amann M, Sidhu SK, Weavil JC, Mangum TS, Venturelli M (2015) Autonomic responses to exercise: group III/IV muscle afferents and fatigue. Auton Neurosci 188:19–23PubMed Amann M, Sidhu SK, Weavil JC, Mangum TS, Venturelli M (2015) Autonomic responses to exercise: group III/IV muscle afferents and fatigue. Auton Neurosci 188:19–23PubMed
go back to reference Amjad AM, Halliday DM, Rosenberg JR, Conway BA (1997) An extended difference of coherence test for comparing and combining several independent coherence estimates: theory and application to the study of motor units and physiological tremor. J Neurosci Methods 3:69–79 Amjad AM, Halliday DM, Rosenberg JR, Conway BA (1997) An extended difference of coherence test for comparing and combining several independent coherence estimates: theory and application to the study of motor units and physiological tremor. J Neurosci Methods 3:69–79
go back to reference Barry BK, Pascoe MA, Jesunathadas M, Enoka RM (2007) Rate coding is compressed but variability is unaltered for motor units in a hand muscle of old adults. J Neurophysiol 97:3206–3218PubMed Barry BK, Pascoe MA, Jesunathadas M, Enoka RM (2007) Rate coding is compressed but variability is unaltered for motor units in a hand muscle of old adults. J Neurophysiol 97:3206–3218PubMed
go back to reference Beck TW, Stock MS, Defreitas JM (2012) Effects of fatigue on intermuscular common drive to the quadriceps femoris. Int J Neurosci 122:574–582PubMed Beck TW, Stock MS, Defreitas JM (2012) Effects of fatigue on intermuscular common drive to the quadriceps femoris. Int J Neurosci 122:574–582PubMed
go back to reference Castronovo AM, Negro F, Conforto S, Farina D (2015) The proportion of common synaptic input to motor neurons increases with an increase in net excitatory input. J Appl Physiol 119:1337–1346PubMed Castronovo AM, Negro F, Conforto S, Farina D (2015) The proportion of common synaptic input to motor neurons increases with an increase in net excitatory input. J Appl Physiol 119:1337–1346PubMed
go back to reference Chen YC, Lin YT, Chang GC, Hwang IS (2017a) Paradigm shifts in voluntary force control and motor unit behaviors with the manipulated size of visual error perception. Front Physiol 8:140PubMedPubMedCentral Chen YC, Lin YT, Chang GC, Hwang IS (2017a) Paradigm shifts in voluntary force control and motor unit behaviors with the manipulated size of visual error perception. Front Physiol 8:140PubMedPubMedCentral
go back to reference Chen YC, Lin LL, Lin YT, Hu CL, Hwang IS (2017b) Variations in static force control and motor unit behavior with error amplification feedback in the elderly. Front Hum Neurosci 11:538PubMedPubMedCentral Chen YC, Lin LL, Lin YT, Hu CL, Hwang IS (2017b) Variations in static force control and motor unit behavior with error amplification feedback in the elderly. Front Hum Neurosci 11:538PubMedPubMedCentral
go back to reference Collins JJ, De Luca CJ (1993) Open-loop and closed-loop control of posture: a random-walk analysis of center-of-pressure trajectories. Exp Brain Res 95:308–318PubMed Collins JJ, De Luca CJ (1993) Open-loop and closed-loop control of posture: a random-walk analysis of center-of-pressure trajectories. Exp Brain Res 95:308–318PubMed
go back to reference Collins JJ, De Luca CJ (1995) The effects of visual input on open-loop and closed-loop postural control mechanisms. Exp Brain Res 103:151–163PubMed Collins JJ, De Luca CJ (1995) The effects of visual input on open-loop and closed-loop postural control mechanisms. Exp Brain Res 103:151–163PubMed
go back to reference Collins JJ, De Luca CJ, Burrows A, Lipsitz LA (1995) Age-related changes in open-loop and closed-loop postural control mechanisms. Exp Brain Res 104:480–492PubMed Collins JJ, De Luca CJ, Burrows A, Lipsitz LA (1995) Age-related changes in open-loop and closed-loop postural control mechanisms. Exp Brain Res 104:480–492PubMed
go back to reference Contessa P, Adam A, De Luca CJ (2009) Motor unit control and force fluctuation during fatigue. J Appl Physiol 107:235–243PubMedPubMedCentral Contessa P, Adam A, De Luca CJ (2009) Motor unit control and force fluctuation during fatigue. J Appl Physiol 107:235–243PubMedPubMedCentral
go back to reference Contessa P, De Luca CJ, Kline JC (2016) The compensatory interaction between motor unit firing behavior and muscle force during fatigue. J Neurophysiol 116(4):1579–1585PubMedPubMedCentral Contessa P, De Luca CJ, Kline JC (2016) The compensatory interaction between motor unit firing behavior and muscle force during fatigue. J Neurophysiol 116(4):1579–1585PubMedPubMedCentral
go back to reference Delignières D, Torre K, Bernard PL (2011) Transition from persistent to anti-persistent correlations in postural sway indicates velocity-based control. PLoS Comput Biol 7:e1001089PubMedPubMedCentral Delignières D, Torre K, Bernard PL (2011) Transition from persistent to anti-persistent correlations in postural sway indicates velocity-based control. PLoS Comput Biol 7:e1001089PubMedPubMedCentral
go back to reference De Luca CJ, LeFever RS, McCue MP, Xenakis AP (1982) Control scheme governing concurrently active human motor units during voluntary contractions. J Physiol 329:129–142PubMedPubMedCentral De Luca CJ, LeFever RS, McCue MP, Xenakis AP (1982) Control scheme governing concurrently active human motor units during voluntary contractions. J Physiol 329:129–142PubMedPubMedCentral
go back to reference De Luca CJ, Roy AM, Erim Z (1993) Synchronization of motor-unit firings in several human muscles. J Neurophysiol 70:2010–2023PubMed De Luca CJ, Roy AM, Erim Z (1993) Synchronization of motor-unit firings in several human muscles. J Neurophysiol 70:2010–2023PubMed
go back to reference De Luca CJ, Adam A, Wotiz R, Gilmore LD, Nawab SH (2006) Decomposition of surface EMG signals. J Neurophysiol 96:1646–1657PubMed De Luca CJ, Adam A, Wotiz R, Gilmore LD, Nawab SH (2006) Decomposition of surface EMG signals. J Neurophysiol 96:1646–1657PubMed
go back to reference Dideriksen JL, Farina D, Enoka RM (2010) Influence of fatigue on the simulated relation between the amplitude of the surface electromyogram and muscle force. Philos Trans A Math Phys Eng Sci 368(1920):2765–2781PubMed Dideriksen JL, Farina D, Enoka RM (2010) Influence of fatigue on the simulated relation between the amplitude of the surface electromyogram and muscle force. Philos Trans A Math Phys Eng Sci 368(1920):2765–2781PubMed
go back to reference Edwards RH (1981) Human muscle function and fatigue. Ciba Found Symp 82:1–18PubMed Edwards RH (1981) Human muscle function and fatigue. Ciba Found Symp 82:1–18PubMed
go back to reference Enoka RM, Robinson GA, Kossev AR (1989) Task and fatigue effects on low-threshold motor units in human hand muscle. J Neurophysiol 62:1344–1359PubMed Enoka RM, Robinson GA, Kossev AR (1989) Task and fatigue effects on low-threshold motor units in human hand muscle. J Neurophysiol 62:1344–1359PubMed
go back to reference Farina D, Negro F (2015) Common synaptic input to motor neurons, motor unit synchronization, and force control. Exerc Sport Sci Rev 43:23–33PubMed Farina D, Negro F (2015) Common synaptic input to motor neurons, motor unit synchronization, and force control. Exerc Sport Sci Rev 43:23–33PubMed
go back to reference Farina D, Negro F, Muceli S, Enoka RM (2016) Principles of motor unit physiology evolve with advances in technology. Physiology 31:83–94PubMed Farina D, Negro F, Muceli S, Enoka RM (2016) Principles of motor unit physiology evolve with advances in technology. Physiology 31:83–94PubMed
go back to reference Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789PubMed Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789PubMed
go back to reference Gimmon Y, Riemer R, Oddsson L, Melzer I (2011) The effect of plantar flexor muscle fatigue on postural control. J Electromyogr Kinesiol 21:922–928PubMed Gimmon Y, Riemer R, Oddsson L, Melzer I (2011) The effect of plantar flexor muscle fatigue on postural control. J Electromyogr Kinesiol 21:922–928PubMed
go back to reference Hwang IS, Lin YT, Huang WM, Yang ZR, Hu CL, Chen YC (2017) Alterations in neural control of constant isometric contraction with the size of error feedback. PLoS ONE 12(1):e0170824PubMedPubMedCentral Hwang IS, Lin YT, Huang WM, Yang ZR, Hu CL, Chen YC (2017) Alterations in neural control of constant isometric contraction with the size of error feedback. PLoS ONE 12(1):e0170824PubMedPubMedCentral
go back to reference Johnson KV, Edwards SC, Van Tongeren C, Bawa P (2004) Properties of human motor units after prolonged activity at a constant firing rate. Exp Brain Res 154:479–487PubMed Johnson KV, Edwards SC, Van Tongeren C, Bawa P (2004) Properties of human motor units after prolonged activity at a constant firing rate. Exp Brain Res 154:479–487PubMed
go back to reference Joseph MF, Lillie KR, Bergeron DJ, Cota KC, Yoon JS, Kraemer WJ, Denegar CR (2014) Achilles tendon biomechanics in response to acute intense exercise. J Strength Cond Res 28:1181–1186PubMed Joseph MF, Lillie KR, Bergeron DJ, Cota KC, Yoon JS, Kraemer WJ, Denegar CR (2014) Achilles tendon biomechanics in response to acute intense exercise. J Strength Cond Res 28:1181–1186PubMed
go back to reference Kay AD, Blazevich AJ (2009) Isometric contractions reduce plantar flexor moment, Achilles tendon stiffness, and neuromuscular activity but remove the subsequent effects of stretch. J Appl Physiol 107:1181–1189PubMed Kay AD, Blazevich AJ (2009) Isometric contractions reduce plantar flexor moment, Achilles tendon stiffness, and neuromuscular activity but remove the subsequent effects of stretch. J Appl Physiol 107:1181–1189PubMed
go back to reference Lacour M, Dosso NY, Heuschen S, Thiry A, Van Nechel C, Toupet M (2018) How eye movements stabilize posture in patients with bilateral vestibular hypofunction. Front Neurol 9:744PubMedPubMedCentral Lacour M, Dosso NY, Heuschen S, Thiry A, Van Nechel C, Toupet M (2018) How eye movements stabilize posture in patients with bilateral vestibular hypofunction. Front Neurol 9:744PubMedPubMedCentral
go back to reference Laine CM, Yavuz SU, Farina D (2014) Task-related changes in sensorimotor integration influence the common synaptic input to motor neurones. Acta Physiol 211:229–239 Laine CM, Yavuz SU, Farina D (2014) Task-related changes in sensorimotor integration influence the common synaptic input to motor neurones. Acta Physiol 211:229–239
go back to reference Mandelbrot BB, van Ness JW (1968) Fractional Brownian motions, fractional noises and applications. SIAM Rev 10:422–437 Mandelbrot BB, van Ness JW (1968) Fractional Brownian motions, fractional noises and applications. SIAM Rev 10:422–437
go back to reference McManus L, Hu X, Rymer WZ, Suresh NL, Lowery MM (2016) Muscle fatigue increases beta-band coherence between the firing times of simultaneously active motor units in the first dorsal interosseous muscle. J Neurophysiol 115:2830–2839PubMedPubMedCentral McManus L, Hu X, Rymer WZ, Suresh NL, Lowery MM (2016) Muscle fatigue increases beta-band coherence between the firing times of simultaneously active motor units in the first dorsal interosseous muscle. J Neurophysiol 115:2830–2839PubMedPubMedCentral
go back to reference Mesin L, Dardanello D, Rainoldi A, Boccia G (2016) Motor unit firing rates and synchronisation affect the fractal dimension of simulated surface electromyogram during isometric/isotonic contraction of vastus lateralis muscle. Med Eng Phys 38:1530–1533PubMed Mesin L, Dardanello D, Rainoldi A, Boccia G (2016) Motor unit firing rates and synchronisation affect the fractal dimension of simulated surface electromyogram during isometric/isotonic contraction of vastus lateralis muscle. Med Eng Phys 38:1530–1533PubMed
go back to reference Nagamori A, Laine CM, Valero-Cuevas FJ (2018) Cardinal features of involuntary force variability can arise from the closed-loop control of viscoelastic afferented muscles. PLoS Comput Biol 14:e1005884PubMedPubMedCentral Nagamori A, Laine CM, Valero-Cuevas FJ (2018) Cardinal features of involuntary force variability can arise from the closed-loop control of viscoelastic afferented muscles. PLoS Comput Biol 14:e1005884PubMedPubMedCentral
go back to reference Nawab SH, Chang SS, De Luca CJ (2010) High-yield decomposition of surface EMG signals. Clin Neurophysiol 121:1602–1615PubMedPubMedCentral Nawab SH, Chang SS, De Luca CJ (2010) High-yield decomposition of surface EMG signals. Clin Neurophysiol 121:1602–1615PubMedPubMedCentral
go back to reference Negro F, Farina D (2011) Linear transmission of cortical oscillations to the neural drive to muscles is mediated by common projections to populations of motoneurons in humans. J Physiol 589(Pt 3):629–637PubMed Negro F, Farina D (2011) Linear transmission of cortical oscillations to the neural drive to muscles is mediated by common projections to populations of motoneurons in humans. J Physiol 589(Pt 3):629–637PubMed
go back to reference Negro F, Farina D (2012) Factors influencing the estimates of correlation between motor unit activities in humans. PLoS ONE 7:e44894PubMedPubMedCentral Negro F, Farina D (2012) Factors influencing the estimates of correlation between motor unit activities in humans. PLoS ONE 7:e44894PubMedPubMedCentral
go back to reference 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(Pt 24):5925–5938PubMedPubMedCentral 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(Pt 24):5925–5938PubMedPubMedCentral
go back to reference Negro F, Yavuz UŞ, Farina D (2016) The human motor neuron pools receive a dominant slow-varying common synaptic input. J Physiol 594:5491–5505PubMedPubMedCentral Negro F, Yavuz UŞ, Farina D (2016) The human motor neuron pools receive a dominant slow-varying common synaptic input. J Physiol 594:5491–5505PubMedPubMedCentral
go back to reference Pettorossi VE, Della Torre G, Bortolami R, Brunetti O (1999) The role of capsaicin-sensitive muscle afferents in fatigue-induced modulation of the monosynaptic reflex in the rat. J Physiol 515:599–607PubMedPubMedCentral Pettorossi VE, Della Torre G, Bortolami R, Brunetti O (1999) The role of capsaicin-sensitive muscle afferents in fatigue-induced modulation of the monosynaptic reflex in the rat. J Physiol 515:599–607PubMedPubMedCentral
go back to reference Slifkin AB, Vaillancourt DE, Newell KM (2000) Intermittency in the control of continuous force production. J Neurophysiol 84:1708–1718PubMed Slifkin AB, Vaillancourt DE, Newell KM (2000) Intermittency in the control of continuous force production. J Neurophysiol 84:1708–1718PubMed
go back to reference Taylor JL, Butler JE, Gandevia SC (2000) Changes in muscle afferents, motoneurons and motor drive during muscle fatigue. Eur J Appl Physiol 83:106–115PubMed Taylor JL, Butler JE, Gandevia SC (2000) Changes in muscle afferents, motoneurons and motor drive during muscle fatigue. Eur J Appl Physiol 83:106–115PubMed
go back to reference Tecchio F, Porcaro C, Zappasodi F, Pesenti A, Ercolani M, Rossini PM (2006) Cortical short-term fatigue effects assessed via rhythmic brain-muscle coherence. Exp Brain Res 174:144–151PubMed Tecchio F, Porcaro C, Zappasodi F, Pesenti A, Ercolani M, Rossini PM (2006) Cortical short-term fatigue effects assessed via rhythmic brain-muscle coherence. Exp Brain Res 174:144–151PubMed
go back to reference Ushiyama J, Katsu M, Masakado Y, Kimura A, Liu M, Ushiba J (2011) Muscle fatigue-induced enhancement of corticomuscular coherence following sustained submaximal isometric contraction of the tibialis anterior muscle. J Appl Physiol 110:1233–1240PubMed Ushiyama J, Katsu M, Masakado Y, Kimura A, Liu M, Ushiba J (2011) Muscle fatigue-induced enhancement of corticomuscular coherence following sustained submaximal isometric contraction of the tibialis anterior muscle. J Appl Physiol 110:1233–1240PubMed
go back to reference Vaillancourt DE, Newell KM (2003) Aging and the time and frequency structure of force output variability. J Appl Physiol 94:903–912PubMed Vaillancourt DE, Newell KM (2003) Aging and the time and frequency structure of force output variability. J Appl Physiol 94:903–912PubMed
go back to reference Vaillancourt DE, Larsson L, Newell KM (2002) Time-dependent structure in the discharge rate of human motor units. Clin Neurophysiol 113:1325–1338PubMed Vaillancourt DE, Larsson L, Newell KM (2002) Time-dependent structure in the discharge rate of human motor units. Clin Neurophysiol 113:1325–1338PubMed
go back to reference Yang Q, Fang Y, Sun CK, Siemionow V, Ranganathan VK, Khoshknabi D, Davis MP, Walsh D, Sahgal V, Yue GH (2009) Weakening of functional corticomuscular coupling during muscle fatigue. Brain Res 1250:101–112PubMed Yang Q, Fang Y, Sun CK, Siemionow V, Ranganathan VK, Khoshknabi D, Davis MP, Walsh D, Sahgal V, Yue GH (2009) Weakening of functional corticomuscular coupling during muscle fatigue. Brain Res 1250:101–112PubMed
Metadata
Title
Fatigue-related modulation of low-frequency common drive to motor units
Authors
Ing-Shiou Hwang
Yen-Ting Lin
Chien-Chun Huang
Yi-Ching Chen
Publication date
01-06-2020
Publisher
Springer Berlin Heidelberg
Keyword
Fatigue
Published in
European Journal of Applied Physiology / Issue 6/2020
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-020-04363-z

Other articles of this Issue 6/2020

European Journal of Applied Physiology 6/2020 Go to the issue