Abstract
There is substantial evidence that fatiguing exercise is accompanied by changes within the central nervous system that reduce the force that can be produced by working muscles. Here we review studies that used non-invasive neurophysiological techniques to show that sustained single-joint contractions have the capacity to increase corticospinal responsiveness and reduce motoneuronal responsiveness. We contrast these findings with new evidence from our laboratory regarding corticospinal responsiveness during sustained cycling exercise. There seems to be a similar increase in responsiveness of the intracortical inhibitory interneurons during sustained locomotor and single-joint exercise which might be due to acute exercise responses that are common to fatiguing exercise of any nature, such as local accumulation of fatigue metabolites. In contrast, the pattern of changes in corticospinal responsiveness is fundamentally different between the two modes of exercise which might be due to greater systemic fatigue responses to locomotor exercises.
Similar content being viewed by others
References
Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev. 2001;81(4):1725–89.
Fitts RH. Cellular mechanisms of muscle fatigue. Physiol Rev. 1994;74:49–94.
Taylor JL, Gandevia SC. A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol. 2008;104:542–50.
Taylor JL, Allen GM, Butler JE, Gandevia SC. Supraspinal fatigue during intermittent maximal voluntary contractions of the human elbow flexors. J Appl Physiol. 2000;89:305–13.
Gandevia SC, Allen GM, Butler JE, Taylor JM. Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol. 1996;490:529–36.
Kjaer M, Hanel B, Worm L, Perko G, Lewis SF, sahlin K, et al. Cardiovascular and neuroendocrine responses to exercise in hypoxia during imapried neural feedback from muscle. Am J Physiol Regul Integr Comp Physiol. 1999;277(1 Pt 2):R76–85.
Brink-Elfegoun T, Kaijser L, Gustafsson T, Ekblom B. Maximal oxygen uptake is not limited by a central nervous system governor. J Appl Physiol. 2007;102:781–6.
Amann M, Dempsey JA. Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol. 2008;586(1):161–73.
Marcora S. Is peripheral locomotor muscle fatigue during endurance exercise a variable carefully regulated by a negative feedback system? J Physiol. 2008;586(7):2027–8 (author reply 9–30).
Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol. 2011;589(Pt 21):5299–309.
Goodall S, Ross EZ, Romer LM. Effect of graded hypoxia on supraspinal contributions to fatigue with unilateral knee-extensor contractions. J Appl Physiol. 2010;109(6):1842–51.
Periard JD, Caillaud C, Thompson MW. Central and peripheral fatigue during passive and exercise-induced hyperthermia. Med Sci Sports Exerc. 2011;43(9):1657–65.
Dempsey JA, Amann M, Romer LM, Miller JD. Respiratory system determinants of peripheral fatigue and endurance performance. Med Sci Sports Exerc. 2008;40(3):457–61.
Romer LM, Polkey MI. Exercise-induced respiratory muscle fatigue: implications for performance. J Appl Physiol. 2008;104:879–88.
Amann M, Romer LM, Subudhi AW, Pegelow DF, Dempsey JA. Severity of arterial hypoxaemia affects the relative contributions of peripheral muscle fatigue to exercise performance in healthy humans. J Physiol. 2007;581:389–403.
Bhambhani Y, Malik R, Mookerjee S. Cerebral oxygenation declines at exercise intensities above the respiratory compensation threshold. Respir Physiol Neurobiol. 2007;156:196–202.
Subudhi AW, Dimmen AC, Roach RC. Effects of acute hypoxia on cerebral and muscle oxygenation during incremental exercise. J Appl Physiol. 2007;103:177–83.
Rupp T, Perrey S. Prefrontal cortex oxygenation and neuromuscular responses to exhaustive exercise. Eur J Appl Physiol. 2008;102:153–63.
Secher NH, Seifert T, Van Lieshout JJ. Cerebral blood flow and metabolism during exercise: implications for fatigue. J Appl Physiol. 2008;104:306–14.
Hasegawa H, Piacentini MF, Sarre S, Michotte Y, Ishiwata T, Meeusen R. Influence of brain catecholamines on the development of fatigue in exercising rats in the heat. J Physiol. 2007;586:141–9.
Tallent J, Goodall S, Hortobagyi T, St Clair Gibson A, French DN, Howatson G. Recovery time of motor evoked potentials following lengthening and shortening muscle action in the tibialis anterior. J Clin Neurosci. 2012;19(9):1328–9.
Smith JL, Martin PG, Gandevia SC, Taylor JL. Sustained contraction at very low forces produces prominent supraspinal fatigue in human elbow flexor muscles. J Appl Physiol. 2007;103:560–8.
Todd G, Petersen NT, Taylor JL, Gandevia SC. The effect of contralateral contraction on maximal voluntary activation and central fatigue in elbow flexor muscles. Exp Brain Res. 2003;150:308–13.
Sidhu SK, Bentley DJ, Carroll TJ. Locomotor exercise induces long-lasting impairments in the capacity of the human motor cortex to voluntarily activate knee extensor muscles. J Appl Physiol. 2009;106(2):556–65.
Hoffman BW, Oya T, Carroll TJ, Cresswell AG. Increases in corticospinal responsiveness during a sustained submaximal plantar flexion. J Appl Physiol. 2009;107(1):112–20.
Lévénez M, Garland SJ, Klass M, Duchateau J. Cortical and spinal modulation of antagonist coactivation during a submaximal fatiguing contraction in humans. J Neurophysiol. 2008;99(2):554–63.
Søgaard K, Gandevia SC, Todd G, Petersen NT, Taylor JL. The effect of sustained low-intensity contractions on supraspinal fatigue in human elbow flexor muscles. J Physiol. 2006;573(2):511–23.
Benwell NM, Sacco P, Hammond GR, Byrnes ML, Mastaglia FL, Thickbroom GW. Short-interval cortical inhibition and corticomotor excitability with fatiguing hand exercise: a central adaptation to fatigue? Exp Brain Res. 2006;170:191–8.
Todd G, Taylor JL, Gandevia SC. Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol. 2003;551(2):661–71.
Kalmar JM, Cafarelli E. Central excitability does not limit postfatigue voluntary activation of quadriceps femoris. J Appl Physiol. 2006;100:1757–64.
Klass M, Roelands B, Levenez M, Fontenelle V, Pattyn N, Meeusen R, et al. Effects of noradrenaline and dopamine on supraspinal fatigue in well-trained men. Med Sci Sports Exerc. 2012;44(12):2299–308.
Gandevia SC, Herbert RD, Leeper JB. Voluntary activation of human elbow flexor muscles during maximal concentric contractions. J Physiol. 1998;512(Pt 2):595–602.
Sidhu SK, Cresswell AG, Carroll TJ. Motor cortex excitability does not increase during sustained cycling exercise to volitional exhaustion. J Appl Physiol. 2012;113(3):401–9.
Sidhu SK, Hoffman BW, Cresswell AG, Carroll TJ. Corticospinal contributions to lower limb muscle activity during cycling in humans. J Neurophysiol. 2012;107(1):306–14.
Porter R, Lemon RN. Corticospinal function and voluntary movement. Oxford: Oxford University Press; 1993.
Ashe J. Force and the motor cortex. Behav Brain Res. 1997;87(2):255–69.
Forssberg H, Grillner S, Rossignol S. Phasic gain control of reflexes from the dorsum of the paw during spinal locomotion. Brain Res. 1977;132(1):121–39.
Grillner S, McClellan A, Perret C. Entrainment of the spinal pattern generators for swimming by mechano-sensitive elements in the lamprey spinal cord in vitro. Brain Res. 1981;217(2):380–6.
Schubert M, Curt A, Jensen L, Dietz V. Corticospinal input in human gait: modulation of magnetically evoked motor responses. Exp Brain Res. 1997;115:234–46.
Capaday C, Lavoie BA, Barbeau H, Schneider C, Bonnard M. Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J Neurophysiol. 1999;81(1):129–39.
Pyndt HS, Nielsen JB. Modulation of transmission in the corticospinal and group Ia afferent pathways to soleus motoneurons during bicycling. J Neurophysiol. 2003;89:304–14.
Petersen NT, Butler JE, Marchand-Pauvert V, Fisher R, Ledebt A, Pyndt HS, et al. Suppression of EMG activity by transcranial magnetic stimulation in human subjects during walking. J Physiol. 2001;537(2):651–6.
Barthelemy D, Nielsen JB. Corticospinal contribution to arm muscle activity during human walking. J Physiol. 2010;588(Pt 6):967–79.
Zuur AT, Lundbye-Jensen J, Leukel C, Taube W, Grey MJ, Gollhofer A, et al. Contribution of afferent feedback and descending drive to human hopping. J Physiol. 2010;588(Pt 5):799–807.
Farina D, Merletti R, Enoka RM. The extraction of neural strategies from surface EMG. J Appl Physiol. 2004;96:1486–95.
Keenan KG, Farina D, Maluf KS, Merletti R, Enoka RM. Influence of amplitude cancellation on the simulated surface electromyogram. J Appl Physiol. 2005;98(1):120–31.
Farina D, Cescon C, Negro F, Enoka RM. Amplitude cancellation of motor-unit action potentials in the surface electromyogram can be estimated with spike-triggered averaging. J Neurophysiol. 2008;100(1):431–40.
Garland SJ, Enoka RM, Serrano LP, Robinson GA. Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. J Appl Physiol. 1994;76(6):2411–9.
Löscher WN, Cresswell AG, Thorstensson A. Electromyographic responses of the human triceps surae and force tremor during sustained submaximal isometric plantar flexion. Acta Physiol Scand. 1994;152(1):73–82.
Löscher WN, Cresswell AG, Thorstensson A. Central fatigue during a long-lasting submaximal contraction of the triceps surae. Exp Brain Res. 1996;108:305–14.
Bigland-Ritchie B, Furbush F, Woods JJ. Fatigue of intermittent submaximal voluntary contractions: central and peripheral factors. J Appl Physiol. 1986;61(2):421–9.
Enoka RM. Morphological features and activation patterns of motor units. J Clin Neurophysiol. 1995;12(6):538–59.
Bigland-Ritchie B, Jones DA, Hosking GP, Edwards RHT. Central and peripheral fatigue in sustained maximum voluntary contractions of human quadriceps muscle. Clin Sci Mol Med. 1978;54:609–14.
Löscher WN, Cresswell AG, Thorstensson A. Excitatory drive to the alpha-motoneuron pool during a fatiguing submaximal contraction in man. J Physiol. 1996;491(1):271–80.
Sacco P, Thickbroom GW, Byrnes ML, Mastaglia FL. Changes in corticomotor excitability after fatiguing muscle contractions. Muscle Nerve. 2000;23(12):1840–6.
Bigland-Ritchie B, Johansson R, Lippold OC, Woods JJ. Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol. 1983;50(1):313–24.
Lepers R, Maffiuletti N, Rochette L, Brugniaux J, Millet GY. Neuromuscular fatigue during a long duration cycling exercise. J Appl Physiol. 2002;92:1487–93.
Place N, Lepers R, Deley G, Millet GY. Time course of neuromuscular alterations during prolonged running exercise. Med Sci Sports Exerc. 2004;36(8):1347–56.
Dorel S, Drouet JM, Couturier A, Champoux Y, Hug F. Changes of pedaling technique and muscle coordination during an exhaustive exercise. Med Sci Sports Exerc. 2009;41(6):1277–86.
Stewart D, Farina D, Shen C, Macaluso A. Muscle fibre conduction velocity during a 30-s Wingate anaerobic test. J Electromyogr Kinesiol. 2011;21(3):418–22.
Billaut F, Basset FA. Effect of different recovery patterns on repeated-sprint ability and neuromuscular responses. J Sports Sci. 2007;25(8):905–13.
Hautier CA, Arsac LM, Deghdegh K, Souquet J, Belli A, Lacour JR. Influence of fatigue on EMG/force ratio and cocontraction in cycling. Med Sci Sports Exerc. 2000;32(4):839–43.
Mendez-Villanueva A, Hamer P, Bishop D. Physical fitness and performance. Fatigue responses during repeated sprints matched for initial mechanical output. Med Sci Sports Exerc. 2007;39(12):2219–25.
Mendez-Villanueva A, Hamer P, Bishop D. Fatigue in repeated-sprint exercise is related to muscle power factors and reduced neuromuscular activity. Eur J Appl Physiol. 2008;103(4):411–9.
Racinais S, Bishop D, Denis R, Lattier G. Muscle deoxygenation and neural drive to the muscle during repeated sprint cycling. Med Sci Sports Exerc. 2007;39(2):268–74.
Bigland-Ritchie B, Johanson R, Lippold OC, Woods JJ. Contractile speed and EMG changes during fatigue of sustained maximal contractions. J Neurophysiol. 1983;50:313–24.
Theurel J, Crepin M, Foissac M, Temprado JJ. Effects of different pedalling techniques on muscle fatigue and mechanical efficiency during prolonged cycling. Scand J Med Sci Sports. 2012;22:714–21.
Amann M, Romer LM, Pegelow DF, Jacques AJ, Hess CJ, Dempsey JA. Effects of arterial oxygen content on peripheral locomotor muscle fatigue. J Appl Physiol. 2006;101:119–27.
Goodall S, Gonzalez-Alonso J, Ali L, Ross EZ, Romer LM. Supraspinal fatigue after normoxic and hypoxic exercise in humans. J Physiol. 2012;590(Pt 11):2767–82.
Farina D. Interpretation of the surface electromyogram in dynamic contractions. Exerc Sport Sci Rev. 2006;34(3):121–7.
Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet. 1985;1:1106–7.
Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD. Stimulation of the human motor cortex through the scalp. Exp Physiol. 1991;76:159–200.
Merton PA, Morton HB. Stimulation of the cerebral cortex in the intact human subject. Nature. 1980;285:227.
Day BL, Dressler D, Maertens de Noordhout A, Marsden CD, Nakashima K, Rothwell JC, et al. Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J Physiol. 1989;412:449–73.
Di Lazzaro V, Oliviero A, Pilato F, Saturno E, Dileone M, Mazzone P, et al. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol. 2004;115:255–66.
Taylor JL, Gandevia SC. Noninvasive stimulation of the human corticospinal tract. J Appl Physiol. 2004;96:1496–503.
Nielsen J, Petersen N. Is presynaptic inhibition distributed to corticospinal fibres in man? J Physiol. 1994;477(Pt 1):47–58.
Ugawa Y, Rothwell JC, Day BL, Thompson PD, Marsden CD. Percutaneous electrical stimulation of corticospinal pathways at the level of the pyramidal decussation in humans. Ann Neurol. 1991;29(4):418–27.
Taylor JL, Petersen NT, Butler JE, Gandevia SC. Interaction of transcranial magnetic stimulation and electrical transmastoid stimulation in human subjects. J Physiol. 2002;541(3):949–58.
Martin PG, Butler JE, Gandevia SC, Taylor JL. Non-invasive stimulation of human corticospinal axons innervating the leg muscles. J Neurophysiol. 2008;100(2):1080–6.
Sammi A, Wassermann EM, Hallett M. Post-exercise depression of motor evoked potentials as a function of exercise duration. Electroencephalogr Clin Neurophysiol. 1997;105:352–6.
Todd G, Taylor JL, Butler JE, Martin PG, Gorman RB, Gandevia SC. Use of motor cortex stimulation to measure simultaneously the changes in dynamic muscle properties and voluntary activation in human muscles. J Appl Physiol. 2007;102:1756–66.
Schmitz JP, van Dijk JP, Hilbers PA, Nicolay K, Jeneson JA, Stegeman DF. Unchanged muscle fiber conduction velocity relates to mild acidosis during exhaustive bicycling. Eur J Appl Physiol. 2012;112:1593–602.
Di Lazzaro V, Restuccia D, Oliviero A, Profice P, Ferrara L, Insola A, et al. Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J Physiol. 1998;508(Pt 2):625–33.
Carroll TJ, Riek S, Carson RG. Reliability of the input-output properties of the cortico-spinal pathway obtained from transcranial magnetic and electrical stimulation. J Neurosci Methods. 2001;112(2):193–202.
Martin PG, Gandevia SC, Taylor JL. Output of the human motoneuron pools to corticospinal inputs during voluntary contractions. J Neurophysiol. 2006;95:3512–8.
Ugawa Y, Terao Y, Hanajima R, Sakai K, Kanazawa I. Facilitatory effect of tonic voluntary contraction on responses to motor cortex stimulation. Electroencephalogr Clin Neurophysiol. 1995;97:451–4.
Burke D, Adams RW, Skuse NF. The effects of voluntary contraction on the H reflex of human limb muscles. Brain. 1989;112(2):417–33.
Oya T, Hoffman BW, Cresswell AG. Corticospinal-evoked responses in lower limb muscles during voluntary contractions at varying strengths. J Appl Physiol. 2008;105(5):1527–32.
Lee M, Gandevia SC, Carroll TJ. Cortical voluntary activation can be reliably measured in human wrist extensors using transcranial magnetic stimulation. Clin Neurophysiol. 2008;119(5):1130–8.
Todd G, Gorman RB, Gandevia SC. Measurement and reproducibility of strength and voluntary activation of lower-limb muscles. Muscle Nerve. 2004;29:834–42.
Sidhu SK, Bentley DJ, Carroll TJ. Cortical voluntary activation of the human knee extensors can be reliably estimated using transcranial magnetic stimulation. Muscle Nerve. 2009;39(2):186–96.
McNeil CJ, Giesebrecht S, Gandevia SC, Taylor JL. Behaviour of the motoneurone pool in a fatiguing submaximal contraction. J Physiol. 2011;589(Pt 14):3533–44.
Brasil-Neto JP, Pascual-Leone A, Valls-Sole J, Cammarota A, Cohen LG, Hallet M. Postexercise depression of motor evoked potentials: a measure of central nervous system fatigue. Exp Brain Res. 1993;93:181–4.
Zanette G, Bonato C, Polo A, Tinazzi M, Manganotti P, Fiaschi A. Long-lasting depression of motor-evoked potentials to transcranial magnetic stimulation following exercise. Exp Brain Res. 1995;107(1):80–6.
Gandevia SC, Petersen N, Butler JE, Taylor JL. Impaired response of human motoneurones to corticospinal stimulation after voluntary exercise. J Physiol. 1999;521(Pt 3):749–59.
McKay WB, Tuel SM, Sherwood AM, Stokić DS, Dimitrijević MR. Focal depression of cortical excitability induced by fatiguing muscle contraction: a transcranial magnetic stimulation study. Exp Brain Res. 1995;105(2):276–82.
Sammi A, Wassermann EM, Ikoma K, Mercuri B, Hallet M. Characterization of postexercise facilitation and depression of motor evoked potentials to transcranial magnetic stimulation. Neurology. 1996;46(5):1376–82.
Di Lazzaro V, Oliviero A, Tonali PA, Mazzone P, Insola A, Pilato F, et al. Direct demonstration of reduction of the output of the human motor cortex induced by a fatiguing muscle contraction. Exp Brain Res. 2003;149(4):535–8.
Mills KR, Thomson CC. Human muscle fatigue investigated by transcranial magnetic stimulation. Neuroreport. 1995;23(6):1966–8.
McKay WB, Stokie DS, Sherwood AM, Vrbova G, Dimitrijevic MR. Effect of fatiguing maximal voluntary contraction in excitatory and inhibitory responses elicited by transcranial magnetic motor cortex stimulation. Muscle Nerve. 1996;19:1017–24.
Taylor JL, Butler JE, Allen GM, Gandevia SC. Changes in motor cortical excitability during human muscle fatigue. J Physiol. 1996;490:519–28.
Smith JL, Butler JE, Martin PG, McBain RA, Taylor JL. Increased ventilation does not impair maximal voluntary contractions of the elbow flexors. J Appl Physiol. 2008;104:1674–82.
Löscher WN, Nordlund MM. Central fatigue and motor cortical excitability during repeated shortening and lengthening actions. Muscle Nerve. 2002;25:864–72.
Butler JE, Taylor JL, Gandevia SC. Responses of human motoneurons to corticospinal stimulation during maximal voluntary contractions and ischemia. J Neurosci. 2003;23(32):10224–30.
Martin PG, Smith JL, Butler JE, Gandevia SC, Taylor JL. Fatigue-sensitive afferents inhibit extensor but not flexor motoneurons in humans. J Neurosci. 2006;26(18):4796–802.
McNeil CJ, Martin PG, Gandevia SC, Taylor JL. The response to paired motor cortical stimuli is abolished at a spinal level during human muscle fatigue. J Physiol. 2009;587(Pt 23):5601–12.
Inghilleri M, Berardelli A, Cruccu G, Manfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol. 1993;466:521–34.
Siebner HR, Dressnandt J, Auer C, Conrad B. Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve. 1998;21(9):1209–12.
Todd G, Butler JE, Taylor JL, Gandevia SC. Hyperthermia: a failure of the motor cortex and the muscle. J Physiol. 2005;563(2):621–31.
Sacco P, Thickbroom GW, Thompson PD, Mastaglia FL. Changes in corticomotor excitation and inhibition during prolonged submaximal muscle contractions. Muscle Nerve. 1997;20:1158–66.
Andersen B, Westlund B, Krarup C. Failure of activation of spinal motorneurons after muscle fatigue in healthy subjects studies by transcranial magnetic stimulation. J Physiol. 2003;551(1):345–56.
Benwell NM, Mastaglia FL, Thickbroom GW. Paired-pulse rTMS at transynaptic intervals increases corticomotor excitability and reduces the rate of force loss during a fatiguing exercise of the hand. Exp Brain Res. 2006;175:626–32.
Benwell NM, Mastaglia FL, Thickbrrom GW. Differential changes in long-interval intracortical inhibition and silent period duration during fatiguing hand exercise. Exp Brain Res. 2007;179:255–62.
Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, et al. Corticocortical inhibition in human motor cortex. J Physiol. 1993;471(501–19).
Valls-Sole J, Pascual-Leone A, Wassermann EM, Hallett M. Human motor evoked responses to paired transcranial magnetic stimuli. Electroencephalogr Clin Neurophysiol. 1992;85(6):355–64.
Sanger TD, Garg RR, Chen R. Interactions between two different inhibitory systems in the human motor cortex. J Physiol. 2001;530(Pt 2):307–17.
Chen R. Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res. 2004;154(1):1–10.
Hanajima R, Ugawa Y, Terao Y, Sakai K, Furubayashi T, Machii K, et al. Paired-pulse magnetic stimulation of the human motor cortex: differences among I waves. J Physiol. 1998;509(Pt 2):607–18.
Wassermann EM, Samii A, Mercuri B, Ikoma K, Oddo D, Grill SE, et al. Responses to paired transcranial magnetic stimuli in resting, active, and recently activated muscles. Exp Brain Res. 1996;109(1):158–63.
Chen R, Lozano AM, Ashby P. Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Exp Brain Res. 1999;128(4):539–42.
Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol. 1999;517(Pt 2):591–7.
McNeil CJ, Giesebrecht S, Khan SI, Gandevia SC, Taylor JL. The reduction in human motoneurone responsiveness during muscle fatigue is not prevented by increased muscle spindle discharge. J Physiol. 2011;589(Pt 15):3731–8.
Davey NJ, Romaiguere P, Maskill DW, Ellaway PH. Suppression of voluntary motor activity revealed using transcranial magnetic stimulation of the motor cortex in man. J Physiol. 1994;477(2):223–35.
Butler JE, Larsen TS, Gandevia SC, Petersen NT. The nature of corticospinal paths driving human motoneurons during voluntary contractions. J Physiol. 2007;584(2):651–9.
Seifert T, Petersen NC. Changes in presumed motor cortical activity during fatiguing muscle contraction in humans. Acta Physiol (Oxf). 2010;199(3):317–26.
Ross EZ, Middleton N, Shave R, George K, Nowicky A. Corticomotor excitability contributes to neuromuscular fatigue following marathon running in man. Exp Physiol. 2007;92(2):417–26.
Verin E, Ross E, Demoule A, Hopkinson N, Nickol A, Fauroux B, et al. Effects of exhaustive incremental treadmill exercise on diaphragm and quadriceps motor potentials evoked by transcranial magnetic stimulation. J Appl Physiol. 2004;96:253–9.
Sidhu SK, Lauber B, Cresswell AG, Carroll TJ. Sustained cycling exercise increases intracortical inhibition. Med Sci Sports Exerc. 2012. doi:10.1249/MSS.0b013e31827b119c.
Rasmussen P, Nielsen J, Overgaard M, Krogh-Madsen R, Gjedde A, Secher NH, et al. Reduced muscle activation during exercise related to brain oxygenation and metabolism in humans. J Physiol. 2010;588(Pt 11):1985–95.
Martin PG, Weerakkody N, Gandevia SC, Taylor JL. Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans. J Physiol. 2008;586(5):1277–89.
Hilty L, Lutz K, Maurer K, Rodenkirch T, Spengler CM, Boutellier U, et al. Spinal opioid receptor-sensitive muscle afferents contribute to the fatigue-induced increase in intracortical inhibition in healthy humans. Exp Physiol. 2011;96(5):505–17.
Romer LM, Lovering AT, Haverkamp HC, Pegelow DF, Dempsey JA. Effect of inspiratory muscle work on peripheral fatigue on locomotor muscles in healthy humans. J Physiol. 2006;571(2):425–39.
Duchateau J, Hainault K. Electrical and mechanical failures during sustained and intermittent contractions in humans. J Appl Physiol. 1985;58(3):942–7.
Metzger JM, Moss RL. pH modulation of the kinetics of a Ca2+ sensitive cross-bridge state transition in mammalian single skeletal muscle fibres. J Physiol. 1990;428:751–64.
Westerblad H, Duty S, Allen DG. Intracellular calcium concentration during low- frequency fatigue in isolated single fibres of mouse skeletal muscle. J Appl Physiol. 1993;75:382–8.
Spriet LL, Soderland K, Bergstrom M, Hultman E. Anaerobic energy release in skeletal muscle during electrical stimulation in men. J Appl Physiol. 1987;62(2):611–5.
Spriet LL, Soderlund K, Bergstrom M, Hultman E. Skeletal muscle glycogenolysis, glycolysis, and pH during electrical stimulation in men. J Appl Physiol. 1987;62(2):616–21.
Amann M, Pegelow DF, Jacques AJ, Dempsey JA. Inspiratory muscle work in acute hypoxia influences locomotor muscle fatigue and exercise performance of healthy humans. Am J Physiol Regul Integr Comp Physiol. 2007;293(5):R2036–45.
Nybo L, Nielson OB. Hyperthermia and central fatigue during prolonged exercise in humans. J Appl Physiol. 2001;91:1055–60.
Gonzalez-Alonso J. Hyperthermia impairs brain, heart and muscle function in exercising humans. Sports Med. 2007;37(4–5):371–3.
Blomstrand E. Amino acids and central fatigue. Amino Acids. 2001;20(1):25–34.
Nybo L, Nielsen B, Blomstrand E, Moller K, Secher N. Neurohumoral responses during prolonged exercise in humans. J Appl Physiol. 2003;95(3):1125–31.
Blomstrand E, Møller K, Secher NH, Nybo L. Effect of carbohydrate ingestion on brain exchange of amino acids during sustained exercise in human subjects. Acta Physiol Scand. 2005;185(3):203–9.
Davis JM, Bailey SP. Possible mechanisms of central nervous system fatigue during exercise. Med Sci Sports Exerc. 1997;29(1):45–57.
Newsholme EA, Acworth IN, Bloomstrand E. Amino acids, brain neurotransmitters and a functional link between muscle and brain that is important in sustained exercise. In: Benzi G, editor. Advances in myochemistry. London: Libbey Eurotext; 1987, p. 127–33.
Blomstrand E. A role for branched-chain amino acids in reducing central fatigue. J Nutr. 2006;136:544S–7S.
Taylor BJ, Romer LM. Effect of expiratory muscle fatigue on exercise tolerance and locomotor muscle fatigue in healthy humans. J Appl Physiol. 2008;104:1442–51.
Harms CA, Babcock MA, McClaran SR, Pegelow DF, Nickele GA, Nelson WB, et al. Respiratory muscle work compromises leg blood flow during maximal exercise. J Appl Physiol. 1997;82(5):1573–83.
Amann M, Dempsey JA. The concept of peripheral locomotor muscle fatigue as a regulated variable. J Physiol. 2008;586:2029–30.
Noakes TD. Physiological models to understand exercise fatigue and the adaptations that predict or enhance athletic performance. Scand J Med Sci Sports. 2000;10:123–45.
Marcora SM, Staiano W, Manning V. Mental fatigue impairs physical performance in humans. J Appl Physiol. 2009;106(3):857–64.
Amann M, Eldridge MW, Lovering AT, Stickland MK, Pegelow DF, Dempsey JA. Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue. J Physiol. 2006;575:937–52.
Romer LM, Haverkamp HC, Amann M, Lovering AT, Pegelow DF, Dempsey JA. Effect of acute severe hypoxia on peripheral fatigue and endurance capacity in healthy humans. Am J Physiol Regul Integr Comp Physiol. 2007;292:R598–606.
Amann M, Proctor LT, Sebranek JJ, Eldridge MW, Pegelow DF, Dempsey JA. Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise. J Appl Physiol. 2008;105(6):1714–24.
Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol. 2009;587(Pt 1):271–83.
Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Group III and IV muscle afferents contribute to ventilatory and cardiovascular response to rhythmic exercise in humans. J Appl Physiol. 2010;109(4):966–76.
Neyroud D, Maffiuletti NA, Kayser B, Place N. Mechanisms of fatigue and task failure induced by sustained submaximal contractions. Med Sci Sports Exerc. 2012;44(7):1243–51.
Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S. Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scand J Med Sci Sports. 2012;22(3):381–91.
St Clair Gibson A, Baden DA, Lambert MI, Lamber EV, Harley YX, Hampson D, et al. The conscious perception of the sensation of fatigue. Sports Med. 2003;33:167–76.
Marcora SM, Bosio A, de Morree HM. Locomotor muscle fatigue increases cardiorespiratory responses and reduces performance during intense cycling exercise independently from metabolic stress. Am J Physiol Regul Integr Comp Physiol. 2008;294(3):R874–83.
Crewe H, Tucker R, Noakes TD. The rate of increase in rating of perceived exertion predicts the duration of exercise to fatigue at fixed power output in different environmental conditions. Eur J Appl Physiol. 2008;103:569–77.
Conflict of interest
No conflict of interest, financial or otherwise, is declared by the author.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sidhu, S.K., Cresswell, A.G. & Carroll, T.J. Corticospinal Responses to Sustained Locomotor Exercises: Moving Beyond Single-Joint Studies of Central Fatigue. Sports Med 43, 437–449 (2013). https://doi.org/10.1007/s40279-013-0020-6
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40279-013-0020-6