Skeletal Muscle Fatigue

Exercise Physiology > Fundamentals of Exercise Physiology > Metabolic Homeostasis

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Jane A. Kent‐Braun, Robert H. Fitts, Anita Christie

10.1002/cphy.c110029

Source: Volume 2, Issue 2, April 2012

Published online: April 2012

Full Article on Wiley Online Library

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Abstract

Skeletal muscle fatigue is defined as the fall of force or power in response to contractile activity. Both the mechanisms of fatigue and the modes used to elicit it vary tremendously. Conceptual and technological advances allow the examination of fatigue from the level of the single molecule to the intact organism. Evaluation of muscle fatigue in a wide range of disease states builds on our understanding of basic function by revealing the sources of dysfunction in response to disease. © 2012 American Physiological Society. Compr Physiol 2:997‐1044, 2012.

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	Figure 1. Pathway of force production. Schematic of the events leading to muscle activation. Beginning with 1. Cortical excitation, 2. Motor unit activation, 3. Depolarization of the sarcolemma and subsequent calcium release, 4. Actin‐Myosin binding, dephosphorylation of ATP and force generation. Figure courtesy of Damien M. Callahan, 2010.
	Figure 2. Schmatic model of actomyosin ATP hydrolysis reaction during contraction in skeletal muscle, where A is actin and M is the myosin head (myosin S1). Scheme is adapted from current models of ATP hydrolysis, and shows the conventional path (steps 1‐8), and the unconventional branched path (steps 9 and 10). Figure is a modification of the scheme reprinted, with permission 222, p. 23.
	Figure 3. Application of 10 mM caffeine in control (A) and during 2 successive fatigue runs (B and C). Bars below tension records in top panels indicate caffeine exposure during fatiguing stimulation; caffeine was applied after 22 fatiguing tetani (B) and when tetanic tension was depressed to 0.36 P₀ by 187 tetani (C). Fluorescence ratio and tension records from tetani elicited before application of caffeine (a) and in presence of caffeine (b) are shown in middle and bottom panels. Dashed lines represent resting ratio in control prefatigued fiber; stimulation periods are displayed below tension records. Note that tetanic ratio increase induced by caffeine in late fatigue was accompanied by a substantially enhanced tension production, whereas tension was not markedly affected by increased ratios in the other two states. Reprinted, with permission, from 363, p. 625.
	Figure 4. A plot of tetanic force versus intracellular calcium ([Ca²⁺]_i) summarizing the mechanisms involved in the reduction of isometric force in fatigue: 1 reduced maximal force; 2 reduced myofibrillar Ca²⁺ sensitivity; and 3 reduced tetanic [Ca²⁺]_i. The normal pattern during fatigue is schematically illustrated by the dashed line. The arrow shows the direction of time. Reprinted, with permission, from 8, p. 1101.
	Figure 5. (A) Electron micrograph (EM) showing a myofilament from a rat flexor digitorum brevis muscle fiber. The arrows show the position of the triads (T‐tubule plus the sarcoplasmic reticulum terminal cisternae) at the A‐I junctions providing two triad junctions for each sarcomere. (B) A schematic representation of E‐C coupling showing a representative sarcolemma action potential (AP) at rest (no. 1) and following fatigue (no. 2) with resting potentials of –80 and –70 mv, and action potential amplitudes of 84 and 73 mv, respectively. It is unknown how fatigue affects the AP in the depths of the T‐tubule. The displayed AP record (no. 3) showing a resting potential of –60 mv and action potential amplitude of 58 mv (i.e., spike potential reaching –2 mv) represents hypothesized rather than real values for a T‐tubular AP. The SR Ca²⁺ release channel (ryanodine receptor) is shown as no. 4, while nos. 5 and 6 represent the sarcolemma Na⁺‐K⁺ pump and the SR ATPase pump, respectively. The question mark (?) indicates that the composition of the extracellular fluid in the depths of the T‐tubule in a fatigued muscle is currently unknown. The white line to the left of each AP represents the zero overshoot potentials. Figure modified, with permission, from that originally published in Fitts, R.H. Chapter 26, Cellular, molecular, and metabolic basis of muscle fatigue. In: Handbook of Physiology, Section 12, Exercise: Regulation and Integration of Multiple Systems. Edited by L.B. Rowell and J.T. Shepherd. New York: Oxford University Press, pp. 1151‐1183, 1995. The AP records are data acquired, with permission, by Metzger and Fitts 258. The EM in part A was provided by DA Riley.
	Figure 6. Slowing of relaxation during fatiguing stimulation of a single fiber isolated from the mouse flexor brevis muscle. A typical fatigue curve is shown in the upper part. Each tetanus appears as a vertical line. The lower part displays the relaxation of the tetani indicated above the fatigue curve (a‐d). The tension bar refers to the upper part only. Reprinted, with permission, from 366, p. 326.
	Figure 7. Sites of stimulation for assessing neuromuscular function. (1) Transcranial magnetic stimulation (TMS) is applied to the motor cortex, and is optimized to activate the muscle of interest. The muscular response to that stimulation is known as the motor‐evoked potential (MEP). TMS is used to assess cortical excitability and inhibition. (2) Electrical stimulation is applied in the cervicomedullary region to activate the corticospinal tract at a subcortical level. The muscular response is known as the cervicomedullary motor‐evoked potential (CMEP). Comparisons between the MEP and CMEP allow for the localization of changes in excitability to a cortical or subcortical level. (3) Low‐intensity electrical stimulation of the peripheral nerve preferentially activates the Ia sensory fibers, which synapse with the α‐motoneuron. The muscular response is known as the Hoffmann reflex (H‐reflex), and is used to assess spinal excitability and inhibition. (4) Higher‐intensity stimulation of the peripheral nerve directly activates the α‐motoneuron, evoking a motor response (m‐wave) from the muscle. The m‐wave is used to assess peripheral excitability of the muscle membrane and transmission at the neuromuscular junction. All evoked responses are recorded via EMG electrodes placed on the muscle.
	Figure 8. Changes in motor‐evoked potential (MEP) and cervicomedullary motor‐evoked potential (CMEP) for an individual subject, during a sustained 2‐min maximal voluntary contraction (MVC) of the elbow flexors. MEP (left) and CMEP (right) responses were recorede at baseline (control), throughout the 2‐min sustained MVC (exercise) and during recovery from the biceps brachii. For this individual, the MEP and CMEP responses were both abolished approximately 30 s into the 2‐min maximal contraction, and both recovered to baseline values following the contraction. The similar changes in the MEP and CMEP suggest that the observed inhibition during the fatiguing contraction was primarily due to spinal mechanisms. Reprinted, with permission, from 253, p. 5604.
	Figure 9. Change in the H‐reflex during a fatiguing task where participants were asked to maintain isometric elbow flexion force, or arm postion while supporting a load. H‐relfexes were evoked by stimulation of the brachial plexus and were recorded from the biceps brachii. (A) Sample H‐reflex recordings from one subject at the beginning, middle, and end of the force (left) and position (right) tasks. (B) Group data (mean ± SE) showing changes in H‐reflex amplitude during the force (•) and position (○) tasks. Data are expressed as a percentage of the H‐reflex amplitude in the absence of muscle fatigue. Reprinted, with permission, from 209, p. 1101.
	Figure 10. Mean motor unit firing rates recorded from the brachioradiailis during sustained isometric contractions at 25% MVC. Motor unit firing rates were reduced by ∼20% at the middle of the sustained contraction, and by ∼30% at task failure. Reprinted, with permission, from 54, p. 9.
	Figure 11. Contractile properties and excitation‐contraction coupling. The tibialis anterior muscle was held ischaemic and was stimulated 20 times at 50 Hz for 1.6 s with 1.6 s rest. (A) Peak force, expressed as a percentage of the initial isometric contraction (Po) decreased over the 20 stimulated contractions. (B) The rate of force relaxtion, expressed as the half‐time of force decay, increased over the 20 stimulated contractions, indicating slowed contractile characteristics of the muscle. (C) The slowed rate of force relaxation was related to the accumulation of [H⁺] in the muscle Reprinted, with permission, from 195, pp. 4332, 4334.
	Figure 12. Metabolic inhibition of contraction. (A) Cross‐bridge: Actin filament velocities along myosin molecules (V_actin) versus ATP. V_actin from in vitro motility assays as a function of [ATP]. Squares and circles represent data for pH 7.4 and pH 6.4, respectively. Each data set was fit to a Michaelis‐Menten equation, yielding values for maximal velocity (V_max, 6.4 and 4.1 μm/s at pH 7.4 and 6.4, respectively) and K_m (83 and 850 μM at pH 7.4 and 6.4, respectively). [Reprinted, with permission, from 117.] (B) Single fiber: Effects of pH (left) and Pi (right) on peak single fiber power production [Reprinted with permission from 89] (C) In vivo: intermittent, submaximal contractions. Relationship between fatigue and [H₂PO₄⁻] during incremental, isometric contractions in the ankle dorsiflexor muscles of young men. [Reprinted, with permission, from 205.] (D) In vivo: sustained MVC. Again, strong linear associations were observed between fatigue and [H₂PO₄⁻], in this case during intermittent maximal contractions with free‐flow (FF, •) and ischemia by cuff occlusion (ISC, ○). Reprinted, with permission, from 216.
	Figure 13. Changes in force, electromyogram, and metabolites during a maximal voluntary dorsiflexion contraction sustained for 4 min. (A) Fall of force. (B) Change in surface EMG. (C) Changes in PCr, Pi, and H₂PO₄⁻. (D) Changes in pH. Note the pronounced fatigue, with little change in surface electromyography (EMG), but significant alterations to intracellular metabolites and pH. Reprinted, with permission, from 201, pp. 59, 60.
	Figure 14. Effect of modified sensory feedback on electromyography and power output during a 5‐km cycling time trial. Trained cylists performed a 5‐km time trial on three separate occasions: (1) placebo condition, with interspineous ligament injection of saline (5K_Plac); (2) fentanyl condition, with intrathecal fentanyl injection, to block sensory feedback from the muscles (5K_fent); and (3) control condition, with no injection (5K_Ctrl). (A) Group mean integrated electromyography (iEMG) of vastus lateralis during the three conditions, normalized to the iEMG obtained from preexercise MVC manoeuvres on each occasion. The iEMG was not different across the three conditions at baseline, but was significantly higher during the first 2.5 km of the time trial in the 5K_fen condition, with no difference in the second 2.5 km. (B) Group mean power output was significantly higher in the 5K_fen condition over the first 2.5 km, and was significantly lower over the last 2.5 km. This “overshoot” of electromyographic activity and power output during the first 2.5 km of the time trial led to greater fatigue in the 5K_fen condition. Reprinted, with permission, from 17, p. 276.
	Figure 15. Effect of joint angle on fatigue of the knee extensor muscles during a submaximal sustained contraction. (A) At baseline (prefatigue), mean (± SE) maximal voluntary force was greater for the long quadriceps muscle length (knee angle = 75°) compared with the short muscle length (knee angle = 35°). (B) The mean (± SE) endurance time for a sustained contraction at 20% MVC longer at 35° than at 75°. (C) The mean (± SE) voluntary activation was reduced following the fatiguing contraction at both 35° and 75°, with no difference in the degree of reduction between the two joint angles. Reprinted, with permission, from 292, p. 431, 432.
	Figure 16. Endurance time and its relation to target force level during a sustained submaximal contraction of the first dorsal interosseous in men and women. Men and women were matched for maximal isometric force production. (A) Men and women matched for MVC force showed no difference in endurance time during contractions maintained at 20%, 35%, or 60% MVC. (B) Endurance times for men (closed symbols) and women (open symbols) across three contraction intensities (20%, 35%, and 60% MVC) was exponentially related to the absolute target force level, suggesting a relationship between target force level and muscle fatigue. Reprinted, with permission, from 179, p. 2691
	Figure 17. Sex differences were abolished by ischemia during and following intermittent MVCs. (A) Voluntary fatigue (MVIC force, % initial) and (B) central activation ratio (CAR) for men and women in free‐flow (FF, solid symbols) and ischemic (I, open symbols) conditions. Values are means ± SE. Hatched bar indicates contraction period. For all four experimental groups, force was lower than baseline from the first minute of fatigue until the end of fatigue. After 2 min of recovery, MVIC force was still reduced for all groups, except for the women in the FF condition. At end of the I protocol, CAR was reduced relative to baseline in both men and women. During the FF protocol, only the men exhibited a reduction in CAR. In all groups, CAR was fully recovered after 10 min. For a given time point, s = effect of sex, c = effect of condition, sc = sex X condition interaction. *Difference between men and women in the FF but not I condition. Reprinted, with permission, from 307, p. 2418.
	Figure 18. ATP Flux during a 60‐s maximal voluntary contraction in young (top) and older (bottom) adults. Relative contributions to ATP production from nonoxidative glycolysis (black bars), oxidative phosphorylation (gray bars), and the creatine kinase reaction (hatched bars) are shown. Oxidative phosphorylation contributed relatively more to ATP flux in older compared with young group. Reprinted, with permission, from 215, p. 1741
	Figure 19. Effect of age on the age‐related difference in fatigue‐induced reduction of power in the ankle dorsiflexor muscles. Mean (±SE) isotonic power, over 25 maximal contractions is shown for young (26 years, solid line), old (64 years, dotted line), and very old men (84 years, dashed line). Power is averaged over blocks of five contractions and is expressed relative to the average power of the first five contractions. Mean isotonic power declined in all age groups, but very old men had a significantly greater loss than young men. Reprinted, with permission, from 255, p. 627.
	Figure 20. Interaction between contraction intensity and endurance time. (A) Endurance time of ten subjects for a fatiguing contraction at 65% MVC target force and (B) 20% MVC target force before (○) and immediately after (•) immobilization, and after 2 weeks of recovery (∇). Most subjects showed increased endurance time for both fatigue tasks after immobilization. Reprinted, with permission, from 385, p. 578.
	Figure 21. Fatigue resistance in spinal cord injury; changes in force parameters during and after fatigue. Single subject and group data showing changes (% initial) in peak force (A and E), force time integral (B and F), half‐relaxation time (C and G), and time to peak force (D and H) during the fatigue protocol (A‐D), and for maximal force (50 Hz), doublet force, and twitch force measured before and after fatigue (E‐H; data are normalized to prefatigue values). Data are shown for control (open symbols and bars) and contraction experiments (filled symbols and bars). Reprinted, with permission, from 50, p. 580.
	Figure 22. Blood flow in spinal cord injury and controls. Representative example of the blood flow response before, during, and after exercise at a low workload for a spinal cord injury (SCI) and able‐bodied individual. Electrical stimulation occurred between −180 and 0 s. Reprinted, with permission, from 277, p. 479.
	Figure 23. Fatigue in persons with multiple sclerosis. Changes in isometric force parameters during a series of fatiguing contractions. Force (A), maximal rate of force rise (B), and half‐relaxation time (C) are expressed as percentages of prefatigue values (= 100%). Mean data ± SEM are shown for every fifth contraction for magnetic stimulation (MS) patients (open circles; n = 13) and control subjects (closed squares; n = 15). Reprinted, with permission, from 82, p. 1538.
	Figure 24. Interactions between peripheral metabolic changes and cardiovascular function during fatigue in control and multiple sclerosis groups. Changes in mean arterial pressure (MAP), heart rate (HR), and rating of perceived exertion (RPE) during sustained isometric dorsiflexion exercise (left). Change in MAP from baseline (A, left) was less in MS versus control throughout exercise. Change in HR from baseline (B, left) and RPE (C, left) were similar in MS and control subjects. Changes in Pi and intracellular pH, expressed as a percentage of endurance time for both groups (right). Note the smaller metabolic perturbation in the MS group, which suggested an appropriate response in MAP. Reprinted, with permission, from 272, p. 875.

Figure 1.

Pathway of force production. Schematic of the events leading to muscle activation. Beginning with 1. Cortical excitation, 2. Motor unit activation, 3. Depolarization of the sarcolemma and subsequent calcium release, 4. Actin‐Myosin binding, dephosphorylation of ATP and force generation.

Figure courtesy of Damien M. Callahan, 2010.

Figure 2.

Schmatic model of actomyosin ATP hydrolysis reaction during contraction in skeletal muscle, where A is actin and M is the myosin head (myosin S1). Scheme is adapted from current models of ATP hydrolysis, and shows the conventional path (steps 1‐8), and the unconventional branched path (steps 9 and 10).

Figure is a modification of the scheme reprinted, with permission 222, p. 23.

Figure 3.

Application of 10 mM caffeine in control (A) and during 2 successive fatigue runs (B and C). Bars below tension records in top panels indicate caffeine exposure during fatiguing stimulation; caffeine was applied after 22 fatiguing tetani (B) and when tetanic tension was depressed to 0.36 P₀ by 187 tetani (C). Fluorescence ratio and tension records from tetani elicited before application of caffeine (a) and in presence of caffeine (b) are shown in middle and bottom panels. Dashed lines represent resting ratio in control prefatigued fiber; stimulation periods are displayed below tension records. Note that tetanic ratio increase induced by caffeine in late fatigue was accompanied by a substantially enhanced tension production, whereas tension was not markedly affected by increased ratios in the other two states.

Reprinted, with permission, from 363, p. 625.

Figure 4.

A plot of tetanic force versus intracellular calcium ([Ca²⁺]_i) summarizing the mechanisms involved in the reduction of isometric force in fatigue: 1 reduced maximal force; 2 reduced myofibrillar Ca²⁺ sensitivity; and 3 reduced tetanic [Ca²⁺]_i. The normal pattern during fatigue is schematically illustrated by the dashed line. The arrow shows the direction of time.

Reprinted, with permission, from 8, p. 1101.

Figure 5.

(A) Electron micrograph (EM) showing a myofilament from a rat flexor digitorum brevis muscle fiber. The arrows show the position of the triads (T‐tubule plus the sarcoplasmic reticulum terminal cisternae) at the A‐I junctions providing two triad junctions for each sarcomere. (B) A schematic representation of E‐C coupling showing a representative sarcolemma action potential (AP) at rest (no. 1) and following fatigue (no. 2) with resting potentials of –80 and –70 mv, and action potential amplitudes of 84 and 73 mv, respectively. It is unknown how fatigue affects the AP in the depths of the T‐tubule. The displayed AP record (no. 3) showing a resting potential of –60 mv and action potential amplitude of 58 mv (i.e., spike potential reaching –2 mv) represents hypothesized rather than real values for a T‐tubular AP. The SR Ca²⁺ release channel (ryanodine receptor) is shown as no. 4, while nos. 5 and 6 represent the sarcolemma Na⁺‐K⁺ pump and the SR ATPase pump, respectively. The question mark (?) indicates that the composition of the extracellular fluid in the depths of the T‐tubule in a fatigued muscle is currently unknown. The white line to the left of each AP represents the zero overshoot potentials.

Figure modified, with permission, from that originally published in Fitts, R.H. Chapter 26, Cellular, molecular, and metabolic basis of muscle fatigue. In: Handbook of Physiology, Section 12, Exercise: Regulation and Integration of Multiple Systems. Edited by L.B. Rowell and J.T. Shepherd. New York: Oxford University Press, pp. 1151‐1183, 1995. The AP records are data acquired, with permission, by Metzger and Fitts 258. The EM in part A was provided by DA Riley.

Figure 6.

Slowing of relaxation during fatiguing stimulation of a single fiber isolated from the mouse flexor brevis muscle. A typical fatigue curve is shown in the upper part. Each tetanus appears as a vertical line. The lower part displays the relaxation of the tetani indicated above the fatigue curve (a‐d). The tension bar refers to the upper part only.

Reprinted, with permission, from 366, p. 326.

Figure 7.

Sites of stimulation for assessing neuromuscular function. (1) Transcranial magnetic stimulation (TMS) is applied to the motor cortex, and is optimized to activate the muscle of interest. The muscular response to that stimulation is known as the motor‐evoked potential (MEP). TMS is used to assess cortical excitability and inhibition. (2) Electrical stimulation is applied in the cervicomedullary region to activate the corticospinal tract at a subcortical level. The muscular response is known as the cervicomedullary motor‐evoked potential (CMEP). Comparisons between the MEP and CMEP allow for the localization of changes in excitability to a cortical or subcortical level. (3) Low‐intensity electrical stimulation of the peripheral nerve preferentially activates the Ia sensory fibers, which synapse with the α‐motoneuron. The muscular response is known as the Hoffmann reflex (H‐reflex), and is used to assess spinal excitability and inhibition. (4) Higher‐intensity stimulation of the peripheral nerve directly activates the α‐motoneuron, evoking a motor response (m‐wave) from the muscle. The m‐wave is used to assess peripheral excitability of the muscle membrane and transmission at the neuromuscular junction. All evoked responses are recorded via EMG electrodes placed on the muscle.

Figure 8.

Changes in motor‐evoked potential (MEP) and cervicomedullary motor‐evoked potential (CMEP) for an individual subject, during a sustained 2‐min maximal voluntary contraction (MVC) of the elbow flexors. MEP (left) and CMEP (right) responses were recorede at baseline (control), throughout the 2‐min sustained MVC (exercise) and during recovery from the biceps brachii. For this individual, the MEP and CMEP responses were both abolished approximately 30 s into the 2‐min maximal contraction, and both recovered to baseline values following the contraction. The similar changes in the MEP and CMEP suggest that the observed inhibition during the fatiguing contraction was primarily due to spinal mechanisms.

Reprinted, with permission, from 253, p. 5604.

Figure 9.

Change in the H‐reflex during a fatiguing task where participants were asked to maintain isometric elbow flexion force, or arm postion while supporting a load. H‐relfexes were evoked by stimulation of the brachial plexus and were recorded from the biceps brachii. (A) Sample H‐reflex recordings from one subject at the beginning, middle, and end of the force (left) and position (right) tasks. (B) Group data (mean ± SE) showing changes in H‐reflex amplitude during the force (•) and position (○) tasks. Data are expressed as a percentage of the H‐reflex amplitude in the absence of muscle fatigue.

Reprinted, with permission, from 209, p. 1101.

Figure 10.

Mean motor unit firing rates recorded from the brachioradiailis during sustained isometric contractions at 25% MVC. Motor unit firing rates were reduced by ∼20% at the middle of the sustained contraction, and by ∼30% at task failure.

Reprinted, with permission, from 54, p. 9.

Figure 11.

Contractile properties and excitation‐contraction coupling. The tibialis anterior muscle was held ischaemic and was stimulated 20 times at 50 Hz for 1.6 s with 1.6 s rest. (A) Peak force, expressed as a percentage of the initial isometric contraction (Po) decreased over the 20 stimulated contractions. (B) The rate of force relaxtion, expressed as the half‐time of force decay, increased over the 20 stimulated contractions, indicating slowed contractile characteristics of the muscle. (C) The slowed rate of force relaxation was related to the accumulation of [H⁺] in the muscle

Reprinted, with permission, from 195, pp. 4332, 4334.

Figure 12.

Metabolic inhibition of contraction. (A) Cross‐bridge: Actin filament velocities along myosin molecules (V_actin) versus ATP. V_actin from in vitro motility assays as a function of [ATP]. Squares and circles represent data for pH 7.4 and pH 6.4, respectively. Each data set was fit to a Michaelis‐Menten equation, yielding values for maximal velocity (V_max, 6.4 and 4.1 μm/s at pH 7.4 and 6.4, respectively) and K_m (83 and 850 μM at pH 7.4 and 6.4, respectively).

[Reprinted, with permission, from 117.] (B) Single fiber: Effects of pH (left) and Pi (right) on peak single fiber power production [Reprinted with permission from 89] (C) In vivo: intermittent, submaximal contractions. Relationship between fatigue and [H₂PO₄⁻] during incremental, isometric contractions in the ankle dorsiflexor muscles of young men. [Reprinted, with permission, from 205.] (D) In vivo: sustained MVC. Again, strong linear associations were observed between fatigue and [H₂PO₄⁻], in this case during intermittent maximal contractions with free‐flow (FF, •) and ischemia by cuff occlusion (ISC, ○). Reprinted, with permission, from 216.

Figure 13.

Changes in force, electromyogram, and metabolites during a maximal voluntary dorsiflexion contraction sustained for 4 min. (A) Fall of force. (B) Change in surface EMG. (C) Changes in PCr, Pi, and H₂PO₄⁻. (D) Changes in pH. Note the pronounced fatigue, with little change in surface electromyography (EMG), but significant alterations to intracellular metabolites and pH.

Reprinted, with permission, from 201, pp. 59, 60.

Figure 14.

Effect of modified sensory feedback on electromyography and power output during a 5‐km cycling time trial. Trained cylists performed a 5‐km time trial on three separate occasions: (1) placebo condition, with interspineous ligament injection of saline (5K_Plac); (2) fentanyl condition, with intrathecal fentanyl injection, to block sensory feedback from the muscles (5K_fent); and (3) control condition, with no injection (5K_Ctrl). (A) Group mean integrated electromyography (iEMG) of vastus lateralis during the three conditions, normalized to the iEMG obtained from preexercise MVC manoeuvres on each occasion. The iEMG was not different across the three conditions at baseline, but was significantly higher during the first 2.5 km of the time trial in the 5K_fen condition, with no difference in the second 2.5 km. (B) Group mean power output was significantly higher in the 5K_fen condition over the first 2.5 km, and was significantly lower over the last 2.5 km. This “overshoot” of electromyographic activity and power output during the first 2.5 km of the time trial led to greater fatigue in the 5K_fen condition.

Reprinted, with permission, from 17, p. 276.

Figure 15.

Effect of joint angle on fatigue of the knee extensor muscles during a submaximal sustained contraction. (A) At baseline (prefatigue), mean (± SE) maximal voluntary force was greater for the long quadriceps muscle length (knee angle = 75°) compared with the short muscle length (knee angle = 35°). (B) The mean (± SE) endurance time for a sustained contraction at 20% MVC longer at 35° than at 75°. (C) The mean (± SE) voluntary activation was reduced following the fatiguing contraction at both 35° and 75°, with no difference in the degree of reduction between the two joint angles.

Reprinted, with permission, from 292, p. 431, 432.

Figure 16.

Endurance time and its relation to target force level during a sustained submaximal contraction of the first dorsal interosseous in men and women. Men and women were matched for maximal isometric force production. (A) Men and women matched for MVC force showed no difference in endurance time during contractions maintained at 20%, 35%, or 60% MVC. (B) Endurance times for men (closed symbols) and women (open symbols) across three contraction intensities (20%, 35%, and 60% MVC) was exponentially related to the absolute target force level, suggesting a relationship between target force level and muscle fatigue.

Reprinted, with permission, from 179, p. 2691

Figure 17.

Sex differences were abolished by ischemia during and following intermittent MVCs. (A) Voluntary fatigue (MVIC force, % initial) and (B) central activation ratio (CAR) for men and women in free‐flow (FF, solid symbols) and ischemic (I, open symbols) conditions. Values are means ± SE. Hatched bar indicates contraction period. For all four experimental groups, force was lower than baseline from the first minute of fatigue until the end of fatigue. After 2 min of recovery, MVIC force was still reduced for all groups, except for the women in the FF condition. At end of the I protocol, CAR was reduced relative to baseline in both men and women. During the FF protocol, only the men exhibited a reduction in CAR. In all groups, CAR was fully recovered after 10 min. For a given time point, s = effect of sex, c = effect of condition, sc = sex X condition interaction. *Difference between men and women in the FF but not I condition.

Reprinted, with permission, from 307, p. 2418.

Figure 18.

ATP Flux during a 60‐s maximal voluntary contraction in young (top) and older (bottom) adults. Relative contributions to ATP production from nonoxidative glycolysis (black bars), oxidative phosphorylation (gray bars), and the creatine kinase reaction (hatched bars) are shown. Oxidative phosphorylation contributed relatively more to ATP flux in older compared with young group.

Reprinted, with permission, from 215, p. 1741

Figure 19.

Effect of age on the age‐related difference in fatigue‐induced reduction of power in the ankle dorsiflexor muscles. Mean (±SE) isotonic power, over 25 maximal contractions is shown for young (26 years, solid line), old (64 years, dotted line), and very old men (84 years, dashed line). Power is averaged over blocks of five contractions and is expressed relative to the average power of the first five contractions. Mean isotonic power declined in all age groups, but very old men had a significantly greater loss than young men.

Reprinted, with permission, from 255, p. 627.

Figure 20.

Interaction between contraction intensity and endurance time. (A) Endurance time of ten subjects for a fatiguing contraction at 65% MVC target force and (B) 20% MVC target force before (○) and immediately after (•) immobilization, and after 2 weeks of recovery (∇). Most subjects showed increased endurance time for both fatigue tasks after immobilization.

Reprinted, with permission, from 385, p. 578.

Figure 21.

Fatigue resistance in spinal cord injury; changes in force parameters during and after fatigue. Single subject and group data showing changes (% initial) in peak force (A and E), force time integral (B and F), half‐relaxation time (C and G), and time to peak force (D and H) during the fatigue protocol (A‐D), and for maximal force (50 Hz), doublet force, and twitch force measured before and after fatigue (E‐H; data are normalized to prefatigue values). Data are shown for control (open symbols and bars) and contraction experiments (filled symbols and bars).

Reprinted, with permission, from 50, p. 580.

Figure 22.

Blood flow in spinal cord injury and controls. Representative example of the blood flow response before, during, and after exercise at a low workload for a spinal cord injury (SCI) and able‐bodied individual. Electrical stimulation occurred between −180 and 0 s.

Reprinted, with permission, from 277, p. 479.

Figure 23.

Fatigue in persons with multiple sclerosis. Changes in isometric force parameters during a series of fatiguing contractions. Force (A), maximal rate of force rise (B), and half‐relaxation time (C) are expressed as percentages of prefatigue values (= 100%). Mean data ± SEM are shown for every fifth contraction for magnetic stimulation (MS) patients (open circles; n = 13) and control subjects (closed squares; n = 15).

Reprinted, with permission, from 82, p. 1538.

Figure 24.

Interactions between peripheral metabolic changes and cardiovascular function during fatigue in control and multiple sclerosis groups. Changes in mean arterial pressure (MAP), heart rate (HR), and rating of perceived exertion (RPE) during sustained isometric dorsiflexion exercise (left). Change in MAP from baseline (A, left) was less in MS versus control throughout exercise. Change in HR from baseline (B, left) and RPE (C, left) were similar in MS and control subjects. Changes in Pi and intracellular pH, expressed as a percentage of endurance time for both groups (right). Note the smaller metabolic perturbation in the MS group, which suggested an appropriate response in MAP.

Reprinted, with permission, from 272, p. 875.

References
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EXPANDED BIBLIOGRAPHY: SKELETAL MUSCLE FATIGUE

(relevant publications, 1995- March, 2010)

This review encompasses the body of literature available through the PubMed database, with major focus on studies published after 1995. Our initial search using keywords “skeletal”, “muscle”, and “fatigue” yielded 3,045 peer-reviewed publications. This list was reviewed and narrowed to those papers that focused on the topic of muscle fatigue as discussed here. Clearly, the scope of work covered in the literature exceeds the capacity of this review. However, because we anticipate that many of these studies will be of interest to the reader, an expanded bibliography is provided here. Of these 928 papers, 183 were reviews; these are listed separately, at the beginning of this expanded bibliography.

Exclusions: The following topics are beyond the scope of this work, but are recommended as further avenues of investigation. Studies of back and shoulder fatigue, case studies, pilot studies, ergonomics, mathematical modeling of fatigue, athletic performance, effects of muscle fatigue on other factors (e.g., postural control), fatigue and functional electrical stimulation (FES), studies of pelvic floor fatigue, studies of muscle damage, techniques and models for the study of fatigue, studies that do not include a measure of muscle force, power or velocity as the index of fatigue or endurance.

Review Papers

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Allen DG, Kabbara AA, Westerblad H. Muscle fatigue: the role of intracellular calcium stores. Can J Appl Physiol. 2002 Feb;27(1):83-96. PMID: 11880693.

Allen DG, Lamb GD, Westerblad H. Impaired calcium release during fatigue. J Appl Physiol. 2008 Jan;104(1):296-305. Epub 2007 Oct 25. PMID: 17962573.

Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev. 2008 Jan;88(1):287-332. PMID: 18195089.

Allen DG, Westerblad H. Role of phosphate and calcium stores in muscle fatigue. J Physiol. 2001 Nov 1;536(Pt 3):657-65. PMID: 11691862; PubMed Central PMCID: PMC2278904.

Allen DG. Skeletal muscle function: role of ionic changes in fatigue, damage and disease. Clin Exp Pharmacol Physiol. 2004 Aug;31(8):485-93. PMID: 15298539.

Allman BL, Rice CL. Neuromuscular fatigue and aging: central and peripheral factors. Muscle Nerve. 2002 Jun;25(6):785-96. PMID: 12115966.

Amann M, Calbet JA. Convective oxygen transport and fatigue. J Appl Physiol. 2008 Mar;104(3):861-70. Epub 2007 Oct 25. PMID: 17962570.

Ament W, Verkerke GJ. Exercise and fatigue. Sports Med. 2009;39(5):389-422. PMID: 19402743.

Ameredes BT. Viewpoint: Fatigue mechanisms determining exercise performance: integrative physiology is systems physiology. J Appl Physiol. 2008 May;104(5):1545. PMID: 18504823.

Astra LI, Stephenson LW. Skeletal muscle as a myocardial substitute. Proc Soc Exp Biol Med. 2000 Jul;224(3):133-40. PMID: 10865227.

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Barat M, Dehail P, de Seze M. Fatigue after spinal cord injury. Ann Readapt Med Phys. 2006 Jul;49(6):277-82, 365-9. Epub 2006 Apr 25. Review. English, French. PubMed PMID: 16716437.

Berchtold MW, Brinkmeier H, Müntener M. Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease. Physiol Rev. 2000 Jul;80(3):1215-65. Review. PubMed PMID: 10893434.

Biering-Sørensen B, Kristensen IB, Kjaer M, Biering-Sørensen F. Muscle after spinal cord injury. Muscle Nerve. 2009 Oct;40(4):499-519. Review. PubMed PMID: 19705475.

Binder-Macleod SA. Variable-frequency stimulation patterns for the optimization of force during muscle fatigue. Muscle wisdom and the catch-like property. Adv Exp Med Biol. 1995;384:227-40. Review. PubMed PMID: 8585453.

Brown WF, Doherty TJ, Chan M, Andres A, Provost SM. Human motor units in health and disease. Muscle Nerve Suppl. 2000;9:S7-18. Review. PubMed PMID: 11135279.

Bruton JD, Lännergren J, Westerblad H. Mechanisms underlying the slow recovery of force after fatigue: importance of intracellular calcium. Acta Physiol Scand. 1998 Mar;162(3):285-93. Review. PubMed PMID: 9578374.

Burnley M, Jones AM. Viewpoint: Fatigue mechanisms determining exercise performance: integrative physiology is systems physiology. J Appl Physiol. 2008 May;104(5):1545-6. PubMed PMID: 18504821.

Cairns SP, Lindinger MI. Do multiple ionic interactions contribute to skeletal muscle fatigue? J Physiol. 2008 Sep 1;586(Pt 17):4039-54. Epub 2008 Jun 26. Review. PubMed PMID: 18591187; PubMed Central PMCID: PMC2652190.

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Casey A, Greenhaff PL. Does dietary creatine supplementation play a role in skeletal muscle metabolism and performance? Am J Clin Nutr. 2000 Aug;72(2 Suppl):607S-17S. Review. PubMed PMID: 10919967.

Chariot P, Bignani O. Skeletal muscle disorders associated with selenium deficiency in humans. Muscle Nerve. 2003 Jun;27(6):662-8. Review. PubMed PMID: 12766976.

Cheung SS. The mind-body connection remains key to understanding fatigue. J Appl Physiol. 2009 Aug;107(2):633-4; author reply 635. PubMed PMID: 19731450.

Clark AL, Poole-Wilson PA, Coats AJ. Exercise limitation in chronic heart failure: central role of the periphery. J Am Coll Cardiol. 1996 Nov 1;28(5):1092-102. Review. PubMed PMID: 8890800.

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Cooke R. Modulation of the actomyosin interaction during fatigue of skeletal muscle. Muscle Nerve. 2007 Dec;36(6):756-77. Review. PubMed PMID: 17823954.

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Deffieux X, Hubeaux K, Damphousse M, Raibaut P, Sheikh Ismael S, Thoumie P, Amarenco G, Lapeyre E, Jousse M. Perineal neuromuscular fatigue. Ann Readapt Med Phys. 2006 Jul;49(6):331-6, 413-7. Epub 2006 Apr 19. Review. English, French. PubMed PMID: 16698109.

Dimitrova NA, Dimitrov GV. Interpretation of EMG changes with fatigue: facts, pitfalls, and fallacies. J Electromyogr Kinesiol. 2003 Feb;13(1):13-36. Review. PubMed PMID: 12488084.

Dobkin BH. Fatigue versus activity-dependent fatigability in patients with central or peripheral motor impairments. Neurorehabil Neural Repair. 2008 Mar-Apr;22(2):105-10. Review. PubMed PMID: 18285599.

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Dugan SA, Frontera WR. Muscle fatigue and muscle injury. Phys Med Rehabil Clin N Am. 2000 May;11(2):385-403. Review. PubMed PMID: 10810767.

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Echegaray M, Rivera MA. Role of creatine kinase isoenzymes on muscular and cardiorespiratory endurance: genetic and molecular evidence. Sports Med. 2001;31(13):919-34. Review. PubMed PMID: 11708401.

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Fitts RH, Balog EM. Effect of intracellular and extracellular ion changes on E-C coupling and skeletal muscle fatigue. Acta Physiol Scand. 1996 Mar;156(3):169-81. Review. PubMed PMID: 8729677.

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Fitts RH. The cross-bridge cycle and skeletal muscle fatigue. J Appl Physiol. 2008 Feb;104(2):551-8. Epub 2007 Dec 27. Review. PubMed PMID: 18162480.

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Fuglsang-Frederiksen A. The utility of interference pattern analysis. Muscle Nerve. 2000 Jan;23(1):18-36. Review. PubMed PMID: 10590403.

Gandevia SC, Butler JE, Taylor JL. Viewpoint: Fatigue mechanisms determining exercise performance: integrative physiology is systems physiology. J Appl Physiol. 2008 May;104(5):1546. PubMed PMID: 18504822.

Gandevia SC, Taylor JL. Supraspinal fatigue: the effects of caffeine on human muscle performance. J Appl Physiol. 2006 Jun;100(6):1749-50. PubMed PMID: 16714410.

Gandevia SC. Mind, muscles and motoneurones. J Sci Med Sport. 1999 Oct;2(3):167-80. Review. PubMed PMID: 10668756.

Gandevia SC. Neural control in human muscle fatigue: changes in muscle afferents, motoneurones and motor cortical drive [corrected]. Acta Physiol Scand. 1998 Mar;162(3):275-83. Review. Erratum in: Acta Physiol Scand 1998 Jul;163(3):305. PubMed PMID: 9578373.

Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev. 2001 Oct;81(4):1725-89. Review. PubMed PMID: 11581501.

Gandevia SC. Voluntary muscle strength and endurance: 'The mechanism of voluntary muscle fatigue' by Charles Reid. Exp Physiol. 2008 Sep;93(9):1030-3. PubMed PMID: 18710919.

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Muscle, the Motor
Electrophysiology and Excitation‐Contraction Coupling
Diseases of Skeletal Muscle
Energetics of Muscle Contraction
Cardiac Sarcoplasmic Reticulum Ca2+‐ATPase
Mechanism of Ca2+ Transport by Sarcoplasmic Reticulum

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Jane A. Kent‐Braun, Robert H. Fitts, Anita Christie. Skeletal Muscle Fatigue. Compr Physiol 2012, 2: 997-1044. doi: 10.1002/cphy.c110029

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