The effect of sustained low-intensity contractions on supraspinal fatigue in human elbow flexor muscles

Abstract

Subjects quickly fatigue when they perform maximal voluntary contractions (MVCs). Much of the loss of force is from processes within muscle (peripheral fatigue) but some occurs because voluntary activation of the muscle declines (central fatigue). The role of central fatigue during submaximal contractions is not clear. This study investigated whether central fatigue developed during prolonged low-force voluntary contractions. Subjects (n=9) held isometric elbow flexions of 15% MVC for 43 min. Voluntary activation was measured during brief MVCs every 3 min. During each MVC, transcranial magnetic stimulation (TMS) was followed by stimulation of either brachial plexus or the motor nerve of biceps brachii. After nerve stimulation, a resting twitch was also evoked before subjects resumed the 15% MVC. Perceived effort, elbow flexion torque and surface EMG from biceps, brachioradialis and triceps were recorded. TMS was also given during the sustained 15% MVC. During the sustained contraction, perceived effort rose from approximately 2 to approximately 8 (out of 10) while ongoing biceps EMG increased from 6.9+/-2.1% to 20.0+/-7.8% of initial maximum. Torque in the brief MVCs and the resting twitch fell to 58.6+/-14.5 and 58.2+/-13.2% of control values, respectively. EMG in the MVCs also fell to 62.2+/-15.3% of initial maximum, and twitches evoked by nerve stimulation and TMS grew progressively. Voluntary activation calculated from these twitches fell from approximately 98% to 71.9+/-38.9 and 76.9+/-18.3%, respectively. The silent period following TMS lengthened both in the brief MVCs (by approximately 40 ms) and in the sustained target contraction (by approximately 18 ms). After the end of the sustained contraction, the silent period recovered immediately, voluntary activation and voluntary EMG recovered over several minutes while MVC torque only returned to approximately 85% baseline. The resting twitch showed no recovery. Thus, as well as fatigue in the muscle, the prolonged low-force contraction produced progressive central fatigue, and some of this impairment of the subjects' ability to drive the muscle maximally was due to suboptimal output from the motor cortex. Although caused by a low-force contraction, both the peripheral and central fatigue impaired the production of maximal voluntary force. While central fatigue can only be demonstrated during MVCs, it may have contributed to the disproportionate increase in perceived effort reported during the prolonged low-force contraction.

Figure 1. Experimental protocol, and torque and EMG traces

A, experimental protocol. After performing 6 pairs of brief control contractions (100 and 50% maximal voluntary contractions (MVCs)) followed by a set of 5 brief 15% MVC efforts, subjects maintained a 15% MVC for 43 min. This sustained effort was interrupted by a brief MVC every 3 min. Sets of 15, 100 and 50% MVCs were performed during a recovery period. Motor cortex (white arrow), brachial plexus (black arrow) and motor nerve (double ended arrow) stimuli were delivered during the brief and sustained contractions as indicated in the insets. RPE, rating of perceived effort. B, raw traces of elbow flexion torque and EMG recorded from biceps brachii in one subject throughout the sustained 15% MVC. The torque record shows the maintained 15% maximal torque and the fall in voluntary torque in the brief MVCs. The EMG record shows the progressive increase in EMG required to maintain the torque. The EMG trace has been truncated during the MVCs and with stimulation. C, raw traces of elbow flexion torque responses to motor cortical stimulation (superimposed twitch) during brief MVCs in the same subject as in B. Superimposed twitches were seen during control MVCs and increased in amplitude during MVCs performed during the sustained low-force effort (5 overlaid traces in each set).

Figure 2. Rating of perceived effort during the sustained 15% maximal voluntary contraction (MVC)

Subjects rated the effort to maintain the target torque once every 3 min during the sustained contraction using a modified Borg scale. ○, mean ± s.e.m for the group (n = 9). •, individual ratings.

Figure 3. Voluntary EMG, and torque and EMG responses to motor cortical stimulation during the sustained 15% maximal voluntary contraction (MVC) and in brief recovery 15% MVCs

All data are shown as mean ± s.e.m for the group of 9 subjects. Two breaks in each data set show periods when subjects pulled with the hand strap rather than the wrist strap and no stimuli were given. The end of the sustained 15% MVC is indicated by the vertical broken lines. A, voluntary EMG recorded from biceps brachii (○) and brachioradialis (•). Rms EMG recorded from both elbow flexor muscles increased throughout the sustained 15% MVC and recovered towards initial values during brief 15% MVCs performed in the recovery period. EMG is normalized to the maximum recorded during the brief control MVCs. B, motor evoked potentials (MEPs) elicited from biceps brachii (○), brachioradialis (•) and triceps brachii (▵) by stimulation of the motor cortex. The areas of the MEPs are expressed relative to the maximal M-wave (M_max) recorded under the same conditions. In biceps and brachioradialis, an initial fall in the MEP area (probably due to potentiation of the muscle by the first brief MVC), was followed by a gradual increase throughout the 15% MVC. The MEP in triceps remained small throughout the experiment. C, torque response to motor cortical stimulation (superimposed twitch). The superimposed twitch increased during the sustained effort. D, change in the duration of the silent period following motor cortical stimulation in biceps brachii (○) and brachioradialis (•). The difference in the duration of the silent period from the mean measured during brief control contractions is shown. The silent period lengthened during the sustained contraction and recovered quickly.

Figure 4. Voluntary and evoked torque and EMG during brief maximal voluntary contractions (MVCs) performed during the sustained low-force effort and in the recovery period

All data are shown as mean ± s.e.m (n = 9). The vertical broken lines indicate the end of the sustained contraction. A, voluntary torque during brief MVCs (large filled circles), 15% MVC target torque (small filled circles) and amplitude of the twitch evoked from the resting muscle by motor nerve stimulation (open square). Maximal voluntary torque and target torque are expressed relative to the maximal torque recorded during brief control MVCs. While subjects held the target torque for 43 min as planned, the torque produced during occasional brief MVCs declined. It returned to about 85% of control values during the recovery period. The twitch was evoked in the resting muscle by paired stimulation over biceps and was always potentiated by a preceding MVC. The amplitude of the twitch (expressed relative to the mean control amplitude) decreased during the sustained contraction and showed minimal recovery over 20 min. B, voluntary EMG recorded from biceps brachii (○) and brachioradialis (•). Rms EMG is expressed relative to the maximum recorded during brief control MVCs. EMG during MVCs declined in both elbow flexors over the course of the sustained low-force effort and recovered towards initial values after the end of the fatiguing contraction.

Figure 5. Voluntary activation and the superimposed twitches evoked by motor nerve and motor cortex stimulation during brief maximal voluntary contractions (MVCs)

All data are shown as mean ± s.e.m (n = 9). The vertical broken lines indicate the end of the sustained contraction. A, motor nerve stimulation. The increments in torque (superimposed twitch, □) evoked by paired motor nerve stimulation during brief control MVCs, MVCs during the sustained contraction and in the recovery period are shown (left axis). Voluntary activation (▪, right axis) was calculated by comparing the superimposed twitch to the twitch in the resting muscle. B, motor cortex stimulation. The increments in torque (superimposed twitch, □) evoked by motor cortex stimulation during MVCs are shown (left axis). For the control and recovery period, voluntary activation (♦, right axis) was calculated by comparing the superimposed twitch to an estimated resting twitch (see Methods).

Figure 6. EMG responses to motor cortical stimulation during brief maximal voluntary contractions (MVCs)

All data are shown as mean ± s.e.m (n = 9). The vertical broken lines indicate the end of the sustained contraction. A, motor evoked potentials (MEPs) in biceps brachii (○), brachioradialis (•) and triceps brachii (▵). The areas of the MEPs are expressed relative to the maximal M-waves (M_max) recorded in the same conditions and at close to the same time. B, change in the duration of the silent period in biceps brachii (○) and brachioradialis (•) following motor cortical stimulation. The difference in duration of the silent period from the mean during brief control MVCs is shown. Silent periods in both elbow flexors lengthen through the sustained low-force contraction and recover quickly.