Maximal force, voluntary activation and muscle soreness after eccentric damage to human elbow flexor muscles

Abstract

Muscle damage reduces voluntary force after eccentric exercise but impaired neural drive to the muscle may also contribute. To determine whether the delayed-onset muscle soreness, which develops approximately 1 day after exercise, reduces voluntary activation and to identify the possible site for any reduction, voluntary activation of elbow flexor muscles was examined with both motor cortex and motor nerve stimulation. We measured maximal voluntary isometric torque (MVC), twitch torque, muscle soreness and voluntary activation in eight subjects before, immediately after, 2 h after, 1, 2, 4 and 8 days after eccentric exercise. Motor nerve stimulation and motor cortex stimulation were used to derive twitch torques and measures of voluntary activation. Eccentric exercise immediately reduced the MVC by 38 +/- 3% (mean +/- s.d., n = 8). The resting twitch produced by motor nerve stimulation fell by 82 +/- 6%, and the estimated resting twitch by cortical stimulation fell by 47 +/- 15%. While voluntary torque recovered after 8 days, both measures of the resting twitch remained depressed. Muscle tenderness occurred 1-2 days after exercise, and pain during contractions on days 1-4, but changes in voluntary activation did not follow this time course. Voluntary activation assessed with nerve stimulation fell 19 +/- 6% immediately after exercise but was not different from control values after 2 days. Voluntary activation assessed by motor cortex stimulation was unchanged by eccentric exercise. During MVCs, absolute increments in torque evoked by nerve and cortical stimulation behaved differently. Those to cortical stimulation decreased whereas those to nerve stimulation tended to increase. These findings suggest that reduced voluntary activation contributes to the early force loss after eccentric exercise, but that it is not due to muscle soreness. The impairment of voluntary activation to nerve stimulation but not motor cortical stimulation suggests that the activation deficit lies in the motor cortex or at a spinal level.

Figure 1. Main measurement protocol and calculation of the estimated resting twitch

A, first, electrical stimulation was delivered to the motor nerve during a 2 s MVC and then after 4 s of rest. Second, transcranial magnetic stimulation of the motor cortex was delivered during a sequence of three contractions: 100% MVC, 75% MVC and 50% MVC. Third, supramaximal stimulation of the brachial plexus was delivered during a similar sequence of three contractions, and also at rest after the MVC. In each session, this measurement sequence was repeated 5 times with rest intervals of 1–1.5 min between all MVCs. Stimulus timing is indicated by the arrows. B, typical twitch torques evoked by motor cortical stimulation during contraction at 100% MVC, 75% MVC and 50% MVC from the control session in a typical subject. C, data from this subject to show linear regression between the twitch torques evoked by motor cortical stimulation and voluntary torque from the control day (•) and for day 1 after eccentric exercise (○). Extrapolation was used to estimate the resting twitch (r²= 0.98 for the control day and r²= 0.95 for day 1).

Figure 2. Twitch responses and EMG responses in one subject

A, typical traces from one subject of the resting twitch (longer twitch) and superimposed twitch evoked by motor nerve stimulation (overlaid in upper panels) and superimposed twitch evoked by motor cortical stimulation (lower panels) in the control session (left panels) and day 1 after eccentric exercise (right panels). Calibration bars for the superimposed twitches represent 1 Nm and 20 ms (i.e. these traces are amplified two fold). When the maximal voluntary torque decreased to 60% at day 1, impaired voluntary activation from motor nerve stimulation was decreased as indicated by the twitch responses during MVCs and a marked decrease in the resting twitches. B, traces of motor evoked potentials (MEP, upper panels) evoked by motor cortical stimulation and maximal M-wave (M_max, lower panels) evoked by brachial plexus stimulation during 100% MVC (left panel). Stimulus timing indicated by arrows. There were no changes in the EMG responses to cortical stimulation or brachial plexus stimulation after eccentric exercise.

Figure 3. Maximal voluntary torque and changes in relaxed elbow angle after eccentric exercise

Maximal voluntary torque and elbow angle were measured under control conditions (C), immediately after (0), 2 h after (2 h), and days 1, 2, 4 and 8 after eccentric exercise for the group of subjects. The time scale from day 1 is linear. In this and subsequent figures, the vertical hatched area shows the period of exercise, the horizontal line indicates a baseline value, and * indicates a statistically significant difference from control values (P < 0.05). Mean ±s.e.m. (n = 8) is plotted in this and subsequent figures. A, maximal isometric voluntary torque decreased to ∼60% of the control value immediately after eccentric exercise (as required by the protocol), and then improved gradually over the subsequent 8 days. B, relaxed elbow angle became more flexed immediately after exercise and recovered over 8 days.

Figure 4. Force required to elicit pain at rest and the scores for pain during contractions

A, group data for the external force required to elicit local pain in the muscle. Data for one spot (▴) identified as tender on day 1 and studied on subsequent days. Pain was prominent on days 1 and 2. The horizontal continuous line and broken lines indicate the mean and 95% confidence interval for the force required to elicit pain at the reference points on the muscle before exercise. B, subjective pain induced in the muscle by voluntary contractions at 50% MVC (▪) and 100%MVC (□). Across contraction intensities from 50% to 100% MVC, muscle pain was most intense 1–4 days after the exercise and recovered after 8 days. A score of 2 is described as ‘mild’.

Figure 5. Twitch properties after eccentric exercise

A, group data for twitch torque for biceps measured from motor nerve stimulation under resting conditions (resting twitch, □). Twitch torque from elbow flexor muscles estimated using TMS (▴; see Methods). Twitch torques produced by nerve stimulation were depressed more than the MVC after eccentric exercise (compare Fig. 3A). s.e.m.s are smaller than the symbol size for some □. B, time-to peak value for the resting potentiated twitch of biceps evoked by nerve stimulation (▪) increased slightly at day 2–8 and the half-relaxation time (□) decreased immediately after exercise.

Figure 6. Voluntary activation determined by motor nerve stimulation and motor cortical stimulation for the group of subjects

Voluntary activation calculated from motor nerve stimulation (▪) decreased by ∼23% immediately after eccentric exercise, and remained significantly decreased for 24 h. The time course of this reduction differed from the time course of muscle pain and tenderness, which peaked at day 1–2 (see Fig. 4). Voluntary activation calculated from motor cortex stimulation (□) did not change significantly after eccentric exercise.

Figure 7. Size of superimposed twitches from motor cortex stimulation and motor nerve stimulation

A, group data for superimposed responses to motor nerve stimulation during MVCs (▪) and for superimposed responses to cortical stimulation during MVCs (□). Superimposed twitch torques evoked by nerve stimulation during MVCs did not significantly change after eccentric exercise. Superimposed twitch torques evoked by motor cortex stimulation during MVCs were larger and decreased significantly at 2 h after exercise and at day 8. B, for each subject, the mean of sizes of superimposed twitches evoked by nerve stimulation are plotted against those evoked by motor cortical stimulation in the same measurement sessions. Data for different times are shown using different symbols. Values are expressed relative to control data obtained before exercise. A line of identity is shown.

Figure 8. Force–EMG relationship

Mean levels of EMG required to produce 50%, 75% and 100% MVC are shown. Data for different times after exercise are shown using different symbols. As force-generating capacity recovered, there was a gradual reduction in the relative level of EMG required to generate 50% MVC.