Trevor J. Allen

Damage to Skeletal Muscle from Eccentric Exercise

Evidence is provided for a mechanical event as the first step in the process leading to muscle damage after a series of eccentric contractions. Aspects discussed include the decline in active tension, increase in passive tension, shift in length–tension relation, soreness, swelling, and disturbed proprioception.

Changes in the mechanical properties of human and amphibian muscle after eccentric exercise.

Abstract Following a series of eccentric contractions, that is stretching of the muscle while generating active tension, the length-tension relationship of isolated amphibian muscle has been shown to shift towards longer muscle lengths (Katz 1939; Wood et al. 1993). Here we report observations of electrically stimulated ankle extensor muscles of nine human subjects, demonstrating a similar shift in optimum angle for torque generation [3.9 (1.5)°] following exercise on an inclined treadmill that involved eccentric contractions in one leg. (All values are means with the SEMs in parentheses.) The shift in the unexercised, control leg was significantly less [mean 0.4 (0.7)°P < 0.05]. Correlated with this shift was a drop in torque [25.1 (5.6)% for the experimental leg; 1.6 (0.7)% for the control leg, P < 0.002]. Optimum angles returned to pre-exercise values by 2 days post-exercise, while torque took a week to recover. A similar shift in optimum length [12 (1.3)% of rest length] was obtained for five toad (Bufo marinus) sartorius muscles subjected to 25 eccentric contractions. Isometrically contracted control muscles showed a smaller shift [3.5 (1.6)%, n = 5]. Accompanying the shift was a drop in tension of 46 (3)% after the eccentric contractions [control isometric, 23 (6)%, P < 0.0001]. By 5 h after the eccentric contractions the shift had returned to control values, while tension had not recovered. When viewed with an electron microscope, sartorius muscles fixed immediately after the eccentric contractions exhibited many small, and a few larger, regions of myofilament disruption. In muscles fixed 5 h after the contractions, no small regions of disruption were visible, and the number of large regions was no greater than in those muscles fixed immediately after the eccentric contractions. These disruptions are interpreted as the cause of the shift in length-tension relationship.

Muscle spindle signals combine with the sense of effort to indicate limb position

Experiments were carried out to test the hypothesis that, in the absence of vision, position sense at the human forearm is generated by the combined input from muscle spindles in elbow flexor muscles and signals of central origin giving rise to a sense of effort. In a forearm position‐matching task, to remove a possible contribution from the sense of effort, the reference arm was held supported at the test angle. Subjects were less accurate in matching elbow position of the supported forearm than when it was unsupported. Adding a 2 kg weight to the unsupported reference arm led subjects to make matching errors consistent with an increase in the effort signal. Evidence of a contribution from muscle spindles was provided by showing that the direction of position matching errors could be systematically altered by flexion or extension conditioning of the reference arm before its placement at the test angle. Such changes in errors with conditioning could be shown to be present when the reference arm was supported, unsupported, or unsupported and weighted. It is concluded that both peripheral signals from muscle spindles and signals of central origin, associated with the motor command required to maintain arm position against the force of gravity, can provide information about forearm position.

Effect of muscle fatigue on the sense of limb position and movement

We have recently shown that in an unsupported forearm-matching task blindfolded human subjects are able to achieve an accuracy of 2–3°. If one arm was exercised to produce significant fatigue and the matching task was repeated, it led subjects to make position-matching errors. Here that result is confirmed using fatigue from a simple weight-lifting exercise. A 30% drop in maximum voluntary force after the exercise was accompanied by a significant matching error of 1.7° in the direction of extension when the reference arm had been fatigued, and 1.9° in the direction of flexion when the indicator arm had been fatigued. We also tested the effect of fatigue on a simple movement tracking task where the reference forearm was moved into extension at a range of speeds from 10 to 50°s−1. Fatigue was found not to significantly reduce the movement-tracking accuracy. In a second experiment, movement tracking was measured while one arm was vibrated. When it was the reference arm, the subject perceived the movement to be significantly faster (3.7°s−1) than it actually was. When it was the indicator, it was perceived to be slower (4.6°s−1). The data supports the view that muscle spindles are responsible for the sense of movement, and that this sense is not prone to the disturbance from fatigue. By contrast, the sense of position can be disturbed by muscle fatigue. It is postulated, that the sense of effort experienced by holding the arm against the force of gravity is able to provide information about the position in space of the limb and that the increased effort from fatigue produces positional errors.

Damage to human muscle from eccentric exercise after training with concentric exercise

1 It is known that a period of eccentric exercise provides protection against damage to muscle from subsequent eccentric exercise. Here we ask, does concentric exercise do the opposite, make muscle more prone to damage? 2 The triceps surae muscle group of one leg in each of eight human subjects was subjected to 30 min of concentric exercise per day, for 5 days. At the end of the training period there was a small but significant increase in passive torque in the exercised muscle (P < 0.05), with no changes in the untrained muscle. 3 After a single period of eccentric exercise, angle‐torque curves for muscles of both legs shifted in the direction of longer muscle lengths, suggestive of an increase in series compliance. The shift in the concentrically trained muscle was significantly greater over the first 48 h post‐exercise (P < 0.05). 4 The volume of the trained leg increased significantly more than the untrained leg for five subjects over 72 h post‐exercise (P < 0.05). Peak torque fell, passive stiffness increased and both muscles became sore, but with no significant differences between the two legs. 5 It is concluded that a period of concentric exercise increases the susceptibility of muscle to changes associated with the damage from eccentric exercise.

Length-dependent changes in voluntary activation, maximum voluntary torque and twitch responses after eccentric damage in humans

To assess the contribution of central and peripheral factors to changes in maximum voluntary force and its length dependence after eccentric muscle damage, voluntary and twitch torque were measured across a wide angular range, along with voluntary activation using twitch interpolation. Isometric torque from both maximum voluntary contractions (MVCs) and paired twitches to motor nerve stimulation were measured from 60 to 150 deg elbow flexion in 10 deg increments in eight subjects. Optimal angles were determined by curve fitting. Each subject then performed eccentric contractions until voluntary torque had decreased by ∼40%. Measurements were repeated at 2 h, 1 day and 8 days post‐exercise to follow acute and longer‐term changes. Before exercise, the optimal angle was in the mid‐range (93 ± 10 deg; mean ±s.d.) for MVCs, and at a more extended elbow angle for the twitch (106 ± 6 deg, P < 0.05). Voluntary activation was generally high (> 94%) but depended on elbow angle, with activation being ∼4% lower at the most flexed compared to the most extended angle. Two hours after exercise, MVCs decreased 40%, while twitch torque declined 70%. All subjects showed a shift in optimal angle to longer muscle lengths for MVCs (17 ± 16 deg at 2 h, 14 ± 7 deg at day 1, P < 0.05). This shift contributed minimally (∼3%) to the reduction in torque at 90 deg, as the torque–angle relation was relatively flat around the optimum. The twitch showed a smaller shift (∼4 deg) to longer lengths which was not statistically significant. Voluntary activation was significantly impaired in the early stages after exercise (2 h and day 1, P < 0.05), particularly at short muscle lengths. By 8 days after exercise, the optimal angle had returned to pre‐exercise values, but MVC, twitch torque and voluntary activation had not fully recovered. Eccentric exercise causes a short‐term shift in the optimal angle for MVCs and produces a length‐dependent impairment in voluntary activation. Therefore, it appears that both central and peripheral factors limit muscle performance following eccentric damage, with limits to voluntary drive being especially important at short lengths.

Investigation of transabdominal real-time ultrasound to visualise the muscles of the pelvic floor

Clinical measurement of pelvic floor muscle activity commonly involves techniques that are both physically and psychologically invasive. This study investigated transabdominal application of ultrasound to measure pelvic floor muscle action. The specific aims were to establish the face validity of ultrasound measures of displacement of the posterior bladder wall as a reflection of pelvic floor muscle contraction, and the reliability of measurement between raters and between testing occasions. Non-pregnant adult female subjects aged 24 to 57 years were tested in lying with a 3.5 MHz 35 mm curved array ultrasound transducer over the lower abdomen. Posterior bladder wall displacement was observed in both sagittal and transverse planes. Digital vaginal palpation and transabdominal ultrasound were undertaken simultaneously during pelvic floor muscle contractions to confirm that pelvic floor contractions were performed correctly and to grade pelvic floor muscle strength. Displacement (mm) was measured using electronic calipers on the ultrasound monitor screen. In all subjects, a correct pelvic floor muscle contraction was confirmed on digital palpation, and consistent anterior and cephalic movement was observed on screen. Digital strength grading did not correlate with ultrasound measures in either transverse or sagittal planes (r = 0.21 and -0.13). Average intra-class correlation coefficients for within session inter-rater reliability ranged between 0.86 and 0.88 (95% CI 0.68 to 0.97), and for inter session intra-rater reliability between 0.81 and 0.89 (95% CI 0.51 to 0.96). Transabdominal application of diagnostic ultrasound is a personally non-invasive method for imaging and assessing pelvic floor muscle activity and is both valid and reliable.

The effect of quadriceps muscle fatigue on position matching at the knee

This is a report of the effects of exercise on position matching at the knee. Young adult subjects were required to step down a set of stairs (792 steps), representing eccentric‐biased exercise of the quadriceps muscle, or step up them, concentric‐biased exercise. Immediately after eccentric exercise subjects showed a mean force drop of 28% (± 6%, s.e.m.) of the control value in their exercised quadriceps muscle, which was accompanied by 4.8 deg (± 0.8 deg) of error between reference and matching legs in a position matching task at the knee. Similarly concentric exercise was followed by a force drop of 15% (± 3%) and matching errors of 3.7 deg (± 0.4 deg). These effects were significant. The direction of the errors suggested that subjects perceived their exercised muscles to be longer that they actually were. This finding was not consistent with the hypothesis that the increase in effort required to support the leg after fatigue from exercise was responsible for the errors. It is hypothesized that position sense in an unsupported leg arises, in part, from operation of an internal forward model. When the motor command is increased to compensate for the effects of fatigue, the comparison between predicted and actual feedback from quadriceps leads to the impression that the muscle is longer than it actually is. The exercise effects on proprioception may have implications for sports injuries and for evaluation of the factors leading to falls in the elderly.

The effect of fatigue from exercise on human limb position sense

We have previously shown, in a two‐limb position‐matching task in human subjects, that exercise of elbow flexors of one arm led the forearm to be perceived as more extended, while exercise of knee extensors of one leg led the lower leg to be perceived as more flexed. These findings led us to propose that exercise disturbs position sense because subjects perceive their exercised muscles as longer than they actually are. In order to obtain further support for this hypothesis, in the first experiment reported here, elbow extensors were exercised, with the prediction that the exercised arm would be perceived as more flexed after exercise. The experiment was carried out under three load conditions, with the exercised arm resting on a support, with it supporting its own weight and with it supporting a load of 10% of its voluntary contraction strength. For each condition, the forearm was perceived as more extended, not more flexed, after exercise. This result was confirmed in a second experiment on elbow flexors. Again, under all three conditions the exercised arm was perceived as more extended. To explore the distribution of the phenomenon, in a third experiment finger flexor muscles were exercised. This had no significant effect on position sense at the elbow. In a fourth experiment, position sense at the knee was measured after knee flexors of one leg were exercised and, as for knee extensors, it led subjects to perceive their exercised leg to be more flexed at the knee than it actually was. Putting all the observations together, it is concluded that while the influences responsible for the effects of exercise may have a peripheral origin, their effect on position sense occurs centrally, perhaps at the level of the sensorimotor cortex.

Position sense at the human forearm in the horizontal plane during loading and vibration of elbow muscles

When blindfolded subjects match the position of their forearms in the vertical plane they rely on signals coming from the periphery as well as from the central motor command. The command signal provides a positional cue from the accompanying effort sensation required to hold the arm against gravity. Here we have asked, does a centrally generated effort signal contribute to position sense in the horizontal plane, where gravity cannot play a role? Blindfolded subjects were required to match forearm position for the unloaded arm and when flexors or extensors were bearing 10%, 25% or 40% of maximum loads. Before each match the reference arm was conditioned by contracting elbow muscles while the arm was held flexed or extended. For the unloaded arm conditioning led to a consistent pattern of errors which was attributed to signals from flexor and extensor muscle spindles. When elbow muscles were loaded the errors from conditioning converged, presumably because the spindles had become coactivated through the fusimotor system during the load‐bearing contraction. However, this convergence was seen only when subjects supported a static load. When they moved the load differences in errors from conditioning persisted. Muscle vibration during load bearing or moving a load did not alter the distribution of errors. It is concluded that for position sense of an unloaded arm in the horizontal plane the brain relies on signals from muscle spindles. When the arm is loaded, an additional signal of central origin contributes, but only if the load is moved.