Caroline Nicol

The Stretch-Shortening Cycle A Model to Study Naturally Occurring Neuromuscular Fatigue

Neuromuscular fatigue has traditionally been examined using isolated forms of either isometric, concentric or eccentric actions. However, none of these actions are naturally occurring in human (or animal) ground locomotion. The basic muscle function is defined as the stretch-shortening cycle (SSC), where the preactivated muscle is first stretched (eccentric action) and then followed by the shortening (concentric) action. As the SSC taxes the skeletal muscles very strongly mechanically, its influence on the reflex activation becomes apparent and very different from the isolated forms of muscle actions mentioned above. The ground contact phases of running, jumping and hopping etc. are examples of the SSC for leg extensor muscles; similar phases can also be found for the upper-body activities. Consequently, it is normal and expected that the fatigue phenomena should be explored during SSC activities.The fatigue responses of repeated SSC actions are very versatile and complex because the fatigue does not depend only on the metabolic loading, which is reportedly different among muscle actions. The complexity of SSC fatigue is well reflected by the recovery patterns of many neuromechanical parameters. The basic pattern of SSC fatigue response (e.g. when using the complete exhaustion model of hopping or jumping) is the bimodality showing an immediate reduction in performance during exercise, quick recovery within 1–2 hours, followed by a secondary reduction, which may often show the lowest values on the second day post-exercise when the symptoms of muscle soreness/damage are also greatest. The full recovery may take 4–8 days depending on the parameter and on the severity of exercise. Each subject may have their own time-dependent bimodality curve.Based on the reviewed literature, it is recommended that the fatigue protocol is ‘completely’ exhaustive to reduce the important influence of inter-subject variability in the fatigue responses. The bimodality concept is especially apparent for stretch reflex responses, measured either in passive or active conditions. Interestingly, the reflex responses follow parallel changes with some of the pure mechanical parameters, such as yielding of the braking force during an initial ground contact of running or hopping. The mechanism of SSC fatigue and especially the bimodal response of performance deterioration and its recovery are often difficult to explain. The immediate post-exercise reduction in most of the measured parameters and their partial recovery 1–2 hours post-exercise can be explained primarily to be due to metabolic fatigue induced by exercise. The secondary reduction in these parameters takes place when the muscle soreness is highest.The literature gives several suggestions including the possible structural damage of not only the extrafusal muscle fibres, but also the intrafusal ones. Temporary changes in structural proteins and muscle-tendon interaction may be related to the fatigue-induced force reduction. Neural adjustments in the supraspinal level could naturally be operative, although many studies quoted in this article emphasise more the influences of exhaustive SSC fatigue on the fusimotor-muscle spindle system. It is, however, still puzzling why the functional recovery lasts several days after the disappearance of muscle soreness. Unfortunately, this and many other possible mechanisms need more thorough testing in animal models provided that the SSC actions can be truly performed as they appear in normal human locomotion.

Motor unit activation patterns during isometric, concentric and eccentric actions at different force levels

Motor unit activation patterns were studied during four different force levels of concentric and eccentric actions. Eight male subjects performed concentric and eccentric forearm flexions with the movement range from 100 degrees to 60 degrees in concentric and from 100 degrees to 140 degrees elbow angle in eccentric actions. The movements were started either from zero preactivation or with isometric preactivation of the force levels of 20, 40, 60 and 80% MVC. The subjects were then instructed to maintain the corresponding relative force levels during the dynamic actions. Intramuscular and surface EMG was recorded from biceps brachii muscle. Altogether 28 motoneuron pools were analyzed using the intramuscular spike-amplitude frequency (ISAF) analysis technique of Moritani et al. The mean spike amplitude was lower and the mean spike frequency higher in the isometric preactivation phase than in the consequent concentric and eccentric actions. When the movements started with isometric preactivation the mean spike amplitude increased significantly (P<0.001) up to 80% in isometric and concentric actions but in eccentric actions the increase continued only up to 60% (P<0.01). The mean spike frequency in isometric preactivation and in concentric action with preactivation was lower only at the 20% force level (P<0.01) as compared to the other force levels while in eccentric action with preactivation the increase between the force levels was significant (P<0.01) up to 60%. When the movement was started without preactivation the mean spike amplitude at 20% and at 40% force level was higher (P<0.01) in eccentric action than in concentric actions. It was concluded that the recruitment threshold may be lower in dynamic as compared to isometric actions. The recruitment of fast motor units may continue to higher force levels in isometric and in concentric as in eccentric actions which, on the other hand, seems to achieve the higher forces by increasing the firing rate of the active units. At the lower force levels mean spike amplitude was higher in eccentric than in concentric actions which might indicate selective activation of fast motor units. This was, however, the case only when the movements were started without isometric preactivation.

Acute and prolonged reduction in joint stiffness in humans after exhausting stretch-shortening cycle exercise

Abstract. The purpose of the present study was to examine the acute and long-term fatigue effects of exhausting stretch-shortening cycle (SSC) exercise on the stiffness of ankle and knee joints. Five subjects were fatigued on a sledge apparatus by 100xa0maximal rebound jumps followed by continuous submaximal jumping until complete exhaustion. Neuromuscular fatigue effects were examined in submaximal hopping (HOP) and in maximal drop jumps (DJ) from 35 (DJ35) and 55xa0cm (DJ55) heights on a force plate. Additional force and reflex measurements were made using an ankle ergometer. Jumping tests and ankle ergometer tests were carried out before, immediately after, 2xa0h (2H), 2xa0days and 7xa0days (7D) after the SSC exercise. Kinematics, force and electromyography (EMG) recordings were complemented with inverse dynamics, which was used to calculate joint moments. The quotient of changes in joint moment divided by changes in joint angle was used as a value of joint stiffness (JS). In addition, blood lactate concentrations and serum creatine kinase activities were determined. The exercise induced a clear decrease in knee joint stiffness by [mean (SD)] 29xa0(13)% (P<0.05) in HOP, 31xa0(6)% (P<0.05) in DJ35 and 34xa0(14)% (P<0.05) in DJ55. A similar trend was observed in the ankle joint stiffness with significant post-exercise reductions of 22xa0(8)% (P<0.05) in DJ35 and of 27xa0(19)% (P<0.05) at 2H in DJ55. The subsequent recovery of JS was slow and in some cases incomplete still at 7D. Generally, all the EMG parameters were fully recovered by 2H, whereas the force recovery was still incomplete at this time. These data indicate that the immediate reduction in JS was probably related to the effects of both central (neural) and peripheral (metabolic) fatigue, whereas the prolonged impairment was probably due to peripheral fatigue (muscle damage).

Effects of long- and short-term fatiguing stretch-shortening cycle exercises on reflex EMG and force of the tendon-muscle complex

This study examined the fatigue effects of stretch-shortening cycle exercises of different intensity and duration on stretch reflex EMG and mechanical responses of the triceps surae muscle. Twelve subjects performed either a 10-km run (n=6) or short but exhaustive rebound exercise on a sledge apparatus (n=6). Passive reflex tests (mechanically induced ankle dorsiflexions) were examined before, after as well as 2xa0h, 2 and 7xa0days after exercise. Mechanical reflex responses were recorded from the ergometer torque signal. An acute contractile failure was observed as large reductions in twitch responses, especially in the sledge subgroup who showed high post-exercise peak blood lactate and an increased EMG/torque ratio. Independently of the exercise, the delayed fatigue analysis revealed strong relationships between the reflex-induced EMG and mechanical changes. In addition to muscle damage, these results may be explained by inhibitory effects via the sensitisation of small muscle afferents particularly during the exercise-induced delayed recovery process.

Acute and delayed neuromuscular adjustments of the triceps surae muscle group to exhaustive stretch–shortening cycle fatigue

Stretch–shortening cycle (SSC)-type fatigue is associated with acute and delayed functional defects, and appears to be a useful model to reveal the flexibility of both central and reflex adjustments to the contractile failure. SSC fatigue was induced in an experimental (EXP) group (n=6) on a sledge ergometer with an exhaustive rebound exercise with submaximal effort. The acute (POST) and 2-day delayed (2D) neuromuscular changes with fatigue were examined in a short submaximal rebound task (REBOUND) and in a maximal isometric plantarflexion test (ISOM). The EXP group results were compared to those of a control group (n=6) who did not perform the exhaustive SSC exercise and did not present any change in the tests. In the EXP group, the ISOM test revealed mostly a large decrease in maximal plantarflexion force at 2D that was correlated with the reduced mean soleus muscle (SOL) activation. Indicating “task-dependent” fatigue effects on the neural changes, the REBOUND test revealed both acute and delayed increases in SOL activation. Supporting central neural changes, SOL preactivation increased in POST and 2D. The neural flexibility along time and across muscles was demonstrated by the shifted increase in SOL activation from the braking phase in POST to the push-off phase in 2D, and associated increased gastrocnemius medialis preactivation in 2D. In contrast, activation during the stretch–reflex period was constant in POST, and decreased in 2D. These results would support the influence of musculotendinous afferents on the flexible neural adjustments to the SSC-induced contractile failure.

Changes in the soleus muscle architecture after exhausting stretch-shortening cycle exercise in humans

This study focused on the architectural changes in the muscle–tendon complex during the immediate and secondary (delayed) reductions of performance (bimodal recovery) caused by an exhaustive rebound type stretch-shortening cycle (SSC) exercise. The isometric plantar flexor torque during maximum voluntary contraction (MVC) was measured together with recording of electromyography (EMG) and ultrasonography from the soleus muscle before (BEF), after (AFT), 2xa0h (2H), 2 and 8xa0days (2D, 8D) after the SSC exercise (nxa0=xa08). The performance variables (MVC torque and EMG activation) followed the bimodal recovery patterns. This was not the case in the changes of the fascicle length and muscle thickness. The relative torque changes in MVC correlated positively (Rxa0=xa00.78, Pxa0=xa00.02) to the corresponding averaged EMG changes between BEF and 2H (BEFxa0→xa02H); the significance disappeared in the comparison between 2H and 2D (2Hxa0→xa02D), during which period MVC showed a secondary reduction. The relative torque changes in MVC showed no correlation with the changes in muscle thickness between BEF–2H. However, this correlation between 2H–2D was negative (Rxa0= –0.85, Pxa0<xa00.01). The fascicle shortening/average EMG ratio in MVC increased at 2H, and then decreased more at 2D than 2H (Pxa0<xa00.05). Thus, the secondary performance decline was not related to the corresponding EMG reduction but to the increased muscle thickness, which peaked at 2D. The results suggest clearly that the secondary decline in MVC could be related to the increase in muscle volume.

Exhaustive stretch-shortening cycle exercise: no contralateral effects on muscle activity in maximal motor performances

Minor cross‐over effects of unilateral muscle fatigue have been reported after isometric exercises. The present study re‐examined this possibility after an exhaustive stretch‐shortening cycle (SSC)‐type exercise. Twenty‐five subjects performed on a sledge apparatus a unilateral exhaustive rebound exercise involving mostly the triceps surae muscle group. Ipsilateral vs contralateral fatigue effects were compared in uni‐ and bilateral tests that included a maximal isometric voluntary contraction (MVC) and a series of 10 maximal drop jumps (DJ). These tests were carried out just before and after (POST) the exhaustive SSC exercise, and were repeated 2 days later (D2), at the expected time of major inflammation and pain. The exercised (fatigued) leg analysis revealed significant declines in MVC and DJ performances at POST and D2, the latter ones being associated with significant decreases in voluntary muscle activity. In contrast, no significant change was found for the non‐fatigued leg. These results do not support the existence of cross‐over effects after exhaustive SSC exercise, at least when tested in maximal static and dynamic unilateral motor tasks.

Repeated maximal eccentric actions causes long-lasting disturbances in movement control

This study examined acute and long-lasting effects of fatigue and muscle damage on fast and accurate elbow flexion and extension target movements (TM) with eight male students. An isokinetic machine was used to perform 100 maximal eccentric and concentric elbow flexions at 4-week intervals. Movement range was 40–170° in eccentric exercise (ECCE) and 170–40° in concentric exercise (CONE), with an angular velocity of 2xa0radxa0s−1. TM was performed in sitting position with the right forearm fixed to lever arm above protractor. Subjects performed TM in horizontal plane (amplitude 60°) by visual feedback of movement from a television monitor. Surface EMG was recorded from the biceps brachii and triceps brachii muscles. TM measurements and serum creatine kinase (CK) determinations were conducted before, after, 0.5xa0h, 2xa0days, and 7xa0days after both exercises. Blood lactate was taken before, after, and 0.5xa0h after the exercises. Both ECCE and CONE led to a large decline in maximal voluntary contractions, but the recovery was slower after ECCE when it remained incomplete even until dayxa07 post-exercise. Lactate increased (P<0.001) similarly after both exercises. Delayed-onset muscle soreness peaked on dayxa02 and CK peaked on dayxa07 after ECCE. Exhaustive eccentric exercise of agonistic muscles impaired the flexion TM performance, and had a long-duration modulation effect on the triphasic EMG activity pattern of flexion and extension TM. In the acute phase, the observed changes in performance and in the EMG patterns are suggested to be related to metabolic changes via III and IV muscle afferents. The delayed recovery, on the other hand, may be related to problems in the proprioceptive feedback caused by muscle damage.

Delayed influence of stretch-shortening cycle fatigue on large ankle joint position coded with static positional signals

This study examines the static position sense from the ankle joint following a unilateral exhaustive stretch‐shortening cycle (SSC)‐type exercise involving mostly the triceps surae muscle group. Fatigue effects were quantified within the exercised and non‐exercised leg through a maximal isometric voluntary plantarflexion test (MVC) performed immediately before (Pre) and after the SSC exercise, and repeated 2 (D2) and 8 (D8) days later. The static position sense test consisted in active reproductions with the non‐exercised ankle of two target dorsiflexed positions (small and large) previously maintained with either the non‐exercised (control procedure) or the exercised ankle (fatigue procedure). This test was carried out at Pre, D2, and D8. At D2, the MVC test revealed significant decreases in voluntary soleus muscle activity and peak plantarflexion force. The position sense test showed no error in reproduction accuracy in the control procedure. In contrast, the fatigue procedure revealed an overestimation of the large dorsiflexed position, only, with an associated increase of the agonist tibialis muscle activity. In agreement with the antagonist (stretched) muscle influence on the position sense, this overestimation is mostly attributed to potential SSC fatigue effects on ascending proprioceptive afferents issued from the exercised/inflamed antagonist muscles.

Neuromuscular control in landing from supra-maximal dropping height

The present study utilized high-impact supra-maximal landings to examine the influence of the pre-impact force level on the post-impact electromyographic (EMG) activity and, in particular, on the short latency EMG reflex (SLR) component. Unilateral-leg landings were performed in a sitting position on a sledge apparatus after release from high, but individually constant dropping height. A lower limb guiding device fixed to the front of the sledge seat allowed the subjects to sustain a given pre-set force level up to impact. This force level was either freely chosen or set at 20, 35, and 50% of maximal isometric plantarflexion force. EMG activity was recorded from eight major lower limb muscles. It was expected that the increase in the pre-impact force level would require the intervention of a protective neural strategy during the post-impact phase that would attenuate the SLR amplitude. The ultrasonography recordings confirmed that the soleus fascicles were stretched to induce SLR. The main finding was the similarity across all tested conditions of the impact peak force and post-impact EMG activity, including the SLR response. Both observations are mostly attributed to the similar EMG levels and close force levels reached toward impact. The instruction to maintain a given pre-set force level was indeed overruled when getting close to impact. It is suggested that, in the present supra-maximal landing condition, a protective central neural strategy did occur that took into account the pre-set force level to secure similar impact loads.