Medicine & Science in Sports & Exercise:
BASIC SCIENCES: Original Investigations
Bimodal Recovery Pattern in Human Skeletal Muscle Induced by Exhaustive Stretch-Shortening Cycle Exercise
DOUSSET, ERICK2; AVELA, JANNE1; ISHIKAWA, MASAKI1; KALLIO, JOUNI1; KUITUNEN, SAMI1; KYRÚLàINEN, HEIKKI1; LINNAMO, VESA1; KOMI, PAAVO V.1
1Neuromuscular Research Centre, Department of Biology of Physical Activity, University of Jyvaäskylaä, FINLAND; and 2Department of Physiology of Physical Activity, University of the Mediterranean, Marseille, FRANCE
Address for correspondence: Erick Dousset, Ph.D., Neuromuscular Research Centre, Department of Biology of Physical Activity, PO Box 35 (VIV), 40014 University of Jyväskylä, Finland; E-mail: Herpola@sport.jyu.fi.
Submitted for publication March 2006.
Accepted for publication October 2006.
Introduction/Purpose: Recovery of force and stretch reflex from exhaustive stretch-shortening cycle (SSC) exercise is usually bimodal, characterized as immediate exercise-induced performance reduction, with its quick recovery followed by a longer-lasting reduction in performance. A clear parallel exists between the respective changes in performance, neural activation, and metabolic or structural exercise-induced changes. This implies the existence of potential coupling between muscle failure and the induced neural adjustments that take place along its recovery. The present study was designed to explore the evidence of this coupling more thoroughly.
Methods: H- and stretch reflexes were measured before and periodically after exhaustive SSC exercise in human subjects. Several markers of muscle damage and inflammation were also measured during the 8-d postexercise follow-up period.
Results: The results indicate that acute changes of H- and stretch reflex patterns and maximal isometric force are associated with significant increases in lactate, interleukin 6, and prostaglandin E2 concentrations. The delayed changes in reflexes and isometric force occurred concomitantly with increases in muscle thickness, C reactive protein, and substance P concentrations and also in serum creatine kinase activity.
Conclusion: The immediate postexercise decreases in H- and stretch reflexes are probably partially caused by activation of group III and IV afferent fibers by high lactate concentration in combination with possible increases in potassium outflow. Both of these parameters recovered quickly (i.e., 2 h after exercise). The events after the 2-h postexercise point are very likely to be related to muscle damage and associated inflammation. Group III and IV afferent fibers are probably reactivated during this period by mechanical factors.
Recent experiments in humans (26) have shown a bimodal pattern of force recovery after intensive stretch-shortening cycle (SSC) exercise. A similar trend has been reported for both active (5) and passive (4) stretch reflexes after intensive (about 1 h) as well as long-lasting (from 2 h 20 min to 3 h 30 min) SSC exercise. These studies indicate a fast (1-2 d) recovery of exercise-induced reduction in force and stretch reflex, followed by a second, longer-lasting (2-6 d), reduction of performance. The immediate decline in performance and reflexes is classically related to acute, metabolically induced reaction, followed by a short-term recovery that, in turn, is followed by a secondary reduction associated with inflammatory and remodeling processes (33). The neural control (i.e., central activation changes and/or failure) plays a key role in exercise- and recovery adjustments and might be modulated by corresponding changes in mechanical behavior and structural modifications of the muscle (14). The neural adaptations to exercise are sometimes so dramatic that they have influence on the overall control of movement of the exercising muscle (14).
Bimodality was first observed in an animal experiment after lengthening contractions (eccentric)-induced fatigue by Faulkner et al. (12). In their experiment, force decline was associated with an initial injury that was primarily mechanical and a secondary injury related to membrane alteration and muscle damage. The ability to produce force could be reduced for several days (up to 1 wk) (2). Armstrong (1) has defined four stages of muscle damage processes and subsequent recovery. The first stage is characterized by increased muscle stiffness (7), altered force and position sense (6), swelling (9), and muscle structure damage (13), including loss of membrane integrity leading to an inflammatory reaction (12). Occurrence of muscle damage and inflammation has been suggested to be related to an increase in muscle thickness that reaches peak values 2 d after eccentric exercise (39). The second stage (autogenic) may begin with the degradation of cellular structures by proteolytic and lipolytic systems. The inflammatory response is initiated at 2-6 h after exercise (1). This is followed by a phagocytic stage, beginning with the inflammatory response and lasting between 6 h and 6 d, depending on the subject's physical level (1). During the last stage (regenerative), muscle starts to be repaired; it may take from 6 to 14 d for a full recovery (1).
The present study was undertaken to investigate possible interactions between muscular changes (fatigue-induced release of metabolites for a short period, and events related to muscle damage for a longer period) and central events (reflex adaptation, central activation level) that occur immediately after intensive SSC exercise and during the subsequent recovery period. It was hypothesized that force production might be modulated through the activation of sensory motor loops by chemical and mechanical changes within the muscle. To test this hypothesis, the kinetics of lactate (LA) concentration, muscle damage, and inflammatory blood markers, as well as muscle volume, were measured for 8 d after exhaustive SSC exercise. These parameters were compared with the time course of recovery of H-reflex and short latency components of stretch reflex. The activation level also was measured.
Twelve male subjects (age: 28 ± 1.5 yr; body mass: 81 ± 3.3 kg; height: 179 ± 2.5 cm) participated in the present study. None of the subjects had any history of neuromuscular or metabolic disorders, and all were recreationally active. Experimental procedures involved in the study and possible risks were carefully explained to the subjects, whose written consent was obtained. Experiments were conducted according to the Declaration of Helsinki and were approved by the ethics committee of the University of Jyväskylä in Finland.
A series of measurements were taken before, immediately after, 2 h after, and 2 and 8 d after a fatiguing SSC exercise (Fig. 1). This exercise consisted of an exhaustive series of rebounds on a sledge ergometer (Fig. 1). During the testing protocol, electromyograms (muscle activity and reflexes) and maximal isometric force were measured from the plantar flexor muscles. Activation level (AL) also was determined during maximal isometric voluntary plantar flexion. H- and stretch reflexes also were evoked. Before each test session, blood was sampled to measure concentrations of indirect markers of muscle damage (serum creatine kinase (S-CK) and C-reactive protein (CRP)) as markers of the development of an inflammatory reaction (induced by muscle damage)-that is, interleukin 6 (IL-6), prostaglandin E2 (PG E2), and substance P.
FIGURE 1-Schematic p...Image Tools
Each subject performed SSC fatiguing exercise, executing a series of drop jumps in a sitting position on a sledge apparatus (Fig. 1). Drop jumps consisted of a series of rebounds on this device at a predetermined dropping height. To maximize the involvement of the triceps surae muscle group, the contribution of gluteus maximus muscle and of quadriceps was reduced, respectively, by fixing the seat angle at 120° and by training the subjects to let their knees flex freely between take-off and the subsequent impact. After determination of the individual maximal rebound height, the subjects performed 100 successive maximal drop jumps. Then, they performed rebounds set at 70% of maximal height until exhaustion (24). During the fatigue session, verbal feedback was given to help to maintain the correct level of exercise (i.e., 70% of maximal height).
All plantar flexion tests were performed using an ankle ergometer similar to the one introduced by Gollhofer and Schmidtbleicher (17). Each subject was in a sitting position on the ergometer chair, with his right foot firmly attached to the ergometer pedal. The axis of rotation of the ankle joint was carefully aligned to the axis of the pedal. The other leg was relaxed. The knee angle of the right leg was fixed at 130°, and the ankle angle was fixed at 103°.
Verbal encouragement was given to the subjects during measurement of maximal isometric plantar flexion force. To further encourage maximal effort, visual feedback of force was shown on an oscilloscope (Fluke PM 33484B 100 MHz; Fluke, Helsinki, Finland). The isometric force level was indicated on the oscilloscope by a dotted line, the level of which was progressively increased until the subject was unable to perform at a higher force. Force signals were sent to a computer through an analog-to-digital converter (Power 1401; Cambridge Electronics Design Ltd, Cambridge, England). Force and angle of movements were low-pass filtered at 15 and 100 Hz, respectively, to avoid noise.
EMG (bipolar) from the soleus muscle (Sol) was recorded from a pair of surface electrodes (Beckman 650437 miniature skin electrodes, England) spaced 20 mm apart. According to SENIAM recommendations (40), the interelectrode resistance was kept below 5000 Ω by careful skin shaving and abrasion with alcohol. The electrodes were placed at two thirds of the line between condile of the femur to the medial malleolus and were firmly fixed by band tape. To allow within-subject comparisons of the EMG signal recorded on the different testing days, the electrode positions were marked carefully on the skin. The ground electrode, an ECG electrode (short-term ECG electrodes; Unilect, Stonehouse, England) was positioned on the greater femoral trochanter.
The EMG signals were sent to a microcomputer through an analog-to-digital converter for further processing (Power 1401; Cambridge Electronics Design Ltd, Cambridge, England). The EMG signal was amplified (×10,000; Glonner Electric GmbH, Germany), sampled at a rate of 2 kHz, band-pass filtered (10 to 500 Hz), and analyzed through the software Signal 2.10. (Cambridge Electronics Design Ltd, Cambridge, England).
To estimate the level of central activation reached by a subject, the twitch-interpolation technique was used. Numerous authors have used double maximal shocks superimposed to maximal contraction (29,42). According to the methods of Strojnik and Komi (42), the activation level was assessed using a superimposed double stimulation (rectangular pulses, 200-μs duration, separated by 10 ms) applied 2 s after the subject reached maximal isometric contraction. Superimposed force was compared against the maximal force and against the twitch elicited by the double stimulation applied in resting muscle. The current intensity was fixed at 25% above the level used to obtain maximal evoked muscle action potential (M wave). In the present study, the activation level was calculated by the following formula:
Equation (Uncited)Image Tools
where MIVC is maximal isometric voluntary contraction, Sf is superimposed force, Tb is force before stimulation, and twitch is the force induced by double supramaximal stimulation.
Short latency reflex (SLR) of the plantar flexors was measured from a passive condition at a starting ankle angle of 103°. This reflex was induced by the ergometer and was repeated 30 times at 0.175-rad amplitude and at a mean stretching velocity of 1.9 rad·s−1.
M- and H-wave measurements.
To evoke M- and H waves from the soleus muscle, stimulation of the soleus muscle via the tibial nerve was delivered through one cathode placed over the tibial nerve on the popliteal fossa and one anode placed above the patella. The position of the subject was the same as in the other tests. Single rectangular pulses of 200-μs duration were used. The pulses were delivered by a computer-driven stimulator (Digitimer DS7 A LTD; Welwin Garden City, Hertforshire, England). The current intensity used for the evoked maximal H wave was determined as follows: First, the maximal M wave was determined, and then the current intensity was adjusted to obtain 20% of the maximal M wave in rest conditions. This intensity was used during all measurements. Between 10 to 15 measurements of H reflexes were obtained. Corresponding H- and M waves were shown on an oscilloscope (Agilent 54624A; Agilent Technologies, Colorado Springs, CO). During H-wave recordings, subjects were asked to avoid any movement and to be completely relaxed to avoid any M waves caused by parameters other than α-motoneuron excitability.
To quantify myoelectric activity during maximal voluntary contractions, root mean square (RMS) amplitude of EMG was analyzed within 100-ms windows surrounding the peak force value. To quantify SLR response to a stretching perturbation, 10 successive reproducible records were averaged. Subsequently, the peak-to-peak amplitude and area of the M wave as well as the H reflex were measured from the average of five repeatable H waves in each test. Then, H/M ratio was calculated from previous values. Theoretically, the H/M ratios should not have been affected by any changes in the peripheral excitability of the muscle fibers consequent on fatigue and, so determined, should only imply changes in α-motoneuron pool excitability.
Blood was sampled at rest before each test. Samples were obtained from the antecubital vein of the right arm. Blood analysis included measurements of the concentration of leukocytes, CRP, IL-6, PG E2, and substance P. A complete blood count (CBC) including white cell differential was made using a Bayer Advia 120 analyzer. The activity of serum creatine kinase (S-CK) was measured using an optimized standard method conformed to the recommendations of Deutsche Gesellschaft for Clinical Chemistry using a Hitachi 917 analyzer and reagents produced by Roche. CRP was analyzed by nephelometric method using reagents made by Fitzgerald according to the recommendation of DADE (Behring, Germany). Substance P was analyzed with immunoassay kit, PG E2 with immunoassay DE 100, and IL-6 with human sensitive IL-6 immunoassay HS600 (R&D system Inc. Minneapolis, MN). The measurement of LA concentration (Biochemica Boehringer, Mannheim, Germany) by enzymatic method was done with blood sampled from the fingertip.
Estimation of the soleus muscle volume was obtained by measuring muscle thickness of the right-leg soleus (Sol) muscle by using a brightness-mode ultrasound apparatus (7.5-MHz probe; Aloka SSD-2000). The probe was moved slowly to scan the longitudinal sections of Sol. Three parts of the muscle (distal, central, and proximal) were taken for analysis. The Sol thickness was defined as the length between the anterior to posterior aponeurosis. The three repeated values of each part were grand mean averaged.
Significant changes in each condition were determined with respect to the corresponding averaged control values (before). Mean values are given ± SEM. Statistical analyses were performed with a commercially available software program (SPSS 11.0.1, SPSS Inc., Chicago, IL). One-way ANOVA followed by analysis of simple effect was used to compare changes in values. Change to probability (P) values less than 0.05 were considered statistically significant.
Maximal isometric voluntary plantar flexor force first decreased immediately after the fatiguing trial (−20%, P < 0.01), as did the corresponding EMG values (−17%, nonsignificant). These parameters recovered within 2 h (Fig. 2) and showed a second decrease 2 d after the fatiguing trial (for MVC: −6%, P < 0.05; for EMG: −14%), with full recovery at 8 d.
FIGURE 2-Bimodal cha...Image Tools
The level of central activation during isometric maximal condition showed a decline after the fatiguing trial (−9%, P < 0.05). This parameter also followed a bimodal pattern of recovery (Fig. 3). The same was observed also for H/M ratio (Fig. 4A). This ratio exhibited a 22% decline immediately after the fatiguing exercise (P < 0.05). It recovered again in 2 h, followed by a second decline (−23%, P < 0.05) 2 d after exercise. This latter value differed significantly from the one at the 8-d measurement point (P < 0.01). Peak-to-peak amplitudes of SLR are shown in Figure 4B. Two significant declines were observed for SLR after fatigue and 2 d after exercise (−19%, P < 0.05; −32%, P < 0.05). Although measured, SLR area is not reported here because it presents a redundant measure with peak-to-peak amplitude.
Figures 5 and 6 show, respectively, that IL-6 and LA concentrations peaked immediately after fatigue (P < 0.01). These parameters recovered progressively, but recovery took place faster for LA than for IL-6. PG E2 concentration (Fig. 5) peaked at 2 h after exercise (P < 0.05), followed by complete recovery at the 8-d point.
Leukocyte concentration peaked at 2 h after fatigue (+89%, P < 0.01; Fig. 7). Figure 8 shows a peak increase at 2 d after exercise for CRP concentration (+204%, P < 0.05, Fig. 8A), S-CK activity (+156%, P < 0.001, Fig. 8B), substance P concentration (+6%, P < 0.05; Fig. 8A), and muscle thickness (+7%, P < 0.001, Fig. 8B).
The major finding of the present study was the confirmation of the bimodal recovery of most of the measured parameters. The time course of decline and recovery in muscular force was paralleled by activation level, H/M ratio, and stretch reflexes. The acute (2 h after SSC exercise) changes in these measures are likely associated with the fatigue processes, and they correspond nicely with the production and clearance of LA, IL-6, and PG E2 concentrations. The subsequent decline (2 d) and recovery (8 d) of muscular force is likely associated with the processes of muscle damage (delayed onset of muscle soreness and muscle inflammation), corresponding with changes in CRP, substance P, and CK.
Acute changes after exhaustive SSC exercise.
In our study, the period after the SSC exercise was characterized by a decline in isometric force. This result was not surprising because several studies have reported similar changes after drop jumps with arms (16) or with legs (3,20). A decrease in muscle activation (EMG RMS amplitude) also has been reported to occur immediately after SSC exercise (32). The immediate reduction in EMG could indicate a decrease in central activation responsible for the subsequent decline in force. This hypothesis is supported by the decrease in activation level immediately after SSC exercise. However, the measurement was not sufficient to distinguish supraspinal fatigue and reflex adjustment of the neural activation. Moreover, the normalized H reflex (H/M ratio) exhibited a drastic reduction after the SSC protocol. This pattern was also observed for peak-to-peak amplitude of SLR. It is usually, although not always, agreed that SLR is mediated by Ia afferent fibers (18). Consequently, the first reduction of combined H/M ratio and SLR values indirectly support a possible presynaptic inhibition of Ia afferent fibers that could be the cause for the decline in maximal force and corresponding RMS EMG amplitude measured in our study. Several authors (5,11) have suggested that the presynaptic inhibition of Ia afferent fibers is partially mediated by activation of group III and IV afferent fibers. In addition, Pettorossi et al. (35) have shown that the presynaptic influence dominates the postsynaptic effects on the monosynaptic reflex after tetanic contractions. It is unfortunate that we could not measure directly the activity of group III and IV afferent fibers. Consequently, the following discussion must be considered with this limitation in mind.
As expected, LA increased immediately after the exercise, with a progressive fast recovery lasting between 5 min and 2 h. Group III and IV afferent fibers are strongly activated by LA (37) and H+ (41). At 2 h, we observed a peak increase in PG E2 concentrations, another specific activator of group III and IV afferent fibers (37). To the best of our knowledge, we have no information on the kinetics of the response of group III and IV afferent fibers to various concentrations of PG E2. We can only speculate that the response of group III and IV afferent fibers to this substance in combination with LA was maximal immediately after SSC exercise. Moreover, this peak increase in PG E2 concentration (2 h after the exercise) was observed when the partial recovery in force and reflexes took place. Another limitation of our study is that the highest value may not represent the actual physiological peak of the variable, because the times when the blood were drawn may have missed the true physiological peak of a variable in question. On the other hand, Marcos and Ribas (28) have reported an increase in peak concentration of potassium after dynamic exercise. Potassium is also known to be a potent stimulator of group III and IV afferent fibers (38) and probably acts in combination with LA.
A recovery was observed in maximal isometric force as well as in the corresponding RMS EMG 2 h after the exhaustive SSC exercise. LA concentration had also recovered. In line with this observation, Marcos and Ribas (28) have shown that potassium recovery is a very short-lasting (about 5 min) phenomenon. The present study showed that the recovery in force occurred in a way similar to that of the recovery in H/M ratio and in SLR, in response to stretching perturbations. This suggests a possible decrease or suppression of the presynaptic inhibition of Ia afferent fibers. Moreover, a recovery was also observed in the activation level. This may indicate probable deactivation of group III and IV afferent fibers after the decrease in activating metabolites. A peak increase in leukocytes was observed at this point, whereas IL-6 concentration exhibited a peak increase immediately after exercise. IL-6 is known to participate in reactions to produce increases in leukocyte concentration (27,34). Unfortunately, no knowledge is available to indicate what role IL-6 might play in activation of group III and IV afferent fibers. However, one study has shown that IL-6 activates mechanosensitive group IV afferent fibers (19). On the other hand, the increase in plasma concentration in leukocyte and its recovery suggests that these cells begin muscle infiltration to repair muscle damage inside the skeletal muscle (27,34).
Delayed changes after SSC exercise.
The observed secondary decline in maximal force and corresponding RMS is likely associated with the well-known inflammatory process related to muscle damage (12). Thus, as opposed to the acute changes, as observed in our study, metabolic disturbances could not be involved in this delayed force decrease because LA had already recovered. As in acute changes, it is interesting to note that H- and stretch reflexes as well as activation level behaved in a similar manner. These results could suggest occurrence of a secondary increase in presynaptic inhibition of Ia afferent fibers. Numerous studies report that muscle injuries after SSC exercise are associated with increased CK activity around the second day after this kind of exercise (5,12,20). Although we found similar results, we should be cautious in interpreting changes in CK activity, an indirect marker of muscle damage. Because inflammatory processes are correlated with muscle damage (1), it was interesting to analyze some delayed markers of inflammation, such as CRP (27). This molecule concentration exhibited a peak increase 2 d after the SSC exercise. During the inflammatory process, inflammatory cells (leukocytes) infiltrate the area of muscle damage (23) and could cause edema (39). This has been confirmed by the increase in muscle volume estimated by the measurement of muscle thickness (30). Moreover, these processes are associated with an increase in temperature (8) and are also correlated with increases in substance P (36). Circulating levels of substance P have been found to be elevated in humans only after exercise (25). A peak increase in substance P was measured in our experiment 2d after the SSC exercise. Substance P is well known to be a neurotransmitter released by group III and IV afferent fibers (21). Subsequently, substance P (10) and intramuscular pressure, more than other mechanical factors (15) reported 2 d after SSC exercise in the present experiment, could activate group III and IV afferent fibers. This notion could partly explain the secondary decline in force after SSC exercise.
The previous discussion is based primarily on the possibility that bimodal recovery pattern after exhaustive SSC exercise could be attributable to the neural pathways. In parallel or independently of the neural pathways, the fatigue-induced changes in muscular performance could also be related to mechanical changes in the muscle tissue. According to the review of Nicol and Komi (31), acute changes in performance could be induced by sarcomere-length instabilities caused by sarcolemmal, tubular system, muscle fiber, and sarcomere disruption and/or disorganization. The failure in cross-bridge detachment attributable to reduced oxidative capacity also could explain partly acute changes after fatigue. Several studies have proposed that the secondary decline in performance after exercise or SSC exercise could be caused by (i) change in passive stiffness in the injured muscle (20,22) or (ii) damage in intrafusal fiber, particularly at the level of structural proteins such as titin and desmin (5,22).
In conclusion, the immediate postexercise decline of performance could be induced by group III and IV afferent fiber activation caused by high LA concentration, in combination with probable increases in potassium outflow. Both of these parameters recover quickly (i.e., 2 h after exercise), leading to possible reductions of group III and IV afferent activation and force recovery. The events following the 2-h postexercise point are very likely related to muscle damage and associated inflammation. Group III and IV afferent fibers could probably be reactivated during the recovery period following the 2-h postexercise by mechanical factors such as muscle pressure and by the release of substance P. Independently of the neural pathway, muscle damage such as structural protein disruption could also be a cause for reductions in performance. It seems reasonable that muscular force-recovery processes might result from different combinations between activation of group III and IV afferent fibers by fatigue-induced factors and with parallel muscle damage and/or mechanical factors. This is in accordance with the concept of a task-dependent effect (31) of neuromuscular adjustment to fatigue. Indeed, Nicol and Komi (31) analyzed the relevant literature and have shown the flexibility of neural adjustment to meet the functional requirements of the muscle system. This flexibility depends clearly on the nature of the tasks and its intensities.
The authors would like to express their gratitude to Mr. Risto Puurtinen, Ms. Pirkko Puttonen, Ms. Marja-Liisa Romppanen, and Mr. Markku Ruuskanen for their technical assistance during the experiments.
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