Deterioration in athletic performance during practice and competition is generally attributed to “fatigue,” without a great deal of consideration for the exact cause(s) of the fatigue or the type of fatigue that is occurring. When analyzed from a movement analysis perspective, all sports activities can be described as a combination of concentric, isometric, and eccentric muscle actions. The relative contribution of each of these muscle action types to the activity obviously varies from one sport to the next. However, an understanding of the metabolic and physical demands of the 3 contraction types is important in discerning the cause(s) for deteriorations in performance.
Eccentric muscle actions are unique in the sense that they are most responsible for the muscle soreness felt 24–72 hours after unaccustomed exercise; commonly referred to as delayed-onset muscle soreness (DOMS) (1,6,19). This does not mean that concentric and isometric muscle actions cannot cause low levels of muscle soreness. However, it has been well documented (7,14,15) that activities with a high intensity or a high volume of eccentric muscle actions or both elicit the greatest levels of muscle soreness. Although many theories have been proposed to isolate the cause for DOMS, it is generally accepted that the pain reflects an injury response to microtrauma (2,11,19,23). This microtrauma is additionally important from a functional standpoint because it is also the cause for the acute decrements in strength and power that occur immediately after eccentric exercise (8,10). Mechanical disruption of the structural and contractile proteins is a logical explanation for at least part of this performance decrement (20). However, substantial evidence suggests that there is also a neural component to eccentric exercise–induced strength loss (9,21,24,28,29). Also, recent investigations (24,28) have reported acute decreases in surface electromyographic (EMG) amplitude after eccentric exercise. Whether these decreases in muscle activation are the result of decruitment of motor units, reductions in motor unit firing rates, a combination of both, or potentially some other factor remains to be seen.
However, concentric exercise does not cause muscle damage, so any acute decrements in performance are because of more traditional fatigue-related phenomena, such as metabolite accumulation and substrate depletion (12,13,18). Interestingly, similar decreases in EMG amplitude have been reported after concentric exercise as those after eccentric exercise (28). However, given the distinct differences between these 2 types of exercise, it would not be appropriate to assume that the same mechanism is causing these decrements in muscle activation. Further research is needed to investigate the etiology of these decreases in EMG amplitude.
Additionally, it is unclear if unilateral concentric or eccentric exercise affects the motor control properties of the contralateral limb. The known neural pathways responsible for cross-education suggest that a contralateral crossover effect could occur, and this crossover effect could differ between concentric and eccentric exercises. However, to our knowledge, no previous investigations have examined this issue. The results from a study that examines the potential crossover effect of exercise-induced force loss are important from a functional standpoint because they provide coaches and practitioners with information regarding the cause(s) for unilateral performance decrements. Many sporting activities have a unilateral component (e.g., arm wrestling, gymnastics, track and field jumpers, baseball pitchers, and the like), so improving our understanding of why performance decreases after unilateral activities is important from a coaching perspective. Thus, the purpose of this study was to examine the EMG intensity patterns after unilateral concentric vs. eccentric exercise in the dominant (DOM) and nondominant (NONDOM) forearm flexors. We hypothesize that there will be differences between the intensity patterns after concentric vs. eccentric exercise. In addition, these differences will be evident for both the exercised and nonexercised contralateral limbs. This investigation serves as a follow-up to the original study by Ye et al. (28), who reported decreases in strength and EMG amplitude after both concentric and eccentric exercises of the forearm flexors. However, the cause(s) for the decrease in EMG amplitude could not be discerned (28). It is the aim of this study to try to shed light on this very issue.
Experimental Approach to the Problem
This study used a within-subjects design to examine 2 problems: (a) if there is a difference between the acute effects of unilateral concentric vs. eccentric exercise on the muscle activation pattern of the biceps brachii and (b) if these potential changes in the muscle activation pattern after exercise occur for both the DOM, exercised, and NONDOM, nonexercised limbs. The concentric and eccentric exercise interventions were randomly ordered and performed on days separated by at least 48 hours of rest. A bipolar surface EMG signal was detected from the biceps brachii during isometric maximum voluntary contractions (MVCs) of the forearm flexors. The MVCs were performed before (PRE) and immediately after (POST) the concentric and eccentric exercise interventions. The resulting EMG signal during each MVC was analyzed with a wavelet analysis, and the resulting intensity pattern was further processed with a paired pattern classification procedure. The randomized nature of the concentric and eccentric exercise protocols allowed for unequivocal determination of differences in how the 2 contraction types affected the neuromuscular system. Furthermore, the fact that the exercise was unilateral gave us the opportunity to isolate the purely neural mechanisms, without any possible contribution from mechanical factors.
Twenty-six healthy men (mean ± SD: age, 24.0 ± 3.7 years; range, 20.0–25.0 years; height, 179.8 ± 6.3 cm; bodyweight, 86.8 ± 14.1 kg) volunteered to participate in this investigation. The study was approved by the Institutional Review Board for Human Subjects of the University of Oklahoma, and all subjects signed an informed consent form and completed a health history questionnaire before testing. The purpose of the study and all testing procedures were fully described to the subjects before signing the informed consent form, and the subjects were provided with as much time as they needed to make a decision about whether to participate. All subjects were recreationally active (i.e., were currently performing at least 2 resistance or aerobic training sessions or both per week) and reported no current or recent neuromuscular or musculoskeletal disorders that could have affected the outcome of the study. In addition, all subjects were instructed to maintain their normal dietary and sleep habits during the study and to refrain from using ice or any other medications to control soreness from the eccentric muscle actions. The time of day that each subject was tested was also kept as consistent as possible.
The purpose of the first visit to the laboratory was to familiarize the subjects with the strength testing procedures. All subjects were tested for unilateral strength of the DOM (based on throwing preference) and NONDOM forearm flexors. The isometric muscle actions were performed in a custom-built apparatus designed specifically for isometric testing of the forearm flexors (Figure 1). The subjects were in an upright, seated position for each muscle action, with the elbow in a padded cuff, and a 90° angle between the arm and the forearm. Isometric forearm flexion force was measured with an S-beam load cell (Model SSM-AJ-500; Interface, Inc., Scottsdale, AZ, USA). One end of the load cell was fixed to the isometric testing apparatus, and the other end was attached to a padded strap that was placed around the subject's wrist. The purpose of the wrist strap (as opposed to a handle that would be grasped by the subject's hand) was to isolate the forearm flexors and eliminate any possible contribution of the hand flexors to isometric force production. The subjects began the familiarization session by performing a warm-up of 5 separate 6-second isometric muscle actions of the DOM forearm flexors. The subjects were instructed to provide an effort corresponding to approximately 50% of their maximum for each muscle action, with 30 seconds of rest between the muscle actions. Following the warm-up and a 2-minute rest period, the subjects performed 2 separate 6-second isometric MVCs of the DOM forearm flexors, with 2 minutes of rest between the MVCs. The padded wrist strap was then placed around the wrist of the NONDOM arm, and the warm-up and MVC testing procedure were repeated and performed in the same manner as that for the DOM arm. Following the isometric testing, the subjects were removed from the isometric strength testing apparatus and seated in front of a calibrated Loredan isokinetic dynamometer (LIDO Multi-Joint II; Loredan Biomedical, West Sacramento, CA, USA). The subjects then practiced maximal concentric isokinetic and eccentric isokinetic muscle actions of the DOM forearm flexors at a velocity of 30°·s−1. Specifically, the subjects first practiced 10 consecutive maximal concentric isokinetic muscle actions. These muscle actions were followed by 30 seconds of rest and then 10 consecutive maximal eccentric isokinetic muscle actions. The subjects were provided with strong verbal encouragement to produce maximum torque during both the concentric isokinetic and eccentric isokinetic muscle actions. Following the maximal isokinetic muscle actions, the subjects were removed from the dynamometer and allowed to leave the laboratory. It should be noted that the purpose of the familiarization session was only to provide the subjects with practice for the subsequent testing sessions and to remove any possible learning effect. Thus, no data were collected during the familiarization session.
Following a minimum of 48 hours of rest, the subjects returned to the laboratory for the first of 2 randomly ordered isometric testing sessions. During these sessions, the subjects performed the isometric strength testing of the DOM and NONDOM arms in a randomized order but with the same procedures that were used during the familiarization session. For both the DOM and NONDOM arms, the highest force output from the 2 maximal muscle actions was designated as the PRE isometric strength value. The subjects then performed either the maximal concentric isokinetic or the eccentric isokinetic exercise protocol on the Loredan isokinetic dynamometer. This protocol required the subjects to perform 6 sets of 10 maximal isokinetic muscle actions of the DOM forearm flexors, with 2 minutes of rest between each set. The subjects received strong verbal encouragement to provide maximum effort during each muscle action. Immediately after the maximal isokinetic muscle actions, the subjects were placed back on the isometric strength testing apparatus and performed the POST isometric strength testing in the same manner as the PRE testing. The subjects were then allowed to leave the laboratory and were provided with 72 hours of rest before they had to return to perform the same testing sequence but with the opposite exercise intervention. Thus, if the subjects performed the maximal concentric isokinetic exercise during the first testing session, they performed the maximal eccentric isokinetic exercise for the second testing session and vice versa.
A bipolar surface EMG signal was detected from the biceps brachii with a preamplified EMG sensor (DE-2.1; Delsys, Inc., Boston, MA, USA). This sensor uses 2 silver bars (10.0 × 1.0 mm) with an interelectrode distance of 10.0 mm. Before placing the sensor over the biceps brachii, the skin on the anterior portion of the arm was prepared by careful shaving and cleansing with rubbing alcohol. The sensor was then placed over the biceps brachii in accordance with the recommendations from the SENIAM project (17), with the reference electrode located over the C7 vertebrae. The skin where the sensor was placed was also marked with a permanent marker to ensure a consistent sensor location between the 2 trials.
The analog EMG signal from the biceps brachii was preamplified, band-pass filtered from 20 to 500 Hz, and sampled at a rate of 20,000 samples per second. These data were stored in a personal computer for subsequent analyses. The portion of the EMG signal that corresponded to the 2-second period with the highest force production was selected for further signal processing. The selected EMG signals were then processed with the wavelet analysis described by von Tscharner (25). This analysis has been discussed in detail in the original publication (25), so only a cursory description will be given here. Briefly, however, this analysis uses a filter bank of 11 nonlinearly scaled Cauchy wavelets to separate the EMG signal into partially overlapping frequency bands. These wavelets are optimized to provide the best possible compromise between time and frequency resolution for surface EMG signals (25). The result of the wavelet analysis is an intensity pattern that shows the time locations and frequency distributions of the events that comprise the EMG signal (Figure 1). The intensity pattern for each EMG signal was then downsampled by a factor of 10 for further processing. This processing involved a paired pattern classification procedure that has been described in previous publications (3,4). This procedure is based on an adaptation of the original method that was described by von Tscharner and Goepfert (26). The interested reader is encouraged to consult the previous publications (3,4,26) for the details regarding these procedures. Briefly, however, the procedure uses a principal component analysis to project the intensity patterns into a multidimensional pattern space (26). Once projected into this space, the best possible discriminant between the patterns from the 2 testing occasions can be established, thereby allowing for determination of the separability of the intensity patterns. The paired pattern classification can then be done using the “leave-one-out” cross-validation method (26). This technique involves removing an intensity pattern from the data set, reestablishing pattern space and the discriminant, and projecting the removed pattern into pattern space to see if it was classified correctly. This was repeated for all patterns, and the percentage of correctly classified patterns was determined. A binomial test was used to determine if the overall classification was significantly better than random at an alpha level of ≤0.05.
Four separate paired pattern classification analyses were performed: DOM limb PRE vs. POST concentric exercise, DOM limb PRE vs. POST eccentric exercise, NONDOM limb PRE vs. POST concentric exercise, and NONDOM limb PRE vs. POST eccentric exercise. The results from these classifications are shown in Table 1. Of the 4 classifications that were performed, the only one that was significantly better than random was for the DOM limb when comparing PRE vs. POST eccentric exercise.
The present study provided 2 important findings: (a) the acute effects of eccentric exercise on the patterns of neuromuscular activation are different from those of concentric exercise and (b) the pattern of neuromuscular activation is affected differently for the exercised vs. nonexercised limbs. These results are significant from the standpoint that they serve as a follow-up to the original study by Ye et al. (28). As discussed by the authors (28), the concentric and eccentric isokinetic exercise interventions resulted in similar (17 and 21%) decreases in isometric strength. However, the authors (28) also reported similar decreases in EMG amplitude following the concentric and eccentric isokinetic exercise interventions. It was suggested (28) that at least part of the strength losses after both concentric and eccentric exercises was the result of neural factors. However, an important limitation is that the etiology of these neural factors could not be determined. For example, the decreases in EMG amplitude could have been the result of a reduced number of active motor units, lower firing rates, a combination of these 2 factors, or any other neural factor that can decrease EMG amplitude. The inability to get any information about which of these factors is most important served as one of the major driving factors for conducting the present study.
Our results indicated that the differences between the EMG signals from before vs. after the eccentric exercise could not be localized to any specific bandwidth. The difference intensity pattern and intensity pattern for the t-vector shown in Figures 1B, C, respectively, demonstrated inconsistency in both the time locations and the bandwidths of the events that make up these patterns. An important consideration when analyzing EMG intensity patterns is that they provide information regarding the “macroscopic aspects” of muscle contraction (26). This requires a very different interpretation from traditional EMG variables, such as EMG amplitude, center frequency, conduction velocity, and the like, which are useful in obtaining information about the macroscopic aspects (e.g., muscle activation, firing rate patterns, synchronization, and the like) of muscle contraction. As discussed by von Tscharner and Goepfert (26), analyzing EMG intensity patterns is a meticulous process that requires the researcher to be aware of the many ways that the intensity pattern can change. The timing, magnitude, and frequency aspects of muscle activation are all important features of an EMG intensity pattern that can change because of an intervention.
The fact that the eccentric exercise had an acute effect on the muscle activation pattern of the biceps brachii is important because it suggested that the microtrauma caused by the eccentric exercise influenced both the amount of activation sent to the muscle by the central nervous system and also the pattern of that activation. Several studies (5,16,22,27) have reported changes in the proprioceptive feedback immediately after eccentric exercise. Saxton et al. (22) found increases in physiological tremor of the forearm flexors immediately after an eccentric exercise protocol. The authors (22) speculated that possible damage to afferent receptors within the skeletal muscle and tendonous regions could be responsible for reduced proprioception, thereby diminishing the ability to maintain constant neural drive to the muscle. The suggestion that eccentric exercise may cause damage to a component of the afferent skeletal muscle pathway is important because it suggests that the extrafusal fibers are not the only fibers damaged with eccentric exercise. The results of Brockett et al. (5) provided further support for this hypothesis. Specifically, the authors (5) reported reduced position sense (i.e., a distorted perception of where their arm was located in space) after eccentric exercise of the forearm flexors. The subjects also demonstrated a reduced ability to perceive forearm flexion force because they typically undershot a target force by 10% MVC. The authors (5) hypothesized that the eccentric exercise protocol damaged the muscle spindles and golgi tendon organs, thereby decreasing both the positional and force awareness senses of the subjects. Weerakkody et al. (27) also reported alterations in the muscle spindle response after eccentric exercise of the plantar flexors. Also, Gregory et al. (16) found an increase in golgi tendon organ activity after eccentric exercise of the cat medial gastrocnemius, thereby supporting the possibility of changes in proprioception and motor control after eccentric exercise. It is important to note that our results do not directly verify eccentric exercise–induced damage to muscle spindles or golgi tendon organs. However, the fact that both the magnitude and the overall pattern of muscle activation were altered by the eccentric exercise suggests that the spindles or golgi tendon organs or both could potentially have been involved. Additional research is needed to further investigate this issue.
In summary, our findings demonstrated that a bout of eccentric exercise designed to mimic a traditional resistance training protocol acutely affected the muscle activation pattern of the biceps brachii of the DOM, exercised limb. However, the muscle activation pattern of the same limb was unaffected by a comparable volume of concentric exercise, and the NONDOM, unexercised limb, was not affected by either exercise protocol. These findings are important from a mechanistic standpoint because they suggest that microtrauma after eccentric exercise that is responsible for strength loss and DOMS also affects the way that the central nervous system controls the muscle. We hypothesize that eccentric exercise–induced damage to some component(s) of the peripheral afferent feedback system, possibly the muscle spindles or golgi tendon organs or both, could be affecting muscle activation. This feedback would not only reduce the overall central drive to the muscle but also significantly alter the overall pattern of muscle activation.
Our findings indicated that eccentric exercise had a unique effect on the neuromuscular system. It is possible that the responses of the muscle spindles or golgi tendon organs or both were altered by the eccentric exercise, thereby influencing the muscle activation pattern that is used to activate the forearm flexors. These results are important for coaches and athletes involved in sports who have a high eccentric component. It is well established that acute strength losses after eccentric exercise are the result of a combination of mechanical and neural factors. Disruption of structural and contractile proteins within the muscle provides a clear mechanical mechanism for reducing the force-producing capabilities of the muscle. However, there is less clarity regarding the neural component of this strength loss. Specifically, is there damage to the intrafusal fibers that could potentially reduce the overall neural drive to the muscle during high-intensity contractions? Our findings support this hypothesis and suggest that training programs with a high eccentric component could be helpful for “toughening up” the muscle and reducing eccentric exercise–induced force loss. These results are also important for coaches and practitioners because they provide information regarding neuromuscular mechanisms underlying bilateral force loss from unilateral exercise. Decreases in performance of the nonexercised limb are therefore the result of neural rather than mechanical factors.
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