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Muscle Fascicle and Tendon Behavior During Human Locomotion Revisited

Ishikawa, Masaki1,2; Komi, Paavo V.1

Exercise and Sport Sciences Reviews: October 2008 - Volume 36 - Issue 4 - p 193-199
doi: 10.1097/JES.0b013e3181878417
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High-speed ultrasonography has revealed that, in human locomotion, the nature of fascicle and tendon length changes varies depending on the task, contraction intensity, and the muscles involved. The findings emphasize that the active fascicles of the gastrocnemius muscle are suddenly stretched, although they are shortening. This short-lasting stretch triggers the stretch reflex, timing of which is dependent on running speed.

High-speed ultrasonography illustrates muscle- and task-specific behavior of fascicles and shows how the stretch reflex can be triggered during locomotion.

1Department of Biology of Physical Activity, Neuromuscular Research Center, University of Jyväskylä, Jyväskylä, Finland; and 2Osaka University of Health and Sport Sciences, Osaka, Japan

Address for correspondence: Masaki Ishikawa, Ph.D., Osaka University of Health and Sport Sciences, Asashirodai 1-1, Kumatori-Cho, Sennan-gun, Osaka, 590-0496, Japan (E-mail: masaki@ouhs.ac.jp).

Accepted for publication: March 8, 2008.

Associate Editor: Roger M. Enoka, Ph.D.

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INTRODUCTION

The exploration of muscle mechanics during natural human locomotion is a continuous challenge. The problems are obvious, particularly when the stretch-shortening cycle (SSC) of muscle function is considered. The SSC is reportedly the fundamental concept that describes skeletal muscle function in unrestricted human locomotion (23). By definition, SSC refers to a preactivated muscle, which undergoes stretching (eccentric action) before shortening (concentric action).

This sequence of stretching and shortening in natural situations (e.g., the contact phase of running in the triceps surae muscle) serves a fundamental purpose: to enhance a final push-off phase (concentric action) when compared with the concentric action performed without the preceding stretching phase (e.g., 23). More specifically, in addition to the metabolic loading, SSC actions are characterized by repeated impact loads and considerable stretch reflex activations. The experimental conditions required to achieve natural SSC performances are not always easy. The pioneering work of Cavagna et al. (2) introduced the SSC concept in isolated muscle preparations by using constant electrical stimulation throughout the cycle. In nature, however, skeletal muscle is very seldom, if at all, stimulated by constant activation signal. Consequently, in most locomotor tasks involving SSC actions, the muscle activation profile is variable and may not simply rely on central activation but on the reflex pathways as well (e.g., 22).

Human (or animal) skeletal muscle is, however, more than just a "muscle." It contains two basic elements: contractile and tensile. In the contractile element, bundles of fibers are called muscle fascicles, and they play an important role in the function of the entire muscle-tendon unit (MTU). By definition, the SSC involves the entire MTU, although the fascicles and tendons may experience different changes in length. Furthermore, synergists can also experience different length changes. For example, soleus and medial gastrocnemius (MG) show considerable difference in the activation strategy during the simple task of hopping (25). As the fascicles are controlled both by external stretch and internal activation, it is important to study the differences in length changes of fascicles and tendons in various muscles during SSC exercises. Ultrasonography is a technique, which can be used to study the fascicle and tendon length changes during movements. However, many of the earlier studies were unable to precisely identify how the fascicles behave in different muscles. In addition, because the muscle spindles are located inside the contractile tissue, it is important to determine the role that stretch reflexes may play during rapid and intensive SSC exercises. The ultrasound techniques that are currently used, with scanning rates of 25-50 Hz, may not be precise enough to characterize the movement of the fascicles. This may have caused misleading generalizations. Based on modern application of high-speed ultrasound scanning to the study of fascicle behavior, we present the hypotheses that, in addition to the existence of the stretch reflex potentiation during human SSC, changes in length of the fascicles and tendon, when acting together, depend on the movement task, movement intensity, and muscles involved.

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MONITORING MUSCLE FASCICLE BEHAVIOR IN DYNAMIC MOVEMENTS

The ultrasound probes that are currently used operate between 5 and 13 MHz and, when correctly attached over the muscle, are capable of scanning fascicles and tendons at a resolution range of 0.12-0.15 mm. Development of this technology has led to several new findings regarding fascicle behavior. For example, Fukunaga and colleagues (6) clearly demonstrated that the length change of the overall MTU is not the same as that of the muscle fascicles (c.f. 6,19) during human movements. An increase in the scanning frequency of ultrasonography (16-18) was an important step in the study of how fascicles and tendons truly interact in rapid SSC movements. It is now also possible to study whether (and how) stretch reflexes operate during the contact phase of SSC exercises, such as running and hopping. This fundamental question includes also the timing of the stretch to the muscle spindles that triggers the stretch reflex.

The measurement setup may have different requirements depending on the movement tasks in question. Figure 1A presents a situation where high-speed ultrasound scanning (96-169 Hz) of two muscles is performed while the subject is running on a 10-m-long force plate at various speeds. The setup is demanding because it requires two separate ultrasound machines placed on a carriage. The carriage is then pushed by the experimenter along a rail constructed at the side of the force plate system. The measurements can be combined with the recording of electromyogram (EMG) activities of the relevant muscles and/or direct in vivo measurements of the Achilles (and patellar) tendon forces (12,14). The results to be reported are very consistent and show typical intermuscular differences and reliable behavior of the single muscle.

Figure 1

Figure 1

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MOVEMENT TASK SPECIFICITY

Indirect modeling experiments of the behavior of the contractile and tensile components (fascicle and tendon) during SSC exercises suggest that tendons can operate as springs, with fascicles acting as tension generators that undergo little or no length changes and, hence, perform no mechanical work when the active MTU is lengthened during the eccentric phase of SSC (1,9,29). It has been suggested that during this action, muscle activation works to maintain a fixed contractile component (fascicles) length, which corresponds to the plateau phase of the estimated force-length relationship (e.g., 9). This effectively favors greater relative force generation in terms of the force-length and force-velocity properties of the contractile component. Maintenance of a fixed fascicle length during the muscle function has often been referred to as "concerted action" (1,8). It has been reported to take place in the MG muscle during the contact phase of human walking (5,6) and during low-intensity plantar flexion SSC exercises (18).

However, the force-length relationship of human skeletal muscle can adapt to the functional requirements of specific sport activities (7). Muscle activation can also be altered to adapt to the demands of the different SSC movement tasks (25). This indicates that the working length of muscle fibers may be also movement specific. Ultrasonographic studies of human fascicles have confirmed this assumption. During walking and running, the MG fascicles exhibited different patterns of behavior (Fig. 2B), when examined in the same subject group (16). In walking, the fascicles remained isometric (5) or even lengthened during the single-leg stance phase (25%-75% contact period in Fig. 2) similar to the MTU length changes (14,24). In running, however, the MG fascicles shortened throughout the entire contact phase after a clear short-lasting stretch of the fascicles (P < 0.05) (see "Role of the Stretch Reflex" section), although the stretch of the MTU was greater in terms of amplitude and velocity during running (Fig. 2B). In addition, the MG fascicles started to shorten just before contact in running because of the higher preactivation (P < 0.05). The length at which the fascicles operate may thus be different in walking than in running. In fact, after the fascicle length curves began to differ between running and walking during the MTU stretching phase (Fig. 2B), the difference was maintained statistically significant toward the end of contact phase. In walking, this fascicle length could correspond to the plateau part of the sarcomere force-length relationship (6,14). In running, it could correspond to the ascending limb of this force-length relationship (Fig. 3 in (16)).

Figure 2

Figure 2

One question that has yet to be answered is why the working length of the fascicles is not the same during running and walking. The shorter fascicle length during contact phase of running implies a reduced relative force output of the fascicles. However, the shorter fascicles may be beneficial as they result in a larger stretch of the tendon in running than in walking. The peak tendon length in Figure 2D was significantly greater in running than in walking (P < 0.05). It is therefore likely that, in running, where the MG fascicles are initially (at contact) very short and continue shortening during the short braking phase, the tendon stretch rate can be increased. The corresponding tendon recoil can then occur more rapidly because of the tendon's viscoelastic properties. Thus, no fixed "position" of the working length can be identified in the MG sarcomere force-length relationship for all SSC activities. It was also observed that the MG fascicle length was dependent on running speed so that it became shorter with higher speeds of running (17). It is therefore likely that regulation of MG fascicle length occurs in response to changes in effort intensity in specific SSC tasks to use tendon elasticity effectively.

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INTENSITY SPECIFICITY

The finding of a change in fascicle length with different movement tasks prompts further questions concerning whether the behavior of fascicle and tendon is modulated by movement efforts and intensities. For example, a common finding of drop jump studies is that as the height of the drop preceding the rebound is increased, performance can initially improve but will eventually decline (e.g., 20). This may imply that the behavior of fascicle and tendon differs when both impact (braking phase) loads and rebound efforts are involved and when these parameters are varied.

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Effects of Impact Load on Fascicle-Tendon Interaction

The rationale behind the possible modification of fascicle and tendon behavior with changes in impact force during the contact phase is based on the finding that muscle activation can vary depending on the impact loads (21). When the dropping height was varied and the subsequent jumping height was kept constant (13), the increased impact force resulted in shorter fascicle lengths of the examined vastus lateralis muscle at the peak MTU stretching point, with greater EMG activity during the braking phase. It also resulted in an increase in the amplitude and rate of tendon stretch, even when the stretch of the MTU was similar (Fig. 3A). The subsequent constant rebound performance was then associated with an increase in tendon recoil and reductions of EMG activity and fascicle shortening work during the push-off phase. Thus, in this experimental setup, tendons demonstrated shortening as a function of the preceding intensity of the impact loads. At the fascicle level, the push-off phase was characterized by the decreased EMG activities (P < 0.05) with the corresponding lengthening of fascicles in the higher drop height condition (Fig. 3A). This pattern of fascicle and tendon behavior during the push-off phase is in line with the concept of "timing of the muscle lengthening for effective release of elastic energy" proposed by Ettema (4). This could be interpreted to mean the reduction of fascicle work. A reduction of fascicle work with a concomitant increase of the storage and release of elastic energy in the tendons can explain how an increased impact load affects the efficiency of the push-off phase of SSC exercises.

Figure 3

Figure 3

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Effects of Push-off Intensity on Fascicle-Tendon Interaction

When drop jumps were performed from a constant drop height with variations in the subsequent push-off (rebound) heights (12), the preactivation and initial impact forces were similar because of the constant drop height (Fig. 3B). However, as the rebound height was increased up to maximal efforts, the EMG activation increased from the late braking phase, corresponding to the smaller fascicle stretch. This resulted in additional tendon stretch and recoil. This emphasizes the fact that the external stretch load in the braking phase is not the only factor that determines fascicle and tendon behavior during human SSC exercises. These results clearly indicate the existence of the push-off intensity-specific interactions between fascicles and tendons.

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Extremely High-Impact Loads

The fundamental rebound performance versus rebound height curves (e.g., 20) include conditions in which the performance decreases when a certain critical level of drop height is exceeded. Fascicle and tendon behavior can be used to explain this performance reduction. When the dropping height exceeded the optimal impact load before the rebound performance started to decrease, the MG fascicles were suddenly stretched during the braking phase (Fig. 4C), indicating a loss of tolerance of the MG fascicles to the high-impact loads (15,28). In the initial braking phase of these extreme drop height conditions, tendons can still be stretched rapidly and can reach high forces (Achilles tendon force: 10-12 times body weight) in the early braking phase (15). If the MG fascicles were able to tolerate this extremely high-impact braking phase, the elastic energy stored in the tendon could be increased and used during the push-off phase, or tendons could experience structural changes due to extreme strain. However, as a result of this sudden stretch of the fascicles during the braking phase (asterisk in Fig. 4C), the elastic energy stored in the tendon will be partially lost before the start of the push-off phase. Thus, the extremely high-drop conditions do not favor effective use of elastic energy in tendons or fascicles. When plotting the rate of change in the MG fascicle length against the Achilles tendon force slope measured during the braking phase of drop jumps, we obtain the relationship shown in Figure 5. The filled circle point of this quadratic relationship may be indicative of the critical stretch load for the MG fascicles to use tendon elasticity effectively (15,28).

Figure 4

Figure 4

Figure 5

Figure 5

The precise cause of this sudden MG fascicle stretch during the high-impact braking phase remains to be determined. Possible reasons for this behavior may be as follows: 1) the stretch load is so mechanically high and rapid that actin-myosin cross-bridge interactions are simply detached or slip apart, 2) inhibitory Golgi tendon responses aimed at injury protection may become more dominant, 3) increased central input may cause presynaptic Ia afferent inhibition as a protective strategy to prevent tendomuscular injury due to the high stretch load. All of these mechanisms may be operative either together or independently during extremely high-impact SSC exercises.

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MUSCLE SPECIFICITY

The preceding discussions of fascicle and tendon behavior during SSC exercises may seem relatively uncomplicated. Unfortunately, the observations previously presented cannot be generalized to the function of all skeletal muscles. In the same motor task, the muscles of the same and/or different joints may not behave similarly in terms of fascicle and tendon behavior. As already mentioned, the lengthening or shortening of the MG fascicles during SSC exercises can be varied to use tendon elasticity effectively and to facilitate protection from injury. In contrast, during the same SSC exercises, the fascicles of the synergistic soleus muscle exhibited a stretch-shortening behavior during the contact phase (Fig. 4) (28). When the drop jump was performed with an extremely high-drop height condition and maximal rebound effort, the soleus fascicle behavior was similar to that exhibited in the lower drop height conditions. They were thus still able to function "normally" without any additional rapid fascicle yielding. Interestingly, with increasing drop height, the peak tendon strain estimated during the contact phase remained the same in MG but increased in soleus. The observed differences in fascicle and tendon behavior between muscles may simply be related to differences in functional requirements between monoarticular and biarticular muscles (c.f. 14,15). The monoarticular soleus muscle may act mainly as a force generator or load bearer during SSC exercises, whereas the biarticular gastrocnemius muscle is likely to function as a fine tendon strain regulator. These different functions may not be surprising as the synergistic MG and soleus muscles respond selectively to an SSC task such as hopping (25). Regardless of the reason for the differences in fascicle behavior between the MG and soleus muscles during SSC exercises, muscle-specific behavior must be taken into consideration. It is possible that this specificity will become even more important when studies of fascicle and tendon behavior are extended to other muscles (e.g., arm muscles).

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ROLE OF THE STRETCH REFLEX

The matter of whether stretch reflexes operate in SSC actions, and how they operate, is somewhat controversial. It is difficult to imagine that proprioceptive reflexes, the existence of which has been known for centuries, would not play any role in human locomotion. It has been clearly demonstrated that the stretch reflex is important in stiffness regulation of isolated muscle (10), in the reduction of global EMG activity as demonstrated by ischemic blocking studies (3), and in the sensitivity of passively induced stretch reflexes and the M1 component in response to exhaustive SSC fatigue (c.f. 27). Therefore, it seems likely that the stretch reflex is of importance in human locomotion (22). However, the use of ultrasonography has given the impression that the MG fascicles are not rapidly stretched during the contact phase (5,12,14,18), implying that the stretch load and preactivation are not high enough to induce such a stretch. Conversely, when we started to work with higher frequencies of ultrasound scanning, a clear short-lived stretch of the MG fascicles occurred during the very early stance phase of running (Fig. 6B) (16,17), resulting in the occurrence of short-latency stretch reflexes (SLR) (Fig. 6A). We believe that this was simply due to the fact that the new scanning frequency was 96-169 Hz, which is much higher than what we and many others had routinely used before.

Figure 6

Figure 6

In the synergist soleus muscle, the muscle fascicles were stretched continuously during the braking (MTU stretching) phase, and the timing of the resulting stretch reflex was the same in different conditions. However, the timing of the short-lasting MG fascicle stretch differed between different conditions (17). Stiffness regulation of the MG fascicles due to the preactivation may affect this timing. For example, the MG fascicles shortened more clearly at a faster running speed (6.5 m·s−1) compared with slower speed running (5.0 m·s−1). Although a sudden fascicle stretch was evident in both conditions, its timing was slightly delayed at the faster running speed, where the MG fascicle stretch occurred approximately 26 ms after ground contact (18 ms in the 5.0-m·s−1 condition), and the corresponding peak SLR occurred approximately 69 ms (56 ms in the 5.0-m·s−1 condition) after ground contact. The end of the braking phase was approximately 68 ms and 87 ms after ground contact in the 6.5- and 5.0-m·s−1conditions, respectively (Fig. 6). When we consider the electromechanical delay (10-15 ms) between the onset of SLR activities and the mechanical response (26), it is clear that SLR activities can still contribute to force enhancement during the push-off phase in the 6.5-m·s−1 condition. Consequently, the results imply that the MG SLR during the stance phase of running either influences fascicle stiffness in the braking phase of slower speed running (5.0 m·s−1) or stretch-induced force potentiation during the push-off phase of faster running (6.5 m·s−1) and that the contribution of the stretch reflex can be specific depending on running speed. The occurrence of a sudden MG fascicle stretch during the braking phase of running is a unique but expected finding and in accordance with the logical nature of the stretch reflex contribution.

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CONCLUSIONS AND PERSPECTIVES

The MG muscle is perhaps the most frequently studied muscle with regard to fascicle and tendon behavior in locomotion. When involved in SSC actions, the MG fascicle length is continuously modulated for two purposes: 1) optimal force production in terms of sarcomere force-length and force-velocity properties; 2) effective use of tendon elasticity. The patterns of these modulations cannot be generalized to all types of SSC activities and movement intensities. In this report, we have attempted to provide evidence that, when performing natural locomotion involving the SSC, human skeletal muscle may not exhibit a fixed pattern of fascicle and tendon behavior. Within a muscle, this pattern is modulated under the varied conditions of exercise, including both the preactivated impact loads and intensity effort levels of the final push-off phase of SSC. It is important to note that these modulations are considerably different between muscles, even when they are involved as synergists in the same motor tasks. These observations have been based on the use of modern high-speed ultrasonographic scanning to examine muscle fascicle and tendon length changes during locomotion. The methodology that was used was also able to provide convincing support for the role of stretch reflexes in SSC exercises. Notwithstanding, there are still a great number of considerations regarding fascicle and tendon behavior (Fig. 7). For example, fascicle and tendon behavior is likely to differ between young and elderly subjects during SSC exercises (11,24), as well as before and after fatigue and before and after training adaptations. In addition, stretching of the tendinous tissues, which include the thick outer tendon and thin aponeurosis sheets, may be unequally distributed and have different roles during SSC exercises.

Figure 7

Figure 7

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Acknowledgment

The authors thank Mr. N. Cronin for checking the English language.

The study was supported by a grant 88/627/2005 from the Ministry of Education, Finland.

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Keywords:

muscle fiber; gait; ultrasonography; tendon elasticity; muscle mechanics

©2008 The American College of Sports Medicine