Human movement is performed by contractions of muscle fibers that are connected to tendons to compose muscle-tendon complex (MTC). Muscle fibers not only transmit force to tendons, but also interact with them due to tendon compliance. Therefore, to know functional characteristics of muscle fiber and tendon during human movements, we need to measure directly and successively the in vivo geometric arrangements of muscle and tendon. This article reviews our recent approaches to estimate interactions between muscle fibers and tendinous tissues during human movements using ultrasonography.
In Vivo Estimation of Architecture of MTC by Real-Time Ultrasonography
To estimate the geometric arrangements of the MTC for leg muscles (i.e., vastus lateralis, VL; gastrocnemius medialis, MG; tibialis anterior, TA), we used ultrasonography. The ultrasonic apparatus (SSD-2000, ALOKA, Okayama, Japan) was constructed with an electronic linear array probe of 7.5-MHz wave frequency that was attached to the dermal surface longitudinally along the muscle of interest. The echoes from interfascicle connective tissues were visualized, and the length and angle of the fascicle were measured (Fig. 1). The precision and linearity of this technique for estimating the length of fascicle and tendon and the pennation angle have been confirmed (5,6,7,9,12,13).
The architectural characteristics of the VL, MG, and TA muscles are summarized in Table 1. The MG has shorter fascicle lengths and longer tendinous tissues compared with the other two muscles. Thus, the ratios of tendinous-tissue length to fascicle length are greater in MG than in TA and VL.
Because a muscle fiber consists of sarcomeres in series, the muscle fiber length (i.e., number of sarcomeres in series) indicates the velocity potential of a muscle during a contraction. The TA and VL are composed of longer fascicles and, therefore, have a greater velocity potential. In contrast, due to the compliance of tendon (5,6,9,12,13) and longer tendinous tissues, the MG has a greater potential to store elastic energy.
Estimation of Elastic Property in Tendinous Tissues
Visualizing of muscle and tendon with real-time ultrasonic images made it possible to estimate the elastic properties of tendon in vivo in the humans (5,9,12). On the longitudinal ultrasonic image, we can define the intersection point (P) of the echo from one fascicle on the aponeurosis. The point P moves proximally during a muscle action when the joint is fixed; that is, during an “isometric” action (Fig. 1). The distance traveled by the P indicates the length change (elongation) of tendinous tissues during the contraction. The strain of the tendinous tissues can be estimated from the tendon elongation relative to the initial length of the distal tendon, which was estimated over the skin. The strain increased nonlinearly with increasing joint torque, and the maximal strain was observed when the joint torque was maximal. The maximal strain was greater in VL and MG than in TA.
The tendinous tissues consist of outer tendon and aponeurosis. One question we considered is whether the elastic strain of the outer tendon and aponeurosis is the same or not? We measured the length changes of the Achilles tendon and aponeurosis for MG and TA. There was no significant difference in the strain at a given contraction intensity (%MVC) between the Achilles tendon and aponeurosis (Fig. 2). In addition, there was no difference in the strain of the distal and proximal aponeurosis of MG (13) or TA (12).
We observed that the strain along the tendinous tissues in MG and TA was homogeneous. This was in accordance with a previous report that the thickness of the aponeurosis systematically decreases as it extends from the muscle-tendon junction to the muscle belly, which parallels changes in the force exerted on the aponeurosis (16). Conversely, heterogeneity of the strain along the tendinous tissues would predispose the region with larger strain to greater damage. The observation of homogeneous strain in tendinous tissues indicates that there is not a region of greater relative weakness.
When the TA was activated isometrically, a curvilinear relation was observed between lengthening of tendinous tissues and tendon force (Fig. 3). The linear region, with an approximately constant modulus of elasticity after the toe region, was used to determine tendon stiffness. To calculate tendon stress, a cross-sectional image of the distal tendon of TA was taken by using ultrasongraphy (5), which enabled the force-length relation for tendinous tissues to be converted to a stress-strain relation (Fig. 3). The corresponding Young’s modulus was found to increase with the tendon force.
The maximal strain was the greatest in VL and least in TA (Table 2), suggesting that the functional properties of the MTC differ significantly among muscles. The elasticity of tendon is advantageous when the tendon acts as a spring. In daily human movement, such as locomotion, VL and MG are activated as main agonist muscles to propel the body, and the relatively compliant tendinous tissues in VL and MG (i.e., lower Young’s modulus and higher strain) have a greater capacity to store and reuse the elastic energy. In contrast, TA does not exert a propulsive force but controls ankle position during locomotion and has a lower strain and Young’s modulus so that the tendinous tissues do not impede the control of fine movement (14).
Estimation of Internal Shortening of Fascicle
When the joint torque increases at a fixed joint angles, the muscle performs an isometric action and the fascicles shorten, which we refer to as internal shortening (Table 2). Changes in the internal shortening of fascicle and tendon strain were presented as a function of contraction intensity (%MVC) for TA, MG, and VL (Fig. 4). Internal shortening decreased and tendon strain increased in %MVC in each muscle. Smaller internal shortening and higher tendon strain was observed in TA compared with MG and VL. It is likely that the magnitude of internal shortening of the fascile depends on such architectural factors as the tendon-length to fiber-length ratio and the elastic property of tendinous tissues. More internal fiber shortening has been observed in isolated muscles with higher tendon-length to fiber-length ratio (16). However, significantly lower internal shortening was found in TA than in VL, although the tendon-length to fiber-length ratios were almost identical. The smaller internal shortening of TA, therefore, may be caused by significantly higher Young’s modulus of TA tendon compared with other muscles. On the contrary, the internal shortening of MG was larger, which would have been caused by significantly higher tendon-length to fascicle-length ratio and lower Young’s modulus of MG tendon (Table 2, Fig. 5).
Behavior of Muscle Fiber and Tendon During Human Movements
Changes in the lengths of the fascicle and tendinous tissues were estimated during ankle-bending exercise, jumping, walking, and bicycle pedaling (Fig. 6).
1. Ankle-bending exercise
The behavior of fascicle and tendinous tissues for MG were observed during a heel-up and heel-down exercise. Subjects lowered their heels (dorsiflexion) from a toe-standing position and immediately raised them (plantar flexion) back to a toe-standing position at low and high frequencies. When the exercise was performed at a rapid rate, the fascicle length of MG showed no significant changes in the first half of the plantar flexion phase with higher EMG activation, whereas the tendinous tissues shortened abruptly (8). This indicates that the MG fiber acts in a nearly isometric manner just after the end of the transition from dorsiflexion to plantar flexion.
2. Vertical jumping
To estimate the behavior of the fascicle and tendinous tissues during a squat jump, a sequence of ultrasonic images were taken from MG. In the first half of push-off phase, there was a shortening of the fascicle (26%) and a lengthening of the tendinous tissues (6%) whereas the MTC length remained constant. In contrast, the fascicle contracted nearly isometrically before take-off, as indicated by an abrupt shortening of both tendinous tissues and MTC (5%). We found that the mechanical energy generated by the muscle contraction in the early push-off phase was stored predominantly in the tendinous tissues as elastic energy (5 J) and 88% of the stored energy (4.4 J) was reused before take-off (10).
We investigated length changes in the fascicles and tendinous tissues of MG during walking. In the stance phase, the MG muscle was active and the fascicles maintained constant length (nearly 50 mm) as the tendinous tissues was stretched by 7 mm. In the push-off phase, both the MTC and tendinous tissues shortened rapidly. These results show that MG fascicle was activated nearly isometrically during walking, whereas the tendinous tissues performed a stretch-recoil cycle (2).
4. Bicycle pedaling
Ultrasonic images were obtained from VL during bicycle pedaling at 98 W at 40 rpm. The fascicle length of VL shortened from 127 to 91 mm during the knee-extension phase, whereas the tendinous tissues were elongated by 10 mm. The average shortening velocity of the fascicle increased by 50% early in the knee-extension phase and decreased by 29% in latter half of that phase, compared with that of the MTC. The maximal shortening velocity of the fascicle was 22% less than that of MTC. These results suggest that the elasticity of the tendinous tissues enabled the VL fascicles to develop force with lower contraction velocity than MTC (11).
Length-Force Characteristics of Muscle Fiber During Human Movements
It is known that the length of the sarcomeres in a muscle influences the force generated by the muscle fiber. The sarcomere length can be estimated by dividing the fascicle length by the average number of sarcomeres in series within the fascicles (1). The average sarcomere length during human movements was estimated and superimposed on a sarcomere length-force relation for human muscle derived from the data of Walker and Schrodt (15). The results indicate that the working ranges of sarcomere length are over the plateau and the upper part of both descending and ascending limbs, where a relatively larger force can be generated (Fig. 7).
Taken together, these results indicate that in such stretch-shortening cycle exercises as ankle bending, jumping, and walking, the muscle fiber can contract with a nearly constant fiber length, which is around the plateau region of the sarcomere force-length curve. This quasi-isometric contraction of muscle fiber was caused by lengthening-shortening behavior of tendinous tissues (catapult action) (4). In contrast, in activities that do not employ the stretch-shorten cycle, such as bicycle pedaling, the muscle fiber can contract at a relatively lower velocity than the shortening velocity of MTC, which is advantageous for the force production by the muscle fiber.
Real-time ultrasonography enabled in vivo scanning of the MTC and a realistic determination of the interactions between muscle and tendon during human movement. The results indicate that the tendinous tissues are quite compliant and that the elastic differs among muscles. Internal shortening of the fascicle during a contraction was facilitated by the tendon elasticity. In human movements such as jumping, walking, and ankle bending, the muscle fiber contracts at a nearly constant length, whereas the tendon performs a stretch-shorten cycle. These results indicate that the human MTC is designed to match the capacity of muscle to generate force and the elasticity of tendon for efficient movement performance.
1. Bobbert, M. F., Huijing, P. A. van Ingen Schenau. G. A. A model of the human triceps surae muscle-tendon complex applied to jumping. J. Biomech. 19: 887–898, 1986.
2. Fukunaga, T., Kubo, K. Kawakami, Y. Fukashiro, S. Kanehisa H. Maganaris C. N. In vivo behavior of human muscle tendon during walking. Proc. Roy. Soc. Lond. B. 268: 1–5, 2000
3. Griffiths, R. I. Shortening of muscle fibers during stretch of the active cat medial gastrocnemius muscle: The role of tendon compliance. J. Physiol. 436: 219–236, 1991.
4. Hof, A. L., Geelen, B. A. Van den Berg. J. Calf muscle moment, work and efficiency in level walking: Role of series elasticity
. J. Biomech. 16: 523–537, 1983.
5. Ito, M., Kawakami, Y. Ichinose, Y. Fukashiro S. Fukunaga. T. Nonisometiric behavior of fascicle
during isometric contractions of a human muscle. J. Appl. Physiol. 85: 1230–1235, 1998.
6. Kawakami, Y., Ichinose, Y. Fukunaga. T. Architectural and functional features of human triceps surae muscles during contraction. J. Appl. Physiol. 85: 398–404, 1998.
7. Kawakami, Y., Ichinose, Y. Kubo, K. Ito, M. Imai M. Fukunaga. T. Architecture of contracting human muscles and its functional significance. J. Appl. Biomech. 16: 88–98, 2000.
8. Kubo, K., Kanehisa, H. Takeshita, D. Kawakami, Y. Fukashiro S. Fukunaga. T. In vivo dynamics of human medial gastrocnemius muscle-tendon complex during stretch-shortening cycle exercise. Acta Physiol. Scand. 170: 127–135, 2000.
9. Kubo, K., Kawakami Y. Fukunaga. T. Influence of elastic properties of tendon structures on jump performance in humans. J. Appl. Physiol. 87: 2090–2096, 1999.
10. Kurokawa, S., Fukunaga T. Fukashiro. S. Behavior of fascicles and tendinous structures of human gastrocnemius during vertical jumping. J. Appl. Physiol. 90: 1349–1358, 2001.
11. Muraoka, T., Kawakami, Y. Tachi, M. Fukunaga. T. Muscle fiber and tendon length changes in the human vastus lateralis during slow pedaling. J. Appl. Physiol. 91: 2035–2040, 2001.
12. Muramatsu, T., Muraoka, T. Takeshita, D. Kawakami Y. Fukunaga. T. In vivo mechanical properties of proximal and distal aponeurosis in human tibialis anterior muscle. Cells Tissues Organs. 170: 162–169, 2002.
13. Muramatsu, T., Muraoka, T. Takeshita, D. Kawakami, Y. Hirano Y. Fukunaga. T. Mechanical properties of tendon and aponeurosis of human gastrocnemius muscle in vivo. J. Appl. Physiol. 90: 1671–1678, 2001.
14. Proske, V. Morgan. D. L. Tendon stiffness: methods of measurement and significance for the control of movement. J. Biomech. 20: 75–82, 1987.
15. Walker, S. M., Schrodt. G. R. I segment length and thin filament periods in skeletal muscle fibers of the Rhesus monkey and the human. Anat. Rec. 178: 63–82, 1973.
16. Zajac, F. E. Muscle and tendon: properties, models, scaling and application to biomechanics and motor control. Crit. Rev. Biomed. Engl. 17: 359–411, 1989.