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Commentary to Accompany

Tendons: Energy Managers During Movement

Daley, Monica

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Exercise and Sport Sciences Reviews: October 2013 - Volume 41 - Issue 4 - p 185
doi: 10.1097/JES.0b013e3182a4e707
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Tendons stretch, store energy, and release this energy when unloaded. Simple… right? Well, tendons may seem to be relatively simple passive structures, but they play complex roles in controlling movement and managing the energy demand on muscles. When the energy stored in a tendon is released, the direction of energy flow can vary, by either driving body motion or being absorbed by muscle fascicles, depending on the precise interplay of muscle activation and intrinsic muscle dynamics relative to tendon recoil. As our understanding of muscle-tendon dynamics expands, so, too, does the list of tendon’s mechanical roles in movement. Therefore, we should not let structural simplicity lull us into a false sense of functional simplicity.

Few robots are designed with elasticity in-series with actuated joints, despite the many demonstrated benefits of tendon elasticity in animal locomotion for economy, peak power performance, stability, and injury protection. Most robots use stiffly jointed systems. Compliant designs with in-series elasticity can provide energetic benefits but also can make a system challenging to control. Effective flow of energy in a series-elastic system requires precise coordination between the spring and actuator. Because passive springs cannot be controlled directly, effective control of compliant systems demands rapid and accurate sensing. Biological systems have resolved this problem through millions of years of coevolution of morphology, muscle and tendon tissue properties, and neuromuscular physiology. We are only beginning to appreciate how these factors function together to allow animals to reap the benefits of elasticity.

The enduring challenge of understanding muscle-tendon dynamics arises, in part, from the difficulty of direct measurements. Joint dynamics can be studied using external measures and are used to infer concentric, eccentric, and isometric contractions. However, understanding the underlying muscle-tendon dynamics requires direct measures of each in carefully controlled experiments. Roberts has pioneered this area through elegant studies of muscle-tendon dynamics both in situ and in vivo (1–3, 5). Historically, scientific attention has focused mostly on steady and positive work tasks, such as level and incline running, acceleration, and jumping. However, energy-dissipative (negative work) contractions also are essential in movement. Jumping requires successful landing, but the latter is often ignored. The current review by Roberts and Konow (4) in this issue of Exercise and Sport Sciences Reviews highlights the role of tendons in buffering the force and power demands placed on muscle during lengthening contractions, protecting muscles from damage while they dissipate energy.

The work of Roberts and Konow (4) has provided fascinating insights into the complex and diverse roles played by tendon in locomotion. Yet, perhaps the most truly fascinating feature of tendon lies not in any specific task but, instead, on its ability to navigate a continuum of roles seamlessly, depending on the body’s interaction with the environment. Tendon, while passive, is a key energy manager in locomotion — smoothing out the force and energy demands placed on muscles. Tendon facilitates both economic and maximal power movements while protecting muscle fascicles from damage and stabilizing the body against stride-to-stride perturbations.

Monica Daley

Structure and Motion Lab

Royal Veterinary College

Hatfield, Hertfordshire, United Kingdom

References

1. Astley HC, Roberts TJ. Evidence for a vertebrate catapult: elastic energy storage in the plantaris tendon during frog jumping. Biology Letters 2012; 8 (3): 386–389.
2. Azizi E, Roberts TJ. Biaxial strain and variable stiffness in aponeuroses. The Journal of Physiology 2009; 587 (17): 4309–4318.
3. Gabaldón AM, Nelson FE, Roberts TJ. Mechanical function of two ankle extensors in wild turkeys: shifts from energy production to energy absorption during incline versus decline running. Journal of Experimental Biology 2004; 207 (13): 2277–2288.
4. Roberts TJ, Konow N. How tendons buffer energy dissipation by muscle. Exerc. Sport Sci. Rev 2013; 41 (4): 186–193.
5. Roberts TJ, Marsh RL, Weyand PG, Taylor CR. Muscular force in running turkeys: the economy of minimizing work. Science 1997; 275 (5303): 1113–1115.
© 2013 American College of Sports Medicine