Contribution of elastic tissues to the mechanics and energetics of muscle function during movement

Abstract

Muscle force production occurs within an environment of tissues that exhibit spring-like behavior, and this elasticity is a critical determinant of muscle performance during locomotion. Muscle force and power output both depend on the speed of contraction, as described by the isotonic force-velocity curve. By influencing the speed of contractile elements, elastic structures can have a profound effect on muscle force, power and work. In very rapid movements, elastic mechanisms can amplify muscle power by storing the work of muscle contraction slowly and releasing it rapidly. When energy must be dissipated rapidly, such as in landing from a jump, energy stored rapidly in elastic elements can be released more slowly to stretch muscle contractile elements, reducing the power input to muscle and possibly protecting it from damage. Elastic mechanisms identified so far rely primarily on in-series tendons, but many structures within muscles exhibit spring-like properties. Actomyosin cross-bridges, actin and myosin filaments, titin, and the connective tissue scaffolding of the extracellular matrix all have the potential to store and recover elastic energy during muscle contraction. The potential contribution of these elements can be assessed from their stiffness and estimates of the strain they undergo during muscle function. Such calculations provide boundaries for the possible roles these springs might play in locomotion, and may help to direct future studies of the uses of elastic elements in muscle.

Keywords: Elastic energy; Locomotion; Metabolic economy; Tendon.

Fig. 1.

Typical force–velocity relationship for skeletal muscle. For shortening muscle (positive velocities), force declines as a function of shortening velocity. Power is maximum at intermediate shortening velocities, typically ∼0.3 V/V_max (where V_max is the unloaded maximal shortening velocity). Only very low rates of lengthening (negative velocities) are required to develop very high forces and power inputs to the muscle.

Fig. 2.

The influence of tendon elasticity on the timing of muscle length change and work. Examples are shown of (A) a bullfrog jumping and (B) a turkey landing. In both instances, much of the muscle fiber length change occurs as a result of tendon elasticity, rather than joint motion. In the frog plantaris (A), muscle fibers shorten before the ankle extends, so that muscle shortening occurs over a time period that is about twice the duration of the period of ankle extension. In the turkey gastrocnemius (B), ankle flexion immediately following toe-down (arrow) is accompanied by relatively little change in muscle fiber length, indicating that this motion is accommodated by tendon stretch. Most of the muscle fiber lengthening occurs when joint flexion is complete, indicating that active fibers are lengthened by tendon recoil. Tendon action in A allows for high power outputs during the jump; in B, tendon action enables high power inputs to the muscle–tendon system while limiting power input to the muscle. In both cases, the time course of muscle action is altered by tendon action. Arrows indicate toe-off (bullfrog) and toe-down (turkey). Data in A are from Astley and Roberts (2012); data in B are from Konow and Roberts (2015).

Fig. 3.

Elastic energy storage potential for several muscle springs. (A) A diagrammatic representation of some spring elements associated with skeletal muscles. Elastic behavior can be characterized for the myofilaments (mf, which is a lumped spring behavior for myosin and actin), cross-bridges (xb), titin (ti), extracellular matrix (ecm) and tendon (te). (B) Estimates of muscle mass-specific capacity for elastic energy storage in muscle and tendon spring elements. Ranges are given for tendon (dark blue), passive muscle (light blue) and passive isolated muscle fibers (green). Maximum elastic strains within cross-bridges (black) and myofilaments (gray) are small. Note that for all structures, energy storage is calculated per unit muscle mass. Strain is calculated with respect to tendon length for tendon, and relative to muscle length for all other structures. See text for a description of the methods used to calculate the values for B.

Fig. 4.

Stress–strain work loops. Single stress–strain work loops are shown for tendon (A) and passive muscle (B) from wild turkey muscles. Both are cycled with a sine wave at 4 Hz, a value close to the stride frequency for running for this animal. The hysteresis represents the energy lost in the cycle, which is negligible for the tendon and significant (approximately 60%) for the passive muscle. Scales for both stress and strain differ in the two panels. The arrows indicate the direction of length change.