Andrew. A. Biewener

Skeletal muscle has fiber architectures ranging from simple to complex, alongside variations in fiber-type and neuro-anatomical compartmentalization. However, the functional implications of muscle subdivision into discrete functional units remain poorly understood. The rat medial gastrocnemius has well-characterized regions with distinct architectures and fiber type composition. Here, force-length and force-velocity contractions were performed for two stimulation intensities (supramaximal and submaximal) and for three structural units (whole muscle belly, proximal region, and distal region) to assess the effect of muscle compartmentalization on contractile force-length-velocity relationships and optimal speed for power production. Additionally, fiber strain, fiber rotation, pennation, and architectural gearing were quantified. Our results suggest that the proximal and distal muscle regions have fundamentally different physiological function. During supramaximal activation, the proximal region has shorter (8.4 ± 0.8 mm versus 10.9 ± 0.7 mm) fibers and steeper (28.7 ± 11.0° versus 19.6 ± 6.3°) fiber angles at optimum length, and operates over a larger (17.9 ± 3.8% versus 12.6 ± 2.7%) range of its force-length curve. The proximal region also exhibits larger changes in pennation angle (5.6 ± 2.2°/mm versus 2.4 ± 1.5°/mm muscle shortening) and architectural gearing (1.82 ± 0.53 versus 1.25 ± 0.24), whereas the distal region exhibits greater peak shortening speed (96.0 mm/s versus 81.3 mm/s) and 18-27% greater optimal speed. Overall, similar patterns were observed during submaximal activation. These regional differences in physiological function with respect to the whole muscle highlight how variation in motor recruitment could fundamentally shift regional functional patterns within a single muscle, which likely has important implications for whole muscle force and work output in vivo. NEW & NOTEWORTHY We show that muscle compartmentalization can influence whole muscle contractile properties, with slower-fibered proximal rat medial gastrocnemius undergoing larger changes in pennation angle and architectural gearing, whereas the faster-fibered distal region achieves greater peak and optimal shortening velocity, and power output. Consequently, regional variation in motor recruitment can fundamentally influence functional patterns within a single muscle.

Skeletal muscles share many common, highly conserved features of organization at the molecular and myofilament levels, giving skeletal muscle fibers generally similar and characteristic mechanical and energetic properties; properties well described by classical studies of muscle mechanics and energetics. However, skeletal muscles can differ considerably in architectural design (fiber length, pinnation, and connective tissue organization), as well as fiber type, and how they contract in relation to the timing of neuromotor activation and in vivo length change. The in vivo dynamics of muscle contraction is, therefore, crucial to assessing muscle design and the roles that muscles play in animal movement. Architectural differences in muscle–tendon organization combined with differences in the phase of activation and resulting fiber length changes greatly affect the time-varying force and work that muscles produce, as well as the energetic cost of force generation. Intrinsic force–length and force–velocity properties of muscles, together with their architecture, also play important roles in the control of movement, facilitating rapid adjustments to changing motor demands. Such adjustments complement slower, reflex-mediated neural feedback control of motor recruitment. Understanding how individual fiber forces are integrated to whole-muscle forces, which are transmitted to the skeleton for producing and controlling locomotor movement, is therefore essential for assessing muscle design in relation to the dynamics of movement.

Kinematic and center of mass (CoM) mechanical variables used to define terrestrial gaits are compared for various tetrapod species. Kinematic variables (limb phase,duty factor) provide important timing information regarding the neural control and limb coordination of various gaits. Whereas, mechanical variables (potential and kinetic energyrelative phase, %Recovery, %Congruity) provide insight into the underlying mechanisms that minimize muscle work and the metabolic cost of locomotion, and also influence neural control strategies. Two basic mechanisms identified by Cavagna et al. (1977. Am J Physiol 233:R243–R261) are used broadly by various bipedal and quadrupedal species. During walking, animals exchange CoM potential energy (PE) with kinetic energy (KE) via an inverted pendulum mechanism to reduce muscle work. During the stance period of running (including trotting, hopping and galloping) gaits, animals convert PE and KE into elastic strain energy in spring elements of the limbs and trunk and regain this energy later during limb support. The bouncing motion of the body on the support limb(s) is well represented by a simple mass‐spring system. Limb spring compliance allows the storage and return of elastic energy to reduce muscle work. These two distinct patterns of CoM mechanical energy exchange are fairly well correlated with kinematic distinctions of limb movement patterns associated with gait change. However, in some cases such correlations can be misleading. When running (or trotting) at low speeds many animals lack an aerial period and have limb duty factors that exceed 0.5. Rather than interpreting this as a change of gait, the underlying mechanics of the body's CoM motion indicate no fundamental change in limb movement pattern or CoM dynamics has occurred. Nevertheless, the idealized, distinctive patterns of CoM energy fluctuation predicted by an inverted pendulum for walking and a bouncing mass spring for running are often not clear cut, especially for less cursorial species. When the kinematic and mechanical patterns of a broader diversity of quadrupeds and bipeds are compared, more complex patterns emerge, indicating that some animals may combine walking and running mechanics at intermediate speeds or at very large size. These models also ignore energy costs that are likely associated with the opposing action of limbs that have overlapping support times during walking. A recent model of terrestrial gait (Ruina et al., 2005. J Theor Biol, in press) that treats limb contact with the ground in terms of collisional energy loss indicates that considerable CoM energy can be conserved simply by matching the path of CoM motion perpendicular to limb ground force. This model, coupled with the earlier ones of pendular exchange during walking and mass‐spring elastic energy savings during running, provides compelling argument for the view that the legged locomotion of quadrupeds and other terrestrial animals has generally evolved to minimize muscle work during steady level movement.J. Exp. Zool. 305A 2006.

To function over a lifetime of use, materials and structures must be designed to have sufficient factors of safety to avoid failure. Vertebrates are generally built from materials having similar properties. Safety factors are most commonly calculated based on the ratio of a structure's failure stress to its peak operating stress. However, yield stress is a more likely limit, and work of fracture relative to energy absorption is likely the most relevant measure of a structure's safety factor, particularly under impact loading conditions characteristic of locomotion. Yet, it is also the most difficult to obtain. For repeated loading, fatigue damage and eventual failure may be critical to the design of biological structures and will result in lower safety factors. Although area:volume scaling predicts that stresses will increase with size, interspecific comparisons of mammals and birds show that skeletal allometry is modest, with most groups scaling (l∝d^0.89) closer to geometric similarity (isometry: l ∝d^1.0) than to elastic similarity (l ∝d^0.67) or stress similarity (l ∝d^0.5). To maintain similar peak bone and muscle stresses, terrestrial mammals change posture when running, with larger mammals becoming more erect. More erect limbs increases their limb muscle mechanical advantage (EMA) or ratio of ground impulse to muscle impulse (r/R=∫G/∫F_m). The increase in limb EMA with body weight (∝W^0.25) allows larger mammals to match changes in bone and muscle area (∝W^0.72-0.80) to changes in muscle force generating requirements (∝W^0.75), keeping bone and muscle stresses fairly constant across a size range 0.04-300 kg. Above this size, extremely large mammals exhibit more pronounced skeletal allometry and reduced locomotor ability. Patterns of ontogenetic scaling during skeletal growth need not follow broader interspecific scaling patterns. Instead, negative allometric growth (becoming more slender) is often observed and may relate to maturation of the skeleton's properties or the need for younger animals to move at faster speeds compared with adults. In contrast to bone and muscle stress patterns, selection for uniform safety factors in tendons does not appear to occur. In addition to providing elastic energy savings, tendons transmit force for control of motion of more distal limb segments. Their role in elastic savings requires that some tendons operate at high stresses (and strains), which compromises their safety factor. Other `low stress' tendons have larger safety factors, indicating that their primary design is for stiffness to reduce the amount of stretch that their muscles must overcome when contracting to control movement.

Muscular forces generated during locomotion depend on an animal's speed, gait, and size and underlie the energy demand to power locomotion. Changes in limb posture affect muscle forces by altering the mechanical advantage of the ground reaction force (R) and therefore the effective mechanical advantage (EMA = r/R, where r is the muscle mechanical advantage) for muscle force production. We used inverse dynamics based on force plate and kinematic recordings of humans as they walked and ran at steady speeds to examine how changes in muscle EMA affect muscle force-generating requirements at these gaits. We found a 68% decrease in knee extensor EMA when humans changed gait from a walk to a run compared with an 18% increase in hip extensor EMA and a 23% increase in ankle extensor EMA. Whereas the knee joint was extended (154–176°) during much of the support phase of walking, its flexed position (134–164°) during running resulted in a 5.2-fold increase in quadriceps impulse (time-integrated force during stance) needed to support body weight on the ground. This increase was associated with a 4.9-fold increase in the ground reaction force moment about the knee. In contrast, extensor impulse decreased 37% (P < 0.05) at the hip and did not change at the ankle when subjects switched from a walk to a run. We conclude that the decrease in limb mechanical advantage (mean limb extensor EMA) and increase in knee extensor impulse during running likely contribute to the higher metabolic cost of transport in running than in walking. The low mechanical advantage in running humans may also explain previous observations of a greater metabolic cost of transport for running humans compared with trotting and galloping quadrupeds of similar size.