Variable gearing in pennate muscles

Abstract

Muscle fiber architecture, i.e., the physical arrangement of fibers within a muscle, is an important determinant of a muscle's mechanical function. In pennate muscles, fibers are oriented at an angle to the muscle's line of action and rotate as they shorten, becoming more oblique such that the fraction of force directed along the muscle's line of action decreases throughout a contraction. Fiber rotation decreases a muscle's output force but increases output velocity by allowing the muscle to function at a higher gear ratio (muscle velocity/fiber velocity). The magnitude of fiber rotation, and therefore gear ratio, depends on how the muscle changes shape in the dimensions orthogonal to the muscle's line of action. Here, we show that gear ratio is not fixed for a given muscle but decreases significantly with the force of contraction (P < 0.0001). We find that dynamic muscle-shape changes promote fiber rotation at low forces and resist fiber rotation at high forces. As a result, gearing varies automatically with the load, to favor velocity output during low-load contractions and force output for contractions against high loads. Therefore, muscle-shape changes act as an automatic transmission system allowing a pennate muscle to shift from a high gear during rapid contractions to low gear during forceful contractions. These results suggest that variable gearing in pennate muscles provides a mechanism to modulate muscle performance during mechanically diverse functions.biomechanics ͉ force-velocity tradeoff ͉ gear ratio ͉ muscle architecture T he force, speed, and power that can be harnessed from skeletal muscles to power movement are ultimately limited by the mechanical behavior of myofibers, the muscles' contractile cells. Two features of the contractile behavior of myofibers that likely constrain locomotor performance are the well defined limits to contraction velocity and contractile force. The maximum shortening velocity of a myofiber can be characterized by allowing the muscle to contract against near-zero loads, and a maximum isometric force can be defined when a muscle contracts at a fixed length. To understand how these limits to speed and force at the level of skeletal muscle cells translate to limits to speed or force of movement requires a consideration of musculoskeletal components that modulate force and velocity ''downstream'' of the force-producing cells. The most familiar of these are the skeletal lever systems, which define the mechanical advantage (gearing) through which muscle force is transmitted (1, 2). Like any lever or gear, skeletal gearing influences the ratio of muscle force or velocity to output force or velocity.A less obvious potential gearing mechanism resides within the architecture of the muscles themselves (3). It is generally recognized that skeletal muscle architecture influences the force and velocity of a muscle, but in most cases, the analysis of the effects of muscle architecture on force or velocity output has been limited to predictions based on static anatomy. Dynamic changes...

In vivo maximal fascicle-shortening velocity during plantar flexion in humans

“…3, C and D. In line with results reported in the literature on lower angular velocity (49), AGR was always higher than 1. It therefore confirmed the results reported by Azizi et al (4), who argued that AGR could play an important role during high-velocity movements. On the other hand, although AGR allowed the enhancement of almost 10% of muscle-shortening velocity, no significant correlation was found between this criterion and the maximal angular velocity (r ϭ 0.01).…”

“…The higher instantaneous fascicle-shortening velocity and angular velocity were considered as the peak values of VF and , respectively. AGR was calculated as the ratio between horizontal fascicle velocity and absolute fascicle-shortening velocity (4,49). Total plantar flexion force was calculated from the torque divided by the Achilles tendon moment arm (33).…”

“…Thus a shorter moment arm could be considered a mechanical advantage for producing higher maximal joint angular velocities. Second, muscle gearing (i.e., the variation of the pennation angle during contraction) should also play an important role in global muscle shortening (4,49). Third, few studies (10,21,29) have highlighted the significant contribution of tendinous tissues to the total shortening velocity of the muscle-tendon unit even when the latter contracts in a concentric way (i.e., produces positive mechanical work).…”

Local Tissue Geometry Determines Contractile Force Generation of Engineered Muscle Networks

“…10 Muscle architecture, that is, the spatial arrangement of muscle fibers relative to the axis of force generation, is a critical determinant of muscle contractile function. 11 Consequently, changes in muscle tissue architecture in physiological (e.g., fiber rotation during shortening of pennate muscle 12 ) or pathological (e.g., muscle disarray and fibrosis in dystrophic muscle 13 ) conditions can significantly affect generation of muscle contractile force. To recreate native muscle architecture in vitro, researchers have previously applied different topographical, 14 chemical, [15][16][17] or physical 18 cues to align cells in 2D culture, or utilized cylindrically shaped cell-laden hydrogels or self-assembled organoids formed under static uniaxial tension to align muscle cells in 3D culture.…”

Respiratory, postural and spatio-kinetic motor stabilization, internal models, top-down timed motor coordination and expanded cerebello-cerebral circuitry: a review

“…Within each such segment, moreover, exists a more complex internal structure that goes down to one in which each muscle unit consists of a tendon, aponeurosis, and a fascicle of active contractile and passive elements (Brown and Loeb, 2000). Another composite factor is the variation in the internal architecture of the fiber orientation relative to a muscle's line of action, for example, as found in pennate muscles (Azizi et al, 2008). The potential heterogeneity of the different visco-elastic length-and velocity-force relationships of these subparts provides the opportunity for structurally complex muscle biocomposites with highly task-tuned nonlinear visco-elastic length-velocity-force relationships.…”