Stuck in gear: age-related loss of variable gearing in skeletal muscle

Abstract

Skeletal muscles power a broad diversity of animal movements, despite only being able to produce high forces over a limited range of velocities. Pennate muscles use a range of gear ratios, the ratio of muscle shortening velocity to fiber shortening velocity, to partially circumvent these force-velocity constraints. Muscles operate with a high gear ratio at low forces; fibers rotate to greater angles of pennation, enhancing velocity but compromising force. At higher forces, muscles operate with a lower gear ratio; fibers rotate little so limiting muscle shortening velocity, but helping to preserve force. This ability to shift gears is thought to be due to the interplay of contractile force and connective tissue constraints. In order to test this hypothesis, gear ratios were determined in the medial gastrocnemius muscles of both healthy young rats, and old rats where the interaction between contractile and connective tissue properties was assumed to be disrupted. Muscle fiber and aponeurosis stiffness increased with age (P<0.05) from 19.1± 5.0 kPa and 188.5±24.2 MPa, respectively, in young rats to 39.1± 4.2 kPa and 328.0±48.3 MPa in old rats, indicating a mechanical change in the interaction between contractile and connective tissues. Gear ratio decreased with increasing force in young (P<0.001) but not old (P=0.72) muscles, indicating that variable gearing is lost in old muscle. These findings support the hypothesis that variable gearing results from the interaction between contractile and connective tissues and suggest novel explanations for the decline in muscle performance with age.

Muscle architecture dynamics modulate performance of the superficial anterior temporalis muscle during chewing in capuchins

“…1), described as a muscle's architectural gear ratio (AGR). The AGR has been defined as the ratio of whole-muscle strain/fascicle strain 21,22 or its temporal derivative, whole-muscle velocity/fascicle velocity [23][24][25][26] . At lower gear ratios-low muscle strain or shortening relative to fascicle strain or shortening-muscle fibers rotate less during shortening, resulting in a smaller pinnation angle and favoring increased force production.…”

“…Importantly, gearing within a given muscle can vary from one contraction to another, depending on a number of factors. For example, in the gastrocnemius muscle, the AGR decreases as muscle force increases [23][24][25][26] , suggesting that muscle gearing might function as a passive mechanism for modulating force output. This raises the possibility that passive variability in AGR between gape cycles might contribute to inter-cycle muscle performance as food bolus properties change during a feeding sequence.…”

“…However, the dynamic changes in muscle pinnation angles that produce complex relationships between the shortening strain and velocity of whole muscles, and those of muscle fibers and fascicles, are virtually unstudied in mammal feeding systems. Notably, the literature is dominated by in situ studies of locomotor muscles in non-primate mammals, often under conditions of maximal muscle activation, and by in vivo studies of limb muscles in humans during bicycling [23][24][25][26]37,38 . In contrast, there is a distinct lack of studies of muscle architecture dynamics during natural behaviors and at sub-maximal muscle activation levels 22,39 and this is crucial because the presence of inactive or passive muscle fibers can affect the way that active fibers rotate and shorten during contraction, in turn impacting force production.…”

Beyond bouncy gaits: The role of multiscale compliance in skeletal muscle performance

“…Transverse strain in the aponeurosis is also thought to be instrumental in the control of muscle shape change, and therefore responsible for variable gearing (Eng et al, ; Holt et al, ). Pennate muscles exhibit load‐dependent variable gearing; under low loads fibers rotate to higher pennation angles, so enhancing velocity, whereas under high loads contraction occurs with little fiber rotation, so preserving force (Azizi & Roberts, ; Azizi, Brainerd, & Roberts, ; Dick & Wakeling, ).…”

“…As fiber force increases, resistance to increasing thickness is likely to exceed resistance to increasing width. The muscle will then transition to increasing in width, fibers will no longer rotate, and the gear ratio will decrease (Eng et al, ; Holt et al, ). Transverse aponeurosis compliance has been demonstrated to contribute significantly to this control of shape change; however, it cannot be the only factor (Eng et al, ).…”