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Konow, Nicolai

Most of what we know about whole muscle behaviour comes from experiments on single fibres or small muscles that are scaled up in size without considering the effects of the additional muscle mass. Previous modelling studies have shown that tissue inertia acts to slow the rate of force development and maximum velocity of muscle during shortening contractions and decreases the work and power per cycle during cyclic contractions; however, these results have not yet been confirmed by experiments on living tissue. Therefore, in this study we conducted in situ work-loop experiments on rat plantaris muscle to determine the effects of increasing the mass of muscle on mechanical work during cyclic contractions. We additionally simulated these experimental contractions using a mass-enhanced Hill-type model to validate our previous modelling work. We found that greater added mass resulted in lower mechanical work per cycle relative to the unloaded trials in which no mass was added to the muscle (p = 0.041 for both 85% and 123% increases in muscle mass). We additionally found that greater strain resulted in lower work per cycle relative to unloaded trials at the same strain to control for length change and velocity effects on the work output, possibly due to greater accelerations of the muscle mass at higher strains. These results confirm that tissue mass reduces muscle mechanical work at larger muscle sizes, and that this effect is likely amplified for lower activations.

To relate in vivo behavior of fascicle segments within a muscle to their in vitro force-length relationships, we examined the strain behavior of paired segments within each of three vertebrate muscles. After determining in vivo muscle activity patterns and length changes of in-series segments within the semimembranosus muscle (SM) in the American Toad (Bufo americanus) during hopping and within the sternohyoid (SH) muscle in the rat (Rattus rattus) during swallowing, and of spatially separated fascicles within the medial gastrocnemius (MG) muscle in the rat during trotting, we measured their corresponding in vitro (toad) or in situ (rat) force–length relationships (FLRs). For all three muscles, in vivo strain heterogeneity lasted for about 36–57% of the behavior cycle, during which one segment or fascicle shortened while the other segment or fascicle simultaneously lengthened. In the toad SM, the proximal segment shortened from the descending limb across the plateau of its FLR from 1.12 to 0.91 of its optimal length (Lo), while the distal segment lengthened (by 0.04 ± 0.04 Lo) before shortening down the ascending limb from 0.94 to 0.83 Lo. In the rat SH muscle, the proximal segment tended to shorten on its ascending limb from 0.90 to 0.85 Lo while the distal segment tended to lengthen across Lo (0.96–1.12 Lo). In the rat MG muscle, in vivo strains of proximal fascicles ranged from 0.72 to 1.02 Lo, while the distal fascicles ranged from 0.88 to 1.11 Lo. Even though the timing of muscle activation patterns were similar between segments, the heterogeneous strain patterns of fascicle segments measured in vivo coincided with different operating ranges across their FLRs simultaneously, implying differences in force–velocity behavior as well. The three vertebrate skeletal muscles represent a diversity of fiber architectures and functions and suggest that patterns of in vivo contractile strain and the operating range over the FLR in one muscle region does not necessarily represent other regions within the same muscle.

Both biological and artificial fliers must contend with aerial perturbations that are ubiquitous in the outdoor environment. Flapping fliers are generally least stable, but also the most maneuverable in roll, yet roll control in biological fliers remains less well understood. Hummingbirds are suitable models for linking aerodynamic perturbations to flight control strategies, as these small, powerful fliers are capable of remaining airborne even in adverse airflows. We challenged hummingbirds to fly within a longitudinally oriented vortex that imposed a continuous roll perturbation, measured wing kinematics and neuromotor activation of the major flight muscles with synchronized high-speed video and electromyography and used computational fluid dynamics (CFD) to estimate the aerodynamic forces generated by wing motions. Hummingbirds responded to the perturbation using bilaterally different activation of the main flight muscles and maintained symmetry in most major aspects of wing motion including stroke amplitude, stroke plane angle, and flapping frequency. However, hummingbirds also displayed consistent bilateral differences in subtle wing kinematics traits, including wing rotation and elevation. CFD modeling implicate asymmetric responses in wing rotation as important for generating the necessary stabilizing torques, suggesting that intrinsic wing muscles play a critical role in aerodynamic control. The birds also augment flight stabilization by adjusting body and tail posture to expose greater surface area to upwash than to the undesirable downwash. Our results provide insight into the remarkable capacity of hummingbirds to maintain flight control and bio-inspiration for simple yet effective control strategies for robotic fliers to contend with unfamiliar and challenging real-word aerial conditions.

Muscle function changes to meet the varying mechanical demands of locomotion across different gait and grade conditions. A muscle's work output is determined by time-varying patterns of neuromuscular activation, muscle force and muscle length change, but how these patterns change under different conditions in small animals is not well-defined. Here we report the first integrated in vivo force-length and activation patterns in rats, a commonly used small animal model, to evaluate the dynamics of two distal hindlimb muscles (medial gastrocnemius, MG and plantaris, PL) across a range of gait (walk, trot, and gallop) and grade (level versus incline) conditions. We use these data to explore how the pattern of force production, muscle activation and muscle length changes across conditions in a small quadrupedal mammal. As hypothesized, we found that the rat muscles show limited fascicle strains during active force generation in stance across gaits and grades, indicating that these distal rat muscles generate force economically but perform little work, similar to patterns observed in larger animals during level locomotion. Additionally, given differences in fiber type composition and variation in motor unit recruitment across the gait and grade conditions examined here for these muscles, the in vivo force-length behavior and neuromuscular activation data reported here can be used to validate improved two-element Hill-type muscle models.

Contractions of skeletal muscles to generate in vivo movement involve dynamic changes in contractile and elastic tissue strains that likely interact to influence the force and work of a muscle. However, studies of the in vivo dynamics of skeletal muscle and tendon strains remain largely limited to bipedal animals, and rarely cover the broad spectra of movement requirements met by muscles that operate as motors, struts, or brakes across the various gaits that animals commonly use and conditions they encounter. Using high-speed bi-planar fluoromicrometry, we analyze in vivo strains within the rat medial gastrocnemius (MG) across a range of gait and slope conditions. These conditions require changes in muscle force ranging from decline walk (low) to incline gallop (high). Measurements are made from implanted (0.5-0.8 mm) tantalum spheres marking MG mid-belly width, mid-belly thickness, as well as strains of distal fascicles, the muscle belly, and the Achilles tendon. During stance, as the muscle contracts, muscle force increases linearly with respect to gait-slope combinations, and both shortening and lengthening fiber strains increase from approximately 5% to 15% resting length. Contractile change in muscle thickness (thickness strain) decreases (r2 25 = 0.86; p = 0.001); whereas, the change in muscle width (width strain) increases (r2 = 0.88; p = 0.001) and tendon strain increases (r2 26 =27 0.77; p = 0.015). Our results demonstrate force-dependency of contractile and tendinous tissue strains with compensatory changes in shape for a key locomotor muscle in the hind limb of a small quadruped. These dynamic changes are linked to the ability of a muscle to tune its force and work output as requirements change with locomotor speed and environmental conditions.

Muscle can experience post-activation potentiation (PAP), a temporary increase in force and rate of force development, when contractions are closely timed; therefore, cyclical behaviors are likely affected by PAP, as succeeding contraction cycles can lead to potentiation over several subsequent cycles. Here, we examined PAP during in situ cyclical contractions of the mallard lateral gastrocnemius (LG). Surface swimming, a cyclical behavior, was mimicked with work-loops utilizing in vivo LG length change and stimulation parameters. Tests were performed at mallards’ preferred cycle frequency as well as at lower and higher frequencies. Like muscles from mammals, anurans, and arthropods, the mallard LG exhibited PAP with increases in peak force, average force rate, and net work. Staircase potentiation occurred over two or more work-loop cycles, resulting in gradual increases in PAP. The number of cycles needed to reach maximum work varied with cycle frequency, requiring more cycles at higher cycle frequencies. PAP occurred under in vivo like stimulation parameters, suggesting a potentially important role of PAP in animal locomotion, especially in cyclical behaviors.

Muscle models are commonly based on intrinsic properties pooled across a number of individuals, often from a different species, and rarely validated against directly measured muscle forces. Here we use a rich data set of rat medial gastrocnemius muscle forces recorded during in-situ and in-vivo isometric, isotonic, and cyclic contractions to test the accuracy of forces predicted using Hill-type muscle models. We identified force-length and force-velocity parameters for each individual, and used either these subject-specific intrinsic properties, or population-averaged properties within the models. The modeled forces for cyclic in-vivo and in-situ contractions matched with measured muscle-tendon forces with r2 between 0.70 and 0.86, and root-mean square errors (RMSE) of 0.10 to 0.13 (values normalized to the maximum isometric force). The modeled forces were least accurate at the highest movement and cycle frequencies and did not show an improvement in r2 when subject-specific intrinsic properties were used; however, there was a reduction in the RMSE with fewer predictions having higher errors. We additionally recorded and tested muscle models specific to proximal and distal regions of the muscle and compared them to measures and models from the whole muscle belly: there was no improvement in model performance when using data from specific anatomical regions. These results show that Hill-type muscle models can yield very good performance for cyclic contractions typical of locomotion, with small reductions in errors when subject-specific intrinsic properties are used.