Body stiffness and damping depend sensitively on the timing of muscle activation in lampreys

Abstract

Unlike most manmade machines, animals move through their world using flexible bodies and appendages, which bend due to internal muscle and body forces, and also due to forces from the environment. Fishes in particular must cope with fluid dynamic forces that not only resist their overall swimming movements but also may have unsteady flow patterns, vortices, and turbulence, many of which occur more rapidly than what the nervous system can process. Has natural selection led to mechanical properties of fish bodies and their component tissues that can respond very quickly to environmental perturbations? Here, we focus on the mechanical properties of isolated muscle tissue and of the entire intact body in the silver lamprey, Ichthyomyzon unicuspis. We developed two modified work loop protocols to determine the effect of small perturbations on the whole body and on isolated segments of muscle as a function of muscle activation and phase within the swimming cycle. First, we examined how the mechanical properties of the whole lamprey body change depending on the timing of muscle activity. Relative to passive muscle, muscle activation can modulate the effective stiffness by about two-fold and modulate the effective damping by >10-fold depending on the activation phase. Next, we performed a standard work loop test on small sections of axial musculature while adding low-amplitude sinusoidal perturbations at specific frequencies. We modeled the data using a new system identification technique based on time-periodic system analysis and harmonic transfer functions (HTFs) and used the resulting models to predict muscle function under novel conditions. We found that the effective stiffness and damping of muscle varies during the swimming cycle, and that the timing of activation can alter both the magnitude and timing of peak stiffness and damping. Moreover, the response of the isolated muscle was highly nonlinear and length dependent, but the body's response was much more linear. We applied the resulting HTFs from our experiments to explore the effect of pairs of antagonistic muscles. The results suggest that when muscles work against each other as antagonists, the combined system has weaker nonlinearities than either muscle segment alone. Together, these results begin to provide an integrative understanding of how activation timing can tune the mechanical response properties of muscles, enabling fish to swim effectively in their complex and unpredictable environment.

Nanometer-scale structure differences in the myofilament lattice spacing of two cockroach leg muscles correspond to their different functions

“…Campbell et al, 2011a,b). We generally cannot yet predict mechanical work from steady-state physiological properties, especially during perturbed conditions (Powers et al, 2018;Ahn et al, 2006;Tytell et al, 2018;Libby et al, 2020), but our results link nanometer-scale structural differences with functional differences relevant for locomotion. Under activated conditions, the spacing patterns change in part due to the action of active myosin binding and activation of other proteins, such as titin.…”

“…This function versatility enables muscle's diverse roles in animal locomotion and behavior. Muscle's mechanical function can be difficult to predict, especially under perturbed conditions, because of muscle's hierarchical structure across multiple length scales (Powers et al, 2018;Ahn et al, 2006;Tytell et al, 2018).…”

A Computational Model for Tail Undulation and Fluid Transport in the Giant Larvacean

“…The recognition that swimming animals create coherent structures in their wakes [7,8] has led to more detailed studies of how particular morphological features, like peduncles in whales [9] and denticles in sharks [10], can play a role in drag reduction and ultimately swimming performance. Many of these findings, including the discovery of resonance matching between body kinematics and fluid dynamics [11,12], which enables completely passive propulsion as demonstrated in dead fish [13], have important implications for the development of engineered systems, such as underwater vehicles.…”

History-dependent perturbation response in limb muscle

“…Under unsteady conditions, the muscle can dissipate more than 10 times the energy that it does in steady state or convert its function to that of non-linear motor (Sponberg et al, 2011a). It remains challenging to predict function from the quasi-static length-tension and forcevelocity relationships, especially under unsteady conditions (Ahn et al, 2006;Sponberg et al, 2011a;Daley and Biewener, 2011;Tytell et al, 2018). Nonetheless, such conditions likely pose greater performance demands than steady state (Biewener and Daley, 2007).…”

“…However, perturbations around dynamic (time periodic or unsteady) conditions can create even more unexpected shifts in muscle performance (Robertson and Sawicki, 2015;Tytell et al, 2018). During running, muscle can experience large and rapid perturbations against a background strain trajectory where history has the potential to alter function Sponberg et al, 2011b).…”