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

Tytell, Eric D.
Carr, Jennifer A.
Danos, Nicole
Wagenbach, Christopher
Sullivan, Caitlin M.
Kıemel, Tim
Cowan, Noah J.
Ankaralı, Mustafa Mert
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.