High-frequency oscillations as a consequence of neglected serial damping in Hill-type muscle models

Abstract

High-frequency vibrations e.g., induced by legs impacting with the ground during terrestrial locomotion can provoke damage within tendons even leading to ruptures. So far, macroscopic Hill-type muscle models do not account for the observed high-frequency damping at low-amplitudes. Therefore, former studies proposed that protective damping might be explained by modelling the contractile machinery of the muscles in more detail, i.e., taking the microscopic processes of the actin-myosin coupling into account. In contrast, this study formulates an alternative hypothesis: low but significant damping of the passive material in series to the contractile machinery--e.g., tendons, aponeuroses, titin--may well suffice to damp these hazardous vibrations. Thereto, we measured the contraction dynamics of a piglet muscle-tendon complex (MTC) in three contraction modes at varying loads and muscle-tendon lengths. We simulated all three respective load situations on a computer: a Hill-type muscle model including a contractile element (CE) and each an elastic element in parallel (PEE) and in series (SEE) to the CE pulled on a loading mass. By comparing the model to the measured output of the MTC, we extracted a consistent set of muscle parameters. We varied the model by introducing either linear damping in parallel or in series to the CE leading to accordant re-formulations of the contraction dynamics of the CE. The comparison of the three cases (no additional damping, parallel damping, serial damping) revealed that serial damping at a physiological magnitude suffices to explain damping of high-frequency vibrations of low amplitudes. The simulation demonstrates that any undamped serial structure within the MTC enforces SEE-load eigenoscillations. Consequently, damping must be spread all over the MTC, i.e., rather has to be de-localised than localised within just the active muscle material. Additionally, due to suppressed eigenoscillations Hill-type muscle models taking into account serial damping are numerically more efficient when used in macroscopic biomechanical neuro-musculo-skeletal models.