History-dependent perturbation response in limb muscle

Abstract

Statement: The response of muscles to rapid, identical strain perturbations is history 9 dependent, but is captured by a viscoelastic model with memory. Muscle function during pertur-10 bations therefore depends on locomotor frequency. 11 1 1 Abstract 12Muscle mediates movement but movement is typically unsteady and perturbed. Muscle is known 13 to behave non-linearly and with history dependent properties during steady locomotion, but the 14 importance of history dependence in mediating muscles function during perturbations remains less 15 clear. To explore muscle's capacity to mitigate perturbations, we constructed a series of perturba- 16 tions that varied only in kinematic history, keeping instantaneous position, velocity and time from 17 stimulation constant. We discovered that muscle's perturbation response is profoundly history de-18 pendent, varying by four fold as baseline frequency changes, and dissipating energy equivalent to 19 ∼ 6 times the kinetic energy of all the limbs (nearly 2400 W Kg −1 ). Muscle's energy dissipation 20 during a perturbation is predicted primarily by the force at the onset of the perturbation. This 21 relationship holds across different frequencies and timings of stimulation. This history dependence 22 behaves like a viscoelastic memory producing perturbation responses that vary with the frequency 23 of the underlying movement. 24 2 Introduction 25Muscle produces, dissipates, stores, returns, and transits mechanical energy to adopt diverse func-26 tions during locomotion (Dickinson et al., 2000). Even the same muscle can adopt different functions 27 in unsteady or perturbed conditions (Biewener and Daley, 2007;Azizi and Roberts, 2010). A sin-28 gle muscle in the leg of cockroach normally dissipates energy during steady-state running (Ahn 29 et al., 2006;Full et al., 1998). Yet when the animal is perturbed, neural feedback can categorically 30 switch the muscle's function from one stride to the next (Sponberg, Spence, Mullens and Full, 31 2011). Under unsteady conditions the muscle can dissipate more than ten times the energy that it 32 does in steady state or convert its function to that of non-linear motor (Sponberg, Libby, Mullens 33 and Full, 2011). It remains challenging to predict function from the quasi-static length-tension 34 and force-velocity relationships, especially under unsteady conditions. Nonetheless such conditions 35 likely pose greater performance demands than steady-state. 36Strain history-dependent muscle properties are well known to affect muscle's stress develop-37 ment. These properties include force depression during shortening and force enhancement during 38 lengthening. While the specific mechanisms for history dependence remain controversial and are 39 likely multifaceted (Rassier, 2012), there are established consequences for steady, transition, and 40 impulsive behaviors (Josephson, 1999;Roberts and Azizi, 2011;Herzog et al., 2015; Nishikawa, 41 2016). However, muscle function during perturbations during movement is much less explo...

The hawkmoth wingbeat is not at resonance

“…In addition to potential limitations explored in the sensitivity analysis, we use a phenomenological muscle model and simplified bulk thoracic stiffness. While these seem justified for M. sexta , it is possible that nonlinear resonance modes, specialized anatomical structures like the dipteran wing hinge ‘clutch’ [2] and history-dependent muscle dynamics [24] could complicate resonance, especially in specific species. However, the model's simplicity makes it extremely versatile and allows it to serve as a template for added complexity as better insect data become available.…”

Residual force depression is not related to positive muscle fascicle work during submaximal voluntary dorsiflexion contractions in humans

“…However, our ability to predict neuromuscular output under these conditions is poor (Dick et al, 2017), which directly limits our ability to assess tissue and joint loading and effectively inform injury prevention and rehabilitation strategies, as well as understand motor control (Imani Nejad et al, 2020). Inaccurate predictions of neuromuscular output might arise because muscle models typically assume that force output for a given muscle activity level is only dependent on the muscle's instantaneous length and velocity, whereas growing evidence suggests that the amplitude of muscle shortening under submaximal voluntary activation strongly affects neuromuscular output (Roberts et al, 1997), as does the preload force prior to a perturbation (Edman, 1988;Libby et al, 2020). Consequently, modified muscle models that account for additional mechanical factors related to the muscle's previous state or 'history' of force production have shown promise in reducing prediction inaccuracies (McGowan et al, 2013).…”