History-dependent perturbation response in limb muscle

Abstract

Muscle mediates movement but movement is typically unsteady and perturbed. Muscle is known to behave non-linearly and with historydependent properties during steady locomotion, but the importance of history dependence in mediating muscle function during perturbations remains less clear. To explore the capacity of muscles to mitigate perturbations during locomotion, we constructed a series of perturbations that varied only in kinematic history, keeping instantaneous position, velocity and time from stimulation constant. We found that the response of muscle to a perturbation is profoundly history dependent, varying 4-fold as baseline frequency changes, and dissipating energy equivalent to ∼6 times the kinetic energy of all the limbs in 5 ms (nearly 2400 W kg −1 ). Muscle energy dissipation during a perturbation is predicted primarily by the force at the onset of the perturbation. This relationship holds across different frequencies and timings of stimulation. This history dependence behaves like a viscoelastic memory producing perturbation responses that vary with the frequency of the underlying movement.

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.…”

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.…”

“…Under perturbed conditions during locomotion, these muscles can undergo many different strain patterns (Sponberg et al, 2011a;Libby et al, 2020). We next changed the mean strain of the work loop conditions by shifting the mean length by ±5% and +10% of OL.…”

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).…”