The effects of temperature on elastic energy storage and release in a system with a dynamic mechanical advantage latch

Abstract

Changes in temperature alter muscle kinetics and in turn affect whole-organism performance. Some organisms use the elastic recoil of biological springs, structures which are far less temperature sensitive, to power thermally robust movements. For jumping frogs, the use of elastic energy in tendons is facilitated through a geometric latching mechanism that operates through dynamic changes in the mechanical advantage (MA) of the hindlimb. Despite the well-documented use of elastic energy storage, frog jumping is a locomotor behavior that is significantly affected by changes in temperature. Here, we used an in vitro muscle preparation interacting in real-time with an in silico model of a legged jumper to understand how changes in temperature affected the flow of energy in a system using a MA latch. We used the plantaris longus muscle-tendon unit (MTU) to power a virtual limb with changing MA and a mass being accelerated through a real-time feedback controller. We quantified the amount of energy stored in and recovered from elastic structures and the additional contribution of direct muscle work after unlatching. We found that temperature altered the duration of energy loading and recovery phase of the in vitro/in silico experiments. We found that the early phase of loading was insensitive to changes in temperature. However, an increase in temperature did increase the rate of force development which in turn allowed for increased energy storage in the second phase of loading. We also found that the contribution of direct muscle work after unlatching was substantial and increased significantly with temperature. Our results show that the thermal robustness achieved by an elastic mechanism depends strongly on the nature of the latch that mediates energy flow, and that the relative contribution of elastic and direct muscle energy likely shape the thermal sensitivity of locomotor systems.

Linkingin vivomuscle dynamics toin situforce-length and force-velocity reveals that guinea fowl lateral gastrocnemius operates at shorter than optimal lengths

“…Given these results, it is critical that the approaches to studying isolated muscles advance beyond the standard historical protocols. While direct measures of muscle force and length in vivo may not be practical for all systems, recent technical advances provide the potential to bridge the gaps in current understanding by using real-time feedback control to allow isolated muscles to interact dynamically with models (physical or virtual) (Robertson and Sawicki, 2015; Richards and Eberhard 2020; Mendoza et al 2023). Further work and new approaches are needed to understand how the nonlinear interactions between activation and strain trajectory influence muscle force and work output during dynamic contractions in vivo .…”