Perturbing the muscle work loop paradigm to unravel the neuromechanics of unsteady locomotion

Abstract

Muscle function during movement is more than a simple, linear transformation of neural activity into force. The classic work loop technique has pioneered our understanding of muscle, but typically only characterizes function during unperturbed movement cycles, such as those experienced during steady walking, running, swimming and flying. Yet perturbations away from steady movement often place greater demands on muscle structure and function and offer a unique window into muscle's broader capacity. Recently, studies in diverse organisms from cockroaches to humans have started to grapple with muscle function in unsteady (perturbed, transient and fluctuating) conditions, but the vast range of possible parameters and the challenge of connecting in vitro to in vivo experiments are daunting. Here, we review and organize these studies into two broad approaches that extend the classic work loop paradigm. First, in the top-down approach, researchers record length and activation patterns of natural locomotion under perturbed conditions, replay these conditions in isolated muscle work loop experiments to reveal the mechanism by which muscle mediates a change in body dynamics and, finally, generalize across conditions and scale. Second, in the bottom-up approach, researchers start with an isolated muscle work loop and then add structural complexity, simulated loads and neural feedback to ultimately emulate the muscle's neuromechanical context during perturbed movement. In isolation, each of these approaches has several limitations, but new models and experimental methods coupled with the formal language of control theory give several avenues for synthesizing an understanding of muscle function under unsteady conditions.

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“…Such unperturbed length change waveforms are approximate muscle actions during activities such as steady walking and running. Future work should be undertaken to understand if these findings translate to perturbated muscle length cycles that reflect unsteady locomotory performance (Sponberg et al., 2023 ). Furthermore, fibre stimulation and length change waveform may be manipulated during fatiguing contractions in vivo in order to optimise net work (Wakeling & Rozitis, 2005 ).…”

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“… 67 ). In addition, further understanding of muscle properties would aid in understanding how the patterns of neural activities are transformed to muscle tensions and movements ( 68 ).…”

Methodological Advances in Studying Postnatal Locomotor Development

“…It can also be understood in a medical sense: if an individual does not "walk" as expected, locomotion enables the diagnosis of disease (Mielke et al, 2023). Perturbations, both in the environment (Daley, 2018) and in the two systems (De Groote and Falisse, 2021;Sponberg et al, 2023;Ting et al, 2015), and the organism's response to it, can be analyzed to understand the robustness, plasticity, and rehabilitation of motor control. The vertebrate locomotor system is highly complex, therefore sensitive to changes, and therefore a relevant multi-purpose tool for diagnostic and comparative research.…”