Muscle short-range stiffness behaves like a maxwell element, not a spring: Implications for joint stability

• Published in: PloS one Vol. 19; no. 8; p. e0307977
• Main Authors: Barrett, Jeff M, Malakoutian, Masoud, Fels, Sidney, Brown, Stephen H M, Oxland, Thomas R
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 14-08-2024; Public Library of Science (PLoS)
• Subjects: Activities of daily living; Analysis; Biology and Life Sciences; Biomechanical Phenomena; Central nervous system; Complex systems; Computer Simulation; Damping; Engineering and Technology; Equilibrium; Force and energy; Humans; Joint Instability - physiopathology; Joints - physiology; Mechanical analysis; Medicine and Health Sciences; Models, Biological; Moments of inertia; Muscle contraction; Muscle, Skeletal - physiology; Muscles; Numerical analysis; Numerical simulations; Pendulums; Perturbation; Physical Sciences; Potential energy; Reflexes; Simulation methods; Stability; Stiffness
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0307977

Muscles play a critical role in supporting joints during activities of daily living, owing, in part, to the phenomenon of short-range stiffness. Briefly, when an active muscle is lengthened, bound cross-bridges are stretched, yielding forces greater than what is predicted from the force length relationship. For this reason, short-range stiffness has been proposed as an attractive mechanism for providing joint stability. However, there has yet to be a forward dynamic simulation employing a cross-bridge model, that demonstrates this stabilizing role. Therefore, the purpose of this investigation was to test whether Huxley-type muscle elements, which exhibit short-range stiffness, can stabilize a joint while at constant activation.
We analyzed the stability of an inverted pendulum (moment of inertia: 2.7 kg m2) supported by Huxley-type muscle models that reproduce the short-range stiffness phenomenon. We calculated the muscle forces that would provide sufficient short-range stiffness to stabilize the system based in minimizing the potential energy. Simulations consisted of a 50 ms long, 5 Nm square-wave perturbation, with numerical simulations carried out in ArtiSynth.
Despite the initial analysis predicting shared activity of antagonist and agonist muscles to maintain stable equilibrium, the inverted pendulum model was not stable, and did not maintain an upright posture even with fully activated muscles.
Our simulations suggested that short-range stiffness cannot be solely responsible for joint stability, even for modest perturbations. We argue that short-range stiffness cannot achieve stability because its dynamics do not behave like a typical spring. Instead, an alternative conceptual model for short-range stiffness is that of a Maxwell element (spring and damper in series), which can be obtained as a first-order approximation to the Huxley model. We postulate that the damping that results from short-range stiffness slows down the mechanical response and allows the central nervous system time to react and stabilize the joint. We speculate that other mechanisms, like reflexes or residual force enhancement/depression, may also play a role in joint stability. Joint stability is due to a combination of factors, and further research is needed to fully understand this complex system.