It takes a matter of milliseconds for muscles to flex actively in response to a stimulus. But they are capable of responding passively on even shorter timescales — contracting and extending, seemingly without consuming any energy. This behaviour can be attributed to the unfolding of proteins linking the muscle fibres. Just how this is achieved, however, has proved difficult to pin down. As they report in Physical Review Letters, Matthieu Caruel and colleagues have determined that this strange passive response is related to cooperativity between the cross-linking proteins and leads to intriguing material properties, including a negative stiffness in equilibrium and a tailored response to different loading conditions (Phys. Rev. Lett. 110, 248103; 2013).

Credit: © ISTOCKPHOTO/THINKSTOCK

Collective behaviour in biological systems is often associated with a breaking of detailed balance. But as the coordination of proteins linking muscle fibres can be detected during very rapid responses to applied force, Caruel et al. reasoned that the problem can be treated in equilibrium, without taking activity into account. They invoked a well-studied model, showing that the equilibrium response of muscle material involves highly synchronized behaviour at the microscale, which explains its ability to flex passively.

The tell-tale cooperative behaviour was revealed under isotonic loading, in which the muscle length is allowed to vary. The physiological case, for which the length is fixed, is known as isometric loading, and induces a disordered state characterized by randomly distributed cross-linkers. The behavioural difference between these two types of loading has been detected in experiments, but the origin of the disparity has so far proved elusive. Caruel et al. cite the non-equivalence of their equilibrium ensembles as the reason behind this difference — noting that stiffness can be negative under isometric conditions, whereas it is necessarily positive for isotonic loading.

Using their model to fit experimental data, the authors determined that the system lies close to a critical point. The associated diverging correlation length and macroscopic fluctuations are consistent with observations of muscles under stall-force conditions. Caruel et al. argue that marginal stability of the critical state allows the muscle material to amplify interactions, ensuring strong feedback and robustness to perturbation — and offering a way to rapidly switch between synchronized and desynchronized modes of operation. The generality of their formulation suggests that passive collective behaviour may be a property common to many cross-linked biological networks.