Rethinking dynamic muscle function

Muscles have been traditionally viewed as motors that execute force commands from the nervous system. However, this view fails to account for the observation is that muscle force is often uncoupled from activation during dynamic movements. An alternative view is that muscles are not only motors, but also tunable viscoelastic actuators with length- and activation-dependent stiffness and damping tuned by the molecular motors. A path forward is to determine how muscle viscoelastic properties vary with muscle length and activation. We have used system identification of ramp stretch experiments in active and passive muscles across the physiological range of lengths to identify the viscoelastic structure of muscles from mice, rats, cats, and frogs. The experimental data suggest that titin functions as a tunable viscoelastic transmission in muscle sarcomeres. This analysis further elucidates how muscles enable harvesting and dissipation of energy transferred to them from the environments. The view of striated muscles as tunable viscoelastic actuators explains muscle adaptability – why no two heartbeats or running strides are exactly the same. It also explains the energy efficiency of movement – why eagles flying in turbulent air and dolphins swimming in turbulent wakes expend less energy than under calm conditions. And finally, the tunable viscoelastic transmission of muscle sarcomeres reduces the energy burden and computational cost of motor control.