Muscle machine: How water controls the speed of muscle contraction

The flow of water within a muscle fiber may dictate how quickly muscle can contract, according to a University of Michigan study.

Nearly all animals use muscle to move, and it's been known for a long time that muscle, like all other cells, is composed of about 70% water. But researchers don't know what sets the range and upper limits of muscle performance. Previous research into how muscle works focused only on how it worked on a molecular level rather than how muscle fibers are shaped, that they are three-dimensional and are full of fluid.

U-M physicist Suraj Shankar together with L. Mahadevan, a professor of physics at Harvard University, created a theoretical model of water's role in muscle contraction and found that how fluid moves through a muscle fiber determines how quickly a muscle fiber can contract.

They also found that muscle exhibits a new kind of elasticity called odd elasticity that allows muscle to generate power using three dimensional deformations, shown in a common observation that when a muscle fiber contracts lengthwise, it also bulges perpendicularly. Their results are published in the journal Nature Physics.

"Our results suggest that even such basic questions as how quickly muscle can contract or how many ways muscle can generate power have new and unexpected answers when one takes a more integrated and holistic view of muscle as a complex and hierarchically organized material rather than just a bag of molecules," Shankar said. "Muscle is more than the sum of its parts."

The researchers envision each muscle fiber as a self-squeezing active sponge, a water-filled, sponge-like material that can contract and squeeze itself through the action of molecular motors, he says.

"Muscle fibers are composed of many components, such as various proteins, cell nuclei, organelles such as mitochondria, and molecular motors such as myosin that convert chemical fuel into motion and drive muscle contraction," Shankar said. "All of these components form a porous network that is bathed in water. So an appropriate, coarse-grained description for muscle is that of an active sponge."

But the squeezing process takes time to move water around, so the researchers suspected that this movement of water through the muscle fiber set an upper limit on how rapidly a muscle fiber can twitch.

To test their theory, they modeled muscle movements in multiple organisms across mammals, insects, birds, fish and reptiles, focusing on animals that use muscles for very fast motions. They found that muscles that produce sound, such as the rattle in a rattlesnake's tail, that can contract ten to hundreds of times per second typically don't rely on fluid flows. Instead, these contractions are controlled by the nervous system and are more strongly dictated by molecular properties, or the time it takes for molecular motors within cells to bind and generate forces.