A University of Michigan study found that water flow within muscle fibers may control muscle contraction speed.
Most animals use muscles to move, and muscles are about 70% water. However, what limits muscle performance needs to be clarified. Previous research focused on the molecular level, not considering muscle fibers’ three-dimensional, fluid-filled structure.
U-M physicist Suraj Shankar and Harvard’s L. Mahadevan developed a theoretical model showing that fluid movement through muscle fibers dictates contraction speed.
They discovered a new type of elasticity in muscles, called odd elasticity, allowing muscles to generate power through three-dimensional changes. This is seen when a muscle fiber contracts lengthwise and bulges outward. Their findings are published in Nature Physics.
This model can also explain the movements of other water-filled cells and tissues, like unicellular microorganisms, and could improve the design of soft actuators, fast artificial muscles, and shape-morphing materials. These usually have slow contraction speeds because they rely on external triggers.
Researchers describe each muscle fiber as an active sponge. This water-filled material contracts and squeezes itself using molecular motors.
Shankar explained, “Muscle fibers comprise components like proteins, cell nuclei, organelles such as mitochondria, and molecular motors like myosin that convert chemical fuel into motion. These components create a porous network filled with water, so a good description of muscle is an active sponge.”
The researchers suspected that the time it takes to move water through muscle fibers limits how quickly a muscle can twitch. To test this, they modeled muscle movements in various animals, including mammals, insects, birds, fish, and reptiles, focusing on those with swift motions.
Researchers found that muscles producing sound, like a rattlesnake’s tail, rely less on fluid flows and more on nervous system control and molecular properties. In smaller organisms like flying insects, which beat their wings hundreds to thousands of times per second, fluid flows play a more crucial role.
Shankar said, “In these cases, we found that fluid flows within muscle fibers are important, and our mechanism of active hydraulics likely limits the fastest contraction rates. Some insects, like mosquitoes, seem near this theoretical limit, but direct testing is needed.”
The researchers also discovered that when muscle fibers act like an active sponge, they behave as an active elastic engine. Unlike a rubber band, which stores and releases energy while maintaining energy conservation, muscles can generate power by converting chemical fuel into mechanical work, showing “odd elasticity.” This means that when muscles contract and relax, they bulge perpendicularly, not conserving energy and acting like a soft engine.
Shankar said, “These findings contrast with the prevailing view that focuses on molecular details, neglecting muscles’ long, hydrated, and multi-scale nature. Our results suggest a revised understanding of muscle function is essential for grasping the physiology and limits of animal movement.”
Water flow within muscle fibers is crucial in controlling how quickly muscles contract. This discovery highlights the importance of fluid dynamics in muscle function. It suggests a need to rethink our understanding of muscle physiology.
Journal reference:
- Shankar, S., Mahadevan, L. Active hydraulics and odd elasticity of muscle fibers. Nature Physics. DOI: 10.1038/s41567-024-02540-x.