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The Cross-Bridge Spring: Can Cool Muscles Store Elastic Energy?

Science  07 Jun 2013:
Vol. 340, Issue 6137, pp. 1217-1220
DOI: 10.1126/science.1229573

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Lock and Load in the Cold

Muscle extensibility can act as an energy storage vehicle, like springs bouncing back after being compressed. George et al. (p. 1217, published online 25 April) now show that energy can also be stored within muscles as a function of their natural temperature gradient. In hawkmoth muscle myofilaments, reduced cross-bridge cycling regionally constrains myofilaments, resulting in a "lock-spring lattice" that enables elastic energy storage as both the myofilaments and cross-bridges deform. Elastic energy stored in cross-bridges that remain bound and elastically deformed at the end of the first half of a contraction cycle can be released during the second half, thus serving as an additional elastic force. Such "bonus" energy may be especially important given the high energetic demands of flight, but because temperature gradients are a natural result of energy generation and heat dissipation in muscle, this mechanism could be more broadly important in locomotion systems.

Abstract

Muscles not only generate force. They may act as springs, providing energy storage to drive locomotion. Although extensible myofilaments are implicated as sites of energy storage, we show that intramuscular temperature gradients may enable molecular motors (cross-bridges) to store elastic strain energy. By using time-resolved small-angle x-ray diffraction paired with in situ measurements of mechanical energy exchange in flight muscles of Manduca sexta, we produced high-speed movies of x-ray equatorial reflections, indicating cross-bridge association with myofilaments. A temperature gradient within the flight muscle leads to lower cross-bridge cycling in the cooler regions. Those cross-bridges could elastically return energy at the extrema of muscle lengthening and shortening, helping drive cyclic wing motions. These results suggest that cross-bridges can perform functions other than contraction, acting as molecular links for elastic energy storage.

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