Energetic Versatility of Muscle
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Tune, Travis Carver
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Abstract
Muscle in an incredibly versatile, active, soft, crystalline material which makes it very unique. It is ubiquitous in animals across many scales, enabling a diverse range of locomotion types and mechanical functions, capable of operating as a motor, brake, or spring. The fact that muscle is a highly ordered, crystalline material means that x-ray diffraction can be used to observe structural changes at the nanometer scale in muscle, linking its crystal structure to function. While muscle x-ray diffraction is a very well established field, it has only been in the last 15 or so years that very high frequency x-ray detectors have allowed x-ray diffraction experiments to be performed on muscles operating under conditions mimicking their in vivo behavior. In this thesis we use x-ray diffraction combined with stress-strain measurements of muscle operating under in vivo-like conditions in order to link its nanometer scale structure to macroscopic mechanical function. This is difficult because muscle is also a hierarchical material, and interactions between structures on different length scales can have unexpected, emergent effects.
We first examine a pair of muscles in the cockroach Blaberus discoidalis previously established as having very similar quasi-static properties yet very different dynamic stress-strain curves, and therefore mechanical function. Since force in muscle is generated by the interaction between two types of filaments in a crystal lattice, we hypothesized that we could find differences in their lattice structure which may explain these similarities and differences. We show that the radial spacing between these filaments is different between the two muscles, and is of an order of magnitude sufficient to affect force production.
We next used a spatially explicit model in order to further establish that changes at the nanometer scale can affect macroscopic mechanical function. Using a spatially explicit model allows us to examine how small changes at the nanometer scale can affect function at a much larger scale. Using this model, we show that lattice structure changes like those we found in B discoidalis are able to affect mechanical function of muscle.
Finally we return to the simultaneous x-ray diffraction and physiological force experiments and examine the large flight muscles of the hawkmoth Manduca sexta. This muscle is very well ordered and provides many structural features at high time resolution. While there have been previous high-frequency stress-strain x-ray diffraction experiments, these did not examine the behavior of the muscle under physiological conditions mimicking its in vivo conditions. Using M. sexta invertebrate flight muscle operating under dynamic conditions, we examine four hypotheses that have been established using x-ray diffraction in quasi-static and vertebrate skeletal muscles. This is important because these assumptions are sometimes extended to invertebrate muscles under dynamic conditions. We show that we can obtain features from highly time-resolved x-ray diffraction data which can be used to predict macroscopic force through a machine learning model. We also found several structural changes during dynamic oscillations which were inconsistent with expectations established from quasi-static and vertebrate skeletal muscles and offer several hypotheses, including that the relatively slow M. sexta flight muscle may share properties which have been previously thought to be found in high frequency flight muscle.
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Date
2020-08-21
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Dissertation