Internal mechanics of whole muscle contraction

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Much of our understanding of muscle function comes from single fibre and isolated muscle experiments that commonly have steady contractile conditions and maximal activation, and muscle models reflect this. However, our muscles are normally used for unsteady and dynamic movements at submaximal levels of contraction. Contractions of whole muscles are more complex than that of their constituent muscle fibres. Indeed, recent models of whole muscle force production in vivo have large errors, indicating that we still have much to learn about how whole muscles contract. Not only do muscles develop force and change in length along their line of action, but forces and deformations occur across all three dimensions. Recently, the importance of the 3D structure of muscle, and the interactions between contractile and connective tissues have become evident. For example, compressing a muscle supresses the force developed in its line of action (up to 16%), and muscle contractions result in transverse work being done (tensing your glutes whilst you are sitting will raise your body due to transverse muscle work). Additionally, if you maximally activate a muscle then it will never shorten as fast as its constituent fibres are capable of, with this discrepancy (up to 35%) being greatest for large muscles at low levels of activation (typical conditions for our everyday movements). Different labs, including my own, have proposed factors to explain these phenomena, including internal elasticity, force transmission and transverse work, drag of inactive tissues, and inertial properties of the muscle tissue. However, we still lack a general framework that relates all these effects to a muscle's contractile performance. Identifying the mechanisms that contribute to whole-muscle function will increase our basic understanding of muscle biomechanics and enhance our ability to study and maintain animal and human mobility, agility and health. There is finite energy available for muscle contractions and so we propose that mechanisms that use internal energy, or even do external work in a transverse direction, will diminish the work output along its line of action. Not only that, but the efficiency of muscle contractions will be reduced in situations that incur a metabolic cost for using internal energy and doing transverse work. The objective of the proposed research is to use theoretical techniques, validated with cutting-edge experimental data, to relate the distribution of internal energy within a muscle to its 3D shape and force. In particular, we will refine and validate a finite element model of muscle contractions, investigate the relation between transverse compression and bulging on longitudinal force, and investigate the effect of muscle tissue mass on the dynamics and efficiency of muscle contractions. The long-term goal of my research program is to develop our mechanistic understanding of the contractile mechanics of whole muscle.