Mechanics and Energetics of Force Production in Muscle

Abstract

The mechanics and energetics of skeletal muscle force production are important for many movements, including locomotion. But they have been characterized primarily for steady conditions such as constant shortening velocity and fixed muscle length, rather than dynamic or cyclic conditions that resemble daily movements. Although musculoskeletal models are intended to predict how muscles behave during movement, there have been few quantitative experiments to inform such models. In this thesis, I experimentally examine muscle mechanics and energetics for cyclic conditions, and then apply those data to develop a new computational model of muscle. The model reproduces activation and force development dynamics observed experimentally, is more mechanistic than current Hill-type models, and better matches energy expenditure for cyclic conditions. A simple summary of these effects is that muscle behaves like a low-pass filter with respect to excitatory input. A filter predicts a sharp increase in energetic cost with faster cyclic conditions, in agreement with empirical data (Chapter 2). To facilitate quantification of muscle mechanics in vivo, I developed an algorithm to track muscle fascicles in ultrasound images, named ‘TimTrack’ (Chapter 3). Much of the energetic cost of cyclic force production was not explained by traditional measures of work or force, but by rate of force development (termed ‘force-rate’). To expand on the low-pass filter, I proposed a model that combines muscle dynamics with steady relations and series elasticity. Unlike existing models, the proposed model predicts muscle force development across a broad range of conditions in a self-consistent manner (Chapter 4). An essential aspect is a set of dynamics intermediate to calcium activation and muscle cross-bridges, here termed force facilitation. These dynamics help explain the energetic cost of both steady and cyclic muscle contractions, in qualitative agreement with the simple low-pass filter (Chapter 5). Model simulations suggest that most of the force-rate cost is due to increased calcium transport at higher muscle excitation levels. The experiments and computational modeling presented here demonstrate energetic costs not previously identified or modeled and have potential to improve understanding of how muscles contribute to daily movements.