Muscle and tendon mechanical interactions during human locomotion

© 2015 Dr. Adrian LaiDespite the common view that muscles and tendons are two separate entities of the musculoskeletal system, their mechanical functions are inextricably linked. Muscles contract and develop forces, which are transmitted by the tendon to the skeleton to produce joint motion. At the same time, muscles generate work while tendons store and recover elastic strain energy to maintain the exchange of mechanical energy of the body. Understanding muscle and tendon interactions is vital in gaining a full appreciation into how the human lower limb muscles coordinate and power locomotion. Furthermore, alterations in locomotion conditions such as mode and speed can vary the strategies utilised by the lower limb muscles to maintain the mechanical energy of the body as well as to develop sufficient support and propulsive force. Despite the wealth of knowledge of muscle mechanics during human locomotion, muscle fibre and tendon interactions remain unexplored because of the difficulties involved in non-invasively measuring dynamic muscle force and behaviour. Of particular interest is the influence of tendon elasticity on the muscle fibre behaviour and efficiency. In this thesis, we combined experimental data with computational muscle modelling and created a validated framework with which to investigate muscle fibre and tendon interactions in the human ankle plantar-flexors across a range of locomotion conditions from slow walking to fast running, steady-state running to sprint accelerations. Real-time, dynamic ultrasound was used to measure in-vivo muscle and tendon behaviour in the ankle plantar-flexors while computer simulations quantified muscle and tendon behaviour (length and velocity) and energetics. Together, these techniques allowed for non-invasive investigations into the influence of tendon elasticity on muscular work and the operating efficiency of the muscle fibres during human locomotion. The results of this thesis demonstrated that during human locomotion, the muscle fibres in the ankle plantar-flexors maintained high mechanical efficiency for force development as a consequence of tendon elasticity. For instance, with faster steady-state running, the ankle plantar-flexors continued to prioritise tendon elastic strain energy over muscle fibre work for generating the propulsion energy required for steady-state running. This interaction allowed the muscle fibres to develop large forces while remaining at favourable regions of their physiological force-length and force-velocity relationships. This interaction between the muscle fibres and tendon in the ankle plantar-flexors was further affirmed when in-vivo muscle fascicle and tendon behaviour were measured across a range of walking and running speeds. Thus, while muscle fibres developed the support and propulsive forces, the stretch and recoil of the elastic tendon supplemented the propulsion energy generated by the ankle plantar-flexors. Interestingly, our results also suggest that tendon elasticity exists because the muscle fibres in the ankle plantar-flexors alone cannot generate sufficient power and energy required for the acceleration and steady-state sprinting phases of maximal sprint acceleration. Thus, the storage of tendon elastic strain energy in the ankle plantar-flexors is just as vital for enhancing MTU propulsion work output during the acceleration phase as for reducing muscle fibre energy expenditure during the steady-state sprinting phase of sprint acceleration. The key distinction is the mechanism in which the ankle plantar-flexors stored the tendon elastic strain energy during early stance. Hence, even though tendons have been viewed as seemingly simple mechanical structures, they play an indispensable role in controlling skeletal movement, influencing muscle mechanics and managing the energetic demands of the musculoskeletal system during human locomotion. It is hoped that these findings will lead to a better understanding of the relationship between the evolution of muscle-tendon architecture in the human lower-limb and optimal locomotor performance