On the mechanics of skeletal and smooth muscle : linking structure to function

Abstract

Muscle is essential to the health and well-being of animals and humans, performing crucial functions such as enabling movement (skeletal muscle) and facilitating the motility of fluids within hollow organs (smooth muscle). Muscular tissue is pervasive throughout the body, with skeletal muscle alone accounting for approximately 35% of human body mass, underscoring its biological significance. Due to its widespread presence and vital functions, muscular tissue remains a central focus of research in the natural sciences, particularly in medicine. The rigorous study of muscle originated during the 17th-century scientific revolution, when figures like Giovanni Alfonso Borelli and Niels Stensen first recognized the relationship between skeletal muscle structure and force output. Our contemporary understanding encompasses key principles such as the influence of fiber length on muscle excursion and velocity, as well as the functional implications of pennate fiber arrangements. Nonetheless, several important aspects remain insufficiently characterized. In particular, the three-dimensional deformation of muscle fibers during dynamic movement is not yet fully resolved. In the domain of smooth muscle, notable progress has been made in describing its complex mechanical behavior, including nonlinear stress responses, viscoelasticity, and adaptation. However, experimental approaches frequently rely on simplified uniaxial testing, which does not accurately reflect in vivo behavior. Additionally, the impact of smooth muscle length adaptation on testing protocols remains unclear, and the structural and functional heterogeneity of the stomach continues to pose challenges for computational modeling. This thesis was funded by the Deutsche Forschungsgemeinschaft (DFG) under grant SI841/13-1 and addresses three principal research areas: A. Skeletal muscle architecture, B. Constitutive properties of smooth muscle tissue, and C. Mechanical heterogeneity and anisotropy of the stomach. Across nine individual contributions, the thesis investigates the following seven research questions: Skeletal muscle architecture A1. How does muscle architecture adapt during muscle lengthening? A2. How does muscle architecture compare between in situ and isolated conditions? A3. How does muscle architecture adapt throughout the growth process? Constitutive properties of smooth muscle tissue B1. How does the stress-stretch response of urinary smooth muscle compare between uniaxial and biaxial test modes? B2. How can reproducible results be obtained in repeated tensile tests of smooth muscle tissue? Mechanical heterogeneity and anisotropy of the stomach C1. How does stomach wall thickness vary locally? C2. What are the local strain patterns in the stomach wall during passive filling? To address these questions, a range of experimental methodologies was employed. Skeletal muscle architecture was investigated by manually digitizing fiber paths in rabbit calf muscles using a Microscribe MLX. The passive and active mechanical responses of porcine urinary smooth muscle tissue were analyzed through biaxial tensile testing with a custom-built device, and length adaptation was studied via uniaxial tests using an Aurora Scientific 305C-LR. For the stomach, local wall thickness was measured directly, and strain distributions were assessed through optical, marker-based analysis (VICON Motus) during in vitro inflation tests. The research yielded a number of significant findings regarding the structural and mechanical characteristics of muscular tissue. In skeletal muscle, length changes were found to induce compartment-specific alterations in the architecture of the rabbit M. gastrocnemius lateralis. Furthermore, muscle growth during maturation was shown to involve complex architectural remodeling rather than uniform scaling. With respect to smooth muscle, substantial differences in optimal stretch - though not stress - were observed between uniaxial and biaxial testing of urinary bladder tissue. Additionally, it was demonstrated that isometric contractions at reference length can reverse effects of length adaptation. In the stomach, pronounced regional differences were identified in the thickness of muscle and mucosal layers, along with heterogeneous and anisotropic strain patterns during passive inflation. Collectively, these results contribute to a more detailed understanding of the functional specialization and adaptive behavior of muscular tissues. The compartment-specific modifications observed in the M. gastrocnemius lateralis suggest a previously underappreciated level of functional differentiation within individual muscles. The architectural changes associated with growth appear to favor energy storage in the tendon and a reduction of the muscle’s rotational inertia with respect to the knee joint. In smooth muscle, the discrepancy between uniaxial and biaxial results indicates that the bladder may operate closer to its optimal stress in vivo than would be predicted from conventional uniaxial test results. Finally, the complex mechanical behavior of the stomach wall, including its anisotropy and regional thickness variation, reflects its functional compartmentalization and provides essential data for the development of accurate computational models.