Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA, United States of America.
Department of Ecology, Evolution, and Organismal Biology, Brown University, Providence, RI, United States of America.
Bioinspir Biomim. 2024 Jan 24;19(2). doi: 10.1088/1748-3190/ad1b2b.
Pennate muscles are defined by the architectural arrangement of their muscle fibers, which run at an angle to the primary axis of muscle shortening. Pennation angles can vary dynamically over the course of individual contractions, influencing the speed and distance of muscle shortening. Despite their relevance to muscle performance, the physical mechanisms that drive dynamic changes in pennation angle remain poorly understood. Muscle fibers bulge radially as they shorten, a consequence of maintaining a constant internal fluid volume, and we hypothesized that radial interactions between tightly packed muscle fibers are essential to dynamic pennation angle changes. To explore this, we built physical models of pennate muscles in which the radial distance between fiber-like actuators could be experimentally altered. Models were built from pennate arrays of McKibben actuators, a type of pneumatic actuator that forcefully shortens and bulges radially when inflated with compressed air. Consistent with past studies of biological muscle and engineered pennate actuators, we found that the magnitude of pennation angle change during contraction varied with load. Importantly, however, we found that pennation angle changes were also strongly influenced by the radial distance between neighboring McKibben actuators. Increasing the radial distance between neighboring actuators reduced pennation angle change during contraction and effectively eliminated variable responses to load. Radial interactions between muscle fibers are rarely considered in theoretical and experimental analyses of pennate muscle; however, these findings suggest that radial interactions between fibers drive pennation angle changes and influence pennate muscle performance. Our results provide insight into the fundamental mechanism underlying dynamic pennation angle changes in biological muscle and highlight design considerations that can inform the development of engineered pennate arrays.
羽状肌的特征是其肌纤维的结构排列，这些纤维与肌肉缩短的主轴线成一定角度。在单个收缩过程中，肌节角可以动态变化，影响肌肉缩短的速度和距离。尽管羽状肌与肌肉性能有关，但驱动肌节角动态变化的物理机制仍知之甚少。肌肉纤维在缩短时会径向膨出，这是维持恒定内部流体体积的结果，我们假设紧密堆积的肌纤维之间的径向相互作用对于动态羽状肌节角变化至关重要。为了探索这一点，我们构建了羽状肌的物理模型，其中纤维状执行器之间的径向距离可以通过实验改变。模型是由 McKibben 执行器的羽状阵列构建的， McKibben 执行器是一种气动执行器，当用压缩空气充气时，它会强力地径向缩短和膨出。与过去对生物肌肉和工程羽状执行器的研究一致，我们发现收缩过程中羽状肌节角变化的幅度随负载而变化。然而，重要的是，我们发现羽状肌节角的变化也受到相邻 McKibben 执行器之间的径向距离的强烈影响。增加相邻执行器之间的径向距离会减少收缩过程中的羽状肌节角变化，并有效地消除对负载的可变响应。在羽状肌的理论和实验分析中，很少考虑肌纤维之间的径向相互作用；然而，这些发现表明纤维之间的径向相互作用驱动羽状肌节角的变化，并影响羽状肌的性能。我们的研究结果为生物肌肉中动态羽状肌节角变化的基本机制提供了深入的了解，并强调了可以为工程羽状阵列的发展提供信息的设计考虑因素。
