Development of a Biohybrid Tendon Interface for Muscle-Powered Robots

Unlike metal and plastic, biological materials can communicate with their surroundings, adapt to stimuli, and self-repair damage. Thus, incorporating these materials into engineered systems could foster smarter, more adaptable machines. Our lab has shown that a ring of engineered skeletal muscle stretched around a flexible ‘skeleton’ can generate force and drive motion (<i>Raman et al, PNAS 2016</i>). However, the interface between the biotic and abiotic components of this robotic system are friction-based, leading to inefficient force transmission. The ring morphology of the biological actuator also restricts its applicability and modularity in more complex system setups. To solve these issues, we have taken a bioinspired approach. In the body, muscle is covalently tethered to bone via tendons, which efficiently transmit force. Thus, we have developed a bioinspired synthetic tendon to act as a biohybrid stiffness-gradient interface, enabling the design of more modular and efficient bioactuators for adaptive biohybrid machines.<br/><br/>We developed an adhesive hydrogel tendon, composed of a poly(acrylic acid) hydrogel functionalized for tissue adhesion with N-Hydroxysuccinimide esters, in collaboration with the Zhao Lab at MIT. Its characteristics as a tendon material were evaluated. Muscle tissues were manufactured from optogenetic C2C12 mouse myoblasts seeded into a fibrin and Matrigel matrix, and were then differentiated with horse serum. Peel tests of muscle bound between two synthetic tendon sections revealed the biotic-abiotic interface could withstand forces &gt;500mN before breaking. This is significantly greater than force generated from the contraction of engineered muscle (~300uN), demonstrating a robust binding. A cell viability assay and synthetic tendon exposure test confirmed that the hydrogel had no significant impact on muscle health.<br/><br/>Furthermore, we combined this tendon with our engineered muscle to evaluate a new bioactuator composition. We have bound a strip of muscle between two strips of tendon, akin to myotendinous junctions <i>in vivo</i>. Thus, we are leveraging this tendon-muscle-tendon (TMT) construct as a modular actuator that can be mechanically coupled to robotic skeletons to generate force and motion. TMT constructs were mounted onto flexure skeletons to determine force production capabilities (<i>Lynch et al, Adv. Intell. Syst. 2024</i>). In addition, these trials were repeated with tendons backed by two types of polyurethane, Hydromed D3 and hydrothane, with mean stiffnesses of ~900kPa and ~2700kPa, respectively, which are ~7x and ~21x the stiffness of our muscle sections (~130kPa). In all cases, mounted TMTs were variously pretensioned by sweeping across the entire adjustable pin-to-pin distance range (8-14mm) of the flexure skeleton resulting in a general TMT strain of 0-27%. This range corresponds to a rotation angle of the adjustable cam on this skeleton.<br/><br/>We have first evaluated the compatibility of a synthetic tendon material with our bioactuators, finding suitable binding strength and biocompatibility. In addition, we have evaluated the effects of varying synthetic tendon stiffness and preload tension on the force production capability of TMT units, enabling the optimized design and deployment of TMT actuators in untethered machines. Currently, our TMT constructs are being deployed in a robotic gripper skeleton to demonstrate its applicability in isolated robotic systems. Our TMT studies have shown the ability to generate comparable contractile strokes from ~1/2 the volume of previous muscle ring configurations, thus increasing power-to-weight ratio by ~2X. In essence, we have developed a hydrogel tendon system that serves as a robust biocompatible musculoskeletal interface that expands the implementation of biological materials into engineered systems. In addition to robotics, we anticipate future application of our system as an implantable muscle graft with suturable tendons to repair injured and diseased muscle <i>in vivo</i>.