Phototactic guidance of a tissue-engineered soft-robotic ray

Abstract

Inspired by the relatively simple morphological blueprint provided by batoid fish such as stingrays and skates, we create a biohybrid system that enables an artificial animal, a tissue-engineered ray, * Correspondence to: K.K.P. 29 Oxford Street, Pierce Hall Cambridge, MA 02130. kkparker@seas.harvard.edu. Phone: 617-495-2850, 617-835-5920. Fax: 617-496-1793 Bioinspired design, as applied to robotics, aims at implementing naturally occurring features such as soft materials, morphologies, gaits, and control mechanisms in artificial settings to improve performance (1-4). For example, recent soft-robotics studies raised awareness on the importance of material properties (3, 4), shifting the focus from rigid elements to soft materials, while other investigations report successful mimicry of gaits or morphological features inspired by insects (5, 6), fish (7,8), snake (9), salamanders (10) and cheetahs (11). While recent advances have the promise of bridging the performance gap with animals, the current soft-robotic actuators based on, for instance, electroactive polymers, shape memory alloys or pressurized fluids, are yet to mature to the point of replicating the high-resolution complex movements of biological muscles (3, 4).In this context, biosensors and bioactuators (12) are intriguing alternatives, since they can intrinsically respond to a number of control inputs (such as electric fields and optical stimulation). Thanks to recent advances in genetic tools (13) and tissue engineering (12), these responses can be altered and tuned across a wide range of time and length scales. Some pioneering studies have exploited these technologies for self-propulsion, developing miniaturized walking machines (14-16), and flagellar (17) or jellyfish inspired (18) swimming devices. These biohybrid systems operate at high energy efficiency and harvest power from energy dense, locally available nutrients, although at present they require specialized environments (physiological solutions) that may limit their applicability. Moreover and most importantly, these biohybrid locomotors lack of the reflexive control (9, 19) necessary to enable adaptive maneuvering and thus of the ability to respond to spatiotemporally varying external stimuli.Here, we design, build and test a tissue-engineered analog of a batoid fish such as stingrays and skates. By combining soft materials and tissue engineering with optogenetics, we created an integrated sensory-motor system that allowed for coordinated undulating fin movement and phototactically controlled locomotion, that is guided via light stimuli. We drew from fish morphology, neuromuscular dynamics and gait control to implement a living, bio-hybrid system that leads to robust and reproducible locomotion and turning maneuvers. Batoid fish are ideal biological models in robotics (8) because their nearly planar bauplan is characterized by a broad dorsoventral disk, with a flattened body and extended pectoral fins, that enhances stability against roll (20). They swim with high energy efficien...

Batoid locomotion: effects of speed on pectoral fin deformation in the little skate, Leucoraja erinacea

“…Third, batoids are increasingly serving as subjects for robotic models of aquatic propulsion (e.g. Blevins and Lauder, 2013;Cloitre et al, 2012;Dewey et al, 2012;Krishnamurthy et al, 2010;Moored et al, 2011a,b;Park et al, 2016), and yet threedimensional biological data on how the wing moves are extremely limited. Such data are needed to provide a template for programming robotic ray wing surface motions, and we aim to provide a new kinematic data set on wing-based aquatic propulsion for this purpose.…”

Advances in engineering hydrogels

“…Carefully designed microstructures seeded with cells are able to self-fold into predefined architectures through origami (92). Alternatively, cells that spontaneously contract enable mechanical movement of the substrate on which they reside, leading to generation of soft bioactuators (93, 94). Whereas earlier bioactuators were mainly based on elastomeric materials, hydrogel materials have recently attracted increasing attention because of their better biocompatibility.…”

Biomimicry, Biofabrication, and Biohybrid Systems: The Emergence and Evolution of Biological Design

“…Parker and co-workers applied a similar approach toward another natural organism, the stingray, to show that more complex swimming mechanisms could also be accomplished using this methodology. [111] By genetically engineering the cardiomyocytes to respond to a visible light stimulus, they were able to coordinate sequential contraction in separate regions of the biohybrid machine. This enabled biomimicry of the undulating motion of stingrays and demonstrated that visible light signals could be used to steer and the machines through an obstacle course.…”