A vacuum-actuated soft robot inspired by Drosophila larvae to study kinetics of crawling behaviour

PLOS ONE RESEARCH ARTICLE A vacuum-actuated soft robot inspired by Drosophila larvae to study kinetics of crawling behaviour Xiyang Sun1, Akinao Nose1,2, Hiroshi Kohsaka ID1,3* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Department of Complexity Science and Engineering, Graduate School of Frontier Science, the University of Tokyo, Kashiwa, Chiba, Japan, 2 Department of Physics, Graduate School of Science, the University of Tokyo, Tokyo, Japan, 3 Graduate School of Informatics and Engineering, the University of ElectroCommunications, Tokyo, Japan * Abstract OPEN ACCESS Citation: Sun X, Nose A, Kohsaka H (2023) A vacuum-actuated soft robot inspired by Drosophila larvae to study kinetics of crawling behaviour. PLoS ONE 18(4): e0283316. https://doi.org/ 10.1371/journal.pone.0283316 Editor: Jit Muthuswamy, Arizona State University, UNITED STATES Received: October 14, 2022 Accepted: March 6, 2023 Published: April 5, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0283316 Copyright: © 2023 Sun et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting information files. Funding: This work was supported by MEXT/JSPS KAKENHI grants (17K19439, 19H04742, and Peristalsis, a motion generated by the propagation of muscular contraction along the body axis, is one of the most common locomotion patterns in limbless animals. While the kinematics of peristalsis has been examined intensively, its kinetics remains unclear, partially due to the lack of suitable physical models to simulate the locomotion patterns and inner drive in soft-bodied animals. Inspired by a soft-bodied animal, Drosophila larvae, we propose a vacuum-actuated soft robot mimicking its crawling behaviour. The soft structure, made of hyperelastic silicone rubber, was designed to imitate the larval segmental hydrostatic structure. Referring to a numerical simulation by the finite element method, the dynamical change in the vacuum pressure in each segment was controlled accordingly, and the soft robots could exhibit peristaltic locomotion. The soft robots successfully reproduced two previous experimental phenomena on fly larvae: 1. Crawling speed in backward crawling is slower than in forward crawling. 2. Elongation of either the segmental contraction duration or intersegmental phase delay makes peristaltic crawling slow. Furthermore, our experimental results provided a novel prediction for the role of the contraction force in controlling the speed of peristaltic locomotion. These observations indicate that soft robots could serve to examine the kinetics of crawling behaviour in soft-bodied animals. Introduction Over the past few decades, robotics researchers have drawn numerous inspirations from diverse animal species to design robots [1, 2]. One of the recent trends in building animalinspired robots is to utilize soft materials to construct flexible structures, mainly because the flexibility of their body enables adaptive motions in a complex environment [2, 3]. Furthermore, the development of soft robots has shed light on the biological mechanisms of animal motion [4, 5]. In particular, soft robots are useful for understanding the kinematics of softbodied animals’ behaviours that have a high degree of freedom and complicated dynamics [6]. PLOS ONE | https://doi.org/10.1371/journal.pone.0283316 April 5, 2023 1 / 18 PLOS ONE 20H05048 to AN and 17K07042 and 20K06908 to HK). The funders did not play any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. A soft robot inspired by fly larvae The development of biomimetic soft robots has provided valuable platforms for both robotics and neuroscience research fields by referring to animals [7], including caterpillars [1], earthworms [8], and octopi [9]. Crawling is one of the basic animal motions used to move the body in one direction. Several crawling gaits are observed in animal locomotion: two-anchor crawling (e.g. inchworms), peristalsis (e.g. fly larvae), and serpentine (e.g. snakes and nematodes) [10]. In twoanchor crawling, the animal alternatively extends and shortens its body. After the elongation, one end of the body (the head) is anchored to the ground to prevent slipping, and the other end (the tail) is released from the substrate. The subsequent shortening pulls the centre of the animal’s mass forward. In peristalsis, local segmental contraction and relaxation propagate from one end to the other along the body length. The wave of segmental contraction travels in parallel (e.g. fly larvae) or antiparallel (e.g. earthworms) to the crawling direction. In serpentine crawling, waves of bending propagate along the body. These crawling gaits have been mimicked by soft robots, including worm-like robots [8], hornworm-like robots [1], snake-like robots [11], and multigait soft robots [12]. Previously, flexible braided meshtube structures, Meshworm and FabricWorm, have been designed based on the antagonistic muscular arrangement of earthworms [8, 13]. These robots use shape memory alloys and linear springs as actuators, respectively, and are capable of exhibiting crawling. Crawling soft robots have the potential to provide powerful tools to study the kinetics of crawling behavior. However, the use of soft robots in the analyses of animal locomotion is still limited, whereas several physical mechanisms, including how the crawling speed is realized and regulated, remain unclear [14, 15]. Larvae of fruit flies, Drosophila melanogaster, have provided an excellent model of a softbodied organism to investigate peristaltic mechanisms due to their relatively simple structure, stereotyped behaviours, and accumulated knowledge of their neural circuits [16–18]. The third instar fly larva is about 4 mm long and has a segmented body. The dominant larval behaviour is forward crawling, which propels the larval body forward by the propagation of the segmental contraction from tail to head (Fig 1; [19, 20]). Fly larvae also exhibit backward behaviour, where the segmental contraction travels from head to tail [20]. There are spike-like structures at the bottom of fly larvae called denticle bands. The majority of the denticles point Fig 1. Kinematic parameters in fly larval locomotion. (A) A fluorescence image of a third-instar larva expressing a green fluorescent protein in muscle a (...truncated)