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

Xiyang Sun; Akinao Nose; Hiroshi Kohsaka

doi:10.1371/journal.pone.0283316

Peer Review History

Original SubmissionOctober 14, 2022
7 Feb 2023 Decision Letter - Jit Muthuswamy, Editor PONE-D-22-28397A vacuum-actuated soft robot inspired by Drosophila larvae to study kinetics of crawling behaviourPLOS ONE Dear Dr. Kohsaka, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. ============================== I have read through the reviewers comments and I concur with their recommendations for additions and revisions. They have also asked for some clarifications. I suggest you address the clarifications separately in an expanded response document which captures all your revisions and your specific responses to each of the reviewers' comments. ============================== Please submit your revised manuscript by Feb. 20, 2023. 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One of the reviewers has an attachment with comments highlighted. Please make sure you address them as well. Thanks for your patience. Best regards Jit Muthuswamy Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2. Thank you for stating the following in the Acknowledgments Section of your manuscript: "This work was supported by MEXT/JSPS KAKENHI grants (17K19439, 19H04742, and 20H05048 to AN and 17K07042 and 20K06908 to HK). We thank Drs Jane Loveless and Dai Owaki for their critical comments on our manuscript" We note that you have provided funding information that is not currently declared in your Funding Statement. However, funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form. Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows: "This work was supported by MEXT/JSPS KAKENHI grants (17K19439, 19H04742, and 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." Please include your amended statements within your cover letter; we will change the online submission form on your behalf [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Partly Reviewer #2: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: This paper takes a very interesting, bimimetic approach to better understand the propagation of motion by pneumatically controlling segmented, soft, robotic sections to emulate crawling by fly larvae. The robotic emulation of fly larvae movement offers novel insight into how biological, neural circuits may control movement and how to design soft robots using friction asymmetry and direction specific mechanisms. 1. In the introduction, can the authors explain the differences in the mechanics and mechanisms of peristaltic motion vs. inchworm like motion which is often used for soft robotic movement? 2. The concept of asymmetric friction using paper between segments in motion mechanics is an interesting idea to emulate the dendicle band in larvae.While the supplementary Figure 1C shows the contact areas during contractions, a free-body diagram of forces in figure 2 might help to better understand the applied forcesand the direction of motion propagation. How does anisotropic friction arise? Does the angle of the friction force matter? 3. Why does the simulation in Fig.5 for especially for large robots not match the experiment (Fig7D&E) where displacements are smaller? Reviewer #2: Overall, the manuscript was written well, and many different aspect were explored to obtained insight of the biological movement mechanism of fly larva. Below are some detailed comments: Following sentence in abstract should be rewritten to be read well: and limiting the duration of segmental motor bursts slows down larval Following sentence needs rewriting, doesn't read well: However, despite these recent advances in soft robots for studying crawling behaviour, how crawling properties, including speed, are realized and regulated remains unclear (14,15). Authors should be more descriptive between describing the forward and backward crawling of the biological larvae, for example: sequential translation from head to tail, etc. Expand upon following sentence: "Although coordinated motions were generated, this previous maggot robot did not realize crawling behaviour." What exactly was lacking? Fig 1D, what is the difference between the gray and black plots, it should label or write what each are. Mention earlier on that the biological larva features a asymmetric interface, and provide a little more detail about them. Are they active or passive, directional? If I'm not mistaking, the volume of each chamber or the robot as a whole is not being preserved throughout the locomotion process. In other word, if you are deflating chamber(s) and releasing that air, then the the volume is not being preserved. Which is contrary to that of the biological larva, as you mentioned by the body fluid. Therefore, this difference should be mentioned in the text. Furthermore, it would be good to mention how the biological larva actuates each segments via transverse and longitudinal muscle, and how the robot actuates each segment. The differences and overalls between biological and robot larva. Fig 4: It appears that the two rulers channel the path of the robot, if this is the case, it should be mentioned in the text. OCRnA and OCRnB should be spelled out the first time they are used in the text. It is mentioned " One striking difference between the simulation and the soft robot experiment was the existence of asymmetric friction." Could the asymmetric features not be added to the FEM model? Supplementary video of the locomoting robot and FEM analysis would be beneficial for visualization. ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No Reviewer #2: Yes: Hosain Bagheri ******** [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. Attachments Attachment Submitted filename: PONE-D-22-28397_HB.pdf https://doi.org/10.1371/journal.pone.0283316.r001
Revision 1
14 Feb 2023 Author Response Responses to the reviewers’ comments Reviewer #1: This paper takes a very interesting, bimimetic approach to better understand the propagation of motion by pneumatically controlling segmented, soft, robotic sections to emulate crawling by fly larvae. The robotic emulation of fly larvae movement offers novel insight into how biological, neural circuits may control movement and how to design soft robots using friction asymmetry and direction specific mechanisms. 1. In the introduction, can the authors explain the differences in the mechanics and mechanisms of peristaltic motion vs. inchworm like motion which is often used for soft robotic movement? We thank the reviewer for the suggestion. Following the suggestion, we described three gaits of crawling (two-anchor crawling, peristalsis, and serpentine) in the Introduction of the revised manuscript (lines 50-58 in the “Manuscript” document). 2. The concept of asymmetric friction using paper between segments in motion mechanics is an interesting idea to emulate the dendicle band in larvae.While the supplementary Figure 1C shows the contact areas during contractions, a free-body diagram of forces in figure 2 might help to better understand the applied forcesand the direction of motion propagation. How does anisotropic friction arise? Does the angle of the friction force matter? We appreciate the reviewer’s suggestion. The deformation of the soft robot and dynamic change in the contact angle between the soft robot and the substrate underlies the asymmetric friction. We tried to create free-body diagrams, but since the friction changes dynamically during the motion we could not create satisfactory illustrations. Instead, we made schematics of the mechanism on the asymmetric friction and demonstrated them in Figures 2G and 2H. 3. Why does the simulation in Fig.5 for especially for large robots not match the experiment (Fig7D&E) where displacements are smaller? We appreciate this insightful comment. As the reviewer suggested, although the simulation results are qualitatively consistent with the soft robot experiments, there are quantitative differences between the two. The main difference is that the friction force is not implemented in the simulation because the modelling frictional forces is challenging. Thus, the simulation exhibited larger deformation (Figure 5B-5E) than the soft robot experiments (Figure 7B-7E). We described this point in lines 257-259 and 334-337 in the revised “Manuscript” document. Reviewer #2: Overall, the manuscript was written well, and many different aspect were explored to obtained insight of the biological movement mechanism of fly larva. Below are some detailed comments: Following sentence in abstract should be rewritten to be read well: and limiting the duration of segmental motor bursts slows down larval We thank the reviewer for this suggestion. Following the suggestion, we revised this part as “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.” We described this in lines 30-32 in the revised “Manuscript” document. Following sentence needs rewriting, doesn't read well: However, despite these recent advances in soft robots for studying crawling behaviour, how crawling properties, including speed, are realized and regulated remains unclear (14,15). We thank the reviewer for pointing out this issue. As suggested, we revised this part and described it in lines 64-67 in the revised “Manuscript” document. Authors should be more descriptive between describing the forward and backward crawling of the biological larvae, for example: sequential translation from head to tail, etc. We thank the reviewer for raising this point. Following the suggestion, we described the kinematics of the forward and backward larval crawling in lines 71-74 in the revised “Manuscript” document. Expand upon following sentence: "Although coordinated motions were generated, this previous maggot robot did not realize crawling behaviour." What exactly was lacking? We thank the reviewer for pointing out this issue. The previous maggot robot could exhibit propagation patterns of the segmental contraction in water, but the report didn’t present data about peristalsis on a solid substrate. We described this point in lines 78-82 in the revised “Manuscript” document. Fig 1D, what is the difference between the gray and black plots, it should label or write what each are. We thank the reviewer for raising this point. The black and grey curves show the kinematics of one segment boundary and its adjacent anterior segment boundary. We are sorry for this unclearness. We added this explanation in the legend of Figure 1D (lines 88-90 in the revised “Manuscript” document. Mention earlier on that the biological larva features a asymmetric interface, and provide a little more detail about them. Are they active or passive, directional? We thank the reviewer for this suggestion. They are passive and directional structures. We described the properties of the asymmetric interface in lines 74-77 in the revised “Manuscript” document. If I'm not mistaking, the volume of each chamber or the robot as a whole is not being preserved throughout the locomotion process. In other word, if you are deflating chamber(s) and releasing that air, then the the volume is not being preserved. Which is contrary to that of the biological larva, as you mentioned by the body fluid. Therefore, this difference should be mentioned in the text. Furthermore, it would be good to mention how the biological larva actuates each segments via transverse and longitudinal muscle, and how the robot actuates each segment. The differences and overalls between biological and robot larva. We appreciate this insightful suggestion. As the reviewer pointed out, the volume of each chamber can be changed during the locomotion. Following the suggestion, we described the difference in lines 119-124. We also described the difference in the actuation between fly larvae and soft robots in lines 180-182 in the revised “Manuscript” document. Fig 4: It appears that the two rulers channel the path of the robot, if this is the case, it should be mentioned in the text. We thank the reviewer for this suggestion. As suggested, we described this point in lines 232-234 in the revised “Manuscript” document. OCRnA and OCRnB should be spelled out the first time they are used in the text. We thank the reviewer for raising this point. Following the suggestion, we spelled out them in lines 303-305 in the revised “Manuscript” document. It is mentioned " One striking difference between the simulation and the soft robot experiment was the existence of asymmetric friction." Could the asymmetric features not be added to the FEM model? We appreciate this insightful suggestion. Due to the complexity of the dynamics of frictional forces, we could not implement the friction in our simulation. We described this point in lines 257-259 and 334-337 in the revised “Manuscript” document. Supplementary video of the locomoting robot and FEM analysis would be beneficial for visualization. We thank the reviewer this suggestion. We included the videos of the FEM analysis and the locomoting robot as Supplementary Videos 1 and 2, respectively. https://doi.org/10.1371/journal.pone.0283316.r002
8 Mar 2023 Decision Letter - Jit Muthuswamy, Editor A vacuum-actuated soft robot inspired by Drosophila larvae to study kinetics of crawling behaviour PONE-D-22-28397R1 Dear Dr. Kohsaka, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Jit Muthuswamy Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #2: All comments have been addressed ******** 2. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #2: Yes ****** 4. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #2: Yes ****** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #2: Yes ****** 6. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #2: (No Response) ****** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #2: Yes: Hosain Bagheri ******** https://doi.org/10.1371/journal.pone.0283316.r003
Formally Accepted
15 Mar 2023 Acceptance Letter - Jit Muthuswamy, Editor PONE-D-22-28397R1 A vacuum-actuated soft robot inspired by Drosophila larvae to study kinetics of crawling behaviour Dear Dr. Kohsaka: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Jit Muthuswamy Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0283316.r004

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