A neuromechanical model for Drosophila larval crawling based on physical measurements
Abstract Background Animal locomotion requires dynamic interactions between neural circuits, the body (typically muscles), and surrounding environments. While the neural circuitry of movement has been intensively studied, how these outputs are integrated with body mechanics (neuromechanics) is less...
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| Format: | Article |
| Language: | English |
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BMC
2022-06-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-022-01336-w |
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| author | Xiyang Sun Yingtao Liu Chang Liu Koichi Mayumi Kohzo Ito Akinao Nose Hiroshi Kohsaka |
| author_facet | Xiyang Sun Yingtao Liu Chang Liu Koichi Mayumi Kohzo Ito Akinao Nose Hiroshi Kohsaka |
| author_sort | Xiyang Sun |
| collection | DOAJ |
| description | Abstract Background Animal locomotion requires dynamic interactions between neural circuits, the body (typically muscles), and surrounding environments. While the neural circuitry of movement has been intensively studied, how these outputs are integrated with body mechanics (neuromechanics) is less clear, in part due to the lack of understanding of the biomechanical properties of animal bodies. Here, we propose an integrated neuromechanical model of movement based on physical measurements by taking Drosophila larvae as a model of soft-bodied animals. Results We first characterized the kinematics of forward crawling in Drosophila larvae at a segmental and whole-body level. We then characterized the biomechanical parameters of fly larvae, namely the contraction forces generated by neural activity, and passive elastic and viscosity of the larval body using a stress-relaxation test. We established a mathematical neuromechanical model based on the physical measurements described above, obtaining seven kinematic values characterizing crawling locomotion. By optimizing the parameters in the neural circuit, our neuromechanical model succeeded in quantitatively reproducing the kinematics of larval locomotion that were obtained experimentally. This model could reproduce the observation of optogenetic studies reported previously. The model predicted that peristaltic locomotion could be exhibited in a low-friction condition. Analysis of floating larvae provided results consistent with this prediction. Furthermore, the model predicted a significant contribution of intersegmental connections in the central nervous system, which contrasts with a previous study. This hypothesis allowed us to make a testable prediction for the variability in intersegmental connection in sister species of the genus Drosophila. Conclusions We generated a neurochemical model based on physical measurement to provide a new foundation to study locomotion in soft-bodied animals and soft robot engineering. |
| first_indexed | 2024-12-12T16:19:22Z |
| format | Article |
| id | doaj.art-3a0960347fb34be8967843798d96ffed |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-12T16:19:22Z |
| publishDate | 2022-06-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-3a0960347fb34be8967843798d96ffed2022-12-22T00:19:02ZengBMCBMC Biology1741-70072022-06-0120112510.1186/s12915-022-01336-wA neuromechanical model for Drosophila larval crawling based on physical measurementsXiyang Sun0Yingtao Liu1Chang Liu2Koichi Mayumi3Kohzo Ito4Akinao Nose5Hiroshi Kohsaka6Department of Complexity Science and Engineering, Graduate School of Frontier Science, the University of TokyoDepartment of Physics, Graduate School of Science, the University of TokyoDepartment of Advanced Materials Science, Graduate School of Frontier Science, The University of TokyoDepartment of Advanced Materials Science, Graduate School of Frontier Science, The University of TokyoDepartment of Advanced Materials Science, Graduate School of Frontier Science, The University of TokyoDepartment of Complexity Science and Engineering, Graduate School of Frontier Science, the University of TokyoDepartment of Complexity Science and Engineering, Graduate School of Frontier Science, the University of TokyoAbstract Background Animal locomotion requires dynamic interactions between neural circuits, the body (typically muscles), and surrounding environments. While the neural circuitry of movement has been intensively studied, how these outputs are integrated with body mechanics (neuromechanics) is less clear, in part due to the lack of understanding of the biomechanical properties of animal bodies. Here, we propose an integrated neuromechanical model of movement based on physical measurements by taking Drosophila larvae as a model of soft-bodied animals. Results We first characterized the kinematics of forward crawling in Drosophila larvae at a segmental and whole-body level. We then characterized the biomechanical parameters of fly larvae, namely the contraction forces generated by neural activity, and passive elastic and viscosity of the larval body using a stress-relaxation test. We established a mathematical neuromechanical model based on the physical measurements described above, obtaining seven kinematic values characterizing crawling locomotion. By optimizing the parameters in the neural circuit, our neuromechanical model succeeded in quantitatively reproducing the kinematics of larval locomotion that were obtained experimentally. This model could reproduce the observation of optogenetic studies reported previously. The model predicted that peristaltic locomotion could be exhibited in a low-friction condition. Analysis of floating larvae provided results consistent with this prediction. Furthermore, the model predicted a significant contribution of intersegmental connections in the central nervous system, which contrasts with a previous study. This hypothesis allowed us to make a testable prediction for the variability in intersegmental connection in sister species of the genus Drosophila. Conclusions We generated a neurochemical model based on physical measurement to provide a new foundation to study locomotion in soft-bodied animals and soft robot engineering.https://doi.org/10.1186/s12915-022-01336-wBiomechanicsViscoelasticityDrosophila larvaeNeuromechanical model |
| spellingShingle | Xiyang Sun Yingtao Liu Chang Liu Koichi Mayumi Kohzo Ito Akinao Nose Hiroshi Kohsaka A neuromechanical model for Drosophila larval crawling based on physical measurements BMC Biology Biomechanics Viscoelasticity Drosophila larvae Neuromechanical model |
| title | A neuromechanical model for Drosophila larval crawling based on physical measurements |
| title_full | A neuromechanical model for Drosophila larval crawling based on physical measurements |
| title_fullStr | A neuromechanical model for Drosophila larval crawling based on physical measurements |
| title_full_unstemmed | A neuromechanical model for Drosophila larval crawling based on physical measurements |
| title_short | A neuromechanical model for Drosophila larval crawling based on physical measurements |
| title_sort | neuromechanical model for drosophila larval crawling based on physical measurements |
| topic | Biomechanics Viscoelasticity Drosophila larvae Neuromechanical model |
| url | https://doi.org/10.1186/s12915-022-01336-w |
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