IDEAS home Printed from https://ideas.repec.org/a/gam/jmathe/v11y2023i11p2442-d1155399.html
   My bibliography  Save this article

A Connectome-Based Digital Twin Caenorhabditis elegans Capable of Intelligent Sensorimotor Behavior

Author

Listed:
  • Zhongyu Chen

    (School of Computer Science, Fudan University, Shanghai 200438, China)

  • Yuguo Yu

    (Shanghai Artificial Intelligence Laboratory, Shanghai 200232, China
    Research Institute of Intelligent and Complex Systems, Fudan University, Shanghai 200433, China
    State Key Laboratory of Medical Neurobiology, Fudan University, Shanghai 200433, China
    MOE Frontiers Center for Brain Science, Fudan University, Shanghai 200433, China)

  • Xiangyang Xue

    (School of Computer Science, Fudan University, Shanghai 200438, China)

Abstract

Despite possessing a simple nervous system, the Caenorhabditis elegans exhibits remarkably intelligent behavior. However, the underlying mechanisms involved in sensory processing and decision making, which contribute to locomotion behaviors, remain unclear. In order to investigate the coordinated function of neurons in achieving chemotaxis behavior, we have developed a digital twin of the C. elegans that combines a connectome-based neural network model with a realistic digital worm body. Through training the digital worm using offline chemotaxis behavioral data generated with a PID controller, we have successfully replicated faithful sinusoidal crawling and intelligent chemotaxis behavior, similar to real worms. By ablating individual neurons, we have examined their roles in modulating or contributing to the regulation of behavior. Our findings highlight the critical involvement of 119 neurons in sinusoidal crawling, including B-type, A-type, D-type, and PDB motor neurons, as well as AVB and AVA interneurons, which was experimentally demonstrated. We have also predicted the involvement of DD04 and DD05 neurons and the lack of relevance of DD02 and DD03 neurons in crawling, which have been confirmed through experimentation. Additionally, head motor neurons, sublateral motor neurons, layer 1 interneurons, and layer 1 and layer 5 sensory neurons are expected to play a role in crawling. In summary, we present a novel methodological framework that enables the establishment of an animal model capable of closed-loop control, faithfully replicating realistic animal behavior. This framework holds potential for examining the neural mechanisms of behaviors in other species.

Suggested Citation

  • Zhongyu Chen & Yuguo Yu & Xiangyang Xue, 2023. "A Connectome-Based Digital Twin Caenorhabditis elegans Capable of Intelligent Sensorimotor Behavior," Mathematics, MDPI, vol. 11(11), pages 1-23, May.
  • Handle: RePEc:gam:jmathe:v:11:y:2023:i:11:p:2442-:d:1155399
    as

    Download full text from publisher

    File URL: https://www.mdpi.com/2227-7390/11/11/2442/pdf
    Download Restriction: no

    File URL: https://www.mdpi.com/2227-7390/11/11/2442/
    Download Restriction: no
    ---><---

    References listed on IDEAS

    as
    1. Jeffrey P Nguyen & Ashley N Linder & George S Plummer & Joshua W Shaevitz & Andrew M Leifer, 2017. "Automatically tracking neurons in a moving and deforming brain," PLOS Computational Biology, Public Library of Science, vol. 13(5), pages 1-19, May.
    2. Gang Yan & Petra E. Vértes & Emma K. Towlson & Yee Lian Chew & Denise S. Walker & William R. Schafer & Albert-László Barabási, 2017. "Network control principles predict neuron function in the Caenorhabditis elegans connectome," Nature, Nature, vol. 550(7677), pages 519-523, October.
    3. Hiroshi Suzuki & Tod R. Thiele & Serge Faumont & Marina Ezcurra & Shawn R. Lockery & William R. Schafer, 2008. "Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis," Nature, Nature, vol. 454(7200), pages 114-117, July.
    4. Daniel Witvliet & Ben Mulcahy & James K. Mitchell & Yaron Meirovitch & Daniel R. Berger & Yuelong Wu & Yufang Liu & Wan Xian Koh & Rajeev Parvathala & Douglas Holmyard & Richard L. Schalek & Nir Shavi, 2021. "Connectomes across development reveal principles of brain maturation," Nature, Nature, vol. 596(7871), pages 257-261, August.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Zhihao Zheng & Christopher S. Own & Adrian A. Wanner & Randal A. Koene & Eric W. Hammerschmith & William M. Silversmith & Nico Kemnitz & Ran Lu & David W. Tank & H. Sebastian Seung, 2024. "Fast imaging of millimeter-scale areas with beam deflection transmission electron microscopy," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Zhou, Ming-Yang & Xiong, Wen-Man & Wu, Xiang-Yang & Zhang, Yu-Xia & Liao, Hao, 2018. "Overlapping influence inspires the selection of multiple spreaders in complex networks," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 508(C), pages 76-83.
    3. Kate L. Laskowski & David Bierbach & Jolle W. Jolles & Carolina Doran & Max Wolf, 2022. "The emergence and development of behavioral individuality in clonal fish," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    4. Chenxi Lin & Yuxin Shan & Zhongyi Wang & Hui Peng & Rong Li & Pingzhou Wang & Junyan He & Weiwei Shen & Zhengxing Wu & Min Guo, 2024. "Molecular and circuit mechanisms underlying avoidance of rapid cooling stimuli in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Javier J How & Saket Navlakha & Sreekanth H Chalasani, 2021. "Neural network features distinguish chemosensory stimuli in Caenorhabditis elegans," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-38, November.
    6. Li, Sheng & Liu, Wenwen & Wu, Ruizi & Li, Junli, 2023. "An adaptive attack model to network controllability," Reliability Engineering and System Safety, Elsevier, vol. 235(C).
    7. Noa Deshe & Yifat Eliezer & Lihi Hoch & Eyal Itskovits & Eduard Bokman & Shachaf Ben-Ezra & Alon Zaslaver, 2023. "Inheritance of associative memories and acquired cellular changes in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Hyunsoo Yim & Daniel T. Choe & J. Alexander Bae & Myung-kyu Choi & Hae-Mook Kang & Ken C. Q. Nguyen & Soungyub Ahn & Sang-kyu Bahn & Heeseung Yang & David H. Hall & Jinseop S. Kim & Junho Lee, 2024. "Comparative connectomics of dauer reveals developmental plasticity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Liu, Suling & Xu, Qiong & Chen, Aimin & Wang, Pei, 2020. "Structural controllability of dynamic transcriptional regulatory networks for Saccharomyces cerevisiae," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 537(C).
    10. Tobias Clark & Vera Hapiak & Mitchell Oakes & Holly Mills & Richard Komuniecki, 2018. "Monoamines differentially modulate neuropeptide release from distinct sites within a single neuron pair," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-22, May.
    11. Dániel L. Barabási & Taliesin Beynon & Ádám Katona & Nicolas Perez-Nieves, 2023. "Complex computation from developmental priors," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    12. Richard F Betzel & Katherine C Wood & Christopher Angeloni & Maria Neimark Geffen & Danielle S Bassett, 2019. "Stability of spontaneous, correlated activity in mouse auditory cortex," PLOS Computational Biology, Public Library of Science, vol. 15(12), pages 1-25, December.
    13. Duan, Dongli & Wu, Xixi & Bai, Xue & Yan, Qi & Lv, Changchun & Bian, Genqing, 2022. "Dimensionality reduction method of dynamic networks for evolutionary mechanism of neuronal systems," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 599(C).
    14. Shivesh Chaudhary & Sihoon Moon & Hang Lu, 2022. "Fast, efficient, and accurate neuro-imaging denoising via supervised deep learning," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Robert Peach & Alexis Arnaudon & Mauricio Barahona, 2022. "Relative, local and global dimension in complex networks," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    16. Francesca Coraggio & Mahak Bhushan & Spyridon Roumeliotis & Francesca Caroti & Carlo Bevilacqua & Robert Prevedel & Georgia Rapti, 2024. "Age-progressive interplay of HSP-proteostasis, ECM-cell junctions and biomechanics ensures C. elegans astroglial architecture," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    17. Wendy Xueyi Wang & Julie L. Lefebvre, 2022. "Morphological pseudotime ordering and fate mapping reveal diversification of cerebellar inhibitory interneurons," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    18. van Elteren, Casper & Quax, Rick & Sloot, Peter, 2022. "Dynamic importance of network nodes is poorly predicted by static structural features," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 593(C).
    19. Yu, Xiaoyao & Liang, Yongqing & Wang, Xiaomeng & Jia, Tao, 2021. "The network asymmetry caused by the degree correlation and its effect on the bimodality in control," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 572(C).

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:gam:jmathe:v:11:y:2023:i:11:p:2442-:d:1155399. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: MDPI Indexing Manager (email available below). General contact details of provider: https://www.mdpi.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.