IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26748-0.html
   My bibliography  Save this article

Precise visuomotor transformations underlying collective behavior in larval zebrafish

Author

Listed:
  • Roy Harpaz

    (Harvard University
    Harvard University)

  • Minh Nguyet Nguyen

    (Johns Hopkins University)

  • Armin Bahl

    (University of Konstanz)

  • Florian Engert

    (Harvard University
    Harvard University)

Abstract

Complex schooling behaviors result from local interactions among individuals. Yet, how sensory signals from neighbors are analyzed in the visuomotor stream of animals is poorly understood. Here, we studied aggregation behavior in larval zebrafish and found that over development larvae transition from overdispersed groups to tight shoals. Using a virtual reality assay, we characterized the algorithms fish use to transform visual inputs from neighbors into movement decisions. We found that young larvae turn away from virtual neighbors by integrating and averaging retina-wide visual occupancy within each eye, and by using a winner-take-all strategy for binocular integration. As fish mature, their responses expand to include attraction to virtual neighbors, which is based on similar algorithms of visual integration. Using model simulations, we show that the observed algorithms accurately predict group structure over development. These findings allow us to make testable predictions regarding the neuronal circuits underlying collective behavior in zebrafish.

Suggested Citation

  • Roy Harpaz & Minh Nguyet Nguyen & Armin Bahl & Florian Engert, 2021. "Precise visuomotor transformations underlying collective behavior in larval zebrafish," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26748-0
    DOI: 10.1038/s41467-021-26748-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26748-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-021-26748-0?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Lukas Anneser & Ivan C. Alcantara & Anja Gemmer & Kristina Mirkes & Soojin Ryu & Erin M. Schuman, 2020. "The neuropeptide Pth2 dynamically senses others via mechanosensation," Nature, Nature, vol. 588(7839), pages 653-657, December.
    2. Máté Nagy & Zsuzsa Ákos & Dora Biro & Tamás Vicsek, 2010. "Hierarchical group dynamics in pigeon flocks," Nature, Nature, vol. 464(7290), pages 890-893, April.
    3. Iain D. Couzin & Jens Krause & Nigel R. Franks & Simon A. Levin, 2005. "Effective leadership and decision-making in animal groups on the move," Nature, Nature, vol. 433(7025), pages 513-516, February.
    4. Misha B. Ahrens & Jennifer M. Li & Michael B. Orger & Drew N. Robson & Alexander F. Schier & Florian Engert & Ruben Portugues, 2012. "Brain-wide neuronal dynamics during motor adaptation in zebrafish," Nature, Nature, vol. 485(7399), pages 471-477, May.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Caroline L. Wee & Erin Song & Maxim Nikitchenko & Kristian J. Herrera & Sandy Wong & Florian Engert & Samuel Kunes, 2022. "Social isolation modulates appetite and avoidance behavior via a common oxytocinergic circuit in larval zebrafish," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Dániel L. Barabási & Gregor F. P. Schuhknecht & Florian Engert, 2024. "Functional neuronal circuits emerge in the absence of developmental activity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.

    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. Tamás Nepusz & Tamás Vicsek, 2013. "Hierarchical Self-Organization of Non-Cooperating Individuals," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-9, December.
    2. Li, Qing & Zhang, Lingwei & Jia, Yongnan & Lu, Tianzhao & Chen, Xiaojie, 2022. "Modeling, analysis, and optimization of three-dimensional restricted visual field metric-free swarms," Chaos, Solitons & Fractals, Elsevier, vol. 157(C).
    3. Panpan Yang & Maode Yan & Jiacheng Song & Ye Tang, 2019. "Self-Organized Fission-Fusion Control Algorithm for Flocking Systems Based on Intermittent Selective Interaction," Complexity, Hindawi, vol. 2019, pages 1-12, February.
    4. Yandong Xiao & Chuliang Song & Liang Tian & Yang-Yu Liu, 2019. "Accelerating The Emergence Of Order In Swarming Systems," Advances in Complex Systems (ACS), World Scientific Publishing Co. Pte. Ltd., vol. 23(01), pages 1-12, December.
    5. Li Jiang & Luca Giuggioli & Andrea Perna & Ramón Escobedo & Valentin Lecheval & Clément Sire & Zhangang Han & Guy Theraulaz, 2017. "Identifying influential neighbors in animal flocking," PLOS Computational Biology, Public Library of Science, vol. 13(11), pages 1-32, November.
    6. Simon Levin & Anastasios Xepapadeas, 2021. "On the Coevolution of Economic and Ecological Systems," Annual Review of Resource Economics, Annual Reviews, vol. 13(1), pages 355-377, October.
    7. Becco, Ch. & Vandewalle, N. & Delcourt, J. & Poncin, P., 2006. "Experimental evidences of a structural and dynamical transition in fish school," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 367(C), pages 487-493.
    8. Long-Hai Wang & Alexander Ulrich Ernst & Duo An & Ashim Kumar Datta & Boris Epel & Mrignayani Kotecha & Minglin Ma, 2021. "A bioinspired scaffold for rapid oxygenation of cell encapsulation systems," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    9. Richard P Mann, 2011. "Bayesian Inference for Identifying Interaction Rules in Moving Animal Groups," PLOS ONE, Public Library of Science, vol. 6(8), pages 1-10, August.
    10. Liang, Rizhou & Zhang, Jiqiang & Zheng, Guozhong & Chen, Li, 2021. "Social hierarchy promotes the cooperation prevalence," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 567(C).
    11. Ma, Jian & Song, Wei-guo & Zhang, Jun & Lo, Siu-ming & Liao, Guang-xuan, 2010. "k-Nearest-Neighbor interaction induced self-organized pedestrian counter flow," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 389(10), pages 2101-2117.
    12. Carlo Bianca & Marco Menale, 2019. "A Convergence Theorem for the Nonequilibrium States in the Discrete Thermostatted Kinetic Theory," Mathematics, MDPI, vol. 7(8), pages 1-13, July.
    13. Andrew Hoegh & Frank T. Manen & Mark Haroldson, 2021. "Agent-Based Models for Collective Animal Movement: Proximity-Induced State Switching," Journal of Agricultural, Biological and Environmental Statistics, Springer;The International Biometric Society;American Statistical Association, vol. 26(4), pages 560-579, December.
    14. Gergely Tibély & David Sousa-Rodrigues & Péter Pollner & Gergely Palla, 2016. "Comparing the Hierarchy of Keywords in On-Line News Portals," PLOS ONE, Public Library of Science, vol. 11(11), pages 1-15, November.
    15. Amos Korman & Efrat Greenwald & Ofer Feinerman, 2014. "Confidence Sharing: An Economic Strategy for Efficient Information Flows in Animal Groups," PLOS Computational Biology, Public Library of Science, vol. 10(10), pages 1-10, October.
    16. Mathew Titus & George Hagstrom & James R Watson, 2021. "Unsupervised manifold learning of collective behavior," PLOS Computational Biology, Public Library of Science, vol. 17(2), pages 1-20, February.
    17. Zhang, Jiu & Jin, Li-Fu & Zheng, Bo & Li, Yan & Jiang, Xiong-Fei, 2022. "Simplified calculations of time correlation functions in non-stationary complex financial systems," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 589(C).
    18. Sophie Lardy & Daniel Fortin & Olivier Pays, 2016. "Increased Exploration Capacity Promotes Group Fission in Gregarious Foraging Herbivores," PLOS ONE, Public Library of Science, vol. 11(12), pages 1-14, December.
    19. Fan, Kangqi & Pedrycz, Witold, 2016. "Opinion evolution influenced by informed agents," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 462(C), pages 431-441.
    20. De Rosis, Alessandro, 2014. "Hydrodynamic effects on a predator approaching a group of preys," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 414(C), pages 329-339.

    More about this item

    Statistics

    Access and download statistics

    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:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26748-0. 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: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.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.