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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
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    References listed on IDEAS

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    1. Máté Nagy & Zsuzsa Ákos & Dora Biro & Tamás Vicsek, 2010. "Hierarchical group dynamics in pigeon flocks," Nature, Nature, vol. 464(7290), pages 890-893, April.
    2. 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.
    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. 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.
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    Cited by:

    1. Zhicheng Zheng & Yuan Tao & Yalun Xiang & Xiaokang Lei & Xingguang Peng, 2024. "Body orientation change of neighbors leads to scale-free correlation in collective motion," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. 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.
    3. 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.

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