IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1005429.html
   My bibliography  Save this article

Feedback between motion and sensation provides nonlinear boost in run-and-tumble navigation

Author

Listed:
  • Junjiajia Long
  • Steven W Zucker
  • Thierry Emonet

Abstract

Many organisms navigate gradients by alternating straight motions (runs) with random reorientations (tumbles), transiently suppressing tumbles whenever attractant signal increases. This induces a functional coupling between movement and sensation, since tumbling probability is controlled by the internal state of the organism which, in turn, depends on previous signal levels. Although a negative feedback tends to maintain this internal state close to adapted levels, positive feedback can arise when motion up the gradient reduces tumbling probability, further boosting drift up the gradient. Importantly, such positive feedback can drive large fluctuations in the internal state, complicating analytical approaches. Previous studies focused on what happens when the negative feedback dominates the dynamics. By contrast, we show here that there is a large portion of physiologically-relevant parameter space where the positive feedback can dominate, even when gradients are relatively shallow. We demonstrate how large transients emerge because of non-normal dynamics (non-orthogonal eigenvectors near a stable fixed point) inherent in the positive feedback, and further identify a fundamental nonlinearity that strongly amplifies their effect. Most importantly, this amplification is asymmetric, elongating runs in favorable directions and abbreviating others. The result is a “ratchet-like” gradient climbing behavior with drift speeds that can approach half the maximum run speed of the organism. Our results thus show that the classical drawback of run-and-tumble navigation—wasteful runs in the wrong direction—can be mitigated by exploiting the non-normal dynamics implicit in the run-and-tumble strategy.Author summary: Countless bacteria, larvae and even larger organisms (and robots) navigate gradients by alternating periods of straight motion (runs) with random reorientation events (tumbles). Control of the tumble probability is based on previously-encountered signals. A drawback of this run-and-tumble strategy is that occasional runs in the wrong direction are wasteful. Here we show that there is an operating regime within the organism’s internal parameter space where run-and-tumble navigation can be extremely efficient. We characterize how the positive feedback between behavior and sensed signal results in a type of non-equilibrium dynamics, with the organism rapidly tumbling after moving in the wrong direction and extending motion in the right ones. For a distant source, then, the organism can find it fast.

Suggested Citation

  • Junjiajia Long & Steven W Zucker & Thierry Emonet, 2017. "Feedback between motion and sensation provides nonlinear boost in run-and-tumble navigation," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-25, March.
  • Handle: RePEc:plo:pcbi00:1005429
    DOI: 10.1371/journal.pcbi.1005429
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1005429
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1005429&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1005429?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. Diana Clausznitzer & Olga Oleksiuk & Linda Løvdok & Victor Sourjik & Robert G Endres, 2010. "Chemotactic Response and Adaptation Dynamics in Escherichia coli," PLOS Computational Biology, Public Library of Science, vol. 6(5), pages 1-11, May.
    2. Victor Sourjik & Howard C. Berg, 2004. "Functional interactions between receptors in bacterial chemotaxis," Nature, Nature, vol. 428(6981), pages 437-441, March.
    3. Alex Gomez-Marin & Greg J. Stephens & Matthieu Louis, 2011. "Active sampling and decision making in Drosophila chemotaxis," Nature Communications, Nature, vol. 2(1), pages 1-10, September.
    4. Diana Clausznitzer & Gabriele Micali & Silke Neumann & Victor Sourjik & Robert G Endres, 2014. "Predicting Chemical Environments of Bacteria from Receptor Signaling," PLOS Computational Biology, Public Library of Science, vol. 10(10), pages 1-14, October.
    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. Nguyen, Minh D.N. & Pham, Phuc H. & Ngo, Khang V. & Do, Van H. & Li, Shengkai & Phan, Trung V., 2024. "Remark on the entropy production of adaptive run-and-tumble chemotaxis," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 634(C).

    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. Diana Clausznitzer & Gabriele Micali & Silke Neumann & Victor Sourjik & Robert G Endres, 2014. "Predicting Chemical Environments of Bacteria from Receptor Signaling," PLOS Computational Biology, Public Library of Science, vol. 10(10), pages 1-14, October.
    2. Stephan Eismann & Robert G Endres, 2015. "Protein Connectivity in Chemotaxis Receptor Complexes," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-21, December.
    3. Andrea Censi & Andrew D Straw & Rosalyn W Sayaman & Richard M Murray & Michael H Dickinson, 2013. "Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila," PLOS Computational Biology, Public Library of Science, vol. 9(2), pages 1-14, February.
    4. Liangyu Tao & Samuel P. Wechsler & Vikas Bhandawat, 2023. "Sensorimotor transformation underlying odor-modulated locomotion in walking Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    5. Diana Clausznitzer & Olga Oleksiuk & Linda Løvdok & Victor Sourjik & Robert G Endres, 2010. "Chemotactic Response and Adaptation Dynamics in Escherichia coli," PLOS Computational Biology, Public Library of Science, vol. 6(5), pages 1-11, May.
    6. Robert G Endres & Joseph J Falke & Ned S Wingreen, 2007. "Chemotaxis Receptor Complexes: From Signaling to Assembly," PLOS Computational Biology, Public Library of Science, vol. 3(7), pages 1-9, July.
    7. Burton W Andrews & Tau-Mu Yi & Pablo A Iglesias, 2006. "Optimal Noise Filtering in the Chemotactic Response of Escherichia coli," PLOS Computational Biology, Public Library of Science, vol. 2(11), pages 1-12, November.
    8. Liangyu Tao & Siddhi Ozarkar & Vikas Bhandawat, 2020. "Mechanisms underlying attraction to odors in walking Drosophila," PLOS Computational Biology, Public Library of Science, vol. 16(3), pages 1-26, March.
    9. Samuel K. H. Sy & Danny C. W. Chan & Roy C. H. Chan & Jing Lyu & Zhongqi Li & Kenneth K. Y. Wong & Chung Hang Jonathan Choi & Vincent C. T. Mok & Hei-Ming Lai & Owen Randlett & Yu Hu & Ho Ko, 2023. "An optofluidic platform for interrogating chemosensory behavior and brainwide neural representation in larval zebrafish," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

    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:plo:pcbi00:1005429. 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: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .

    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.