Alternation emerges as a multi-modal strategy for turbulent odor navigation

  1. Nicola Rigolli
  2. Gautam Reddy
  3. Agnese Seminara  Is a corresponding author
  4. Massimo Vergassola  Is a corresponding author
  1. University of Genova, Italy
  2. Harvard University, United States
  3. University of Genoa, Italy
  4. CNRS, PSL Research University, France

Abstract

Foraging mammals exhibit a familiar yet poorly characterized phenomenon, 'alternation', a pause to sniff in the air preceded by the animal rearing on its hind legs or raising its head. Rodents spontaneously alternate in the presence of airflow, suggesting that alternation serves an important role during plume-tracking. To test this hypothesis, we combine fully-resolved simulations of turbulent odor transport and Bellman optimization methods for decision-making under partial observability. We show that an agent trained to minimize search time in a realistic odor plume exhibits extensive alternation together with the characteristic cast-and-surge behavior observed in insects. Alternation is linked with casting and occurs more frequently far downwind of the source, where the likelihood of detecting airborne cues is higher relative to ground cues. Casting and alternation emerge as complementary tools for effective exploration with sparse cues. A model based on marginal value theory captures the interplay between casting, surging and alternation.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting file. The dataset with the simulation results has been made public at https://zenodo.org/record/6538177#.Yqrl_5BByJE

Article and author information

Author details

  1. Nicola Rigolli

    Department of Physics, University of Genova, Genova, Italy
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0734-2105
  2. Gautam Reddy

    NSF-Simons Center for Mathematical and Statistical Analysis of Biology, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1276-9613
  3. Agnese Seminara

    Department of Civil, Chemical and Environmental Engineering, University of Genoa, Genoa, Italy
    For correspondence
    agnese.seminara@unige.it
    Competing interests
    Agnese Seminara, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5633-8180
  4. Massimo Vergassola

    CNRS, PSL Research University, Paris, France
    For correspondence
    massimo.vergassola@phys.ens.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7212-8244

Funding

National Science Foundation (1764269)

  • Gautam Reddy

European Research Council (101002724)

  • Agnese Seminara

Air Force Office of Scientific Research (FA8655-20-1-7028)

  • Agnese Seminara

NIH Office of the Director (R01DC018789)

  • Agnese Seminara

National Science Foundation (PHY-1748958)

  • Massimo Vergassola

Gordon and Betty Moore Foundation (2919.02)

  • Gautam Reddy

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Tatyana O Sharpee, Salk Institute for Biological Studies, United States

Version history

  1. Preprint posted: December 16, 2021 (view preprint)
  2. Received: January 11, 2022
  3. Accepted: August 7, 2022
  4. Accepted Manuscript published: August 23, 2022 (version 1)
  5. Version of Record published: September 20, 2022 (version 2)
  6. Version of Record updated: September 26, 2022 (version 3)

Copyright

© 2022, Rigolli et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Nicola Rigolli
  2. Gautam Reddy
  3. Agnese Seminara
  4. Massimo Vergassola
(2022)
Alternation emerges as a multi-modal strategy for turbulent odor navigation
eLife 11:e76989.
https://doi.org/10.7554/eLife.76989

Share this article

https://doi.org/10.7554/eLife.76989

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