Abstract

For many organisms, searching for relevant targets such as food or mates entails active, strategic sampling of the environment. Finding odorous targets may be the most ancient search problem that motile organisms evolved to solve. While chemosensory navigation has been well characterized in micro-organisms and invertebrates, spatial olfaction in vertebrates is poorly understood. We have established an olfactory search assay in which freely-moving mice navigate noisy concentration gradients of airborne odor. Mice solve this task using concentration gradient cues and do not require stereo olfaction for performance. During task performance, respiration and nose movement are synchronized with tens of milliseconds precision. This synchrony is present during trials and largely absent during inter-trial intervals, suggesting that sniff-synchronized nose movement is a strategic behavioral state rather than simply a constant accompaniment to fast breathing. To reveal the spatiotemporal structure of these active sensing movements, we used machine learning methods to parse motion trajectories into elementary movement motifs. Motifs fall into two clusters, which correspond to investigation and approach states. Investigation motifs lock precisely to sniffing, such that the individual motifs preferentially occur at specific phases of the sniff cycle. The allocentric structure of investigation and approach indicate an advantage to sampling both sides of the sharpest part of the odor gradient, consistent with a serial sniff strategy for gradient sensing. This work clarifies sensorimotor strategies for mouse olfactory search and guides ongoing work into the underlying neural mechanisms.

Data availability

Source code is available on github at https://github.com/Smear-Lab/Olfactory_Search, and source data files are uploaded to Dryad.

The following data sets were generated

Article and author information

Author details

  1. Teresa M Findley

    Department of Biology, Institute of Neuroscience, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. David G Wyrick

    Institute of Neuroscience; Department of Biology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8096-5766
  3. Jennifer L Cramer

    Institute of Neuroscience; Department of Biology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Morgan A Brown

    Institute of Neuroscience, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Blake Holcomb

    Institute of Neuroscience; Department of Psychology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Robin Attey

    Institute of Neuroscience; Department of Psychology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9652-8103
  7. Dorian Yeh

    Institute of Neuroscience; Department of Psychology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Eric Monasevitch

    Institute of Neuroscience; Department of Psychology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Nelly Nouboussi

    Institute of Neuroscience; Department of Psychology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Isabelle Cullen

    Institute of Neuroscience; Department of Psychology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Jeremea O Songco

    Institute of Neuroscience; Department of Biology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Jared F King

    Institute of Neuroscience; Department of Psychology, University of Oregon, Eugene, OR, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Yashar Ahmadian

    Institute of Neuroscience; Department of Mathematics, University of Oregon, Eugene, OR, United States
    For correspondence
    ya311@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5942-0697
  14. Matthew C Smear

    Institute of Neuroscience; Department of Psychology, University of Oregon, Eugene, OR, United States
    For correspondence
    smear@uoregon.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4689-388X

Funding

Whitehall Foundation (2015-12-201)

  • Matthew C Smear

National Institute on Deafness and Other Communication Disorders (R56DC015584)

  • Matthew C Smear

National Institute of Neurological Disorders and Stroke (R21NS104935)

  • Matthew C Smear

National Institute of Neurological Disorders and Stroke (R34NS116731)

  • Matthew C Smear

National Institute on Deafness and Other Communication Disorders (F31DC016799)

  • Teresa M Findley

National Institute of Neurological Disorders and Stroke (F32MH118724)

  • Morgan A Brown

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

Ethics

Animal experimentation: his study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (AUP-17-23) of the University of Oregon. All surgery was performed under sodium isofluorane anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Upinder Singh Bhalla, Tata Institute of Fundamental Research, India

Version history

  1. Received: May 3, 2020
  2. Accepted: April 22, 2021
  3. Accepted Manuscript published: May 4, 2021 (version 1)
  4. Version of Record published: June 1, 2021 (version 2)

Copyright

© 2021, Findley 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. Teresa M Findley
  2. David G Wyrick
  3. Jennifer L Cramer
  4. Morgan A Brown
  5. Blake Holcomb
  6. Robin Attey
  7. Dorian Yeh
  8. Eric Monasevitch
  9. Nelly Nouboussi
  10. Isabelle Cullen
  11. Jeremea O Songco
  12. Jared F King
  13. Yashar Ahmadian
  14. Matthew C Smear
(2021)
Sniff-synchronized, gradient-guided olfactory search by freely-moving mice
eLife 10:e58523.
https://doi.org/10.7554/eLife.58523

Share this article

https://doi.org/10.7554/eLife.58523

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