Sniff-synchronized, gradient-guided olfactory search by freely-moving mice
- University of Oregon, United States
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.
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Sniff-synchronized, gradient-guided olfactory search by freely-moving miceDryad Digital Repository, doi:10.5061/dryad.r7sqv9sc0.
Article and author information
Author details
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
- Upinder Singh Bhalla, Tata Institute of Fundamental Research, India
Version history
- Received: May 3, 2020
- Accepted: April 22, 2021
- Accepted Manuscript published: May 4, 2021 (version 1)
- 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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Sniff-synchronized, gradient-guided olfactory search by freely-moving mice
eLife 10:e58523.
https://doi.org/10.7554/eLife.58523
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