Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
- Yale University, United States
Abstract
We and others have shown that during odor plume navigation, walking Drosophila melanogaster bias their motion upwind in response to both the frequency of their encounters with the odor (Demir et al., 2020), and the intermittency of the odor signal, which we define to be the fraction of time the signal is above a detection threshold (Alvarez-Salvado et al., 2018). Here we combine and simplify previous mathematical models that recapitulated these data to investigate the benefits of sensing both of these temporal features, and how these benefits depend on the spatiotemporal statistics of the odor plume. Through agent-based simulations, we find that navigators that only use frequency or intermittency perform well in some environments - achieving maximal performance when gains are near those inferred from experiment - but fail in others. Robust performance across diverse environments requires both temporal modalities. However, we also find a steep tradeoff when using both sensors simultaneously, suggesting a strong benefit to modulating how much each sensor is weighted, rather than using both in a fixed combination across plumes. Finally, we show that the circuitry of the Drosophila olfactory periphery naturally enables simultaneous intermittency and frequency sensing, enhancing robust navigation through a diversity of odor environments. Together, our results suggest that the first stage of olfactory processing selects and encodes temporal features of odor signals critical to real-world navigation tasks.
Data availability
All data analyzed in this study are available from the original publications. Codes are available at https://github.com/emonetlab/plume-temporal-navigation
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Data presented in "Walking Drosophila navigate complex plumes using stochastic decisions biased by the timing of odor encounters"https://creativecommons.org/publicdomain/zero/1.0/.
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Data from: Elementary sensory-motor transformations underlying olfactory navigation in walking fruit flieshttps://creativecommons.org/publicdomain/zero/1.0/.
Article and author information
Author details
Funding
National Institutes of Health (F32MH118700)
- Nirag Kadakia
National Institutes of Health (K99DC019397)
- Nirag Kadakia
National Institutes of Health (R01GM106189)
- Thierry Emonet
Yale University (Program in Physics,Engineering,and Biology)
- Viraaj Jayaram
Sloan-Swartz Foundation
- Nirag Kadakia
National Institutes of Health (R01GM138533)
- Thierry Emonet
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2022, Jayaram 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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Sensing complementary temporal features of odor signals enhances navigation of diverse turbulent plumes
eLife 11:e72415.
https://doi.org/10.7554/eLife.72415
Further reading
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- Neuroscience
When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.
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- Neuroscience
When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.
