Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies

Odor attraction in walking Drosophila melanogaster is commonly used to relate neural function to behavior, but the algorithms underlying attraction are unclear. Here, we develop a high-throughput assay to measure olfactory behavior in response to well-controlled sensory stimuli. We show that odor ev...

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Main Authors: Efrén Álvarez-Salvado, Angela M Licata, Erin G Connor, Margaret K McHugh, Benjamin MN King, Nicholas Stavropoulos, Jonathan D Victor, John P Crimaldi, Katherine I Nagel
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/37815
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spelling doaj-6a258862568f455284a085ca740b4dd62021-05-05T16:06:36ZengeLife Sciences Publications LtdeLife2050-084X2018-08-01710.7554/eLife.37815Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-fliesEfrén Álvarez-Salvado0Angela M Licata1Erin G Connor2Margaret K McHugh3Benjamin MN King4Nicholas Stavropoulos5https://orcid.org/0000-0001-5915-2760Jonathan D Victor6https://orcid.org/0000-0002-9293-0111John P Crimaldi7Katherine I Nagel8https://orcid.org/0000-0002-6701-3901Neuroscience Institute, New York University Langone Medical Center, New York, United StatesNeuroscience Institute, New York University Langone Medical Center, New York, United StatesDepartment of Civil, Environmental and Architectural Engineering, University of Colorado Boulder, Boulder, United StatesDepartment of Civil, Environmental and Architectural Engineering, University of Colorado Boulder, Boulder, United StatesNeuroscience Institute, New York University Langone Medical Center, New York, United StatesNeuroscience Institute, New York University Langone Medical Center, New York, United StatesInstitute for Computational Biomedicine, Weill Cornell Medical College, New York, United States; Feil Family Brain and Mind Research Institute, Weill Cornell Medical College, New York, United StatesDepartment of Civil, Environmental and Architectural Engineering, University of Colorado Boulder, Boulder, United StatesNeuroscience Institute, New York University Langone Medical Center, New York, United StatesOdor attraction in walking Drosophila melanogaster is commonly used to relate neural function to behavior, but the algorithms underlying attraction are unclear. Here, we develop a high-throughput assay to measure olfactory behavior in response to well-controlled sensory stimuli. We show that odor evokes two behaviors: an upwind run during odor (ON response), and a local search at odor offset (OFF response). Wind orientation requires antennal mechanoreceptors, but search is driven solely by odor. Using dynamic odor stimuli, we measure the dependence of these two behaviors on odor intensity and history. Based on these data, we develop a navigation model that recapitulates the behavior of flies in our apparatus, and generates realistic trajectories when run in a turbulent boundary layer plume. The ability to parse olfactory navigation into quantifiable elementary sensori-motor transformations provides a foundation for dissecting neural circuits that govern olfactory behavior.https://elifesciences.org/articles/37815olfactionbehaviornavigationcomputation
collection DOAJ
language English
format Article
sources DOAJ
author Efrén Álvarez-Salvado
Angela M Licata
Erin G Connor
Margaret K McHugh
Benjamin MN King
Nicholas Stavropoulos
Jonathan D Victor
John P Crimaldi
Katherine I Nagel
spellingShingle Efrén Álvarez-Salvado
Angela M Licata
Erin G Connor
Margaret K McHugh
Benjamin MN King
Nicholas Stavropoulos
Jonathan D Victor
John P Crimaldi
Katherine I Nagel
Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies
eLife
olfaction
behavior
navigation
computation
author_facet Efrén Álvarez-Salvado
Angela M Licata
Erin G Connor
Margaret K McHugh
Benjamin MN King
Nicholas Stavropoulos
Jonathan D Victor
John P Crimaldi
Katherine I Nagel
author_sort Efrén Álvarez-Salvado
title Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies
title_short Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies
title_full Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies
title_fullStr Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies
title_full_unstemmed Elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies
title_sort elementary sensory-motor transformations underlying olfactory navigation in walking fruit-flies
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2018-08-01
description Odor attraction in walking Drosophila melanogaster is commonly used to relate neural function to behavior, but the algorithms underlying attraction are unclear. Here, we develop a high-throughput assay to measure olfactory behavior in response to well-controlled sensory stimuli. We show that odor evokes two behaviors: an upwind run during odor (ON response), and a local search at odor offset (OFF response). Wind orientation requires antennal mechanoreceptors, but search is driven solely by odor. Using dynamic odor stimuli, we measure the dependence of these two behaviors on odor intensity and history. Based on these data, we develop a navigation model that recapitulates the behavior of flies in our apparatus, and generates realistic trajectories when run in a turbulent boundary layer plume. The ability to parse olfactory navigation into quantifiable elementary sensori-motor transformations provides a foundation for dissecting neural circuits that govern olfactory behavior.
topic olfaction
behavior
navigation
computation
url https://elifesciences.org/articles/37815
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