Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality

Odorants binding to olfactory receptor neurons (ORNs) trigger bursts of action potentials, providing the brain with its only experience of the olfactory environment. Our recordings made in vivo from locust ORNs showed that odor-elicited firing patterns comprise four distinct response motifs, each de...

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Main Authors: Brian Kim, Seth Haney, Ana P Milan, Shruti Joshi, Zane Aldworth, Nikolai Rulkov, Alexander T Kim, Maxim Bazhenov, Mark A Stopfer
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/79152
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author Brian Kim
Seth Haney
Ana P Milan
Shruti Joshi
Zane Aldworth
Nikolai Rulkov
Alexander T Kim
Maxim Bazhenov
Mark A Stopfer
author_facet Brian Kim
Seth Haney
Ana P Milan
Shruti Joshi
Zane Aldworth
Nikolai Rulkov
Alexander T Kim
Maxim Bazhenov
Mark A Stopfer
author_sort Brian Kim
collection DOAJ
description Odorants binding to olfactory receptor neurons (ORNs) trigger bursts of action potentials, providing the brain with its only experience of the olfactory environment. Our recordings made in vivo from locust ORNs showed that odor-elicited firing patterns comprise four distinct response motifs, each defined by a reliable temporal profile. Different odorants could elicit different response motifs from a given ORN, a property we term motif switching. Further, each motif undergoes its own form of sensory adaptation when activated by repeated plume-like odor pulses. A computational model constrained by our recordings revealed that organizing responses into multiple motifs provides substantial benefits for classifying odors and processing complex odor plumes: each motif contributes uniquely to encode the plume’s composition and structure. Multiple motifs and motif switching further improve odor classification by expanding coding dimensionality. Our model demonstrated that these response features could provide benefits for olfactory navigation, including determining the distance to an odor source.
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spelling doaj.art-35273e50c95843e7a60d57bb991cd1c62023-02-13T16:47:48ZengeLife Sciences Publications LtdeLife2050-084X2023-01-011210.7554/eLife.79152Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionalityBrian Kim0Seth Haney1Ana P Milan2Shruti Joshi3Zane Aldworth4https://orcid.org/0000-0002-0647-8465Nikolai Rulkov5Alexander T Kim6Maxim Bazhenov7https://orcid.org/0000-0002-1936-0570Mark A Stopfer8https://orcid.org/0000-0001-9200-1884Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH), Bethesda, United States; Brown University - National Institutes of Health Graduate Partnership Program, Providence, United StatesDepartment of Medicine, University of California, San Diego, San Diego, United StatesDepartment of Clinical Neurophysiology and MEG Center, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Medicine, University of California, San Diego, San Diego, United StatesEunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH), Bethesda, United StatesBiocircuits Institute, University of California, San Diego, La Jolla, United StatesEunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH), Bethesda, United StatesDepartment of Medicine, University of California, San Diego, San Diego, United StatesEunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH), Bethesda, United StatesOdorants binding to olfactory receptor neurons (ORNs) trigger bursts of action potentials, providing the brain with its only experience of the olfactory environment. Our recordings made in vivo from locust ORNs showed that odor-elicited firing patterns comprise four distinct response motifs, each defined by a reliable temporal profile. Different odorants could elicit different response motifs from a given ORN, a property we term motif switching. Further, each motif undergoes its own form of sensory adaptation when activated by repeated plume-like odor pulses. A computational model constrained by our recordings revealed that organizing responses into multiple motifs provides substantial benefits for classifying odors and processing complex odor plumes: each motif contributes uniquely to encode the plume’s composition and structure. Multiple motifs and motif switching further improve odor classification by expanding coding dimensionality. Our model demonstrated that these response features could provide benefits for olfactory navigation, including determining the distance to an odor source.https://elifesciences.org/articles/79152odorsensory encodingcombinatorialcomputational modelingSchistocerca americanainformation
spellingShingle Brian Kim
Seth Haney
Ana P Milan
Shruti Joshi
Zane Aldworth
Nikolai Rulkov
Alexander T Kim
Maxim Bazhenov
Mark A Stopfer
Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality
eLife
odor
sensory encoding
combinatorial
computational modeling
Schistocerca americana
information
title Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality
title_full Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality
title_fullStr Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality
title_full_unstemmed Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality
title_short Olfactory receptor neurons generate multiple response motifs, increasing coding space dimensionality
title_sort olfactory receptor neurons generate multiple response motifs increasing coding space dimensionality
topic odor
sensory encoding
combinatorial
computational modeling
Schistocerca americana
information
url https://elifesciences.org/articles/79152
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