Mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulb

In olfactory systems, convergence of sensory neurons onto glomeruli generates a map of odorant receptor identity. How glomerular maps relate to sensory space remains unclear. We sought to better characterize this relationship in the mouse olfactory system by defining glomeruli in terms of the odoran...

Full description

Bibliographic Details
Main Authors: Shawn D Burton, Audrey Brown, Thomas P Eiting, Isaac A Youngstrom, Thomas C Rust, Michael Schmuker, Matt Wachowiak
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/80470
_version_ 1828108641051344896
author Shawn D Burton
Audrey Brown
Thomas P Eiting
Isaac A Youngstrom
Thomas C Rust
Michael Schmuker
Matt Wachowiak
author_facet Shawn D Burton
Audrey Brown
Thomas P Eiting
Isaac A Youngstrom
Thomas C Rust
Michael Schmuker
Matt Wachowiak
author_sort Shawn D Burton
collection DOAJ
description In olfactory systems, convergence of sensory neurons onto glomeruli generates a map of odorant receptor identity. How glomerular maps relate to sensory space remains unclear. We sought to better characterize this relationship in the mouse olfactory system by defining glomeruli in terms of the odorants to which they are most sensitive. Using high-throughput odorant delivery and ultrasensitive imaging of sensory inputs, we imaged responses to 185 odorants presented at concentrations determined to activate only one or a few glomeruli across the dorsal olfactory bulb. The resulting datasets defined the tuning properties of glomeruli - and, by inference, their cognate odorant receptors - in a low-concentration regime, and yielded consensus maps of glomerular sensitivity across a wide range of chemical space. Glomeruli were extremely narrowly tuned, with ~25% responding to only one odorant, and extremely sensitive, responding to their effective odorants at sub-picomolar to nanomolar concentrations. Such narrow tuning in this concentration regime allowed for reliable functional identification of many glomeruli based on a single diagnostic odorant. At the same time, the response spectra of glomeruli responding to multiple odorants was best predicted by straightforward odorant structural features, and glomeruli sensitive to distinct odorants with common structural features were spatially clustered. These results define an underlying structure to the primary representation of sensory space by the mouse olfactory system.
first_indexed 2024-04-11T10:49:58Z
format Article
id doaj.art-87f5a0c262b04c39bfdbff85618bdd55
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-11T10:49:58Z
publishDate 2022-07-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-87f5a0c262b04c39bfdbff85618bdd552022-12-22T04:28:57ZengeLife Sciences Publications LtdeLife2050-084X2022-07-011110.7554/eLife.80470Mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulbShawn D Burton0https://orcid.org/0000-0002-8907-6487Audrey Brown1Thomas P Eiting2Isaac A Youngstrom3Thomas C Rust4Michael Schmuker5https://orcid.org/0000-0001-6753-4929Matt Wachowiak6https://orcid.org/0000-0003-4508-9793Department of Neurobiology, University of Utah School of Medicine, Salt Lake City, United StatesDepartment of Neurobiology, University of Utah School of Medicine, Salt Lake City, United StatesDepartment of Neurobiology, University of Utah School of Medicine, Salt Lake City, United StatesDepartment of Neurobiology, University of Utah School of Medicine, Salt Lake City, United StatesDepartment of Neurobiology, University of Utah School of Medicine, Salt Lake City, United StatesBiocomputation Group, Centre of Data Innovation Research, Department of Computer Science, University of Hertfordshire, Hertfordshire, United KingdomDepartment of Neurobiology, University of Utah School of Medicine, Salt Lake City, United StatesIn olfactory systems, convergence of sensory neurons onto glomeruli generates a map of odorant receptor identity. How glomerular maps relate to sensory space remains unclear. We sought to better characterize this relationship in the mouse olfactory system by defining glomeruli in terms of the odorants to which they are most sensitive. Using high-throughput odorant delivery and ultrasensitive imaging of sensory inputs, we imaged responses to 185 odorants presented at concentrations determined to activate only one or a few glomeruli across the dorsal olfactory bulb. The resulting datasets defined the tuning properties of glomeruli - and, by inference, their cognate odorant receptors - in a low-concentration regime, and yielded consensus maps of glomerular sensitivity across a wide range of chemical space. Glomeruli were extremely narrowly tuned, with ~25% responding to only one odorant, and extremely sensitive, responding to their effective odorants at sub-picomolar to nanomolar concentrations. Such narrow tuning in this concentration regime allowed for reliable functional identification of many glomeruli based on a single diagnostic odorant. At the same time, the response spectra of glomeruli responding to multiple odorants was best predicted by straightforward odorant structural features, and glomeruli sensitive to distinct odorants with common structural features were spatially clustered. These results define an underlying structure to the primary representation of sensory space by the mouse olfactory system.https://elifesciences.org/articles/80470imagingcodingodorolfactometrychemoinformatics
spellingShingle Shawn D Burton
Audrey Brown
Thomas P Eiting
Isaac A Youngstrom
Thomas C Rust
Michael Schmuker
Matt Wachowiak
Mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulb
eLife
imaging
coding
odor
olfactometry
chemoinformatics
title Mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulb
title_full Mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulb
title_fullStr Mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulb
title_full_unstemmed Mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulb
title_short Mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulb
title_sort mapping odorant sensitivities reveals a sparse but structured representation of olfactory chemical space by sensory input to the mouse olfactory bulb
topic imaging
coding
odor
olfactometry
chemoinformatics
url https://elifesciences.org/articles/80470
work_keys_str_mv AT shawndburton mappingodorantsensitivitiesrevealsasparsebutstructuredrepresentationofolfactorychemicalspacebysensoryinputtothemouseolfactorybulb
AT audreybrown mappingodorantsensitivitiesrevealsasparsebutstructuredrepresentationofolfactorychemicalspacebysensoryinputtothemouseolfactorybulb
AT thomaspeiting mappingodorantsensitivitiesrevealsasparsebutstructuredrepresentationofolfactorychemicalspacebysensoryinputtothemouseolfactorybulb
AT isaacayoungstrom mappingodorantsensitivitiesrevealsasparsebutstructuredrepresentationofolfactorychemicalspacebysensoryinputtothemouseolfactorybulb
AT thomascrust mappingodorantsensitivitiesrevealsasparsebutstructuredrepresentationofolfactorychemicalspacebysensoryinputtothemouseolfactorybulb
AT michaelschmuker mappingodorantsensitivitiesrevealsasparsebutstructuredrepresentationofolfactorychemicalspacebysensoryinputtothemouseolfactorybulb
AT mattwachowiak mappingodorantsensitivitiesrevealsasparsebutstructuredrepresentationofolfactorychemicalspacebysensoryinputtothemouseolfactorybulb