Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons
Identifieur interne : 000E04 ( Main/Exploration ); précédent : 000E03; suivant : 000E05Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons
Auteurs : Jean-Pierre Rospars [France] ; Alexandre Grémiaux [France] ; David Jarriault [France] ; Antoine Chaffiol [France] ; Christelle Monsempes [France] ; Nina Deisig [France] ; Sylvia Anton [France] ; Philippe Lucas [France] ; Dominique Martinez [France]Source :
- PLoS Computational Biology [ 1553-734X ] ; 2014.
Descripteurs français
- KwdFr :
- MESH :
- métabolisme : Neurorécepteurs olfactifs, Phéromones.
- physiologie : Neurones, Neurorécepteurs olfactifs, Papillons de nuit, Voies olfactives.
- Animaux, Biologie informatique, Modèles neurologiques, Mâle.
English descriptors
- KwdEn :
- MESH :
- chemical , metabolism : Pheromones.
- metabolism : Olfactory Receptor Neurons.
- physiology : Moths, Neurons, Olfactory Pathways, Olfactory Receptor Neurons.
- Animals, Computational Biology, Male, Models, Neurological.
Abstract
In the olfactory system of male moths, a specialized subset of neurons detects and processes the main component of the sex pheromone emitted by females. It is composed of several thousand first-order olfactory receptor neurons (ORNs), all expressing the same pheromone receptor, that contact synaptically a few tens of second-order projection neurons (PNs) within a single restricted brain area. The functional simplicity of this system makes it a favorable model for studying the factors that contribute to its exquisite sensitivity and speed. Sensory information—primarily the identity and intensity of the stimulus—is encoded as the firing rate of the action potentials, and possibly as the latency of the neuron response. We found that over all their dynamic range, PNs respond with a shorter latency and a higher firing rate than most ORNs. Modelling showed that the increased sensitivity of PNs can be explained by the ORN-to-PN convergent architecture alone, whereas their faster response also requires cell-to-cell heterogeneity of the ORN population. So, far from being detrimental to signal detection, the ORN heterogeneity is exploited by PNs, and results in two different schemes of population coding based either on the response of a few extreme neurons (latency) or on the average response of many (firing rate). Moreover, ORN-to-PN transformations are linear for latency and nonlinear for firing rate, suggesting that latency could be involved in concentration-invariant coding of the pheromone blend and that sensitivity at low concentrations is achieved at the expense of precise encoding at high concentrations.
Url:
DOI: 10.1371/journal.pcbi.1003975
PubMed: 25474026
PubMed Central: 4256018
Affiliations:
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Le document en format XML
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Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation></author><author><name sortKey="Gremiaux, Alexandre" sort="Gremiaux, Alexandre" uniqKey="Gremiaux A" first="Alexandre" last="Grémiaux">Alexandre Grémiaux</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation></author><author><name sortKey="Jarriault, David" sort="Jarriault, David" uniqKey="Jarriault D" first="David" last="Jarriault">David Jarriault</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation></author><author><name sortKey="Chaffiol, Antoine" sort="Chaffiol, Antoine" uniqKey="Chaffiol A" first="Antoine" last="Chaffiol">Antoine Chaffiol</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation></author><author><name sortKey="Monsempes, Christelle" sort="Monsempes, Christelle" uniqKey="Monsempes C" first="Christelle" last="Monsempes">Christelle Monsempes</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation></author><author><name sortKey="Deisig, Nina" sort="Deisig, Nina" uniqKey="Deisig N" first="Nina" last="Deisig">Nina Deisig</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation></author><author><name sortKey="Anton, Sylvia" sort="Anton, Sylvia" uniqKey="Anton S" first="Sylvia" last="Anton">Sylvia Anton</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation></author><author><name sortKey="Lucas, Philippe" sort="Lucas, Philippe" uniqKey="Lucas P" first="Philippe" last="Lucas">Philippe Lucas</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation></author><author><name sortKey="Martinez, Dominique" sort="Martinez, Dominique" uniqKey="Martinez D" first="Dominique" last="Martinez">Dominique Martinez</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut National de la Recherche Agronomique (INRA), Unité Mixte de Recherche 1392 Institut d'Ecologie et des Sciences de l'Environnement de Paris, Versailles</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Versailles</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>Laboratoire Lorrain de Recherche en Informatique et ses Applications (LORIA), Unité Mixte de Recherche 7503, Centre National de la Recherche Scientifique (CNRS), Vandœuvre-lès-Nancy, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Laboratoire Lorrain de Recherche en Informatique et ses Applications (LORIA), Unité Mixte de Recherche 7503, Centre National de la Recherche Scientifique (CNRS), Vandœuvre-lès-Nancy</wicri:regionArea><placeName><region type="region" nuts="2">Grand Est</region><region type="old region" nuts="2">Lorraine (région)</region><settlement type="city">Vandœuvre-lès-Nancy</settlement><settlement type="city" wicri:auto="agglo">Nancy</settlement></placeName></affiliation></author></analytic><series><title level="j">PLoS Computational Biology</title><idno type="ISSN">1553-734X</idno><idno type="eISSN">1553-7358</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Computational Biology</term><term>Male</term><term>Models, Neurological</term><term>Moths (physiology)</term><term>Neurons (physiology)</term><term>Olfactory Pathways (physiology)</term><term>Olfactory Receptor Neurons (metabolism)</term><term>Olfactory Receptor Neurons (physiology)</term><term>Pheromones (metabolism)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Animaux</term><term>Biologie informatique</term><term>Modèles neurologiques</term><term>Mâle</term><term>Neurones (physiologie)</term><term>Neurorécepteurs olfactifs (métabolisme)</term><term>Neurorécepteurs olfactifs (physiologie)</term><term>Papillons de nuit (physiologie)</term><term>Phéromones (métabolisme)</term><term>Voies olfactives (physiologie)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Pheromones</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Olfactory Receptor Neurons</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Neurorécepteurs olfactifs</term><term>Phéromones</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Neurones</term><term>Neurorécepteurs olfactifs</term><term>Papillons de nuit</term><term>Voies olfactives</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Moths</term><term>Neurons</term><term>Olfactory Pathways</term><term>Olfactory Receptor Neurons</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Computational Biology</term><term>Male</term><term>Models, Neurological</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Animaux</term><term>Biologie informatique</term><term>Modèles neurologiques</term><term>Mâle</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>In the olfactory system of male moths, a specialized subset of neurons detects and processes the main component of the sex pheromone emitted by females. It is composed of several thousand first-order olfactory receptor neurons (ORNs), all expressing the same pheromone receptor, that contact synaptically a few tens of second-order projection neurons (PNs) within a single restricted brain area. The functional simplicity of this system makes it a favorable model for studying the factors that contribute to its exquisite sensitivity and speed. Sensory information—primarily the identity and intensity of the stimulus—is encoded as the firing rate of the action potentials, and possibly as the latency of the neuron response. We found that over all their dynamic range, PNs respond with a shorter latency and a higher firing rate than most ORNs. Modelling showed that the increased sensitivity of PNs can be explained by the ORN-to-PN convergent architecture alone, whereas their faster response also requires cell-to-cell heterogeneity of the ORN population. So, far from being detrimental to signal detection, the ORN heterogeneity is exploited by PNs, and results in two different schemes of population coding based either on the response of a few extreme neurons (latency) or on the average response of many (firing rate). Moreover, ORN-to-PN transformations are linear for latency and nonlinear for firing rate, suggesting that latency could be involved in concentration-invariant coding of the pheromone blend and that sensitivity at low concentrations is achieved at the expense of precise encoding at high concentrations.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Kay, Lm" uniqKey="Kay L">LM Kay</name></author><author><name sortKey="Stopfer, M" uniqKey="Stopfer M">M Stopfer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Martin, Jp" uniqKey="Martin J">JP Martin</name></author><author><name sortKey="Beyerlein, A" uniqKey="Beyerlein A">A Beyerlein</name></author><author><name sortKey="Dacks, Am" uniqKey="Dacks A">AM Dacks</name></author><author><name sortKey="Reisenman, Ce" uniqKey="Reisenman C">CE Reisenman</name></author><author><name sortKey="Riffell, Ja" uniqKey="Riffell J">JA 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(région)</li><li>Île-de-France</li></region><settlement><li>Nancy</li><li>Vandœuvre-lès-Nancy</li><li>Versailles</li></settlement></list><tree><country name="France"><region name="Île-de-France"><name sortKey="Rospars, Jean Pierre" sort="Rospars, Jean Pierre" uniqKey="Rospars J" first="Jean-Pierre" last="Rospars">Jean-Pierre Rospars</name></region><name sortKey="Anton, Sylvia" sort="Anton, Sylvia" uniqKey="Anton S" first="Sylvia" last="Anton">Sylvia Anton</name><name sortKey="Chaffiol, Antoine" sort="Chaffiol, Antoine" uniqKey="Chaffiol A" first="Antoine" last="Chaffiol">Antoine Chaffiol</name><name sortKey="Deisig, Nina" sort="Deisig, Nina" uniqKey="Deisig N" first="Nina" last="Deisig">Nina Deisig</name><name sortKey="Gremiaux, Alexandre" sort="Gremiaux, Alexandre" uniqKey="Gremiaux A" first="Alexandre" last="Grémiaux">Alexandre Grémiaux</name><name sortKey="Jarriault, David" sort="Jarriault, David" uniqKey="Jarriault D" first="David" last="Jarriault">David Jarriault</name><name sortKey="Lucas, Philippe" sort="Lucas, Philippe" uniqKey="Lucas P" first="Philippe" last="Lucas">Philippe Lucas</name><name sortKey="Martinez, Dominique" sort="Martinez, Dominique" uniqKey="Martinez D" first="Dominique" last="Martinez">Dominique Martinez</name><name sortKey="Martinez, Dominique" sort="Martinez, Dominique" uniqKey="Martinez D" first="Dominique" last="Martinez">Dominique Martinez</name><name sortKey="Monsempes, Christelle" sort="Monsempes, Christelle" uniqKey="Monsempes C" first="Christelle" last="Monsempes">Christelle Monsempes</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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|texte= Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons
}}
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HfdIndexSelect -h $EXPLOR_AREA/Data/Main/Exploration/RBID.i -Sk "pubmed:25474026" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Main/Exploration/biblio.hfd \
| NlmPubMed2Wicri -a InforLorV4
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