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A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth

Recognition of intra-specific olfactory signals within a complex environment of plant-related volatiles is crucial for reproduction in male moths. Sex pheromone information is detected by specific olfactory receptor neurons (Phe-ORNs), highly abundant on the male antenna. The information is then tra...

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Autores principales: Dupuy, Fabienne, Rouyar, Angéla, Deisig, Nina, Bourgeois, Thomas, Limousin, Denis, Wycke, Marie-Anne, Anton, Sylvia, Renou, Michel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5301018/
https://www.ncbi.nlm.nih.gov/pubmed/28239358
http://dx.doi.org/10.3389/fphys.2017.00079
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author Dupuy, Fabienne
Rouyar, Angéla
Deisig, Nina
Bourgeois, Thomas
Limousin, Denis
Wycke, Marie-Anne
Anton, Sylvia
Renou, Michel
author_facet Dupuy, Fabienne
Rouyar, Angéla
Deisig, Nina
Bourgeois, Thomas
Limousin, Denis
Wycke, Marie-Anne
Anton, Sylvia
Renou, Michel
author_sort Dupuy, Fabienne
collection PubMed
description Recognition of intra-specific olfactory signals within a complex environment of plant-related volatiles is crucial for reproduction in male moths. Sex pheromone information is detected by specific olfactory receptor neurons (Phe-ORNs), highly abundant on the male antenna. The information is then transmitted to the pheromone processing macroglomerular complex (MGC) within the primary olfactory center, the antennal lobe, where it is processed by local interneurons and projection neurons. Ultimately a behavioral response, orientation toward the pheromone source, is elicited. Volatile plant compounds (VPCs) are detected by other functional types of olfactory receptor neurons (ORNs) projecting in another area of the antennal lobe. However, Phe-ORNs also respond to some VPCs. Female-produced sex pheromones are emitted within a rich environment of VPCs, some of which have been shown to interfere with the detection and processing of sex pheromone information. As interference between the different odor sources might depend on the spatial and temporal features of the two types of stimuli, we investigated here behavioral and neuronal responses to a brief sex pheromone blend pulse in a VPC background as compared to a control background in the male noctuid moth Agrotis ipsilon. We observed male orientation behavior in a wind tunnel and recorded responses of Phe-ORNs and MGC neurons to a brief sex pheromone pulse within a background of individual VPCs. We also recorded the global input signal to the MGC using in vivo calcium imaging with the same stimulation protocol. We found that VPCs eliciting a response in Phe-ORNs and MGC neurons masked responses to the pheromone and decreased the contrast between background odor and the sex pheromone at both levels, whereas α-pinene did not interfere with first order processing. The calcium signal produced in response to a VPC background was tonic, lasting longer than the VPC stimulus duration, and masked entirely the pheromone response. One percent heptanal and linalool, in addition to the masking effect, caused a clear delay in responses of MGC neurons to the sex pheromone. Upwind flight toward the pheromone in a wind tunnel was also delayed but otherwise not altered by different doses of heptanal.
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spelling pubmed-53010182017-02-24 A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth Dupuy, Fabienne Rouyar, Angéla Deisig, Nina Bourgeois, Thomas Limousin, Denis Wycke, Marie-Anne Anton, Sylvia Renou, Michel Front Physiol Physiology Recognition of intra-specific olfactory signals within a complex environment of plant-related volatiles is crucial for reproduction in male moths. Sex pheromone information is detected by specific olfactory receptor neurons (Phe-ORNs), highly abundant on the male antenna. The information is then transmitted to the pheromone processing macroglomerular complex (MGC) within the primary olfactory center, the antennal lobe, where it is processed by local interneurons and projection neurons. Ultimately a behavioral response, orientation toward the pheromone source, is elicited. Volatile plant compounds (VPCs) are detected by other functional types of olfactory receptor neurons (ORNs) projecting in another area of the antennal lobe. However, Phe-ORNs also respond to some VPCs. Female-produced sex pheromones are emitted within a rich environment of VPCs, some of which have been shown to interfere with the detection and processing of sex pheromone information. As interference between the different odor sources might depend on the spatial and temporal features of the two types of stimuli, we investigated here behavioral and neuronal responses to a brief sex pheromone blend pulse in a VPC background as compared to a control background in the male noctuid moth Agrotis ipsilon. We observed male orientation behavior in a wind tunnel and recorded responses of Phe-ORNs and MGC neurons to a brief sex pheromone pulse within a background of individual VPCs. We also recorded the global input signal to the MGC using in vivo calcium imaging with the same stimulation protocol. We found that VPCs eliciting a response in Phe-ORNs and MGC neurons masked responses to the pheromone and decreased the contrast between background odor and the sex pheromone at both levels, whereas α-pinene did not interfere with first order processing. The calcium signal produced in response to a VPC background was tonic, lasting longer than the VPC stimulus duration, and masked entirely the pheromone response. One percent heptanal and linalool, in addition to the masking effect, caused a clear delay in responses of MGC neurons to the sex pheromone. Upwind flight toward the pheromone in a wind tunnel was also delayed but otherwise not altered by different doses of heptanal. Frontiers Media S.A. 2017-02-10 /pmc/articles/PMC5301018/ /pubmed/28239358 http://dx.doi.org/10.3389/fphys.2017.00079 Text en Copyright © 2017 Dupuy, Rouyar, Deisig, Bourgeois, Limousin, Wycke, Anton and Renou. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Dupuy, Fabienne
Rouyar, Angéla
Deisig, Nina
Bourgeois, Thomas
Limousin, Denis
Wycke, Marie-Anne
Anton, Sylvia
Renou, Michel
A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth
title A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth
title_full A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth
title_fullStr A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth
title_full_unstemmed A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth
title_short A Background of a Volatile Plant Compound Alters Neural and Behavioral Responses to the Sex Pheromone Blend in a Moth
title_sort background of a volatile plant compound alters neural and behavioral responses to the sex pheromone blend in a moth
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5301018/
https://www.ncbi.nlm.nih.gov/pubmed/28239358
http://dx.doi.org/10.3389/fphys.2017.00079
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