Extracting the Behaviorally Relevant Stimulus: Unique Neural Representation of Farnesol, a Component of the Recruitment Pheromone of Bombus terrestris
To trigger innate behavior, sensory neural networks are pre-tuned to extract biologically relevant stimuli. Many male-female or insect-plant interactions depend on this phenomenon. Especially communication among individuals within social groups depends on innate behaviors. One example is the efficie...
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description | To trigger innate behavior, sensory neural networks are pre-tuned to extract biologically relevant stimuli. Many male-female or insect-plant interactions depend on this phenomenon. Especially communication among individuals within social groups depends on innate behaviors. One example is the efficient recruitment of nest mates by successful bumblebee foragers. Returning foragers release a recruitment pheromone in the nest while they perform a 'dance' behavior to activate unemployed nest mates. A major component of this pheromone is the sesquiterpenoid farnesol. How farnesol is processed and perceived by the olfactory system, has not yet been identified. It is much likely that processing farnesol involves an innate mechanism for the extraction of relevant information to trigger a fast and reliable behavioral response. To test this hypothesis, we used population response analyses of 100 antennal lobe (AL) neurons recorded in alive bumblebee workers under repeated stimulation with four behaviorally different, but chemically related odorants (geraniol, citronellol, citronellal and farnesol). The analysis identified a unique neural representation of the recruitment pheromone component compared to the other odorants that are predominantly emitted by flowers. The farnesol induced population activity in the AL allowed a reliable separation of farnesol from all other chemically related odor stimuli we tested. We conclude that the farnesol induced population activity may reflect a predetermined representation within the AL-neural network allowing efficient and fast extraction of a behaviorally relevant stimulus. Furthermore, the results show that population response analyses of multiple single AL-units may provide a powerful tool to identify distinct representations of behaviorally relevant odors. |
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Many male-female or insect-plant interactions depend on this phenomenon. Especially communication among individuals within social groups depends on innate behaviors. One example is the efficient recruitment of nest mates by successful bumblebee foragers. Returning foragers release a recruitment pheromone in the nest while they perform a 'dance' behavior to activate unemployed nest mates. A major component of this pheromone is the sesquiterpenoid farnesol. How farnesol is processed and perceived by the olfactory system, has not yet been identified. It is much likely that processing farnesol involves an innate mechanism for the extraction of relevant information to trigger a fast and reliable behavioral response. To test this hypothesis, we used population response analyses of 100 antennal lobe (AL) neurons recorded in alive bumblebee workers under repeated stimulation with four behaviorally different, but chemically related odorants (geraniol, citronellol, citronellal and farnesol). The analysis identified a unique neural representation of the recruitment pheromone component compared to the other odorants that are predominantly emitted by flowers. The farnesol induced population activity in the AL allowed a reliable separation of farnesol from all other chemically related odor stimuli we tested. We conclude that the farnesol induced population activity may reflect a predetermined representation within the AL-neural network allowing efficient and fast extraction of a behaviorally relevant stimulus. Furthermore, the results show that population response analyses of multiple single AL-units may provide a powerful tool to identify distinct representations of behaviorally relevant odors.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0137413</identifier><identifier>PMID: 26340263</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Action Potentials - drug effects ; Action Potentials - physiology ; Acyclic Monoterpenes ; Aldehydes - pharmacology ; Animal Communication ; Animals ; Antennal lobe ; Aroma compounds ; Arthropod Antennae - cytology ; Arthropod Antennae - drug effects ; Arthropod Antennae - physiology ; Bees - physiology ; Behavior ; Bombus ; Bombus terrestris ; Brain - cytology ; Brain - drug effects ; Brain - physiology ; Bumblebees ; Chemical communication ; Citronellal ; Citronellol ; Dance ; Drosophila ; Drosophila melanogaster ; Farnesol ; Farnesol - metabolism ; Farnesol - pharmacology ; Female ; Flowers ; Flowers - chemistry ; Information processing ; Insects ; Male ; Monoterpenes - pharmacology ; Neural circuitry ; Neural coding ; Neural networks ; Neurons ; Neurons - cytology ; Neurons - drug effects ; Neurons - physiology ; Odorants ; Odorants - analysis ; Odors ; Olfactory Pathways - drug effects ; Olfactory Pathways - physiology ; Olfactory system ; Pheromones ; Pheromones - metabolism ; Pheromones - pharmacology ; Physiological aspects ; Physiology ; Properties ; Recruitment ; Representations ; Sensory evaluation ; Sensory stimulation ; Terpenes - pharmacology ; Workers</subject><ispartof>PloS one, 2015-09, Vol.10 (9), p.e0137413-e0137413</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Strube-Bloss et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Strube-Bloss et al 2015 Strube-Bloss et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-bbfeec9e5aec74b3a6055ed812e10ec0934e0ece066592b07a72084d43bc5e5d3</citedby><cites>FETCH-LOGICAL-c692t-bbfeec9e5aec74b3a6055ed812e10ec0934e0ece066592b07a72084d43bc5e5d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4560401/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4560401/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26340263$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>d'Ettorre, Patrizia</contributor><creatorcontrib>Strube-Bloss, Martin F</creatorcontrib><creatorcontrib>Brown, Austin</creatorcontrib><creatorcontrib>Spaethe, Johannes</creatorcontrib><creatorcontrib>Schmitt, Thomas</creatorcontrib><creatorcontrib>Rössler, Wolfgang</creatorcontrib><title>Extracting the Behaviorally Relevant Stimulus: Unique Neural Representation of Farnesol, a Component of the Recruitment Pheromone of Bombus terrestris</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>To trigger innate behavior, sensory neural networks are pre-tuned to extract biologically relevant stimuli. Many male-female or insect-plant interactions depend on this phenomenon. Especially communication among individuals within social groups depends on innate behaviors. One example is the efficient recruitment of nest mates by successful bumblebee foragers. Returning foragers release a recruitment pheromone in the nest while they perform a 'dance' behavior to activate unemployed nest mates. A major component of this pheromone is the sesquiterpenoid farnesol. How farnesol is processed and perceived by the olfactory system, has not yet been identified. It is much likely that processing farnesol involves an innate mechanism for the extraction of relevant information to trigger a fast and reliable behavioral response. To test this hypothesis, we used population response analyses of 100 antennal lobe (AL) neurons recorded in alive bumblebee workers under repeated stimulation with four behaviorally different, but chemically related odorants (geraniol, citronellol, citronellal and farnesol). The analysis identified a unique neural representation of the recruitment pheromone component compared to the other odorants that are predominantly emitted by flowers. The farnesol induced population activity in the AL allowed a reliable separation of farnesol from all other chemically related odor stimuli we tested. We conclude that the farnesol induced population activity may reflect a predetermined representation within the AL-neural network allowing efficient and fast extraction of a behaviorally relevant stimulus. 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metabolism</subject><subject>Farnesol - pharmacology</subject><subject>Female</subject><subject>Flowers</subject><subject>Flowers - chemistry</subject><subject>Information processing</subject><subject>Insects</subject><subject>Male</subject><subject>Monoterpenes - pharmacology</subject><subject>Neural circuitry</subject><subject>Neural coding</subject><subject>Neural networks</subject><subject>Neurons</subject><subject>Neurons - cytology</subject><subject>Neurons - drug effects</subject><subject>Neurons - physiology</subject><subject>Odorants</subject><subject>Odorants - analysis</subject><subject>Odors</subject><subject>Olfactory Pathways - drug effects</subject><subject>Olfactory Pathways - physiology</subject><subject>Olfactory system</subject><subject>Pheromones</subject><subject>Pheromones - metabolism</subject><subject>Pheromones - pharmacology</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Properties</subject><subject>Recruitment</subject><subject>Representations</subject><subject>Sensory evaluation</subject><subject>Sensory stimulation</subject><subject>Terpenes - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Strube-Bloss, Martin F</au><au>Brown, Austin</au><au>Spaethe, Johannes</au><au>Schmitt, Thomas</au><au>Rössler, Wolfgang</au><au>d'Ettorre, Patrizia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Extracting the Behaviorally Relevant Stimulus: Unique Neural Representation of Farnesol, a Component of the Recruitment Pheromone of Bombus terrestris</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-09-04</date><risdate>2015</risdate><volume>10</volume><issue>9</issue><spage>e0137413</spage><epage>e0137413</epage><pages>e0137413-e0137413</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>To trigger innate behavior, sensory neural networks are pre-tuned to extract biologically relevant stimuli. Many male-female or insect-plant interactions depend on this phenomenon. Especially communication among individuals within social groups depends on innate behaviors. One example is the efficient recruitment of nest mates by successful bumblebee foragers. Returning foragers release a recruitment pheromone in the nest while they perform a 'dance' behavior to activate unemployed nest mates. A major component of this pheromone is the sesquiterpenoid farnesol. How farnesol is processed and perceived by the olfactory system, has not yet been identified. It is much likely that processing farnesol involves an innate mechanism for the extraction of relevant information to trigger a fast and reliable behavioral response. To test this hypothesis, we used population response analyses of 100 antennal lobe (AL) neurons recorded in alive bumblebee workers under repeated stimulation with four behaviorally different, but chemically related odorants (geraniol, citronellol, citronellal and farnesol). The analysis identified a unique neural representation of the recruitment pheromone component compared to the other odorants that are predominantly emitted by flowers. The farnesol induced population activity in the AL allowed a reliable separation of farnesol from all other chemically related odor stimuli we tested. We conclude that the farnesol induced population activity may reflect a predetermined representation within the AL-neural network allowing efficient and fast extraction of a behaviorally relevant stimulus. Furthermore, the results show that population response analyses of multiple single AL-units may provide a powerful tool to identify distinct representations of behaviorally relevant odors.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26340263</pmid><doi>10.1371/journal.pone.0137413</doi><oa>free_for_read</oa></addata></record> |
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recordid | cdi_plos_journals_1710303814 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
subjects | Action Potentials - drug effects Action Potentials - physiology Acyclic Monoterpenes Aldehydes - pharmacology Animal Communication Animals Antennal lobe Aroma compounds Arthropod Antennae - cytology Arthropod Antennae - drug effects Arthropod Antennae - physiology Bees - physiology Behavior Bombus Bombus terrestris Brain - cytology Brain - drug effects Brain - physiology Bumblebees Chemical communication Citronellal Citronellol Dance Drosophila Drosophila melanogaster Farnesol Farnesol - metabolism Farnesol - pharmacology Female Flowers Flowers - chemistry Information processing Insects Male Monoterpenes - pharmacology Neural circuitry Neural coding Neural networks Neurons Neurons - cytology Neurons - drug effects Neurons - physiology Odorants Odorants - analysis Odors Olfactory Pathways - drug effects Olfactory Pathways - physiology Olfactory system Pheromones Pheromones - metabolism Pheromones - pharmacology Physiological aspects Physiology Properties Recruitment Representations Sensory evaluation Sensory stimulation Terpenes - pharmacology Workers |
title | Extracting the Behaviorally Relevant Stimulus: Unique Neural Representation of Farnesol, a Component of the Recruitment Pheromone of Bombus terrestris |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-20T08%3A05%3A03IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Extracting%20the%20Behaviorally%20Relevant%20Stimulus:%20Unique%20Neural%20Representation%20of%20Farnesol,%20a%20Component%20of%20the%20Recruitment%20Pheromone%20of%20Bombus%20terrestris&rft.jtitle=PloS%20one&rft.au=Strube-Bloss,%20Martin%20F&rft.date=2015-09-04&rft.volume=10&rft.issue=9&rft.spage=e0137413&rft.epage=e0137413&rft.pages=e0137413-e0137413&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0137413&rft_dat=%3Cgale_plos_%3EA427722885%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1710303814&rft_id=info:pmid/26340263&rft_galeid=A427722885&rft_doaj_id=oai_doaj_org_article_009f9d1dff1b4cac87d315e55c6ef062&rfr_iscdi=true |