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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Veröffentlicht in:PloS one 2015-09, Vol.10 (9), p.e0137413-e0137413
Hauptverfasser: Strube-Bloss, Martin F, Brown, Austin, Spaethe, Johannes, Schmitt, Thomas, Rössler, Wolfgang
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Brown, Austin
Spaethe, Johannes
Schmitt, Thomas
Rössler, Wolfgang
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.</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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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