Extracting the Behaviorally Relevant Stimulus: Unique Neural Representation of Farnesol, a Component of the Recruitment Pheromone of Bombus terrestris

PLoS One. 2015 Sep 4;10(9):e0137413. doi: 10.1371/journal.pone.0137413. eCollection 2015.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / physiology
  • Acyclic Monoterpenes
  • Aldehydes / pharmacology
  • Animal Communication
  • Animals
  • Arthropod Antennae / cytology
  • Arthropod Antennae / drug effects*
  • Arthropod Antennae / physiology
  • Bees / physiology*
  • Brain / cytology
  • Brain / drug effects*
  • Brain / physiology
  • Farnesol / metabolism
  • Farnesol / pharmacology*
  • Female
  • Flowers / chemistry
  • Male
  • Monoterpenes / pharmacology
  • Neurons / cytology
  • Neurons / drug effects*
  • Neurons / physiology
  • Odorants / analysis
  • Olfactory Pathways / drug effects*
  • Olfactory Pathways / physiology
  • Pheromones / metabolism
  • Pheromones / pharmacology*
  • Terpenes / pharmacology

Substances

  • Acyclic Monoterpenes
  • Aldehydes
  • Monoterpenes
  • Pheromones
  • Terpenes
  • Farnesol
  • geraniol
  • citronellol
  • citronellal

Grants and funding

Austin Brown was funded by the HHMI 52001427 through the BRAVO! program of the University of Arizona. Further support was provided by the DFG Priority Program SPP 1392 “Integrative Analysis of Olfaction” (RO 1177/5-2 to WR). Martin Strube-Bloss was supported by a grant of the German Excellence Initiative to the Graduate School of Life Sciences, University of Würzburg. This publication was funded by the German Research Foundation and the University of Würzburg in the funding program Open Access Publishing.