title: Differential combinatorial coding of pheromones in two olfactory subsystems of the honey bee brain.
abstract: Neural coding of pheromones has been intensively studied in insects with a particular focus on sex pheromones. These studies favored the view that pheromone compounds are processed within specific antennal lobe glomeruli following a specialized labeled-line system. However, pheromones play crucial roles in an insect's life beyond sexual attraction, and some species use many different pheromones making such a labeled-line organization unrealistic. A combinatorial coding scheme, in which each component activates a set of broadly tuned units, appears more adapted in this case. However, this idea has not been tested thoroughly. We focused here on the honey bee Apis mellifera, a social insect that relies on a wide range of pheromones to ensure colony cohesion. Interestingly, the honey bee olfactory system harbors two central parallel pathways, whose functions remain largely unknown. Using optophysiological recordings of projection neurons, we compared the responses of these two pathways to 27 known honey bee pheromonal compounds emitted by the brood, the workers, and the queen. We show that while queen mandibular pheromone is processed by l-ALT (lateral antennal lobe tract) neurons and brood pheromone is mainly processed by m-ALT (median antennal lobe tract) neurons, worker pheromones induce redundant activity in both pathways. Moreover, all tested pheromonal compounds induce combinatorial activity from several AL glomeruli. These findings support the combinatorial coding scheme and suggest that higher-order brain centers reading out these combinatorial activity patterns may eventually classify olfactory signals according to their biological meaning.
authors.affiliation: Evolution, Genomes, Behavior and Ecology Lab, CNRS, Université Paris-Sud, IRD (UMR 9191), F-91198 Gif-sur-Yvette, France, Research Center on Animal Cognition, Université de Toulouse, F-31062 Toulouse Cedex 9, France, and Research Center on Animal Cognition, Centre National de la Recherche Scientifique, F-31062 Toulouse Cedex 9, France.
authors.forename: Julie
authors.initials: J
authors.lastname: Carcaud
authors.affiliation: Research Center on Animal Cognition, Université de Toulouse, F-31062 Toulouse Cedex 9, France, and Research Center on Animal Cognition, Centre National de la Recherche Scientifique, F-31062 Toulouse Cedex 9, France.
authors.forename: Martin
authors.initials: M
authors.lastname: Giurfa
authors.affiliation: Evolution, Genomes, Behavior and Ecology Lab, CNRS, Université Paris-Sud, IRD (UMR 9191), F-91198 Gif-sur-Yvette, France, sandoz@egce.cnrs-gif.fr.
authors.forename: Jean-Christophe
authors.identifier: http://orcid.org/0000-0002-5423-9645
authors.initials: JC
authors.lastname: Sandoz
mesh_terms: D000818:Animals; D057506:Arthropod Antennae / Q000033:anatomy & histology; D001516:Bees; D001921:Brain / Q000033:anatomy & histology; D002118:Calcium / Q000378:metabolism*; D005260:Female; D009415:Nerve Net / Q000502:physiology*; D009812:Odorants; D009833:Olfactory Pathways / Q000166:cytology* / Q000502:physiology*; D055095:Optics and Photonics; D009949:Orientation / Q000502:physiology; D010675:Pheromones / Q000737:chemistry / Q000378:metabolism*; D011984:Sensory Receptor Cells / Q000502:physiology*; D012903:Smell / Q000502:physiology; D012919:Social Behavior
chemical_list: D010675:Pheromones; D002118:Calcium
keywords: insect; olfaction; optical imaging; parallel processing; pheromone