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Characterization and Coding of Behaviorally Significant Odor Mixtures

2009; Elsevier BV; Volume: 19; Issue: 4 Linguagem: Inglês

10.1016/j.cub.2009.01.041

1879-0445

Jeffrey A. Riffell, Hong Lei, Thomas A. Christensen, John G. Hildebrand,

Insect Pheromone Research and Control

For animals to execute odor-driven behaviors, the olfactory system must process complex odor signals and maintain stimulus identity in the face of constantly changing odor intensities [1Bartelt R.J. Schaner A.M. Jackson L.L. cis-Vaccenyl acetate as an aggregation pheromone in Drosophila melanogaster.J. Chem. Ecol. 1985; 11: 1747-1756Crossref PubMed Scopus (234) Google Scholar, 2Boch R. Shearer D.A. Identification of geraniol as the active component in the Nassanoff pheromone of the honey bee.Nature. 1962; 194: 704-706Crossref Scopus (49) Google Scholar, 3Kaissling K.E. Peripheral mechanisms of pheromone reception in moths.Chem. Senses. 1996; 21: 257-268Crossref PubMed Scopus (107) Google Scholar, 4Laska M. Fendt M. Wieser A. Endres T. Hernandez Salazar L.T. Apfelbach R. Detecting danger – or just another odorant? Olfactory sensitivity for the fox odor component 2,4,5-trimethylthiazoline in four species of mammals.Physiol. Behav. 2005; 84: 211-215Crossref PubMed Scopus (48) Google Scholar, 5Williams I.H. Pickett J.A. Martin A.P. The Nasonov pheromone of the honey bee Apis mellifera L. (Hymenoptera, Apidae). Part II. Bioassay of the components using foragers.J. Chem. Ecol. 1981; 7: 225-237Crossref PubMed Scopus (26) Google Scholar]. Surprisingly, how the olfactory system maintains identity of complex odors is unclear [6Bathellier B. Buhl D.L. Accolla R. Carleton A. Dynamic ensemble odor coding in the mammalian olfactory bulb: Sensory information at different timescales.Neuron. 2008; 57: 586-598Abstract Full Text Full Text PDF PubMed Scopus (177) Google Scholar, 7Carlsson M.A. Hansson B.S. Dose-response characteristics of glomerular activity in the moth antennal lobe.Chem. Senses. 2003; 28: 269-278Crossref PubMed Scopus (28) Google Scholar, 8Sachse S. Galizia C.G. The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation.Eur. J. Neurosci. 2003; 18: 2119-2132Crossref PubMed Scopus (158) Google Scholar, 9Stopfer M. Jayaraman V. Laurent G. Intensity versus identity coding in an olfactory system.Neuron. 2003; 39: 991-1004Abstract Full Text Full Text PDF PubMed Scopus (398) Google Scholar, 10Dasgupta S. Weddell S. Learned odor discrimination in Drosophila without combinatorial odor maps in the antennal lobe.Curr. Biol. 2008; 18: 1668-1674Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar]. We took advantage of the plant-pollinator relationship between the Sacred Datura (Datura wrightii) and the moth Manduca sexta [11Raguso R.A. Henzel C. Buchman S.L. Nabhan G.P. Trumpet flowers of the Sonoran Desert: Floral biology of Peniocereus Cacti and Sacred Datura.Int. J. Plant Sci. 2003; 164: 877-892Crossref Scopus (91) Google Scholar, 12Riffell J.A. Alarcon R. Abrell L. Davidowitz G. Bronstein J.L. Hildebrand J.G. Behavioral consequences of innate preferences and olfactory learning in hawkmoth-flower interactions.Proc. Natl. Acad. Sci. USA. 2008; 105: 3404-3409Crossref PubMed Scopus (131) Google Scholar] to determine how olfactory networks in this insect's brain represent odor mixtures. We combined gas chromatography and neural-ensemble recording in the moth's antennal lobe to examine population codes for the floral mixture and its fractionated components. Although the floral scent of D. wrightii comprises at least 60 compounds, only nine of those elicited robust neural responses. Behavioral experiments confirmed that these nine odorants mediate flower-foraging behaviors, but only as a mixture. Moreover, the mixture evoked equivalent foraging behaviors over a 1000-fold range in dilution, suggesting a singular percept across this concentration range. Furthermore, neural-ensemble recordings in the moth's antennal lobe revealed that reliable encoding of the floral mixture is organized through synchronized activity distributed across a population of glomerular coding units, and this timing mechanism may bind the features of a complex stimulus into a coherent odor percept.