Title: Light Activation of an Innate Olfactory Avoidance Response in Drosophila
Abstract: How specific sensory stimuli evoke specific behaviors is a fundamental problem in neurobiology. In Drosophila, most odorants elicit attraction or avoidance depending on their concentration, as well as their identity [1Wang Y. Chiang A.S. Xia S. Kitamoto T. Tully T. Zhong Y. Blockade of neurotransmission in Drosophila mushroom bodies impairs odor attraction, but not repulsion.Curr. Biol. 2003; 13: 1900-1904Abstract Full Text Full Text PDF PubMed Scopus (61) Google Scholar]. Such odorants, moreover, typically activate combinations of glomeruli in the antennal lobe of the brain [2Ng M. Roorda R.D. Lima S.Q. Zemelman B.V. Morcillo P. Miesenbock G. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly.Neuron. 2002; 36: 463-474Abstract Full Text Full Text PDF PubMed Scopus (361) Google Scholar, 3Wang J.W. Wong A.M. Flores J. Vosshall L.B. Axel R. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain.Cell. 2003; 112: 271-282Abstract Full Text Full Text PDF PubMed Scopus (596) Google Scholar, 4Hallem E.A. Carlson J.R. Coding of odors by a receptor repertoire.Cell. 2006; 125: 143-160Abstract Full Text Full Text PDF PubMed Scopus (747) Google Scholar], complicating the dissection of the circuits translating odor recognition into behavior. Carbon dioxide (CO2), in contrast, elicits avoidance over a wide range of concentrations [5Suh G.S. Wong A.M. Hergarden A.C. Wang J.W. Simon A.F. Benzer S. Axel R. Anderson D.J. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila.Nature. 2004; 431: 854-859Crossref PubMed Scopus (393) Google Scholar, 6Faucher C. Forstreuter M. Hilker M. de Bruyne M. Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context.J. Exp. Biol. 2006; 209: 2739-2748Crossref PubMed Scopus (87) Google Scholar] and activates only a single glomerulus, V [5Suh G.S. Wong A.M. Hergarden A.C. Wang J.W. Simon A.F. Benzer S. Axel R. Anderson D.J. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila.Nature. 2004; 431: 854-859Crossref PubMed Scopus (393) Google Scholar]. The V glomerulus receives projections from olfactory receptor neurons (ORNs) that coexpress two GPCRs, Gr21a and Gr63a, that together comprise a CO2 receptor [7Jones W.D. Cayirlioglu P. Kadow I.G. Vosshall L.B. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila.Nature. 2007; 445: 86-90Crossref PubMed Scopus (425) Google Scholar, 8Kwon J.Y. Dahanukar A. Weiss L.A. Carlson J.R. The molecular basis of CO2 reception in Drosophila.Proc. Natl. Acad. Sci. USA. 2007; 104: 3574-3578Crossref PubMed Scopus (318) Google Scholar, 9Scott K. Brady Jr., R. Cravchik A. Morozov P. Rzhetsky A. Zuker C. Axel R. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila.Cell. 2001; 104: 661-673Abstract Full Text Full Text PDF PubMed Scopus (485) Google Scholar]. These CO2-sensitive ORNs, located in the ab1 sensilla of the antenna, are called ab1c neurons [10de Bruyne M. Foster K. Carlson J.R. Odor coding in the Drosophila antenna.Neuron. 2001; 30: 537-552Abstract Full Text Full Text PDF PubMed Scopus (520) Google Scholar]. Genetic silencing of ab1c neurons indicates that they are necessary for CO2-avoidance behavior [5Suh G.S. Wong A.M. Hergarden A.C. Wang J.W. Simon A.F. Benzer S. Axel R. Anderson D.J. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila.Nature. 2004; 431: 854-859Crossref PubMed Scopus (393) Google Scholar]. Whether activation of these neurons alone is sufficient to elicit this behavior, or whether CO2 avoidance requires additional inputs (e.g., from the respiratory system), remains unclear. Here, we show that artificial stimulation of ab1c neurons with light (normally attractive to flies) elicits the avoidance behavior typical of CO2. Thus, avoidance behavior appears hardwired into the olfactory circuitry that detects CO2 in Drosophila.