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• W2091214274 abstract "Olfactory systems possess the remarkable power to discriminate between tens of thousands of distinct odors, covering a wide range of chemical types. How can olfactory systems distinguish the fragrance of a rose from the odor of garlic or a pine forest? The first step in odorant discrimination takes place in the olfactory epithelium (i.e., the nose). Olfactory epithelia of higher organisms contain a multiplicity of functionally distinct olfactory sensory neurons (OSNs), each sensitive to a spectrum of different odorant molecules, that effectively select out components of complex odors and present the specific information to the brain. Once in the brain, odorant information is reconstructed and processed to bestow the organism with a “perception” of smell. Since the initial identification of an astoundingly large family of G protein-coupled odorant receptors (ORs) in the rat (Buck and Axel 1991Buck L. Axel R. Cell. 1991; 65: 175-187Abstract Full Text PDF PubMed Scopus (3442) Google Scholar), there has been a remarkable series of breakthroughs in deciphering the basic principles underlying odorant discrimination. Of particular importance are the surfeit of molecular and anatomical studies that have revealed the basic mechanisms by which odorant information in the periphery is reliably transferred to the brain for higher order processing. The initial step in odorant recognition is the interaction between an odorant and a distinct subpopulation of ORs present on the dendritic membrane of OSNs. Several studies indicate that insect and vertebrate OSNs express only one or a few ORs, which thereby defines the functional phenotype of the OSN. Independent of their physical location in the sensory epithelium, all neurons expressing a given OR project to one of many functionally distinct and spatially invariant neuropil conglomerates in the brain called glomeruli. This topographical correspondence between neurons of the olfactory epithelium and their projections to olfactory glomeruli yields an odorant-specific spatial map of receptor activation in the brain that is likely to be the first level of stimulus encoding (reviewed by Mombaerts 1999Mombaerts P. Science. 1999; 286: 707-711Crossref PubMed Scopus (349) Google Scholar). In the brain, odorant-induced temporal patterns of cellular activity have been proposed to intersect with these spatial representations to produce a more refined “image” of an odor (reviewed by Laurent 1999Laurent G. Science. 1999; 286: 723-728Crossref PubMed Scopus (268) Google Scholar). However, the relative contribution of these odor representations in defining odor quality is currently a topic of controversy in the field. One of the puzzling questions in olfaction is how these spatial and temporal representations interact to form an odorant-specific spatiotemporal map of an odor. An understanding of these mechanisms requires not only a complete topographic map of the olfactory system, but an understanding, among other things, of how the temporal (i.e., physiological) properties of activated OSNs work in concert with this spatial information to encode odor quality. Constructing a comprehensive view of olfaction in this manner is nearly impossible to accomplish in mammals given the cellular complexity of mammalian olfactory systems and the presence of approximately 1000 ORs and 1800 glomeruli in these animals. In contrast, the fruit fly olfactory system is a much simpler system (approximately 61 ORs and 43 glomeruli) and, as such, affords a unique opportunity to understand the complete underpinnings of the olfactory process in a single organism. A recent study by Vosshall et al. 2000Vosshall L.B. Wong A.M. Axel R. Cell. 2000; 102: 147-159Abstract Full Text Full Text PDF PubMed Scopus (760) Google Scholar has provided the first look at the map of receptor activation in the Drosophila brain. Building on this work, along with the current knowledge of Drosophila odorant receptor (“DOR”) expression patterns in the antenna (Clyne et al. 1999Clyne P.J. Warr C.G. Freeman M.R. Lessing D. Kim J. Carlson J.R. Neuron. 1999; 22: 327-338Abstract Full Text Full Text PDF PubMed Scopus (814) Google Scholar, Gao and Chess 1999Gao Q. Chess A. Genomics. 1999; 60: 31-39Crossref PubMed Scopus (360) Google Scholar, Vosshall et al. 1999Vosshall L.B. Amrein H. Morozov P.S. Rzhetsky A. Axel R. Cell. 1999; 96: 725-736Abstract Full Text Full Text PDF PubMed Scopus (825) Google Scholar), it may soon be possible to construct a functional map of the Drosophila antenna that relates the molecular, anatomical, and physiological mechanisms underlying odorant discrimination. In this issue of Neuron, John Carlson and his colleagues (de Bruyne et al., 2001) take the necessary first step in understanding how the physiological properties of OSNs might participate in encoding odorant quality. The authors utilize the relative simplicity and highly organized structure of the Drosophila antenna to characterize the ligand specificity and response dynamics of a large subpopulation of OSNs arrayed along the antennal surface. Insect and vertebrate olfactory systems alike possess bipolar sensory neurons with modified sensory dendrites that are bathed in an aqueous medium (see Figure 1) . One major difference between the two systems is that insect OSNs are compartmentalized into cuticularized hair-like structures called sensilla. This compartmentalization provides a unique environment for odor detection whereby ORs present on the dendrite membranes of OSNs, and possibly proteins located in the extracellular sensillum lymph, define the functional specificity of OSNs within an individual sensillum. In Drosophila, as in many insects, functionally distinct olfactory sensilla are also morphologically distinct, thus providing an ideal tissue source for establishing a functional map of the antenna. De Bruyne et al. have developed such a functional map by systematically recording the responses of hundreds of OSNs of basiconic sensilla to a panel of 47 diverse odors and correlating the response profiles with well-established anatomical maps of the antenna. The results of this study reveal several interesting properties of OSN responses that shed light on some of the fundamental physiological principles of odorant discrimination in the fly. A central finding in the manuscript is that all of the OSNs within basiconic sensilla (some 600 neurons) can be segregated into as few as 16 distinct functional classes with respect to their response profiles to the diagnostic panel of odorants. At first glance, this might suggest that the Drosophila olfactory system, unlike the olfactory systems of rats and mice, is limited in its ability to discriminate odors. However, electrophysiological characterization of OSN responses indicates that different odorants acting on a given OSN can induce a variety of physiological responses, including both stimulation and inhibition of spike frequency, and different kinetics of response termination. These varying response dynamics may effectively increase the discriminatory power of the Drosophila olfactory system by expanding the repertoire of possible odorant-induced physiological responses. In addition, variation in the kinetics of response termination may help explain how odorant information encoded by primary OSNs relates to odorant-specific temporal patterns of postsynaptic projection neuron (PN) activity within the antennal lobe (the first relay station of neuronal input from the antenna). A recent study of the effects of odor-plume dynamics on PN activity in the antennal lobe of the moth Manduca sexta implies that input from primary OSNs can directly influence temporal patterns of PN activity (Vickers et al. 2001Vickers N.J. Christensen T.A. Baker T.C. Hildebrand J.G. Nature. 2001; 410: 466-470Crossref PubMed Scopus (195) Google Scholar). Perhaps the temporal patterns of OSN activity observed by de Bruyne et al. help coordinate odorant-specific projection neuron activity in the antennal lobe. A particularly interesting feature of Drosophila OSNs is the multiplicity of responses exhibited by individual OSNs. While OSNs representing each functional class were stimulated by one or more odorant, at least three of the 16 classes were inhibited by odorant application. Although odorant-induced OSN inhibition has yet to be conclusively demonstrated in mammals, this curious feature of Drosophila OSNs has also been observed in the lobster (reviewed by Ache et al. 1998Ache B.W. Munger S. Zhainazarov A. Ann. NY Acad. Sci. 1998; 855: 194-198Crossref PubMed Scopus (10) Google Scholar), suggesting that odorant-induced OSN inhibition may be common to the arthropod lineage. Another interesting feature of the Drosophila OSNs is the narrow molecular receptive range of their DORs. Electrophysiological recordings of individual Drosophila OSNs indicate that, while 11 of the 16 classes of OSNs respond to more than one test odorant, most classes respond best to odorants exhibiting similar structural features. Recent studies in mammals (Araneda et al. 2000Araneda R.C. Kini A.D. Firestein S. Nat. Neurosci. 2000; 3: 1248-1255Crossref PubMed Scopus (402) Google Scholar) and the moth Manduca sexta (Shields and Hildebrand 2001Shields V.D. Hildebrand J.G. J. Comp. Physiol. A. 2001; 186: 1135-1151Crossref Scopus (110) Google Scholar) make similar observations. The combination of relative OR promiscuity, but within a narrow range of chemical classes, may provide a significant evolutionary advantage, since these same OSN properties have been maintained in organisms separated by over 500 million years. There do appear to be some interesting exceptions to this correlation and a more detailed analysis of the receptive range of the DORs could yield insight into the rules governing specific ligand-receptor relationships. One notable exception is the sex pheromone-sensitive OSNs of male moths, which possess an exquisitely narrow molecular receptive range, responding only to one or a few components of a species-specific female pheromone blend (Meng et al. 1989Meng L.Z. Wu C.H. Wicklein M. Kaissling K.-E. J. Comp. Phys. A. 1989; 165: 139-146Crossref Scopus (78) Google Scholar). Given the importance of mate location for reproductive success in insects, it is likely that sex pheromone-sensitive OSNs with an equivalent molecular receptive range are also present in Drosophila. Identification of these neurons in Drosophila awaits definitive identification of a true sex pheromone in this species. One of the most appealing results of this study are the many similarities between the olfactory systems of organisms separated by hundreds of millions of years of evolutionary time. Olfactory sensory neurons differentially express one of a large family of receptors that recognize multiple odors, and various odors are recognized by more than one receptor, leading to a combinatorial code for potentially hundreds of odors over orders of concentrations. Receptors of similar sensitivities are loosely segregated into stereotyped anatomical regions. Even the classical technique of recording the tuning curves of sensory receptor neurons and pairing them with anatomical and structural data has, in this most molecular of organisms, provided new insights into how the fly “knowses” about its world." @default.
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• W2091214274 title "Unlocking the DOR Code" @default.
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