Trends in Genetics
The odor coding system of Drosophila
Section snippets
Anatomy of the Drosophila olfactory system
The fly has two pairs of olfactory organs, the antennae and the maxillary palps (Figure 1a). Each antenna contains ∼1200 olfactory receptor neurons (ORNs), whereas each maxillary palp contains ∼120 ORNs 6, 7, 8. ORNs are compartmentalized into sensory hairs called sensilla, which can be subdivided into three major morphological types: basiconic, coeloconic and trichoid (Figure 1b). Each sensillum contains the dendrites of up to four ORNs. The antenna contains all three types of olfactory
Olfactory receptor neurons
The ORNs of the antenna and maxillary palp generate action potentials in response to odor stimulation. The odor responses of many of these ORNs have been characterized through extracellular single-unit recordings from individual olfactory sensilla 21, 22, 23, 24. These recordings have revealed that different odorants elicit responses from different subsets of ORNs, and also that ORNs exhibit a remarkable diversity of response properties: responses can be either excitatory or inhibitory and can
Odorant receptor genes
Odorant receptors had been sought in insects for many years with a wide variety of genetic, biochemical and molecular approaches. A large family of candidate odorant receptor genes, the Or genes, was finally discovered in Drosophila in 1999 30, 31, 32. One successful approach to their isolation began with the assumption that odorant receptors in flies, like those in mammals [33] and Caenorhabditis elegans [34], were G protein-coupled-receptors (GPCRs), a superfamily of proteins whose members
Functional analysis of odorant receptors
Despite extensive data concerning Or gene expression, until recently little was known about Or gene function, in part because traditional genetic screens failed to identify odorant receptor mutants. The first Drosophila odorant receptor to be functionally characterized was the antennal receptor Or43a, which was initially characterized physiologically following antennal overexpression [49] and heterologous expression in Xenopus oocytes [50]. Both studies identified cyclohexanone, cyclohexanol,
Odor representations in the antennal lobe
Odors are initially encoded in the diverse responses of the population of ORNs. How is odor information represented in the AL? The ∼1320 ORNs of the antenna and maxillary palp converge onto ∼43 glomeruli in the AL. Studies using Or promoters to drive expression of reporters have revealed that in Drosophila, as in mammals, axons of ORNs expressing the same odorant receptor converge onto only one or a few glomeruli 42, 55, 56. The result is a highly precise spatial map of ORN projections, which
Odor representations in higher brain centers
Spatial patterning of odor-evoked activity has also been reported in the MB. Calcium imaging of MB neurons revealed that different odorants evoke different patterns of spatial activity 58, 62. Higher odorant concentrations also evoke different patterns of spatial activity [62]. Interestingly, the spatial patterning in the MB appears to be highly variable between individual flies [62]. Consistent with this result, a lack of stereotypy among individual flies was observed in the branching patterns
Olfactory sensillum development and the problem of receptor gene choice
The antenna and maxillary palp are highly precise and stereotyped in their organization. For example, ORNs of certain odor specificities are consistently paired in canonical combinations within individual sensilla (Figure 2c). How is this degree of precision established during development?
Sensory organ precursor cells, termed ‘founder cells’ 66, 67, are specified in the antennal imaginal disc during the early stages of pupal development. These founder cells then recruit additional cells to form
Axon pathfinding in the olfactory system
Little is known in Drosophila about the molecular cues that guide ORN axons to their target glomeruli. In vertebrates, the odorant receptor itself has been implicated in this process 75, 76. However, this does not appear to be the case in Drosophila, where ORNs whose Or genes have been deleted, in addition to ORNs expressing different Or genes ectopically, still target their cognate glomeruli [51]. Two signaling components, the adaptor protein Dock and the serine-threonine kinase Pak, have been
Conclusions and future directions
Our understanding of odor coding has increased dramatically in recent years, yet many questions remain. The mechanism by which an ORN selects a particular odorant receptor gene is likely to involve both a combinatorial code of transcription factors and a combinatorial code of cis-acting regulatory sequences adjacent to the odorant receptor genes. A major challenge for the future is to identify these trans- and cis-acting factors and to understand how they operate together to define the
Acknowledgements
The authors’ work is supported by NIH grants DC04729 and DC02174 to J.C., and an NRSA predoctoral fellowship to E.H.
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