Decoding olfaction in Drosophila

Current Opinion in Neurobiology

Volumn 13, Issue 1, 2003, Pages 103-110

  Keller, Andreas ^a   Vosshall, Leslie B ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA; EVOLUTION; GENE FUNCTION; HONEYBEE; IMAGING; MAMMAL; MOLECULAR RECOGNITION; MULTIGENE FAMILY; NERVE CONDUCTION; NONHUMAN; OLFACTORY DISCRIMINATION; OLFACTORY NERVE; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; RECEPTOR GENE; RECEPTOR INTRINSIC ACTIVITY; REVIEW; SENSORY NERVE CELL; SMELLING; STEREOTYPY;

EID: 0037319175     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(03)00011-4     Document Type: Review

References (54)

1. Ohloff G: Scent and Fragrances: The Fascination of Odors and their Chemical Perspectives. Berlin: Springer-Verlag; 1994;154-158.
2. Buck L., Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell. 65:1991;175-187.
3. Mombaerts P. Seven-transmembrane proteins as odorant and chemosensory receptors. Science. 286:1999;707-711.
4. Zhao H., Ivic L., Otaki J.M., Hashimoto M., Mikoshiba K., Firestein S. Functional expression of a mammalian odorant receptor. Science. 279:1998;237-242.
5. Krautwurst D., Yau K.W., Reed R.R. Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell. 95:1998;917-926.
6. Touhara K., Sengoku S., Inaki K., Tsuboi A., Hirono J., Sato T., Sakano H., Haga T. Functional identification and reconstitution of an odorant receptor in single olfactory neurons. Proc. Natl. Acad. Sci. USA. 96:1999;4040-4045.
7. Clyne P.J., Warr C.G., Freeman M.R., Lessing D., Kim J., Carlson J.R. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron. 22:1999;327-338.
8. Gao Q., Chess A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics. 60:1999;31-39.
9. Vosshall L.B., Amrein H., Morozov P.S., Rzhetsky A., Axel R. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell. 96:1999;725-736.
10. Scott K., Brady R. Jr., Cravchik A., Morozov P., Rzhetsky A., Zuker C., Axel R. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell. 104:2001;661-673.
11. Dunipace L., Meister S., McNealy C., Amrein H. Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11:2001;822-835.
12. ••]).
13. ••]).
14. Araneda R.C., Kini A.D., Firestein S. The molecular receptive range of an odorant receptor. Nat. Neurosci. 3:2000;1248-1255.
15. Malnic B., Hirono J., Sato T., Buck L.B. Combinatorial receptor codes for odors. Cell. 96:1999;713-723.
16. •]).
17. ••]).
18. Mombaerts P., Wang F., Dulac C., Chao S.K., Nemes A., Mendelsohn M., Edmondson J., Axel R. Visualizing an olfactory sensory map. Cell. 87:1996;675-686.
19. Ressler K.J., Sullivan S.L., Buck L.B. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell. 79:1994;1245-1255.
20. Vassar R., Chao S.K., Sitcheran R., Nunez J.M., Vosshall L.B., Axel R. Topographic organization of sensory projections to the olfactory bulb. Cell. 79:1994;981-991.
21. Gao Q., Yuan B., Chess A. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci. 3:2000;780-785.
22. Vosshall L.B., Wong A.M., Axel R. An olfactory sensory map in the fly brain. Cell. 102:2000;147-159.
23. Wang F., Nemes A., Mendelsohn M., Axel R. Odorant receptors govern the formation of a precise topographic map. Cell. 93:1998;47-60.
24. Belluscio L., Lodovichi C., Feinstein P., Mombaerts P., Katz L.C. Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature. 419:2002;296-300 Characterization of the novel glomerulus that results from the substitution of rat OR I7 in OSNs that normally express mouse OR M71. These experiments demonstrate for the first time an overlap in the anatomical mapping of OSNs to specific glomeruli and the functional map that emerges from examining glomerular activation in response to specific ligands. Furthermore, the data show that novel glomeruli are innervated by postsynaptic neurons that acquire the functional identity of the glomeruli and establish reciprocal projections between the two ectopic mirror-image glomeruli.
25. Bozza T., Feinstein P., Zheng C., Mombaerts P. Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22:2002;3033-3043 The authors show that substituting one receptor for another in OSNs in mice changes the stimulus response profiles of the neurons and results in the formation of ectopic glomeruli in the olfactory bulb. Therefore the odorant receptor is the principal determinant of the odor-specificity of a given OSN.
26. Jhaveri D., Rodrigues V. Sensory neurons of the Atonal lineage pioneer the formation of glomeruli within the adult Drosophila olfactory lobe. Development. 129:2002;1251-1260.
27. Elmore T., Smith D.P. Putative Drosophila odor receptor OR43b localizes to dendrites of olfactory neurons. Insect Biochem. Mol. Biol. 31:2001;791-798.
28. Jefferis G.S., Marin E.C., Stocker R.F., Luo L. Target neuron prespecification in the olfactory map of Drosophila. Nature. 414:2001;204-208 A systematic clonal analysis of the PNs of Drosophila revealed that PNs are derived from three neuroblasts. The glomerular choice of the PNs is prespecified by the lineage and birth order of the PNs.
29. Marin E.C., Jefferis G.S., Komiyama T., Zhu H., Luo L. Representation of the glomerular olfactory map in the Drosophila brain. Cell. 109:2002;243-255 Labeling of single PNs sending dendrites to specific glomeruli revealed their stereotypical axon branching patterns and terminal fields in higher olfactory centers.
30. Wong A.M., Wang J.W., Axel R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell. 109:2002;229-241 The authors visualized single Drosophila PNs connecting defined glomeruli with higher brain centers to study their innervation patterns. A topographical map of olfactory information is retained in higher sensory centers in the brain.
31. Zou Z., Horowitz L.F., Montmayeur J.-P., Snapper S., Buck L.B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature. 414:2001;173-179 The authors use a transneuronal tracer to visualize neurons in the olfactory cortex receiving input from a particular OR. Thus, they are able to describe a sensory map in the olfactory cortex, in which input from a particular OR is targeted to clusters of neurons conserved between different animals. Signals from different ORs overlap spatially and signals from the same OR are targeted to multiple cortical areas.
32. Luo M., Katz L.C. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron. 32:2001;1165-1179.
33. King J.R., Christensen T.A., Hildebrand J.G. Response characteristics of an identified, sexually dimorphic olfactory glomerulus. J. Neurosci. 20:2000;2391-2399.
34. Friedrich R.W., Korsching S.I. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron. 18:1997;737-752.
35. Joerges J., Küttner A., Galizia C.G., Menzel R. Representation of odours and odour mixtures visualized in the honeybee brain. Nature. 387:1997;285-288.
36. Galizia C.G., Sachse S., Rappert A., Menzel R. The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat. Neurosci. 2:1999;473-478.
37. Rubin B.D., Katz L.C. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron. 23:1999;499-511.
38. Uchida N., Takahashi Y.K., Tanifuji M., Mori K. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat. Neurosci. 3:2000;1035-1043.
39. Meister M., Bonhoeffer T. Tuning and topography in an odor map on the rat olfactory bulb. J. Neurosci. 21:2001;1351-1360 The authors recorded responses of glomeruli in the rat olfactory bulb and showed that the patterns of activated glomeruli are bilaterally symmetric and their extent varies with concentration. Glomeruli with similar tuning properties are shown to be located near each other.
40. Belluscio L., Katz L.C. Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J. Neurosci. 21:2001;2113-2122 Optical imaging of intrinsic signals in rodent olfactory bulbs is used to show that odors generally activate a bilaterally symmetric pattern of glomeruli. A systematic map of molecular chain length is produced on the surface of the olfactory bulb and mixed odors activate a pattern similar to the combination of the patterns elicited by each individual component.
41. Sachse S., Galizia C.G. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J. Neurophysiol. 87:2002;1106-1117 A combination of optically recorded calcium responses of selectively stained PNs and pharmacological experiments revealed that two separate inhibitory networks enhance the contrast between odor representations in the antennal lobe of honeybees.
42. Lei H., Christensen T.A., Hildebrand J.G. Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat. Neurosci. 5:2002;557-565 The authors used simultaneous intracellular recordings from pairs of PNs to reveal that PNs innervating the same glomerulus show odor-evoked synchrony of spike discharges, and that the extent of this synchrony is modulated by inhibitory input from the neighbouring glomerulus.
43. Friedrich R.W., Laurent G. Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. Science. 291:2001;889-894 By investigating mitral cell ensembles in the olfactory bulb of the zebrafish, the authors show that the similarity between distributed temporal patterns that represent related odors reduces progressively over time, whereas the responses of individual cells do not become more specific.
44. Perez-Orive J., Mazor O., Turner G.C., Cassanaer S., Wilson R.I., Laurent G. Oscillations and sparsening of odor representations in the mushroom body. Science. 297:2002;359-365.
45. Daly K.C., Chandra S., Durtschi M.L., Smith B.H. The generalization of an olfactory-based conditioned response reveals unique but overlapping odour representations in the moth Manduca sexta. J. Exp. Biol. 204:2001;3085-3095 The authors use behavioral experiments to assess how the moth Manduca sexta can distinguish between odors that vary in one or more molecular dimensions. They found that odor similarity is a function of differences in the shape and length of the carbon chain and the functional group attached to it.
46. Rubin B.D., Katz L.C. Spatial coding of enantiomers in the rat olfactory bulb. Nat. Neurosci. 4:2001;355-356.
47. Laska M., Galizia C.G. Enantioselectivity of odor perception in honeybees (Apis mellifera carnica). Behav. Neurosci. 115:2001;632-639.
48. Linster C., Johnson B.A., Yue E., Morse A., Xu Z., Hingco E.E., Choi Y., Choi M., Messiha A., Leon M. Perceptual correlates of neural representations evoked by odorant enantiomers. J. Neurosci. 21:2001;9837-9843 In this paper it is shown that enantiomeric pairs that have clearly different glomerular representations but not those having very similar representations are discriminated by rats spontaneously.
49. Linster C., Johnson B.A., Morse A., Yue E., Leon M. Spontaneous versus reinforced olfactory discriminations. J. Neurosci. 22:2002;6842-6845 Here it is shown that enantiomeric pairs that have barely distinguishable activation patterns and are not discriminated spontaneously by rats are discriminated if subjected to differential reinforcement.
50. Faber T., Joerges J., Menzel R. Associative learning modifies neural representations of odors in the insect brain. Nat. Neurosci. 2:1999;74-78.
51. Stopfer M., Bhagavan S., Smith B.H., Laurent G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature. 390:1997;70-74.
52. Ng 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. 36:2002;463-474 Using synapto-pHluorin, synaptic activity is measured in Drosophila OSNs, PNs, and local interneurons. Unique combinatorials of glomeruli are activated by distinct odors and these activity patterns are hypothesized to underlie the odor code that permits the animal to smell.
53. Fiala A., Spall T., Diegelmann S., Eisermann B., Sachse S., Devaud J.M., Buchner E., Galizia C.G. Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr. Biol. 12:2002;1877-1884 Cameleon is used as a genetic tracer of neuronal activity in PNs in the AL and in the calyx of the mushroom body. Odor-specific patterns of activation that are conserved between individuals are seen both in the AL and in the mushroom body.
54. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R: Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 2003, In Press.