Molecular architecture of smell and taste in Drosophila

Annual Review of Neuroscience

Volumn 30, Issue , 2007, Pages 505-533

  Vosshall, Leslie B ^a   Stocker, Reinhard F ^b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Chemosensory brain centers; Chemosensory processing; Glomeruli; Gustatory receptors; Odorant receptors

Indexed keywords

DROSOPHILA; FOOD; INSECT; NEUROANATOMY; NEUROPHYSIOLOGY; NONHUMAN; ODOR; PRIORITY JOURNAL; REVIEW; SMELLING; TASTE;

AFFERENT PATHWAYS; ANIMALS; BRAIN; CHEMORECEPTORS; DROSOPHILA MELANOGASTER; PERIPHERAL NERVOUS SYSTEM; RECEPTORS, ODORANT; SIGNAL TRANSDUCTION; SMELL; TASTE;

EID: 34547668505     PISSN: 0147006X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.neuro.30.051606.094306     Document Type: Review

References (144)

1. Ache BW, Young JM. 2005. Olfaction: diverse species, conserved principles. Neuron 48:417-30
2. Amrein H, Thorne N. 2005. Gustatory perception and behavior in Drosophila melanogaster. Curr. Biol. 15:R673-84
3. Anholt RR, Lyman RF, Mackay TF. 1996. Effects of single P-element insertions on olfactory behavior in Drosophila melanogaster. Genetics 143:293-301
4. Benton R, Sachse S, Michnick SW, Vosshall LB. 2006. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol. 4:e20
5. Bray S, Amrein H. 2003. A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39:1019-29
6. Buck L, Axel R. 1991. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175-87
7. Christensen TA, Waldrop BR, Hildebrand JG. 1998. Multitasking in the olfactory system: context-dependent responses to odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J. Neurosci. 18:5999-6008
8. Chu I, Axtell R. 1971. Fine structure of the dorsal organ of the house fly larva, Musca domestica. L. Z. Zellforsch. Mikrosk. Anat. 117:17-34
9. Chu-Wang I, Axtell R. 1972. Fine structure of the terminal organ of the house fly larva, Musca domestica. L. Z. Zellforsch. Mikrosk. Anat. 127:287-305
10. Clyne PJ, Certel SJ, de Bruyne M, Zaslavsky L, Johnson WA, Carlson JR. 1999a. The odor specificities of a subset of olfactory receptor neurons are governed by Acj6, a POU-domain transcription factor. Neuron 22:339-47
11. Clyne PJ, Warr CG, Carlson JR. 2000. Candidate taste receptors in Drosophila. Science 287:1830-34
12. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. 1999b. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327-38
13. Cobb M. 1999. What and how do maggots smell? Biol. Rev. 74:425-59
14. Cobb M, Domain I. 2000. Olfactory coding in a simple system: adaptation in Drosophila larvae. Proc. R. Soc. London B Biol. Sci. 267:2119-25
15. Colomb J, Grillenzoni N, Ramaekers A, Stocker RF. 2007. Architecture of the primary taste centre of Drosophila melanogaster larvae. J. Comp. Neurol. In press
16. Couto A, Alenius M, Dickson BJ. 2005. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15:1535-47
17. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL. 1998. Tripartite mushroom body architecture revealed by antigenic markers. Learn. Mem. 5:38-51
18. Dahanukar A, Foster K, van der Goes van Naters WM, Carlson JR. 2001. A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat. Neurosci. 4:1182-86
19. Daly KC, Christensen TA, Lei H, Smith BH, Hildebrand JG. 2004. Learning modulates the ensemble representations for odors in primary olfactory networks. Proc. Natl. Acad. Sci. USA 101:10476-81
20. Davis RL. 2005. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu. Rev. Neurosci. 28:275-302
21. de Belle JS, Heisenberg M. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-95
22. de Bruyne M, Clyne PJ, Carlson JR. 1999. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J. Neurosci. 19:4520-32
23. de Bruyne M, Foster K, Carlson JR. 2001. Odor coding in the Drosophila antenna. Neuron 30:537-52
24. Dunipace L, Meister S, McNealy C, Amrein H. 2001. Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11:822-35
25. Elmore T, Ignell R, Carlson JR, Smith DP. 2003. Targeted mutation of a Drosophila odor receptor defines receptor requirement in a novel class of sensillum. J. Neurosci. 23:9906-12
26. Faucher C, Forstreuter M, Hilker M, de Bruyne M. 2006. Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context. J. Exp. Biol. 209:2739-48
27. Fiala A, Spall T, Diegelmann S, Eisermann B, Sachse S, et al. 2002. Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr. Biol. 12:1877-84
28. Fishilevich E, Domingos AI, Asahina K, Naef F, Vosshall LB, Louis M. 2005. Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr. Biol. 15:2086-96
29. Fishilevich E, Vosshall LB. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15:1548-53
30. Fox AN, Pitts RJ, Robertson HM, Carlson JR, Zwiebel LJ. 2001. Candidate odorant receptors from the malaria vector mosquito Anopheles gambiae and evidence of down-regulation in response to blood feeding. Proc. Natl. Acad. Sci. USA 98:14693-97
31. Gao Q, Chess A. 1999. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60:31-39
32. Gao Q, Yuan B, Chess A. 2000. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat. Neurosci. 3:780-85
33. Gendre N, Lüer K, Friche S, Grillenzoni N, Ramaekers A, et al. 2004. Integration of complex larval chemosensory organs into the adult nervous system of Drosophila. Development 131:83-92
34. Goldman AL, van der Goes van Naters W, Lessing D, Warr CG, Carlson JR. 2005. Coexpression of two functional odor receptors in one neuron. Neuron 45:661-66
35. Ha TS, Smith DP. 2006. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J. Neurosci. 26:8727-33
36. Hallem EA, Carlson JR. 2006. Coding of odors by a receptor repertoire. Cell 125:143-60
37. Hallem EA, Fox AN, Zwiebel LJ, Carlson JR. 2004. Olfaction: mosquito receptor for human-sweat odorant. Nature 427:212-13
38. Hammer M. 1993. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59-63
39. Hayar A, Karnup S, Ennis M, Shipley MT. 2004. External tufted cells: a major excitatory element that coordinates glomerular activity. J. Neurosci. 24:6676-85
40. Heimbeck G, Bugnon V, Gendre N, Häberlin C, Stocker RF. 1999. Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J. Neurosci. 19:6599-609
41. Heimbeck G, Bugnon V, Gendre N, Keller A, Stocker RF. 2001. A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 98:15336-41
42. Heisenberg M. 2003. Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4:266-75
43. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20:595-631
44. Hill CA, Fox AN, Pitts RJ, Kent LB, Tan PL, et al. 2002. G protein-coupled receptors in Anopheles gambiae. Science 298:176-78
45. Hiroi M, Meunier N, Marion-Poll F, Tanimura T. 2004. Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61:333-42
46. Inoshita T, Tanimura T. 2006. Cellular identification of water gustatory receptor neurons and their central projection pattern in Drosophila. Proc. Natl. Acad. Sci. USA 103:1094-99
47. Itagaki H, Hildebrand JG. 1990. Olfactory interneurons in the brain of the larval sphinx moth Manduca sexta. J. Comp. Physiol. [A] 167:309-20
48. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D. 1997. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:761-71
49. Jallon JM. 1984. A few chemical words exchanged by Drosophila during courtship and mating. Behav. Genet. 14:441-78
50. Joiner WJ, Crocker A, White BH, Sehgal A. 2006. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441:757-60
51. Jones WD, Cayirlioglu P, Kadow IG, Vosshall LB. 2007. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445:86-90
52. Justice RW, Biessmann H, Walter MF, Dimitratos SD, Woods DF. 2003. Genomics spawns novel approaches to mosquito control. Bioessays 25:1011-20
53. Keene AC, Stratmann M, Keller A, Perrat PN, Vosshall LB, Waddell S. 2004. Diverse odorconditioned memories require uniquely timed dorsal paired medial neuron output. Neuron 44:521-33
54. Kondoh Y, Kaneshiro KY, Kimura K, Yamamoto D. 2003. Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc. R. Soc. London B 270:1005-13
55. 2 reception in Drosophila. Proc. Natl. Acad. Sci. USA 104:3574-78
56. Kreher SA, Kwon JY, Carlson JR. 2005. The molecular basis of odor coding in the Drosophila larva. Neuron 46:445-56
57. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF. 1999. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405:543-52
58. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB. 2004. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43:703-14
59. Laurent G. 1996. Odor images and tunes. Neuron 16:473-76
60. Lee T, Lee A, Luo L. 1999. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065-76
61. Lei H, Christensen TA, Hildebrand JG. 2004. Spatial and temporal organization of ensemble representations for different odor classes in the moth antennal lobe. J. Neurosci. 24:11108-19
62. Liu L, Leonard AS, Motto DG, Feller MA, Price MP, et al. 2003a. Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 39:133-46
63. Liu L, Yermolaieva O, Johnson WA, Abboud FM, Welsh MJ. 2003b. Identification and function of thermosensory neurons in Drosophila larvae. Nat. Neurosci. 6:267-73
64. Luo M, Katz LC. 2001. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32:1165-79
65. Malnic B, Hirono J, Sato T, Buck LB. 1999. Combinatorial receptor codes for odors. Cell 96:713-23
66. Manoli DS, Foss M, Villella A, Taylor BJ, Hall JC, Baker BS. 2005. Male-specific fruitless specifies the neural substrates of Drosophila courtship behavior. Nature 436:395-400
67. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K. 2006. Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285-95
68. Marin EC, Jefferis GS, Komiyama T, Zhu H, Luo L. 2002. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243-55
69. Marin EC, Watts RJ, Tanaka NK, Ito K, Luo L. 2005. Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132:725-37
70. Martin JR, Ernst R, Heisenberg M. 1998. Mushroom bodies suppress locomotor activity in Drosophila melanogaster. Leant. Mem. 5:179-91
71. Masuda-Nakagawa LM, Tanaka NK, O'Kane CJ. 2005. Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc. Natl. Acad. Sci. USA 102:19027-32
72. Matsunami H, Amrein H. 2003. Taste and pheromone perception in mammals and flies. Genome Biol. 4:220
73. McKenna M, Monte P, Helfand SL, Woodard C, Carlson J. 1989. A simple chemosensory response in Drosophila and the isolation of acj mutants in which it is affected. Proc. Natl. Acad. Sci. USA 86:8118-22
74. Melcher C, Pankratz MJ. 2005. Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol. 3:e305
75. Mitchell BK, Itagaki H. 1992. Interneurons of the subesophageal ganglion of Sarcophaga bullata responding to gustatory and mechanosensory stimuli. J. Comp. Physiol. [A] 171:213-30
76. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, et al. 1996. Visualizing an olfactory sensory map. Cell 87:675-86
77. Monte P, Woodard C, Ayer R, Lilly M, Sun H, Carlson J. 1989. Characterization of the larval olfactory response in Drosophila and its genetic basis. Behav. Genet. 19:267-83
78. Nakamura M, Baldwin D, Hannaford S, Palka J, Montell C. 2002. Defective proboscis extension response (DPR), a member of the Ig superfamily required for the gustatory response to salt. J. Neurosci. 22:3463-72
79. Nayak S, Singh RN. 1983. Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int. J. Insect. Morphol. Embryol. 12:273-91
80. Nayak S, Singh RN. 1985. Primary sensory projections from the labella to the brain of Drosophila melanogaster. Int. J. Insect. Morphol. Embryol. 14:115-29
81. Neuhaus EM, Gisselmann G, Zhang W, Dooley R, Stortkuhl K, Hatt H. 2004. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat. Neurosci. 8:15-17
82. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenböck G. 2002. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36:463-74
83. Oppliger FY, Guerin PM, Vlimant M. 2000. Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. J. Insect. Physiol. 46:135-44
84. Park SK, Mann KJ, Lin H, Starostina E, Kolski-Andreaco A, Pikielny CW. 2006. A Drosophila protein specific to pheromone-sensing gustatory hairs delays males' copulation attempts. Curr. Biol. 16:1154-59
85. Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, Laurent G. 2002. Oscillations and sparsening of odor representations in the mushroom body. Science 297:359-65
86. Pitman JL, McGill JJ, Keegan KP, Allada R. 2006. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441:753-56
87. Python F, Stocker RF. 2002a. Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J. Comp. Neurol. 445:374-87
88. Python F, Stocker RF. 2002b. Immunoreactivity against choline acetyltransferase, gamma-aminobutyric acid, histamine, octopamine, and serotonin in the larval chemosensory system of Drosophila melanogaster. J. Comp. Neurol. 453:157-67
89. Quinn WG, Harris WA, Benzer S. 1974. Conditioned behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 71:708-12
90. Rajashekhar K, Singh R. 1994. Organization of motor neurons innervating the proboscis musculature in Drosophila melanogaster. Int. J. Insect. Morphol. Embryol. 23:225-42
91. Ramaekers A, Magnenat E, Marin EC, Gendre N, Jefferis GS, et al. 2005. Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr. Biol. 15:982-92
92. Ressler KJ, Sullivan SL, Buck LB. 1994. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79:1245-55
93. Robertson HM, Warr CG, Carlson JR. 2003. Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 100(Suppl. 2):14537-42
94. Rodrigues V. 1980. Olfactory behavior of Drosophila melanogaster. In Development and Neurobiology of Drosophila, ed. O Siddiqi, P Babu, L Hall, JC Hall, pp. 361-71. New York/London: Plenum
95. Rodrigues V, Siddiqi 0.1981. A gustatory mutant of Drosophila defective in pyranose receptors. Mol. Gen. Genet. 181:406-8
96. Sachse S, Galizia CG. 2002. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J. Neurophysiol. 87:1106-17
97. Sakai T, Kitamoto T. 2006. Differential roles of two major brain structures, mushroom bodies and central complex, for Drosophila male courtship behavior. J. Neurobiol. 66:821-34
98. Schröter U, Menzel R. 2003. A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract. J. Comp. Neurol. 465:168-78
99. Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, et al. 2001. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104:661-73
100. Sengupta P, Chou JH, Bargmann CI. 1996. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84:899-909
101. Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M, et al. 2003. Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302:2088-94
102. Shanbhag SR, Müller B, Steinbrecht RA. 1999. Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation and distribution of olfactory sensilla. Int. J. Insect. Morphol. Embryol. 28:377-97
103. Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenbock G. 2007. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128:601-12
104. Sinakevitch I, Strausfeld NJ. 2006. Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J. Comp. Neurol. 494:460-75
105. Stocker RF. 1994. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275:3-26
106. Stocker RF. 2001. Drosophila as a focus in olfactory research: mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression, and central connectivity. Microsc. Res. Tech. 55:284-96
107. Stocker RF. 2007. Design of the larval chemosensory system. In Brain Development in Drosophila, ed. G Technau. Austin, TX: Eureka-Landes Bioscience. In press
108. Stocker RF, Heimbeck G, Gendre N, de Belle JS. 1997. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J. Neurobiol. 32:443-56
109. Stocker RF, Schorderet M. 1981. Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res. 216:513-23
110. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ. 2005. Neural circuitry that governs Drosophila male courtship behavior. Cell 121:795-807
111. Strausfeld NJ, Hildebrand JG. 1999. Olfactory systems: common design, uncommon origins? Curr. Opin. Neurobiol. 9:634-39
112. Strausfeld NJ, Sinakevitch I, Vilinsky I. 2003. The mushroom bodies of Drosophila melanogaster: an immunocytological and Golgi study of Kenyon cell organization in the calyces and lobes. Microsc. Res. Tech. 62:151-69
113. Suh GS, Wong AM, Hergarden AC, Wang JW, Simon AF, et al. 2004. A single population of olfactory sensory neurons mediates an innate avoidance behavior in Drosophila. Nature 431:854-59
114. Takken W, Knols BG. 1999. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu. Rev. Entomol. 44:131-57
115. Tanaka NK, Awasaki T, Shimada T, Ito K. 2004. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14:449-57
116. Thorne N, Chromey C, Bray S, Amrein H. 2004. Taste perception and coding in Drosophila. Curr. Biol. 14:1065-79
117. Tissot M, Gendre N, Stocker RF. 1998. Drosophila P[Gal4] lines reveal that motor neurons involved in feeding persist through metamorphosis. J. Neurobiol. 37:237-50
118. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI. 1995. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83:207-18
119. Ueno K, Ohta M, Morita H, Mikuni Y, Nakajima S, et al. 2001. Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr. Biol. 11:1451-55
120. van der Goes van Naters W, Carlson JR. 2006. Insects as chemosensors of humans and crops. Nature 444:302-7
121. Vassar R, Chao SK, Sitcheran R, Nunez JM, Vosshall LB, Axel R. 1994. Topographic organization of sensory projections to the olfactory bulb. Cell 79:981-91
122. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R. 1999. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725-36
123. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-59
124. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R. 2003. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271-82
125. 2+ imaging. J. Neurosci. 24:6507-14
126. Wang Z, Singhvi A, Kong P, Scott K. 2004b. Taste representations in the Drosophila brain. Cell 117:981-91
127. Wetzel CH, Behrendt HJ, Gisselmann G, Stortkuhl KF, Hovemann B, Hatt H. 2001. Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system. Proc. Natl. Acad. Sci. USA 98:9377-80
128. Wilson RI, Laurent G. 2005. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25:9069-79
129. Wilson RI, Turner GC, Laurent G. 2004. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366-70
130. Wistrand M, Kall L, Sonnhammer EL. 2006. A general model of G protein-coupled receptor sequences and its application to detect remote homologs. Protein Sci. 15:509-21
131. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-41
132. Woodard C, Huang T, Sun H, Helfand SL, Carlson J. 1989. Genetic analysis of olfactory behavior in Drosophila: a new screen yields the ota mutants. Genetics 123:315-26
133. Xu P, Atkinson R, Jones DN, Smith DP. 2005. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45:193-200
134. Yao CA, Ignell R, Carlson JR. 2005. Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J. Neurosci. 25:8359-67
135. Yasuyama K, Meinertzhagen IA, Schürmann FW. 2002. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J. Comp. Neurol. 445:211-26
136. Yu D, Ponomarev A, Davis RL. 2004. Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron 42:437-49
137. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, et al. 2003. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293-301
138. Zou Z, Horowitz LF, Montmayeur JP, Snapper S, Buck LB. 2001. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Nature 414:173-79
139. FlyBrain: An Online Atlas and Database of the Drosophila Nervous System. http://web.neurobio.arizona.edu/Flybrain/html/index.html
140. Hallem EA, Dahanukar A, Carlson JR. 2006. Insect odor and taste receptors. Annu. Rev. Entomol. 51:113-35
141. Hansson BS. 1999. Insect Olfaction. Berlin/New York/Heidelberg: Springer Verlag
142. Strausfeld NJ. 1976. Atlas of an Insect Brain. Berlin/New York/Heidelberg: Springer Verlag
143. Wilson RI, Mainen ZF. 2006. Early events in olfactory processing. Annu. Rev. Neurosci. 29:163-201
144. Wyatt TD. 2003. Pheromones and Animal Behavior: Communication by Smell and Taste. Cambridge, UK: Cambridge Univ. Press