The Olfactory Sensory Map in Drosophila

  • Philippe P. Laissue
  • Leslie B. Vosshall
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 628)


The fruit fly (Drosophila melanogaster) exhibits robust odor-evoked behaviors in response to cues from diverse host plants and pheromonal cues from other flies. Understanding how the adult olfactory system supports the perception of these odorous chemicals and translates them into appropriate attraction or avoidance behaviors is an important goal in contemporary sensory neuroscience. Recent advances in genomics and molecular neurobiology have provided an unprecedented level of detail into how the adult Drosophila olfactory system is organized. Volatile odorants are sensed by two bilaterally symmetric olfactory sensory appendages, the third segment of the antenna and the maxillary palps, which respectively contain approximately 1200 and 120 olfactory sensory neurons (OSNs) each. These OSNs express a divergent family of seven transmembrane domain odorant receptors (ORs) with no homology to vertebrate ORs, which determine the odor specificity of a given OSN. Drosophila was the first animal for which all OR genes were cloned, their patterns of gene expression determined and axonal projections of most OSNs elucidated. In vivo electrophysiology has been used to decode the ligand response profiles of most of the ORs, providing insight into the initial logic of olfactory coding in the fly. This chapter will review the molecular biology, neuroanatomy and function of the peripheral olfactory system of Drosophila.


Olfactory System Antennal Lobe Odorant Receptor Maxillary Palp Olfactory Sensory Neuron 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Roskies A, Friedman GC, O’Leary DD. Mechanisms and molecules controlling the development of retinal maps. Perspect Dev Neurobiol 1995; 3(1):63–75.PubMedGoogle Scholar
  2. 2.
    Schieber MH. Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol 2001; 86(5):2125–2143.PubMedGoogle Scholar
  3. 3.
    Frostig RD. Functional organization and plasticity in the adult rat barrel cortex: moving out-of-the-box. Curr Opin Neurobiol 2006; 16(4):445–450.PubMedCrossRefGoogle Scholar
  4. 4.
    Shamma SA. Topographic organization is essential for pitch perception. Proc Natl Acad Sci USA 2004; 101(5):1114–1115.PubMedCrossRefGoogle Scholar
  5. 5.
    Rubsamen R. Postnatal development of central auditory frequency maps. J Comp Physiol [A] 1992; 170(2):129–143.Google Scholar
  6. 6.
    Dethier VG. The Hungry Fly: A Physiological Study of the Behavior Associated with Feeding. Cambridge: Harvard University Press, 1976.Google Scholar
  7. 7.
    Arora K, Rodrigues V, Joshi S et al. A gene affecting the specificity of the chemosensory neurons of Drosophila. Nature 1987; 330(6143):62–63.PubMedCrossRefGoogle Scholar
  8. 8.
    Zhang Y, Hoon MA, Chandrashekar J et al. Coding of sweet, bitter and umami tastes: different receptor cells sharing similar signaling pathways. Cell 2003; 112(3):293–301.PubMedCrossRefGoogle Scholar
  9. 9.
    Marella S, Fischler W, Kong P et al. Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 2006; 49(2):285–295.PubMedCrossRefGoogle Scholar
  10. 10.
    Wang Z, Singhvi A, Kong P et al. Taste representations in the Drosophila brain. Cell 2004; 117(7):981–991.PubMedCrossRefGoogle Scholar
  11. 11.
    Thorne N, Chromey C, Bray S et al. Taste perception and coding in Drosophila. Curr Biol 2004; 14(12):1065–1079.PubMedCrossRefGoogle Scholar
  12. 12.
    Jones LM, Fontanini A, Katz DB. Gustatory processing: a dynamic systems approach. Curr Opin Neurobiol 2006; 16(4):420–428.PubMedCrossRefGoogle Scholar
  13. 13.
    Glendinning JI, Davis A, Rai M. Temporal coding mediates discrimination of “bitter” taste stimuli by an insect. J Neurosci 2006; 26(35):8900–8908.PubMedCrossRefGoogle Scholar
  14. 14.
    Firestein S. How the olfactory system makes sense of scents. Nature 2001; 413(6852):211–218.PubMedCrossRefGoogle Scholar
  15. 15.
    Araneda RC, Kini AD, Firestein S. The molecular receptive range of an odorant receptor. Nat Neurosci 2000; 3(12):1248–1255.PubMedCrossRefGoogle Scholar
  16. 16.
    Malnic B, Hirono J, Sato T et al. Combinatorial receptor codes for odors. Cell 1999; 96(5):713–723.PubMedCrossRefGoogle Scholar
  17. 17.
    Hallem EA, Ho MG, Carlson JR. The molecular basis of odor coding in the Drosophila antenna. Cell 2004; 117(7):965–979.PubMedCrossRefGoogle Scholar
  18. 18.
    Katada S, Hirokawa T, Oka Y et al. Structural basis for a broad but selective ligand spectrum of a mouse olfactory receptor: mapping the odorant-binding site. J Neurosci 2005; 25(7):1806–1815.PubMedCrossRefGoogle Scholar
  19. 19.
    Hildebrand JG, Shepherd GM. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 1997; 20:595–631.PubMedCrossRefGoogle Scholar
  20. 20.
    Strausfeld NJ, Hildebrand JG. Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 1999; 9(5):634–639.PubMedCrossRefGoogle Scholar
  21. 21.
    Gao Q, Yuan B, Chess A. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 2000; 3(8):780–785.PubMedCrossRefGoogle Scholar
  22. 22.
    Mombaerts P, Wang F, Dulac C et al. Visualizing an olfactory sensory map. Cell 1996; 87(4):675–686.PubMedCrossRefGoogle Scholar
  23. 23.
    Ressler KJ, Sullivan SL, Buck LB. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 1994; 79(7):1245–1255.PubMedCrossRefGoogle Scholar
  24. 24.
    Vassar R, Chao SK, Sitcheran R et al. Topographic organization of sensory projections to the olfactory bulb. Cell 1994; 79(6):981–991.PubMedCrossRefGoogle Scholar
  25. 25.
    Vosshall LB, Wong AM, Axel R. An olfactory sensory map in the fly brain. Cell 2000; 102:147–159.PubMedCrossRefGoogle Scholar
  26. 26.
    Uchida N, Takahashi YK, Tanifuji M et al. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat Neurosci 2000; 3(10):1035–1043.PubMedCrossRefGoogle Scholar
  27. 27.
    Mori K, Nagao H, Yoshihara Y. The olfactory bulb: coding and processing of odor molecule information. Science 1999; 286(5440):711–715.PubMedCrossRefGoogle Scholar
  28. 28.
    Friedrich RW, Korsching SI. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 1997; 18(5):737–752.PubMedCrossRefGoogle Scholar
  29. 29.
    Couto A, Alenius M, Dickson BJ. Molecular, anatomical and functional organization of the Drosophila olfactory system. Curr Biol 2005; 15(17):1535–1547.PubMedCrossRefGoogle Scholar
  30. 30.
    Fishilevich E, Vosshall LB. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 2005; 15(17):1548–1553.PubMedCrossRefGoogle Scholar
  31. 31.
    Galizia CG, Sachse S, Rappert A et al. The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 1999; 2(5):473–478.PubMedCrossRefGoogle Scholar
  32. 32.
    Hallem EA, Carlson JR. Coding of odors by a receptor repertoire. Cell 2006; 125(1):143–160.PubMedCrossRefGoogle Scholar
  33. 33.
    Stocker RF. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 1994; 275(1):3–26.PubMedCrossRefGoogle Scholar
  34. 34.
    Clyne P, Grant A, O’Connell R et al. Odorant response of individual sensilla on the Drosophila antenna. Invert Neurosci 1997; 3:127–135.PubMedCrossRefGoogle Scholar
  35. 35.
    Shanbhag SR, Mueller B, Steinbrecht RA. Atlas of olfactory organs of Drosophila melanogaster. 2. Internal organization and cellular architecture of olfactory sensilla. Arthr Struct Dev 2000; 29:211–229.CrossRefGoogle Scholar
  36. 36.
    Shanbhag SR, Mueller B, Steinbrecht RA. Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation and distribution of olfactory sensilla. Int J Insect Morphol Embryol 1999; 28(4):377–397.CrossRefGoogle Scholar
  37. 37.
    Reddy GV, Gupta B, Ray K et al. Development of the Drosophila olfactory sense organs utilizes cell-cell interactions as well as lineage. Development 1997; 124(3):703–712.PubMedGoogle Scholar
  38. 38.
    Gupta BP, Rodrigues V. Atonal is a proneural gene for a subset of olfactory sense organs in Drosophila. Genes Cells 1997; 2(3):225–233.PubMedCrossRefGoogle Scholar
  39. 39.
    Sen A, Reddy GV, Rodrigues V. Combinatorial expression of Prospero, Seven-up and Elav identifies progenitor cell types during sense-organ differentiation in the Drosophila antenna. Dev Biol 2003; 254(1):79–92.PubMedCrossRefGoogle Scholar
  40. 40.
    Goulding SE, zur Lage P, Jarman AP. amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge. Neuron 2000; 25:69–78.PubMedCrossRefGoogle Scholar
  41. 41.
    Buck L, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 1991; 65(1):175–187.PubMedCrossRefGoogle Scholar
  42. 42.
    Vosshall LB, Amrein H, Morozov PS et al. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 1999; 96(5):725–736.PubMedCrossRefGoogle Scholar
  43. 43.
    Clyne PJ, Warr CG, Freeman MR et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 1999; 22(2):327–338.PubMedCrossRefGoogle Scholar
  44. 44.
    Gao Q, Chess A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 1999; 60(1):31–39.PubMedCrossRefGoogle Scholar
  45. 45.
    Robertson HM, Warr CG, Carlson JR. Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 2003; 100Suppl 2:14537–14542.PubMedCrossRefGoogle Scholar
  46. 46.
    Benton R, Sachse S, Michnick SW et al. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 2006; 4(2):e20.PubMedCrossRefGoogle Scholar
  47. 47.
    Wistrand M, Kall L, Sonnhammer EL. A general model of G protein-coupled receptor sequences and its application to detect remote homologs. Protein Sci 2006; 15(3):509–521.PubMedCrossRefGoogle Scholar
  48. 48.
    Fishilevich E, Domingos AI, Asahina K et al. Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr Biol 2005; 15(23):2086–2096.PubMedCrossRefGoogle Scholar
  49. 49.
    Kreher SA, Kwon JY, Carlson JR. The molecular basis of odor coding in the Drosophila larva. Neuron 2005; 46:445–456.PubMedCrossRefGoogle Scholar
  50. 50.
    Resslcr KJ, Sullivan SL, Buck LB. A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 1993; 73(3):597–609.CrossRefGoogle Scholar
  51. 51.
    Vassar R, Ngai J, Axel R. Spatial segregation of odorant receptor expression in the mammalian olfactory epithelium. Cell 1993; 74(2):309–318.PubMedCrossRefGoogle Scholar
  52. 52.
    Bhalerao S, Sen A, Stocker R et al. Olfactory neurons expressing identified receptor genes project to subsets of glomeruli within the antennal lobe of Drosophila melanogaster. J Neurobiol 2003; 54(4):577–592.PubMedCrossRefGoogle Scholar
  53. 53.
    Serizawa S, Miyamichi K, Nakatani H et al. Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 2003; 302(5653):2088–2094.PubMedCrossRefGoogle Scholar
  54. 54.
    Larsson MC, Domingos AI, Jones WD et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 2004; 43:703–714.PubMedCrossRefGoogle Scholar
  55. 55.
    Neuhaus EM, Gisselmann G, Zhang W et al. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 2004; 8:15–17.PubMedCrossRefGoogle Scholar
  56. 56.
    Goldman AL, Van der Goes van Naters W, Lessing D et al. Coexpression of two functional odor receptors in one neuron. Neuron 2005; 45(5):661–666.PubMedCrossRefGoogle Scholar
  57. 57.
    de Bruyne M, Clyne PJ, Carlson JR. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 1999; 19(11):4520–4532.PubMedGoogle Scholar
  58. 58.
    de Bruyne M, Foster K, Carlson JR. Odor coding in the Drosophila antenna. Neuron 2001; 30(2):537–552.PubMedCrossRefGoogle Scholar
  59. 59.
    Yao CA, Ignell R, Carlson JR. Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 2005; 25(37):8359–8367.PubMedCrossRefGoogle Scholar
  60. 60.
    Ha TS, Smith DP. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci 2006; 26(34):8727–8733.PubMedCrossRefGoogle Scholar
  61. 61.
    Kondoh Y, Kaneshiro KY, Kimura K et al. Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc R Soc Lond B 2003; 270(1519):1005–1013.CrossRefGoogle Scholar
  62. 62.
    Manoli DS, Foss M, Villella A et al. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 2005; 436:395–400.PubMedGoogle Scholar
  63. 63.
    Stockinger P, Kvitsiani D, Rotkopf S et al. Neural circuitry that governs Drosophila male courtship behavior. Cell 2005; 121(5):795–807.PubMedCrossRefGoogle Scholar
  64. 64.
    Dobritsa AA, van der Goes van Naters W, Warr CG et al. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 2003; 37(5):827–841.PubMedCrossRefGoogle Scholar
  65. 65.
    Suh GS, Wong AM, Hergarden AC et al. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 2004; 431(7010):854–859.PubMedCrossRefGoogle Scholar
  66. 66.
    Scott K, Brady R, Jr., Cravchik A et al. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 2001; 104(5):661–673.PubMedCrossRefGoogle Scholar
  67. 67.
    Jones WD, Cayirlioglu P, Kadow IG et al. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 2007; 445:86–90.PubMedCrossRefGoogle Scholar
  68. 68.
    Laissue PP, Reiter C, Hiesinger PR et al. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 1999; 405(4):543–552.PubMedCrossRefGoogle Scholar
  69. 69.
    Sachse S, Galizia CG. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: A calcium imaging study. J Neurophysiol 2002; 87:1106–1117.PubMedGoogle Scholar
  70. 70.
    Wilson RI, Mainen ZF. Early events in olfactory processing. Annu Rev Neurosci 2006; 29:163–201.PubMedCrossRefGoogle Scholar
  71. 71.
    Fiala A, Spall T, Diegelmann S et al. Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr Biol 2002; 12(21):1877–1884.PubMedCrossRefGoogle Scholar
  72. 72.
    Ng M, Roorda RD, Lima SQ et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 2002; 36(3):463–474.PubMedCrossRefGoogle Scholar
  73. 73.
    Wang JW, Wong AM, Flores J et al. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 2003; 112(2):271–282.PubMedCrossRefGoogle Scholar
  74. 74.
    Wilson RI, Laurent G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 2005; 25(40):9069–9079.PubMedCrossRefGoogle Scholar
  75. 75.
    Wilson RI, Turner GC, Laurent G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 2004; 303(5656):366–370.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  • Philippe P. Laissue
    • 1
  • Leslie B. Vosshall
    • 2
  1. 1.Kent Institute of Medicine and Health Sciences, Medical Image ComputingUniversity of Kent CanterburyKentUK
  2. 2.Laboratory of Neurogenetics and BehaviorThe Rockefeller UniversityNew YorkUSA

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