Internal representations of smell in the Drosophila brain

Abstract

Recent advances in sensory neuroscience using Drosophila olfaction as a model system have revealed brain maps representing the external world. Once we understand how the brain’s built-in capability generates the internal olfactory maps, we can then elaborate how the brain computes and makes decision to elicit complex behaviors. Here, we review current progress in mapping Drosophila olfactory circuits and discuss their relationships with innate olfactory behaviors.

This is a preview of subscription content, access via your institution.

References

  1. 1.

    Hildebrand J.G., and Shepherd G.M., Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu. Rev. Neurosci. 20: 595–631, 1997

    PubMed  Article  CAS  Google Scholar 

  2. 2.

    Laurent G., Stopfer M., Friedrich R.W., Rabinovich M.I., Volkovskii A., and Abarbanel H.D., Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu. Rev. Neurosci. 24: 263–297, 2001

    PubMed  Article  CAS  Google Scholar 

  3. 3.

    Lessing D., and Carlson J.R., Chemosensory behavior: the path from stimulus to response. Curr. Opin. Neurobiol. 9(6): 766–771, 1999

    PubMed  Article  CAS  Google Scholar 

  4. 4.

    Mombaerts P., How smell develops. Nat. Neurosci. 4(Suppl): 1192–1198, 2001

    PubMed  Article  CAS  Google Scholar 

  5. 5.

    Vosshall L.B., Olfaction in Drosophila. Curr. Opin. Neurobiol. 10(4): 498–503, 2000

    PubMed  Article  CAS  Google Scholar 

  6. 6.

    Bargmann C.I., Comparative chemosensation from receptors to ecology. Nature 444(7117): 295–301, 2006

    PubMed  Article  CAS  Google Scholar 

  7. 7.

    Davis R.L., Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu. Rev. Neurosci. 28: 275–302, 2005

    PubMed  Article  CAS  Google Scholar 

  8. 8.

    Margulies C., Tully T., and Dubnau J., Deconstructing memory in Drosophila. Curr. Biol. 15(17): 700–713, 2005

    Article  CAS  Google Scholar 

  9. 9.

    Mombaerts P., Seven-transmembrane proteins as odorant and chemosensory receptors. Science 286(5440): 707–711, 1999

    PubMed  Article  CAS  Google Scholar 

  10. 10.

    Barnea G., O’Donnell S., Mancia F., Sun X., Nemes A., Mendelsohn M., and Axel R., Odorant receptors on axon termini in the brain. Science 304(5676): 1468, 2004

    PubMed  Article  CAS  Google Scholar 

  11. 11.

    Dobritsa A.A., van der Goes van Naters W., Warr C.G., Steinbrecht R.A., and Carlson J.R., Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37(5): 827–841, 2003

    PubMed  Article  CAS  Google Scholar 

  12. 12.

    Elmore T., and Smith D.P., Putative Drosophila odor receptor OR43b localizes to dendrites of olfactory neurons. Insect. Biochem. Mol. Biol. 31(8): 791–798, 2001

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Belluscio L., Gold G.H., Nemes A., and Axel R., Mice deficient in G(olf) are anosmic. Neuron 20(1): 69–81, 1998

    PubMed  Article  CAS  Google Scholar 

  14. 14.

    Bozza T., Feinstein P., Zheng C., and Mombaerts P., Odorant receptor expression defines functional units in the mouse olfactory system. J. Neurosci. 22(8): 3033–3043, 2002

    PubMed  CAS  Google Scholar 

  15. 15.

    Vosshall L.B., Amrein H., Morozov P.S., Rzhetsky A., and Axel R., A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96(5): 725–736, 1999

    PubMed  Article  CAS  Google Scholar 

  16. 16.

    Shang Y., Claridge-Chang A., Sjulson L., Pypaert M., and Miesenbock G., Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128(3): 601–612, 2007

    PubMed  Article  CAS  Google Scholar 

  17. 17.

    Hallem E.A., Ho M.G., and Carlson J.R., The molecular basis of odor coding in the Drosophila antenna. Cell 117(7): 965–979, 2004

    PubMed  Article  CAS  Google Scholar 

  18. 18.

    Malnic B., Hirono J., Sato T., and Buck L.B., Combinatorial receptor codes for odors. Cell 96(5): 713–723, 1999

    PubMed  Article  CAS  Google Scholar 

  19. 19.

    Oka Y., Omura M., Kataoka H., and Touhara K., Olfactory receptor antagonism between odorants. EMBO. J. 23(1): 120–126, 2004

    PubMed  Article  CAS  Google Scholar 

  20. 20.

    Wang J.W., Wong A.M., Flores J., Vosshall L.B., and Axel R., Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell. 112(2): 271–282, 2003

    PubMed  Article  CAS  Google Scholar 

  21. 21.

    Benton R., Sachse S., Michnick S.W., and Vosshall L.B., Atypical membrane topology and heteromeric function of Drosophila odorant receptors in␣vivo. PloS. Biol. 4(2): e20, 2006

    PubMed  Article  CAS  Google Scholar 

  22. 22.

    Larsson M.C., Domingos A.I., Jones W.D., Chiappe M.E., Amrein H., and Vosshall L.B., Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43(5): 703–714, 2004

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    Ng M., Roorda R.D., Lima S.Q., Zemelman B.V., Morcillo P., and Miesenbock G., Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36(3): 463–474, 2002

    PubMed  Article  CAS  Google Scholar 

  24. 24.

    Neuhaus E.M., Gisselmann G., Zhang W., Dooley R., Stortkuhl K., and Hatt H., Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat. Neurosci. 8(1): 15–17, 2005

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    Kreher S.A., Kwon J.Y., and Carlson J.R., The molecular basis of odor coding in the Drosophila larva. Neuron 46(3): 445–456, 2005

    PubMed  Article  CAS  Google Scholar 

  26. 26.

    Python F., and Stocker R.F., Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J. Comp. Neurol. 445(4): 374–387, 2002

    PubMed  Article  Google Scholar 

  27. 27.

    Ramaekers A., Magnenat E., Marin E.C., Gendre N., Jefferis G.S., Luo L., and Stocker R.F., Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr. Biol. 15(11): 982–992, 2005

    PubMed  Article  CAS  Google Scholar 

  28. 28.

    Goulding S.E., zur Lage P., and Jarman A.P., Amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge. Neuron 25(1): 69–78, 2000

    PubMed  Article  CAS  Google Scholar 

  29. 29.

    Jhaveri D., Sen A., Reddy G.V., and Rodrigues V., Sense organ identity in the Drosophila antenna is specified by the expression of the proneural gene atonal. Mech. Dev. 99(1–2): 101–111, 2000

    PubMed  Article  CAS  Google Scholar 

  30. 30.

    Stocker R.F., and Gendre N., Peripheral and central nervous effects of lozenge3: a Drosophila mutant lacking basiconic antennal sensilla. Dev. Biol. 127(1): 12–24, 1988

    PubMed  Article  CAS  Google Scholar 

  31. 31.

    zur Lage P.I., Prentice D.R., Holohan E.E., and Jarman A.P., The Drosophila proneural gene amos promotes olfactory sensillum formation and suppresses bristle formation. Development 130(19): 4683–4693, 2003

    PubMed  Article  CAS  Google Scholar 

  32. 32.

    Couto A., Alenius M., and Dickson B.J., Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15(17): 1535–1547, 2005

    PubMed  Article  CAS  Google Scholar 

  33. 33.

    Fishilevich E., and Vosshall L.B., Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15(17): 1548–1553, 2005

    PubMed  Article  CAS  Google Scholar 

  34. 34.

    Jefferis G.S., Insect olfaction: a map of smell in the brain. Curr. Biol. 15(17): 668–670, 2005

    Article  CAS  Google Scholar 

  35. 35.

    Stocker R.F., 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(5): 284–296, 2001

    PubMed  Article  CAS  Google Scholar 

  36. 36.

    Firestein S., How the olfactory system makes sense of scents. Nature 413(6852): 211–218, 2001

    PubMed  Article  CAS  Google Scholar 

  37. 37.

    McCudden C.R., Hains M.D., Kimple R.J., Siderovski D.P., and Willard F.S., G-protein signaling: back to the future. Cell. Mol. Life. Sci. 62(5): 551–577, 2005

    PubMed  Article  CAS  Google Scholar 

  38. 38.

    Xu P., Atkinson R., Jones D.N., and Smith D.P., Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45(2): 193–200, 2005

    PubMed  Article  CAS  Google Scholar 

  39. 39.

    Hallem E.A., and Carlson J.R., Coding of odors by a receptor repertoire. Cell 125(1): 143–160, 2006

    PubMed  Article  CAS  Google Scholar 

  40. 40.

    Hallem E.A., and Carlson J.R., The odor coding system of Drosophila. Trends. Genet. 20(9): 453–459, 2004

    PubMed  Article  CAS  Google Scholar 

  41. 41.

    Clyne P.J., Warr C.G., Freeman M.R., Lessing D., Kim J., and Carlson J.R., A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22(2): 327–338, 1999

    PubMed  Article  CAS  Google Scholar 

  42. 42.

    Gao Q., and Chess A., Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60(1): 31–39, 1999

    PubMed  Article  CAS  Google Scholar 

  43. 43.

    Robertson H.M., Warr C.G., and Carlson J.R., Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 100(2): 14537–14542, 2003

    PubMed  Article  CAS  Google Scholar 

  44. 44.

    Jefferis G.S., Marin E.C., Stocker R.F., and Luo L., Target neuron prespecification in the olfactory map of Drosophila. Nature 414(6860): 204–208, 2001

    PubMed  Article  CAS  Google Scholar 

  45. 45.

    Rodrigues V., Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain. Res. 453(1–2): 299–307, 1988

    PubMed  Article  CAS  Google Scholar 

  46. 46.

    Rodrigues V., and Buchner E., [3H]2-deoxyglucose mapping of odor-induced neuronal activity in the antennal lobes of Drosophila melanogaster. Brain. Res. 324(2): 374–378, 1984

    PubMed  Article  CAS  Google Scholar 

  47. 47.

    Laissue P.P., Reiter C., Hiesinger P.R., Halter S., Fischbach K.F., and Stocker R.F., Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405(4): 543–552, 1999

    PubMed  Article  CAS  Google Scholar 

  48. 48.

    Stocker R.F., The organization of the chemosensory system in Drosophila melanogaster: a review. Cell. Tissue. Res. 275(1): 3–26, 1994

    PubMed  Article  CAS  Google Scholar 

  49. 49.

    Wilson R.I., and Laurent G., Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J. Neurosci. 25(40): 9069–9079, 2005

    PubMed  Article  CAS  Google Scholar 

  50. 50.

    Wilson R.I., Turner G.C., and Laurent G., Transformation of olfactory representations in the Drosophila antennal lobe. Science 303(5656): 366–370, 2004

    PubMed  Article  CAS  Google Scholar 

  51. 51.

    Marin E.C., Jefferis G.S., Komiyama T., Zhu H., and Luo L., Representation of the glomerular olfactory map in the Drosophila brain. Cell 109(2): 243–255, 2002

    PubMed  Article  CAS  Google Scholar 

  52. 52.

    Wong A.M., Wang J.W., and Axel R., Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109(2): 229–241, 2002

    PubMed  Article  CAS  Google Scholar 

  53. 53.

    Tanaka N.K., Awasaki T., Shimada T., and Ito K., Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr. Biol. 14(6): 449–457, 2004

    PubMed  Article  CAS  Google Scholar 

  54. 54.

    Heisenberg M., Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4(4): 266–275, 2003

    PubMed  Article  CAS  Google Scholar 

  55. 55.

    Technau G., and Heisenberg M., Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295(5848): 405–407, 1982

    PubMed  Article  CAS  Google Scholar 

  56. 56.

    Ito K., Awano W., Suzuki K., Hiromi Y., and Yamamoto D., The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurons and glial cells. Development 124(4): 761–771, 1997

    PubMed  CAS  Google Scholar 

  57. 57.

    Lee T., Lee A., and Luo L., Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126(18): 4065–4076, 1999

    PubMed  CAS  Google Scholar 

  58. 58.

    Zhu S., Chiang A.S., and Lee T., Development of the Drosophila mushroom bodies: elaboration, remodeling and spatial organization of dendrites in the calyx. Development 130(12): 2603–2610, 2003

    PubMed  Article  CAS  Google Scholar 

  59. 59.

    Crittenden J.R., Skoulakis E.M., Han KA., Kalderon D., and Davis R.L., Tripartite mushroom body architecture revealed by antigenic markers. Learn. Mem. 5(1–2): 38–51, 1998

    PubMed  CAS  Google Scholar 

  60. 60.

    Yu D., Ponomarev A., and Davis R.L., Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron 42(3): 437–449, 2004

    PubMed  Article  CAS  Google Scholar 

  61. 61.

    Wang Y., Guo H.F., Pologruto T.A., Hannan F., Hakker I., Svoboda K., and Zhong Y., Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging. J. Neurosci. 24(29): 6507–6514, 2004

    PubMed  Article  CAS  Google Scholar 

  62. 62.

    Lai S.L., and Lee T., Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9(5): 703–709, 2006

    PubMed  Article  CAS  Google Scholar 

  63. 63.

    Stopfer M., Olfactory coding: inhibition reshapes odor responses. Curr. Biol. 15(24): 996–998, 2005

    Article  CAS  Google Scholar 

  64. 64.

    Suh G.S., Wong A.M., Hergarden A.C., Wang J.W., Simon A.F., Benzer S., Axel R., and Anderson D.J., A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431(7010): 854–859, 2004

    PubMed  Article  CAS  Google Scholar 

  65. 65.

    Jones W.D., Cayirlioglu P., Kadow I.G., and Vosshall L.B., Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445(7123): 86–90, 2007

    PubMed  Article  CAS  Google Scholar 

  66. 66.

    Wang Y., Chiang A.S., Xia S., Kitamoto T., Tully T., and Zhong Y., Blockade of neurotransmission in Drosophila mushroom bodies impairs odor attraction, but not repulsion. Curr. Biol. 13(21): 1900–1904, 2003

    PubMed  Article  CAS  Google Scholar 

  67. 67.

    Billeter J.C., Rideout E.J., Dornan A.J., and Goodwin S.F., Control of male sexual behavior in Drosophila by the sex determination pathway. Curr. Biol. 16(17): 766–776, 2006

    Article  CAS  Google Scholar 

  68. 68.

    Stockinger P., Kvitsiani D., Rotkopf S., Tirian L., and Dickson B.J., Neural circuitry that governs Drosophila male courtship behavior. Cell 121(5): 795–807, 2005

    PubMed  Article  CAS  Google Scholar 

  69. 69.

    Manoli D.S., Foss M., Villella A., Taylor B.J., Hall J.C., and Baker B.S., Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436(7049): 395–400, 2005

    PubMed  CAS  Google Scholar 

  70. 70.

    Vrontou E., Nilsen S.P., Demir E., Kravitz E.A., and Dickson B.J., fruitless regulates aggression and dominance in Drosophila. Nat. Neurosci. 9(12): 1469–1471, 2006

    PubMed  Article  CAS  Google Scholar 

  71. 71.

    Choi G.B., Dong H.W., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Swanson L.W., and Anderson D.J., Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46(4): 647–660, 2005

    PubMed  Article  CAS  Google Scholar 

  72. 72.

    Stowers L., Holy T.E., Meister M., Dulac C., and Koentges G., Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295(5559): 1493–1500, 2002

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Drs. Chang-Huain Hsieh and Hsiu-Ming Chang for critical reading and discussion. This work was supported by grants from National Science Council, Brain Research Center of the University System of Taiwan, and the National Center for High-performance Computing.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ann-Shyn Chiang.

Additional information

Hui-Hao lin and Chih-Yung Lin contributed equally to this work.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lin, HH., Lin, CY. & Chiang, AS. Internal representations of smell in the Drosophila brain. J Biomed Sci 14, 453–459 (2007). https://doi.org/10.1007/s11373-007-9168-0

Download citation

Keywords

  • Drosophila
  • Brain circuit
  • Olfaction
  • Mushroom body
  • Map