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Science China Life Sciences

, Volume 53, Issue 4, pp 472–484 | Cite as

The olfactory circuit of the fruit fly Drosophila melanogaster

  • Liang Liang
  • Liqun LuoEmail author
CUSBEA Article Series Review

Abstract

The olfactory circuit of the fruit fly Drosophila melanogaster has emerged in recent years as an excellent paradigm for studying the principles and mechanisms of information processing in neuronal circuits. We discuss here the organizational principles of the olfactory circuit that make it an attractive model for experimental manipulations, the lessons that have been learned, and future challenges.

Keywords

olfactory receptor neurons projection neurons local interneurons antennal lobe mushroom body lateral horn behavior information processing 

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References

  1. 1.
    Luo L, Callaway E M, Svoboda K. Genetic dissection of neural circuits. Neuron, 2008, 57: 634–660 18341986, 10.1016/j.neuron.2008.01.002, 1:CAS:528:DC%2BD1cXjslegt70%3DPubMedPubMedCentralGoogle Scholar
  2. 2.
    Su C Y, Menuz K, Carlson J R. Olfactory perception: receptors, cells, and circuits. Cell, 2009, 139: 45–59 19804753, 10.1016/j.cell.2009.09.015, 1:CAS:528:DC%2BD1MXhsVCjs7jIPubMedPubMedCentralGoogle Scholar
  3. 3.
    Vosshall L B, Stocker R F. Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci, 2007, 30: 505–533 17506643, 10.1146/annurev.neuro.30.051606.094306, 1:CAS:528:DC%2BD2sXptFKnu78%3DPubMedGoogle Scholar
  4. 4.
    Vosshall L B, Amrein H, Morozov P S, et al. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell, 1999, 96: 725–736 10089887, 10.1016/S0092-8674(00)80582-6, 1:CAS:528:DyaK1MXitVChs7o%3DPubMedGoogle Scholar
  5. 5.
    Clyne P J, Warr C G, Freeman M R, et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron, 1999, 22: 327–338 10069338, 10.1016/S0896-6273(00)81093-4, 1:CAS:528:DyaK1MXhs12ksrY%3DPubMedGoogle Scholar
  6. 6.
    Gao Q, Chess A. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics, 1999, 60: 31–39 10458908, 10.1006/geno.1999.5894, 1:CAS:528:DyaK1MXltlShsb4%3DPubMedGoogle Scholar
  7. 7.
    Larsson M C, Domingos A I, Jones W D, et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron, 2004, 43: 703–714 15339651, 10.1016/j.neuron.2004.08.019, 1:CAS:528:DC%2BD2cXns1yms7s%3DPubMedGoogle Scholar
  8. 8.
    Couto A, Alenius M, Dickson B J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol, 2005, 15: 1535–1547 16139208, 10.1016/j.cub.2005.07.034, 1:CAS:528:DC%2BD2MXpslyit7Y%3DPubMedGoogle Scholar
  9. 9.
    Jones W D, Cayirlioglu P, Kadow I G, et al. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature, 2007, 445: 86–90 17167414, 10.1038/nature05466, 1:CAS:528:DC%2BD2sXhsFOltA%3D%3DPubMedGoogle Scholar
  10. 10.
    Kwon J Y, Dahanukar A, Weiss L A, et al. The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci USA, 2007, 104: 3574–3578 17360684, 10.1073/pnas.0700079104, 1:CAS:528:DC%2BD2sXjtVWktLk%3DPubMedPubMedCentralGoogle Scholar
  11. 11.
    Fishilevich E, Vosshall L B. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol, 2005, 15: 1548–1553 16139209, 10.1016/j.cub.2005.07.066, 1:CAS:528:DC%2BD2MXpslyit7c%3DPubMedGoogle Scholar
  12. 12.
    Kreher S A, Kwon J Y, Carlson J R. The molecular basis of odor coding in the Drosophila larva. Neuron, 2005, 46: 445–456 15882644, 10.1016/j.neuron.2005.04.007, 1:CAS:528:DC%2BD2MXksFKmur4%3DPubMedGoogle Scholar
  13. 13.
    Dobritsa A A, van der Goes van Naters W, Warr C G, et al. Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron, 2003, 37: 827–841 12628173, 10.1016/S0896-6273(03)00094-1, 1:CAS:528:DC%2BD3sXitlSrsLc%3DPubMedGoogle Scholar
  14. 14.
    Hallem E A, Ho M G, Carlson J R. The molecular basis of odor coding in the Drosophila antenna. Cell, 2004, 117: 965–979 15210116, 10.1016/j.cell.2004.05.012, 1:CAS:528:DC%2BD2cXlsFWnu7s%3DPubMedGoogle Scholar
  15. 15.
    Hallem E A, Carlson J R. Coding of odors by a receptor repertoire. Cell, 2006, 125: 143–160 16615896, 10.1016/j.cell.2006.01.050, 1:CAS:528:DC%2BD28Xjsl2jsb8%3DPubMedGoogle Scholar
  16. 16.
    Goldman A L, Van der Goes van Naters W, Lessing D, et al. Coexpression of two functional odor receptors in one neuron. Neuron, 2005, 45: 661–666 15748842, 10.1016/j.neuron.2005.01.025, 1:CAS:528:DC%2BD2MXis1yrs70%3DPubMedGoogle Scholar
  17. 17.
    de Bruyne M, Clyne P J, Carlson J R. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci, 1999, 19: 4520–4532 10341252PubMedGoogle Scholar
  18. 18.
    de Bruyne M, Foster K, Carlson J R. Odor coding in the Drosophila antenna. Neuron, 2001, 30: 537–552 11395013, 10.1016/S0896-6273(01)00289-6PubMedGoogle Scholar
  19. 19.
    Yao C A, Ignell R, Carlson J R. Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci, 2005, 25: 8359–8367 16162917, 10.1523/JNEUROSCI.2432-05.2005, 1:CAS:528:DC%2BD2MXhtVert7nOPubMedGoogle Scholar
  20. 20.
    van der Goes van Naters W, Carlson J R. Receptors and neurons for fly odors in Drosophila. Curr Biol, 2007, 17: 606–612 17363256, 10.1016/j.cub.2007.02.043, 1:CAS:528:DC%2BD2sXjslGnu70%3DPubMedPubMedCentralGoogle Scholar
  21. 21.
    Kurtovic A, Widmer A, Dickson B J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature, 2007, 446: 542–546 17392786, 10.1038/nature05672, 1:CAS:528:DC%2BD2sXjsV2itbY%3DPubMedGoogle Scholar
  22. 22.
    Ha T S, Smith D P. A pheromone receptor mediates 11-cis-vaccenyl acetate-induced responses in Drosophila. J Neurosci, 2006, 26: 8727–8733 16928861, 10.1523/JNEUROSCI.0876-06.2006, 1:CAS:528:DC%2BD28Xpt1Srsr0%3DPubMedGoogle Scholar
  23. 23.
    Xu P, Atkinson R, Jones D N, et al. Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron, 2005, 45: 193–200 15664171, 10.1016/j.neuron.2004.12.031, 1:CAS:528:DC%2BD2MXhtFOrt7w%3DPubMedGoogle Scholar
  24. 24.
    Benton R, Vannice K S, Vosshall L B. An essential role for a CD36-related receptor in pheromone detection in Drosophila. Nature, 2007, 450: 289–293 17943085, 10.1038/nature06328, 1:CAS:528:DC%2BD2sXht1yntrvJPubMedGoogle Scholar
  25. 25.
    Jin X, Ha T S, Smith D P. SNMP is a signaling component required for pheromone sensitivity in Drosophila. Proc Natl Acad Sci USA, 2008, 105: 10996–11001 18653762, 10.1073/pnas.0803309105PubMedPubMedCentralGoogle Scholar
  26. 26.
    Laughlin J D, Ha T S, Jones D N, et al. Activation of pheromone-sensitive neurons is mediated by conformational activation of pheromone-binding protein. Cell, 2008, 133: 1255–1265 18585358, 10.1016/j.cell.2008.04.046, 1:CAS:528:DC%2BD1cXosFWrsro%3DPubMedPubMedCentralGoogle Scholar
  27. 27.
    Laissue P P, Reiter C, Hiesinger P R, et al. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol, 1999, 405: 543–552 10098944, 10.1002/(SICI)1096-9861(19990322)405:4<543::AID-CNE7>3.0.CO;2-A, 1:STN:280:DyaK1M7ps1Grsg%3D%3DPubMedGoogle Scholar
  28. 28.
    Vosshall L B, Wong A M, Axel R. An olfactory sensory map in the fly brain. Cell, 2000, 102: 147–159 10943836, 10.1016/S0092-8674(00)00021-0, 1:CAS:528:DC%2BD3cXltl2hsrw%3DPubMedGoogle Scholar
  29. 29.
    Gao Q, Yuan B, Chess A. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nature Neurosci, 2000, 3: 780–785 10903570, 10.1038/75753, 1:CAS:528:DC%2BD3cXlsVOls7o%3DPubMedGoogle Scholar
  30. 30.
    Benton R, Vannice K S, Gomez-Diaz C, et al. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell, 2009, 136: 149–162 19135896, 10.1016/j.cell.2008.12.001, 1:CAS:528:DC%2BD1MXhtFOitrw%3DPubMedPubMedCentralGoogle Scholar
  31. 31.
    Scott K, Brady R Jr., Cravchik A, et al. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell, 2001, 104: 661–673 11257221, 10.1016/S0092-8674(01)00263-X, 1:CAS:528:DC%2BD3MXitFaktbk%3DPubMedGoogle Scholar
  32. 32.
    Stocker R F, Lienhard M C, Borst A, et al. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res, 1990, 262: 9–34 2124174, 10.1007/BF00327741, 1:STN:280:DyaK3M%2Fnsl2isQ%3D%3DPubMedGoogle Scholar
  33. 33.
    Stocker R F, Heimbeck G, Gendre N, et al. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol, 1997, 32: 443–456 9110257, 10.1002/(SICI)1097-4695(199705)32:5<443::AID-NEU1>3.0.CO;2-5, 1:CAS:528:DyaK2sXivVGmtrs%3DPubMedGoogle Scholar
  34. 34.
    Jefferis G S X E, Marin E C, Stocker R F, et al. Target neuron prespecification in the olfactory map of Drosophila. Nature, 2001, 414: 204–208 11719930, 10.1038/35102574, 1:CAS:528:DC%2BD3MXosFahsrY%3DPubMedGoogle Scholar
  35. 35.
    Marin E C, Jefferis G S X E, Komiyama T, et al. Representation of the glomerular olfactory map in the Drosophila brain. Cell, 2002, 109: 243–255 12007410, 10.1016/S0092-8674(02)00700-6, 1:CAS:528:DC%2BD38Xjt1ektbo%3DPubMedGoogle Scholar
  36. 36.
    Wong A M, Wang J W, Axel R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell, 2002, 109: 229–241 12007409, 10.1016/S0092-8674(02)00707-9, 1:CAS:528:DC%2BD38Xjt1ektb0%3DPubMedGoogle Scholar
  37. 37.
    Jefferis G S, Potter C J, Chan A M, et al. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell, 2007, 128: 1187–1203 17382886, 10.1016/j.cell.2007.01.040, 1:CAS:528:DC%2BD2sXkslGms7c%3DPubMedPubMedCentralGoogle Scholar
  38. 38.
    Lai S L, Awasaki T, Ito K, et al. Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development, 2008, 135: 2883–2893 18653555, 10.1242/dev.024380, 1:CAS:528:DC%2BD1cXht1Sns7bPPubMedGoogle Scholar
  39. 39.
    Tanaka N K, Tanimoto H, Ito K. Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol, 2008, 508: 711–755 18395827, 10.1002/cne.21692PubMedGoogle Scholar
  40. 40.
    Wilson R I, Laurent G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci, 2005, 25: 9069–9079 16207866, 10.1523/JNEUROSCI.2070-05.2005, 1:CAS:528:DC%2BD2MXhtFGktr3MPubMedGoogle Scholar
  41. 41.
    Shang Y, Claridge-Chang A, Sjulson L, et al. Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell, 2007, 128: 601–612 17289577, 10.1016/j.cell.2006.12.034, 1:CAS:528:DC%2BD2sXit1WltLk%3DPubMedPubMedCentralGoogle Scholar
  42. 42.
    Ng M, Roorda R D, Lima S Q, et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron, 2002, 36: 463–474 12408848, 10.1016/S0896-6273(02)00975-3, 1:CAS:528:DC%2BD38XosV2htLo%3DPubMedGoogle Scholar
  43. 43.
    Das A, Sen S, Lichtneckert R, et al. Drosophila olfactory local interneurons and projection neurons derive from a common neuroblast lineage specified by the empty spiracles gene. Neural Develop, 2008, 3: 33 10.1186/1749-8104-3-33, 1:CAS:528:DC%2BD1cXhsFCntrfKGoogle Scholar
  44. 44.
    Okada R, Awasaki T, Ito K. Gamma-aminobuyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe. J Comp Neurol, 2009, 514: 74–91 19260068, 10.1002/cne.21971, 1:CAS:528:DC%2BD1MXkvVWktLs%3DPubMedGoogle Scholar
  45. 45.
    Chou Y H, Spletter M L, Yaksi E, et al. Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci, 2010, 13: 439–449 20139975, 10.1038/nn.2489, 1:CAS:528:DC%2BC3cXhs1Olsbs%3DPubMedPubMedCentralGoogle Scholar
  46. 46.
    Olsen S R, Wilson R I. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature, 2008, 452: 956–960 18344978, 10.1038/nature06864, 1:CAS:528:DC%2BD1cXltVGrt7c%3DPubMedPubMedCentralGoogle Scholar
  47. 47.
    Root C M, Masuyama K, Green D S, et al. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron, 2008, 59: 311–321 18667158, 10.1016/j.neuron.2008.07.003, 1:CAS:528:DC%2BD1cXpsFOgt7s%3DPubMedPubMedCentralGoogle Scholar
  48. 48.
    Yasuyama K, Meinertzhagen I A, Schurmann F W. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol, 2002, 445: 211–226 11920702, 10.1002/cne.10155PubMedGoogle Scholar
  49. 49.
    Yasuyama K, Meinertzhagen I A, Schurmann F W. Synaptic connections of cholinergic antennal lobe relay neurons innervating the lateral horn neuropile in the brain of Drosophila melanogaster. J Comp Neurol, 2003, 466: 299–315 14556288, 10.1002/cne.10867PubMedGoogle Scholar
  50. 50.
    Tanaka N K, Awasaki T, Shimada T. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol, 2004, 14: 449–457 15043809, 10.1016/j.cub.2004.03.006, 1:CAS:528:DC%2BD2cXis1Wnu78%3DPubMedGoogle Scholar
  51. 51.
    Lin H H, Lai J S, Chin A L, et al. A map of olfactory representation in the Drosophila mushroom body. Cell, 2007, 128: 1205–1217 17382887, 10.1016/j.cell.2007.03.006, 1:CAS:528:DC%2BD2sXkslGmsL4%3DPubMedGoogle Scholar
  52. 52.
    Ito K, Awano W, Suzuki K, et al. 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, 1997, 124: 761–771 9043058, 1:CAS:528:DyaK2sXhvVyksrk%3DPubMedGoogle Scholar
  53. 53.
    Lee T, Lee A, Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development, 1999, 126: 4065–4076 10457015, 1:CAS:528:DyaK1MXmsleqsb0%3DPubMedGoogle Scholar
  54. 54.
    Zhu S, Chiang A S, Lee T. Development of the Drosophila mushroom bodies: elaboration, remodeling and spatial organization of dendrites in the calyx. Development, 2003, 130: 2603–2610 12736205, 10.1242/dev.00466, 1:CAS:528:DC%2BD3sXltFartrw%3DPubMedGoogle Scholar
  55. 55.
    Crittenden J R, Sloulakis E M C, Han K-A, et al. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem, 1998, 5: 38–51 10454371, 1:STN:280:DyaK1Mzot1Wktg%3D%3DPubMedPubMedCentralGoogle Scholar
  56. 56.
    Watts R J, Hoopfer E D, Luo L. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron, 2003, 38: 871–885 12818174, 10.1016/S0896-6273(03)00295-2, 1:CAS:528:DC%2BD3sXltFanu7s%3DPubMedGoogle Scholar
  57. 57.
    Lee T, Winter C, Marticke S S, et al. Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron, 2000, 25: 307–316 10719887, 10.1016/S0896-6273(00)80896-X, 1:CAS:528:DC%2BD3cXhslOktro%3DPubMedGoogle Scholar
  58. 58.
    Ito K, Suzuki K, Estes P, et al. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem, 1998, 5: 52–77 10454372, 1:STN:280:DyaK1Mzot1Wktw%3D%3DPubMedPubMedCentralGoogle Scholar
  59. 59.
    Waddell S, Armstrong J D, Kitamoto T, et al. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell, 2000, 103: 805–813 11114336, 10.1016/S0092-8674(00)00183-5, 1:CAS:528:DC%2BD3cXos1Snu7g%3DPubMedGoogle Scholar
  60. 60.
    Liu X, Davis R L. The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning. Nat Neurosci, 2009, 12: 53–59 19043409, 10.1038/nn.2235, 1:CAS:528:DC%2BD1cXhsVenu73OPubMedPubMedCentralGoogle Scholar
  61. 61.
    Strausfeld N J, Hansen L, Li Y, et al. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem, 1998, 5: 11–37 10454370, 1:STN:280:DyaK1Mzot1WksQ%3D%3DPubMedPubMedCentralGoogle Scholar
  62. 62.
    Yasuyama K, Salvaterra P M. Localization of choline acetyltrans-ferase-expressing neurons in Drosophila nervous system. Microsc Res Tech, 1999, 45: 65–79 10332725, 10.1002/(SICI)1097-0029(19990415)45:2<65::AID-JEMT2>3.0.CO;2-0, 1:STN:280:DyaK1M3msFWhuw%3D%3DPubMedGoogle Scholar
  63. 63.
    Kazama H, Wilson R I. Homeostatic matching and nonlinear amplification at identified central synapses. Neuron, 2008, 58: 401–413 18466750, 10.1016/j.neuron.2008.02.030, 1:CAS:528:DC%2BD1cXmt1Snu78%3DPubMedPubMedCentralGoogle Scholar
  64. 64.
    Kazama H, Wilson R I. Origins of correlated activity in an olfactory circuit. Nat Neurosci, 2009, 12: 1136–1144 19684589, 10.1038/nn.2376, 1:CAS:528:DC%2BD1MXpvFCrsrk%3DPubMedPubMedCentralGoogle Scholar
  65. 65.
    Wang J W, Wong A M, Flores J, et al. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell, 2003, 112: 271–282 12553914, 10.1016/S0092-8674(03)00004-7, 1:CAS:528:DC%2BD3sXpvVemuw%3D%3DPubMedGoogle Scholar
  66. 66.
    Wilson R I, Turner G C, Laurent G. Transformation of olfactory representations in the Drosophila antennal lobe. Science, 2004, 303: 366–370 14684826, 10.1126/science.1090782, 1:CAS:528:DC%2BD2cXjtFGmsA%3D%3DPubMedGoogle Scholar
  67. 67.
    Jayaraman V, Laurent G. Evaluating a genetically encoded optical sensor of neural activity using electrophysiology in intact adult fruit flies. Front Neural Circuits, 2007, 1: 3 18946545, 10.3389/neuro.04.003.2007PubMedPubMedCentralGoogle Scholar
  68. 68.
    Root C M, Semmelhack J L, Wong A M, et al. Propagation of olfactory information in Drosophila. Proc Natl Acad Sci USA, 2007, 104: 11826–11831 17596338, 10.1073/pnas.0704523104, 1:CAS:528:DC%2BD2sXotVaktrc%3DPubMedPubMedCentralGoogle Scholar
  69. 69.
    Olsen S R, Bhandawat V, Wilson R I. Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron, 2007, 54: 89–103 17408580, 10.1016/j.neuron.2007.03.010, 1:CAS:528:DC%2BD2sXkvVegt7s%3DPubMedPubMedCentralGoogle Scholar
  70. 70.
    Schlief M L, Wilson R I. Olfactory processing and behavior downstream from highly selective receptor neurons. Nat Neurosci, 2007, 10: 623–630 17417635, 10.1038/nn1881, 1:CAS:528:DC%2BD2sXksFShsL0%3DPubMedPubMedCentralGoogle Scholar
  71. 71.
    Bhandawat V, Olsen S R, Gouwens N W, et al. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat Neurosci, 2007, 10: 1474–1482 17922008, 10.1038/nn1976, 1:CAS:528:DC%2BD2sXht1ajtr%2FPPubMedPubMedCentralGoogle Scholar
  72. 72.
    Suh G S, Wong A M, Hergarden A C, et al. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature, 2004, 431: 854–859 15372051, 10.1038/nature02980, 1:CAS:528:DC%2BD2cXotl2ktrg%3DPubMedGoogle Scholar
  73. 73.
    Suh G S, Ben-Tabou de Leon S, Tanimoto H, et al. Light activation of an innate olfactory avoidance response in Drosophila. Curr Biol, 2007, 17: 905–908 17493811, 10.1016/j.cub.2007.04.046, 1:CAS:528:DC%2BD2sXlt1ahtbg%3DPubMedGoogle Scholar
  74. 74.
    Brieger G, Butterworth F M. Drosophila melanogaster: identity of male lipid in reproductive system. Science, 1970, 167: 1262 5411913, 10.1126/science.167.3922.1262, 1:CAS:528:DyaE3cXhtVygtrs%3DPubMedGoogle Scholar
  75. 75.
    Zawistowski S, Richmond R C. Inhibition of courtship and mating of Drosophila melanogaster by the male-produced lipid, cis-vaccenyl acetate. J Insect Physiol, 1986, 32: 189–192 10.1016/0022-1910(86)90057-0, 1:CAS:528:DyaL28Xhs1GrsL8%3DGoogle Scholar
  76. 76.
    Jallon J M, Antony C, Benamar O. Un anti-aphrodisiaque produit par les mâles de Drosophila melanogaster et transferé aux femelles lors de la copulation. C.R. Acad Sci Paris, 1981, 292: 1147–1149Google Scholar
  77. 77.
    Wang L, Anderson D J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature, 2010, 463: 227–231 19966787, 10.1038/nature08678, 1:CAS:528:DC%2BD1MXhsFWksLvEPubMedPubMedCentralGoogle Scholar
  78. 78.
    Semmelhack J L, Wang J W. Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature, 2009, 459: 218–223 19396157, 10.1038/nature07983, 1:CAS:528:DC%2BD1MXltValtL4%3DPubMedPubMedCentralGoogle Scholar
  79. 79.
    Quinn W G, Harris W A, Benzer S. Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci USA, 1974, 71: 708–712 4207071, 10.1073/pnas.71.3.708, 1:STN:280:DyaE2c7kt1KktQ%3D%3DPubMedPubMedCentralGoogle Scholar
  80. 80.
    Tempel B L, Bonini N, Dawson D R, et al. Reward learning in normal and mutant Drosophila. Proc Natl Acad Sci USA, 1983, 80: 1482–1486 6572401, 10.1073/pnas.80.5.1482, 1:STN:280:DyaL3s7ksVSqug%3D%3DPubMedPubMedCentralGoogle Scholar
  81. 81.
    Tully T, Quinn W G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A, 1985, 157: 263–277 3939242, 10.1007/BF01350033, 1:STN:280:DyaL283otFaguw%3D%3DPubMedGoogle Scholar
  82. 82.
    Heisenberg M. Mushroom body memoir: from maps to models. Nat Rev Neurosci, 2003, 4: 266–275 12671643, 10.1038/nrn1074, 1:CAS:528:DC%2BD3sXisFWqt7o%3DPubMedGoogle Scholar
  83. 83.
    Davis R L. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu Rev Neurosci, 2005, 28: 275–302 16022597, 10.1146/annurev.neuro.28.061604.135651, 1:CAS:528:DC%2BD2MXosVegtLk%3DPubMedGoogle Scholar
  84. 84.
    Keene A C, Waddell S. Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci, 2007, 8: 341–354 17453015, 10.1038/nrn2098, 1:CAS:528:DC%2BD2sXksFSis78%3DPubMedGoogle Scholar
  85. 85.
    Gu H, O’Dowd D K. Cholinergic synaptic transmission in adult Drosophila Kenyon cells in situ. J Neurosci, 2006, 26: 265–272 16399696, 10.1523/JNEUROSCI.4109-05.2006, 1:CAS:528:DC%2BD28XmtV2muw%3D%3DPubMedGoogle Scholar
  86. 86.
    Turner G C, Bazhenov M, Laurent G. Olfactory representations by Drosophila mushroom body neurons. J Neurophysiol, 2008, 99: 734–746 18094099, 10.1152/jn.01283.2007PubMedGoogle Scholar
  87. 87.
    Wang Y, Guo H F, Pologruto T A, et al. Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging. J Neurosci, 2004, 24: 6507–6514 15269261, 10.1523/JNEUROSCI.3727-03.2004, 1:CAS:528:DC%2BD2cXmt1ansrs%3DPubMedGoogle Scholar
  88. 88.
    Murthy M, Fiete I, Laurent G. Testing odor response stereotypy in the Drosophila mushroom body. Neuron, 2008, 59: 1009–1023 18817738, 10.1016/j.neuron.2008.07.040, 1:CAS:528:DC%2BD1cXht1amtr7PPubMedPubMedCentralGoogle Scholar
  89. 89.
    Han P L, Meller V, Davis R L. The Drosophila brain revisited by enhancer detection. J Neurobiol, 1996, 31: 88–102 9120439, 10.1002/(SICI)1097-4695(199609)31:1<88::AID-NEU8>3.0.CO;2-B, 1:CAS:528:DyaK28XmtVyhs7s%3DPubMedGoogle Scholar
  90. 90.
    Han K A, Millar N S, Davis R L. A novel octopamine receptor with preferential expression in Drosophila mushroom bodies. J Neurosci, 1998, 18: 3650–3658 9570796, 1:CAS:528:DyaK1cXjtVWlt7k%3DPubMedGoogle Scholar
  91. 91.
    Kim J Y, Koh H C, Lee J Y, et al. Dopaminergic neuronal differentiation from rat embryonic neural precursors by Nurr1 overexpression. J Neurochem, 2003, 85Google Scholar
  92. 92.
    Schwaerzel M, Monastirioti M, Scholz H, et al. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci, 2003, 23: 10495–10502 14627633, 1:CAS:528:DC%2BD3sXpsFGjtb4%3DPubMedGoogle Scholar
  93. 93.
    Schroll C, Riemensperger T, Bucher D, et al. Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol, 2006, 16: 1741–1747 16950113, 10.1016/j.cub.2006.07.023, 1:CAS:528:DC%2BD28XptFSktL0%3DPubMedGoogle Scholar
  94. 94.
    Mao Z, Davis R L. Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circuits, 2009, 3: 5 19597562, 10.3389/neuro.04.005.2009, 1:CAS:528:DC%2BD1MXosVKnsbo%3DPubMedPubMedCentralGoogle Scholar
  95. 95.
    Claridge-Chang A, Roorda R D, Vrontou E, et al. Writing memories with light-addressable reinforcement circuitry. Cell, 2009, 139: 405–415 19837039, 10.1016/j.cell.2009.08.034, 1:CAS:528:DC%2BD1MXhsFWht73IPubMedPubMedCentralGoogle Scholar
  96. 96.
    Krashes M J, DasGupta S, Vreede A, et al. A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell, 2009, 139(2): 416–427 19837040, 10.1016/j.cell.2009.08.035, 1:CAS:528:DC%2BD1MXhsFWht73JPubMedPubMedCentralGoogle Scholar
  97. 97.
    Sinakevitch I, Strausfeld N J. Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J Comp Neurol, 2006, 494: 460–475 16320256, 10.1002/cne.20799, 1:CAS:528:DC%2BD28XktVelsQ%3D%3DPubMedGoogle Scholar
  98. 98.
    Hammer M. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature, 1993, 366: 59–63 10.1038/366059a0PubMedGoogle Scholar
  99. 99.
    Zars T, Fischer M, Schulz R, et al. Localization of a short-term memory in Drosophila. Science, 2000, 288: 672–675 10784450, 10.1126/science.288.5466.672, 1:CAS:528:DC%2BD3cXivFGhurY%3DPubMedGoogle Scholar
  100. 100.
    McGuire S E, Le P T, Osborn A J, et al. Spatiotemporal rescue of memory dysfunction in Drosophila. Science, 2003, 302: 1765–1768 14657498, 10.1126/science.1089035, 1:CAS:528:DC%2BD3sXpsVWnsrg%3DPubMedGoogle Scholar
  101. 101.
    Kandel E R. The molecular biology of memory storage: a dialogue between genes and synapses. Science, 2001, 294: 1030–1038 11691980, 10.1126/science.1067020, 1:CAS:528:DC%2BD3MXot1KksLs%3DPubMedGoogle Scholar
  102. 102.
    Tomchik S M, Davis R L. Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron, 2009, 64: 510–521 19945393, 10.1016/j.neuron.2009.09.029, 1:CAS:528:DC%2BC3cXksFagtw%3D%3DPubMedPubMedCentralGoogle Scholar
  103. 103.
    Gervasi N, Tchenio P, Preat T. PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase. Neuron, 2010, 65: 516–529 20188656, 10.1016/j.neuron.2010.01.014, 1:CAS:528:DC%2BC3cXltlWkurY%3DPubMedGoogle Scholar
  104. 104.
    Pascual A, Preat T. Localization of long-term memory within the Drosophila mushroom body. Science, 2001, 294: 1115–1117 11691997, 10.1126/science.1064200, 1:CAS:528:DC%2BD3MXot1Krur4%3DPubMedGoogle Scholar
  105. 105.
    Isabel G, Pascual A, Preat T. Exclusive consolidated memory phases in Drosophila. Science, 2004, 304: 1024–1027 15143285, 10.1126/science.1094932, 1:CAS:528:DC%2BD2cXjvVCgsrc%3DPubMedGoogle Scholar
  106. 106.
    McGuire S E, Le P T, Davis R L. The role of Drosophila mushroom body signaling in olfactory memory. Science, 2001, 293: 1330–1333 11397912, 10.1126/science.1062622, 1:CAS:528:DC%2BD3MXmtFGjurs%3DPubMedGoogle Scholar
  107. 107.
    Krashes M J, Keene A C, Leung B, et al. Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron, 2007, 53: 103–115 17196534, 10.1016/j.neuron.2006.11.021, 1:CAS:528:DC%2BD2sXpsFSmsg%3D%3DPubMedPubMedCentralGoogle Scholar
  108. 108.
    Dubnau J, Grady L, Kitamoto T, et al. Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature, 2001, 411: 476–480 11373680, 10.1038/35078077, 1:CAS:528:DC%2BD3MXkt1ejtrc%3DPubMedGoogle Scholar
  109. 109.
    Feany M B, Quinn W G. A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science, 1995, 268: 869–873 7754370, 10.1126/science.7754370, 1:CAS:528:DyaK2MXls1Sgs7c%3DPubMedGoogle Scholar
  110. 110.
    Keene A C, Stratmann M, Keller A, et al. Diverse odor-conditioned memories require uniquely timed dorsal paired medial neuron output. Neuron, 2004, 44: 521–533 15504331, 10.1016/j.neuron.2004.10.006, 1:CAS:528:DC%2BD2cXpvVChsL8%3DPubMedGoogle Scholar
  111. 111.
    Keene A C, Krashes M J, Leung B, et al. Drosophila dorsal paired medial neurons provide a general mechanism for memory consolidation. Curr Biol, 2006, 16: 1524–1530 16890528, 10.1016/j.cub.2006.06.022, 1:CAS:528:DC%2BD28XotFWlsLk%3DPubMedGoogle Scholar
  112. 112.
    Yu D, Keene A C, Srivatsan A, et al. Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell, 2005, 123: 945–957 16325586, 10.1016/j.cell.2005.09.037, 1:CAS:528:DC%2BD2MXhtlWntLnKPubMedGoogle Scholar
  113. 113.
    Wang Y, Mamiya A, Chiang A S, et al. Imaging of an early memory trace in the Drosophila mushroom body. J Neurosci, 2008, 28: 4368–4376 18434515, 10.1523/JNEUROSCI.2958-07.2008, 1:CAS:528:DC%2BD1cXlsVWgs74%3DPubMedPubMedCentralGoogle Scholar
  114. 114.
    Komiyama T, Luo L. Development of wiring specificity in the olfactory system. Curr Opin Neurobiol, 2006, 16: 67–73 16377177, 10.1016/j.conb.2005.12.002, 1:CAS:528:DC%2BD28XhsFKqu7k%3DPubMedGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Howard Hughes Medical Institute, Department of BiologyStanford UniversityStanfordUSA
  2. 2.Department of Applied PhysicsStanford UniversityStanfordUSA

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