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Design of the Larval Chemosensory System

  • Reinhard F. Stocker
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 628)

Abstract

Given that smell and taste are vital senses for most animal species, it is not surprising that chemosensation has become a strong focus in neurobiological research. Much of what we know today about how the brain “mirrors” the chemical environment has derived from simple organisms like Drosophila. This is because their chemosensory system includes only a fraction of the cell number of the mammalian system, yet often exhibits the same basic design. Recent studies aimed at establishing fruitfly larvae as a particularly simple model for smell and taste have analyzed the expression patterns of olfactory and gustatory receptors, the circuitry of the chemosensory system and its behavioral output. Surprisingly, the larval olfactory system shares the organization of its adult counterpart, though comprising much reduced cell numbers. It thus indeed provides a “minimal” model system of general importance. Comparing adult and larval chemosensory systems raises interesting questions about their functional capabilities and about the processes underlying its transformation through metamorphosis.

Keywords

Olfactory System Taste Receptor Mushroom Body Antennal Lobe Odorant Receptor 
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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References

  1. 1.
    Buck L, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 1991; 65:175–187.PubMedCrossRefGoogle Scholar
  2. 2.
    Sengupta P, Chou JH, Bargmann CI. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 1996; 84:899–909.PubMedCrossRefGoogle Scholar
  3. 3.
    Clyne PJ, Warr CG, Freeman MR et al. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 1999; 22:327–338.PubMedCrossRefGoogle Scholar
  4. 4.
    Vosshall LB, Amrein H, Morozov PS et al. A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 1999; 96:725–736.PubMedCrossRefGoogle Scholar
  5. 5.
    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; 79:1245–1255.PubMedCrossRefGoogle Scholar
  6. 6.
    Vassar R, Chao SK, Sitcheran R et al. Topographic organization of sensory projections to the olfactory bulb. Cell 1994; 79:981–991.PubMedCrossRefGoogle Scholar
  7. 7.
    Gao Q, Yuan B, Chess A. Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 2000; 3:780–785.PubMedCrossRefGoogle Scholar
  8. 8.
    Vosshall LB, Wong AM, Axel R. An olfactory sensory map in the fly brain. Cell 2000; 102:147–159.PubMedCrossRefGoogle Scholar
  9. 9.
    Hildebrand JG, Shepherd G. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 1997; 20:595–631.PubMedCrossRefGoogle Scholar
  10. 10.
    Strausfeld NJ, Hildebrand JG. Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 1999; 9:634–639.PubMedCrossRefGoogle Scholar
  11. 11.
    Ache BW, Young JM. Olfaction: diverse species, conserved principles. Neuron 2005; 48:417–430.PubMedCrossRefGoogle Scholar
  12. 12.
    Fishilevich E, Domingos AI, Asahina K et al. Chemotaxis behavior mediated by single larval olfactory neurons in Drosophila. Curr Biol 2005; 15:2086–2096.PubMedCrossRefGoogle Scholar
  13. 13.
    Kreher SA, Kwon AY, Carlson JR. The molecular basis of odor coding in the Drosophila larva. Neuron 2005; 46:445–456.PubMedCrossRefGoogle Scholar
  14. 14.
    Masuda-Nakagawa LM, Tanaka NK, O’Kane CJ. Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc Nad Acad Sci USA 2005; 102:19027–19032.CrossRefGoogle Scholar
  15. 15.
    Ramaekers A, Magnenat E, Marin EC et al. Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr Biol 2005; 15:982–992.PubMedCrossRefGoogle Scholar
  16. 16.
    Singh RN, Singh K. Fine structure of the sensory organs of Drosophila melanogaster Meigen Larva (Diptera: Drosophilidae). Int J Insect Morphol Embryol 1984; 13:255–273.CrossRefGoogle Scholar
  17. 17.
    Schmidt-Ott U, Gonzalez-Gaitan M, Jäckie H et al. Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. Proc Natl Acad Sci USA 1994; 91:8363–8367.PubMedCrossRefGoogle Scholar
  18. 18.
    Campos-Ortega JA, Hartenstein V. The Embryonic Development of Drosophila melanogaster. Berlin, Heidelberg, New York: Springer, 1997.Google Scholar
  19. 19.
    Singh RN. Neurobiology of the gustatory systems of Drosophila and some terrestrial insects. Micr Res Techn 1997; 39:547–563.CrossRefGoogle Scholar
  20. 20.
    Python F, Stocker RF. Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J Comp Neurol 2002; 445:374–387.PubMedCrossRefGoogle Scholar
  21. 21.
    Gendre N, Lüer K, Friche S et al. Integration of complex larval chemosensory organs into the adult nervous system of Drosophila. Development 2004; 131:83–92.PubMedCrossRefGoogle Scholar
  22. 22.
    Chu IW, Axtell RC. Fine structure of the dorsal organ of the house fly larva, Musca domestica L. Z Zellforsch Mikrosk Anat 1971; 117:17–34.PubMedCrossRefGoogle Scholar
  23. 23.
    Chu-Wang IW, Axtell RC. Fine structure of the terminal organ of the house fly larva, Musca domestica L. Z. Zellforsch Mikrosk Anat 1972; 127:287–305.CrossRefGoogle Scholar
  24. 24.
    Chu-Wang, IW, Axtell RC. Fine structure of the ventral organ of the house fly larva, Musca domestica L. Z Zellforsch Mikrosk Anat 1972; 130:489–495.PubMedCrossRefGoogle Scholar
  25. 25.
    Oppliger FY, Guerin PM, Vlimant M. 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 2000; 46:135–144.PubMedCrossRefGoogle Scholar
  26. 26.
    Heimbeck G, Bugnon V, Gendre N et al. Smell and taste perception in D. melanogaster larva: toxin expression studies in chemosensory neurons. J Neurosci 1999; 19:6599–6609.PubMedGoogle Scholar
  27. 27.
    Larsson MC, Domingos Al, Jones WD et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 2004; 43:703–714.PubMedCrossRefGoogle Scholar
  28. 28.
    Liu L, Yermolaieva O, Johnson WA et al. Identification and function of thermosensory neurons in Drosophila larvae. Nat Neurosci 2003; 6:267–273.PubMedCrossRefGoogle Scholar
  29. 29.
    Kankel DR, Ferrus A, Garen SH et al. The structure and development of the nervous system. In: Ashburner M, Wright TRF, eds. The Genetics and Biology of Drosophila. London, New York, San Francisco: Academic Press, 1980:295–368.Google Scholar
  30. 30.
    Frederik RD, Denell RE. Embryological origin of the antenno-maxillary complex of the larva of Drosophila melanogaster Meigen. Int J Insect Morphol Embryol 1982; 11:227–233.CrossRefGoogle Scholar
  31. 31.
    Tissot M, Gendre N, Hawken A et al. Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila melanogaster. J Neurobiol 1997; 32:281–297.PubMedCrossRefGoogle Scholar
  32. 32.
    Robertson HM, Warr CG, Carlson JR. Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 2003; 100:14537–14542.PubMedCrossRefGoogle Scholar
  33. 33.
    Hallem EA, Dahanukar A, Carlson JR. Insect odor and taste receptors. Annu Rev Entomol 2006; 51:113–135.PubMedCrossRefGoogle Scholar
  34. 34.
    Clyne PJ, Warr CG, Carlson JR. Candidate taste receptors in Drosophila. Science 2000; 287:1830–1834.PubMedCrossRefGoogle Scholar
  35. 35.
    Dunipace L, Meister S, McNealy C et al. Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 2001; 11:822–835.PubMedCrossRefGoogle Scholar
  36. 36.
    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.PubMedCrossRefGoogle Scholar
  37. 37.
    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; 37:827–841.PubMedCrossRefGoogle Scholar
  38. 38.
    Goldman AL, van der Goes van Naters W, Lessing, D et al. Coexpression of two functional odor receptors in one neuron. Neuron 2005; 45:661–666.PubMedCrossRefGoogle Scholar
  39. 39.
    Hallem EA, Ho MG, Carlson JR. The molecular basis of odor coding in the Drosophila antenna. Cell 2004; 117:965–979.PubMedCrossRefGoogle Scholar
  40. 40.
    Bhalerao S, Sen A, Stocker RF et al. Olfactory neurons expressing identified receptor genes project to subsets of glomeruli within the antennal lobe of Drosophila melanogaster. J Neurobiol 2003; 54:577–592.PubMedCrossRefGoogle Scholar
  41. 41.
    Fiala A, Spall T, Dicgelmann S et al. Genetically expressed cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr Biol 2002; 12:1877–1884.PubMedCrossRefGoogle Scholar
  42. 42.
    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; 36:463–474.PubMedCrossRefGoogle Scholar
  43. 43.
    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; 112:271–282.PubMedCrossRefGoogle Scholar
  44. 44.
    Yu D, Ponomarev A, Davis RL. Altered representation of the spatial code for odors after olfactory classical conditioning: memory trace formation by synaptic recruitment. Neuron 2004; 42:437–449.PubMedCrossRefGoogle Scholar
  45. 45.
    Couto A, Alenius M, Dickson BJ. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 2005; 15:1535–1547.PubMedCrossRefGoogle Scholar
  46. 46.
    Neuhaus E, Gisselmann G, Zhang W et al. Odorant receptor heterodimerization in the olfactory system of Drosophila melanogaster. Nat Neurosci 2004; 8:15–17.PubMedCrossRefGoogle Scholar
  47. 47.
    Benton R, Sachse S, Michnick SW et al. Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biology 2005; 4(2):e20, DOI: 10.1371/journal pbio 004002046.CrossRefGoogle Scholar
  48. 48.
    Komiyama T, Carlson JR, Luo L. Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat Neurosci 2004; 7:819–825.PubMedCrossRefGoogle Scholar
  49. 49.
    Rodrigues V. Olfactory behavior of Drosophila melanogaster. In: Siddiqi O, Babu P, Hall LM, Hall JC, eds. Development and Neurobiology of Drosophila. New York, London: Plenum, 1980:361–371.Google Scholar
  50. 50.
    Monte P, Woodard C, Ayer R et al. Characterization of the larval olfactory response in Drosophila and its genetic basis. Behav Genet 1989; 19:267–283.PubMedCrossRefGoogle Scholar
  51. 51.
    Cobb M. What and how do maggots smell? Biol Rev 1999; 74:425–459.CrossRefGoogle Scholar
  52. 52.
    Marin EC, Watts RJ, Tanaka NK et al. Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 2005; 132:725–737.PubMedCrossRefGoogle Scholar
  53. 53.
    Python F, Stocker RF. Immunoreactivity against choline acetyltransferase, gamma-aminobutyric acid, histamine, octopamine, and serotonin in the larval chemosensory system of Drosophila melanogaster. J Comp Neurol 2002; 453:157–167.PubMedCrossRefGoogle Scholar
  54. 54.
    Wong AM, Wang JW, Axel R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 2002; 109:229–241.PubMedCrossRefGoogle Scholar
  55. 55.
    Stocker RF, Heimbeck G, Gendre N et al. Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 1997; 32:443–456.PubMedCrossRefGoogle Scholar
  56. 56.
    Lee T, Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 1999; 22:451–461.PubMedCrossRefGoogle Scholar
  57. 57.
    Yasuyama K, Meinertzhagen IA, Schürmann FW. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 2002; 445:211–226.PubMedCrossRefGoogle Scholar
  58. 58.
    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.PubMedGoogle Scholar
  59. 59.
    Troemel ER, Chou JH, Dwyer ND et al. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 1995; 83:207–218.PubMedCrossRefGoogle Scholar
  60. 60.
    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
  61. 61.
    Lei H, Christensen TA, Hildebrand JG. Spatial and temporal organization of ensemble representations for different odor classes in the moth antennal lobe. J Neurosci 2004; 24:11108–11119.PubMedCrossRefGoogle Scholar
  62. 62.
    Wilson RI, Turner GC, Laurent G. Transformation of olfactory representations in the Drosophila antennal lobe. Science 2004; 30:366–370.CrossRefGoogle Scholar
  63. 63.
    Wilson RI, Laurent G. Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 2005; 25:9069–9079.PubMedCrossRefGoogle Scholar
  64. 64.
    Perez-Orive J, Mazor O, Turner GC et al. Oscillations and sparsening of odor representations in the mushroom body. Science 2002; 297:359–365.PubMedCrossRefGoogle Scholar
  65. 65.
    Heisenberg M. Mushroom body memoir: from maps to models. Nat Revs Neurosci 2003; 4:266–275.CrossRefGoogle Scholar
  66. 66.
    Laissue PP, Reiter C, Hiesinger PR et al. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 1999; 405:543–552.PubMedCrossRefGoogle Scholar
  67. 67.
    Stocker RF. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tiss Res 1994; 275:3–26.CrossRefGoogle Scholar
  68. 68.
    Stocker RF. Drosophila as a focus in olfactory research: mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression and central connectivity. Micr Res Techn 2001; 55:284–296.CrossRefGoogle Scholar
  69. 69.
    Montmayeur JP, Matsunami H. Receptors for bitter and sweet taste. Curr Opin Neurobiol 2002; 12:366–371.PubMedCrossRefGoogle Scholar
  70. 70.
    Thorne N, Chromey C, Bray S et al. Taste perception and coding in Drosophila. Curr Biol 2004; 14:1065–1079.PubMedCrossRefGoogle Scholar
  71. 71.
    Wang Z, Singhvi A, Kong P et al. Taste representations in the Drosophila brain. Cell 2004; 117:981–991.PubMedCrossRefGoogle Scholar
  72. 72.
    Suh GSB, Wong AM, Hergarden AC et al. A single population of olfactory sensory neurons mediates an innate avoidance behavior in Drosophila. Nature 2004; 431:854–859.PubMedCrossRefGoogle Scholar
  73. 73.
    Liu L, Leonard AS, Motto DG et al. Contribution of Drosophila DEG/ENaC genes to salt taste. Neuron 2003; 39:133–146.PubMedCrossRefGoogle Scholar
  74. 74.
    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; 49:285–295.PubMedCrossRefGoogle Scholar
  75. 75.
    Melcher C, Pankratz MJ. Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol 2005; 3(9):e305, DOI: 10.1371/journal pbio 0030305.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  • Reinhard F. Stocker
    • 1
  1. 1.Department of BiologyUniversity of FribourgFribourgSwitzerland

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