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Journal of Biosciences

, Volume 39, Issue 4, pp 565–574 | Cite as

A map of taste neuron projections in the Drosophila CNS

  • Jae Young Kwon
  • Anupama Dahanukar
  • Linnea A Weiss
  • John R Carlson
Article

Abstract

We provide a map of the projections of taste neurons in the CNS of Drosophila. Using a collection of 67 GAL4 drivers representing the entire repertoire of Gr taste receptors, we systematically map the projections of neurons expressing these drivers in the thoracico-abdominal ganglion and the suboesophageal ganglion (SOG). We define 9 categories of projections in the thoracico-abdominal ganglia and 10 categories in the SOG. The projection patterns are modular, and can be interpreted as combinations of discrete pattern elements. The elements can be interpreted in terms of the taste organ from which the projections originate, the structures from which they originate, and the quality of taste information that they represent. The extensive diversity in projection patterns provides an anatomical basis for functional diversity in responses elicited by different taste stimuli.

Keywords

Drosophila taste taste receptors 

Notes

Acknowledgements

We thank Zev Wisotsky for determining the pattern of Gr64d-GAL4 labelling in the SOG. This work was supported by NIH grants to JC.

References

  1. Arora K, Rodrigues V, Joshi S, Shanbhag S and Siddiqi O 1987 A gene affecting the specificity of the chemosensory neurons of Drosophila. Nature 330 62–63PubMedCrossRefGoogle Scholar
  2. Bray S and Amrein H 2003 A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 39 1019–1029PubMedCrossRefGoogle Scholar
  3. Chyb S, Dahanukar A, Wickens A and Carlson JR 2003 Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc. Natl. Acad. Sci. USA 100 14526–14530PubMedCentralPubMedCrossRefGoogle Scholar
  4. Clyne PJ, Warr CG and Carlson JR 2000 Candidate taste receptors in Drosophila. Science 287 1830–1834PubMedCrossRefGoogle Scholar
  5. Dahanukar A, Foster K, van der Goes van Naters WM and Carlson JR 2001 A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat. Neurosci. 4 1182–1186Google Scholar
  6. Dahanukar A, Lei YT, Kwon JY and Carlson JR 2007 Two Gr genes underlie sugar reception in Drosophila. Neuron 56 503–516Google Scholar
  7. Dethier VG 1976 The Hungry Fly (Harvard University Press: Cambridge)Google Scholar
  8. Dunipace L, Meister S, McNealy C and Amrein H 2001 Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11 822–835PubMedCrossRefGoogle Scholar
  9. Ejima A and Griffith LC 2008 Courtship initiation is stimulated by acoustic signals in Drosophila melanogaster. PLoS ONE 3 e3246PubMedCentralPubMedCrossRefGoogle Scholar
  10. Falk R, Bleiser-Avivi N and Atidia J 1976 Labellar taste organs of Drosophila melanogaster. J. Morphol. 150 327–342CrossRefGoogle Scholar
  11. Freeman EG, Wisotsky Z and Dahanukar A 2014 Detection of sweet tastants by a conserved group of insect gustatory receptors. Proc. Natl. Acad. Sci. USA 111 1598–1603PubMedCentralPubMedCrossRefGoogle Scholar
  12. Fujishiro N, Kijima H and Morita H 1984 Impulse frequency and action potential amplitude in labellar chemosensory neurons of Drosophila melanogaster. J. Insect. Physiol. 30 317–325CrossRefGoogle Scholar
  13. Hiroi M, Marion-Poll F and Tanimura T 2002 Differentiated response to sugars among labellar chemosensilla in Drosophila. Zoolog. Sci. 19 1009–1018PubMedCrossRefGoogle Scholar
  14. Hiroi M, Meunier N, Marion-Poll F and Tanimura T 2004 Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61 333–342PubMedCrossRefGoogle Scholar
  15. Ito M, Masuda N, Shinomiya K, Endo K and Ito K 2013 Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Curr. Biol. 23 644–655PubMedCrossRefGoogle Scholar
  16. Jiao Y, Moon SJ and Montell C 2007 A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc. Natl. Acad. Sci. USA 104 14110–14115PubMedCentralPubMedCrossRefGoogle Scholar
  17. Jiao Y, Moon SJ, Wang X, Ren Q and Montell C 2008 Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr. Biol. 18 1797-1801Google Scholar
  18. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF and Stocker RF 1999 Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405 543–552PubMedCrossRefGoogle Scholar
  19. Lee Y, Kang MJ, Shim J, Cheong CU, Moon SJ and Montell C 2012 Gustatory receptors required for avoiding the insecticide L-canavanine. J. Neurosci. 32 1429–1435PubMedCentralPubMedCrossRefGoogle Scholar
  20. Lee Y, Moon SJ and Montell C 2009 Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. USA 106 4495–4500Google Scholar
  21. Ling F, Dahanukar A, Weiss LA, Kwon JY and Carlson JR 2014 The molecular and cellular basis of taste coding in the legs of Drosophila. J. Neurosci. 34 7148–7164Google Scholar
  22. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E and Scott K 2006 Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49 285–295PubMedCrossRefGoogle Scholar
  23. Meunier N, Ferveur JF and Marion-Poll F 2000 Sex-specific non-pheromonal taste receptors in Drosophila. Curr. Biol. 10 1583–1586PubMedCrossRefGoogle Scholar
  24. Montell C 2009 A taste of the Drosophila gustatory receptors. Curr. Opin. Neurobiol. 19 345–353PubMedCentralPubMedCrossRefGoogle Scholar
  25. Moon SJ, Kottgen M, Jiao Y, Xu H and Montell C 2006 A taste receptor required for the caffeine response in vivo. Curr. Biol. 16 1812–1817PubMedCrossRefGoogle Scholar
  26. Moon SJ, Lee Y, Jiao Y and Montell C 2009 A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr. Biol. 19 1623–1627PubMedCentralPubMedCrossRefGoogle Scholar
  27. Nayak SV and Singh RN 1983 Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster meigen (Diptera: Drosophilidae). Int. J. Insect Morphol. and Embryol. 12 273–291CrossRefGoogle Scholar
  28. Python F and Stocker R 2002 Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J. Comp. Neurol. 445 374–387PubMedCrossRefGoogle Scholar
  29. Ray K, Hartenstein V and Rodrigues V 1993 Development of the taste bristles on the labellum of Drosophila melanogaster. Dev. Biol. 155 26–37PubMedCrossRefGoogle Scholar
  30. Robertson HM, Warr CG and Carlson JR 2003 Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 100 14537–14542PubMedCentralPubMedCrossRefGoogle Scholar
  31. Rodrigues V, Sathe S, Pinto L, Balakrishnan R and Siddiqi O 1991 Closely linked lesions in a region of the X chromosome affect central and peripheral steps in gustatory processing in Drosophila. Mol. Gen. Genet. 226 265–276PubMedCrossRefGoogle Scholar
  32. Rodrigues V and Siddiqi O 1978 Genetic-analysis of chemosensory pathway. Proc. Indian Acad. Sci. [B] 87 147–160CrossRefGoogle Scholar
  33. Rodrigues V and Siddiqi O 1981 A gustatory mutant of Drosophila defective in pyranose receptors. Mol. Gen. Genet. 181 406–408PubMedCrossRefGoogle Scholar
  34. Scott K, Brady R, Jr., Cravchik A, Morozov P, Rzhetsky A, Zuker C and Axel R 2001 A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104 661–673PubMedCrossRefGoogle Scholar
  35. Shanbhag SR, Park SK, Pikielny CW and Steinbrecht RA 2001 Gustatory organs of Drosophila melanogaster: fine structure and expression of the putative odorant-binding protein PBPRP2. Cell Tissue Res. 304 423–437PubMedCrossRefGoogle Scholar
  36. Siddiqi O, Joshi S, Arora K and Rodrigues V 1989 Genetic Investigation of Salt Reception in Drosophila melanogaster. Genome 31 646-651CrossRefGoogle Scholar
  37. Slone J, Daniels J and Amrein H 2007 Sugar receptors in Drosophila. Curr. Biol. 17 1809–1816PubMedCentralPubMedCrossRefGoogle Scholar
  38. Stocker RF 1994 The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res. 275 3–26PubMedCrossRefGoogle Scholar
  39. Thorne N and Amrein H 2008 Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons. J. Comp. Neurol. 506 548–568PubMedCrossRefGoogle Scholar
  40. Thorne N, Chromey C, Bray S and Amrein H 2004 Taste perception and coding in Drosophila. Curr. Biol. 14 1065–1079PubMedCrossRefGoogle Scholar
  41. van der Goes van Naters W and Carlson JR 2006 Insects as chemosensors of humans and crops. Nature 444 302–307PubMedCrossRefGoogle Scholar
  42. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Durrbeck H, Buchner S, Dabauvalle MC, et al. 2006 Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49 833–844PubMedCrossRefGoogle Scholar
  43. Wang Z, Singhvi A, Kong P and Scott K 2004 Taste representations in the Drosophila brain. Cell 117 981–991PubMedCrossRefGoogle Scholar
  44. Weiss LA, Dahanukar A, Kwon JY, Banerjee D and Carlson JR 2011 The molecular and cellular basis of bitter taste in Drosophila. Neuron 69 258–272PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2014

Authors and Affiliations

  • Jae Young Kwon
    • 1
    • 3
  • Anupama Dahanukar
    • 2
    • 3
  • Linnea A Weiss
    • 3
  • John R Carlson
    • 3
  1. 1.Department of Biological SciencesSungkyunkwan UniversitySuwonRepublic of Korea
  2. 2.Department of EntomologyUniversity of CaliforniaRiversideUSA
  3. 3.Department of Molecular, Cellular and Developmental BiologyYale UniversityNew HavenUSA

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