Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston's organ of the fruit fly

Frontiers in Physiology

Volumn 5 MAY, Issue , 2014, Pages

  Matsuo, Eriko ^a   Yamada, Daichi ^a   Ishikawa, Yuki ^a   Asai, Tomonori ^a   Ishimoto, Hiroshi ^a   Kamikouchi, Azusa ^a,b  

^a NAGOYA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Brain; Calcium imaging; Drosophila; Insect; Johnston's organ; Mechanosensory; Neural circuit

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ANTENNA (ORGAN); ANTENNAL MECHANOSENSORY AND MOTOR CENTER; ARTICLE; BRAIN; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; DROSOPHILA MELANOGASTER; FEMALE; IMMUNOHISTOCHEMISTRY; INTERNEURON; JOHNSTON ORGAN; NERVE CELL NETWORK; NERVE PROJECTION; NEUROANATOMY; NEUROIMAGING; NONHUMAN; SENSORY NERVE CELL; SENSORY STIMULATION; THORAX; VENTRAL ROOT; VIBRATION SENSE;

EID: 84904339561     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00179     Document Type: Article

References (44)

1. Albert, J. T., Nadrowski, B., and Göpfert, M. C. (2007). Mechanical signatures of transducer gating in the Drosophila ear. Curr. Biol. 17, 1000-1006. doi: 10.1016/j.cub.2007.05.004.
2. Basler, K., and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214. doi: 10.1038/368208a0.
3. Brand, A. H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
4. Cameron, P., Hiroi, M., Ngai, J., and Scott, K. (2010). The molecular basis for water taste in Drosophila. Nature 465, 91-95. doi: 10.1038/nature09011.
5. de Bruyne, M., Foster, K., and Carlson, J. R. (2001). Odor coding in the drosophila antenna. Neuron 30, 537-552. doi: 10.1016/S0896-6273(01)00289-6.
6. Ebbs, M. L., and Amrein, H. (2007). Taste and pheromone perception in the fruit fly Drosophila melanogaster. Pflugers Arch. 454, 735-747. doi: 10.1007/s00424-007-0246-y.
7. Effertz, T., Nadrowski, B., Piepenbrock, D., Albert, J. T., and Göpfert, M. C. (2012). Direct gating and mechanical integrity of Drosophila auditory transducers require TRPN1. Nat. Neurosci. 15, 1198-1200. doi: 10.1038/nn.3175.
8. Estes, P. S., Ho, G. L., Narayanan, R., and Ramaswami, M. (2000). Synaptic localization and restricted diffusion of a Drosophila neuronal synaptobrevin-green fluorescent protein chimera in vivo. J. Neurogenet. 13, 233-255. doi: 10.3109/01677060009084496.
9. Ewing, A. W., and Bennet-Clark, H. C. (1968). The courtship songs of Drosophila. Behaviour 31, 288-301. doi: 10.1163/156853968X00298.
10. Fiala, A., and Spall, T. (2003). In vivo calcium imaging of brain activity in Drosophila by transgenic cameleon expression. Sci. STKE 2003, PL6. doi: 10.1126/stke.2003.174.pl6.
11. Field, L. H., and Matheson, T. (1998). Chordotonal organs of insects. Adv. Insect Physiol. 27, 1-228. doi: 10.1016/S0065-2806(08)60013-2.
12. Göpfert, M. C., and Robert, D. (2002). The mechanical basis of Drosophila audition. J. Exp. Biol. 205, 1199-1208.
13. Göpfert, M. C., and Robert, D. (2003). Motion generation by Drosophila mechanosensory neurons. Proc. Natl. Acad. Sci. U.S.A 100, 5514-5519. doi: 10.1073/pnas.0737564100.
14. Grosjean, Y., Rytz, R., Farine, J. P., Abuin, L., Cortot, J., Jefferis, G. S., et al. (2011). An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478, 236-240. doi: 10.1038/nature10428.
15. Hayashi, S., Ito, K., Sado, Y., Taniguchi, M., Akimoto, A., Takeuchi, H., et al. (2002). GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34, 58-61. doi: 10.1002/gene.10137.
16. Ito, K., Shinomiya, K., Ito, M., Armstrong, D., Boyan, G., Hartenstein, V., et al. (2014). A systematic nomenclature for the insect brain. Neuron 81, 755-765. doi: 10.1016/j.neuron.2013.12.017.
17. Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D., and Strausfeld, N. J. (1998). The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem. 5, 52-77.
18. Ito, K., Urban, J., and Technau, G. M. (1995). Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux. Arch. Dev. Biol. 204, 284-307. doi: 10.1007/BF02179499.
19. Kamikouchi, A., Inagaki, H. K., Effertz, T., Hendrich, O., Fiala, A., Göpfert, M. C., et al. (2009). The neural basis of Drosophila gravity-sensing and hearing. Nature 458, 165-171. doi: 10.1038/nature07810.
20. Kamikouchi, A., Shimada, T., and Ito, K. (2006). Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J. Comp. Neurol. 499, 317-356. doi: 10.1002/cne.21075.
21. Kamikouchi, A., Wiek, R., Effertz, T., Göpfert, M. C., and Fiala, A. (2010). Transcuticular optical imaging of stimulus-evoked neural activities in the Drosophila peripheral nervous system. Nat. Protoc. 5, 1229-1235. doi: 10.1038/nprot.2010.85.
22. Kavlie, R. G., Kernan, M. J., and Eberl, D. F. (2010). Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics 185, 177-188. doi: 10.1534/genetics.110.114009.
23. Kim, J., Chung, Y. D., Park, D. Y., Choi, S., Shin, D. W., Soh, H., et al. (2003). A TRPV family ion channel required for hearing in Drosophila. Nature 424, 81-84. doi: 10.1038/nature01733.
24. 2+ channel clustering, and vesicle release. Science 312, 1051-1054. doi: 10.1126/science.1126308.
25. 2 reception in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 104, 3574-3578. doi: 10.1073/pnas.0700079104.
26. Lai, J. S., Lo, S. J., Dickson, B. J., and Chiang, A. S. (2012). Auditory circuit in the Drosophila brain. Proc. Natl.Acad. Sci.U.S.A. 109, 2607-2612. doi: 10.1073/pnas.1117307109.
27. Mank, M., Santos, A. F., Direnberger, S., Mrsic-Flogel, T. D., Hofer, S. B., Stein, V., et al. (2008). A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat. Methods 5, 805-811. doi: 10.1038/nmeth.1243.
28. Matsuo, E., and Kamikouchi, A. (2013). Neuronal encoding of sound, gravity, and wind in the fruit fly. J. Comp. Physiol. A 199, 253-262. doi: 10.1007/s00359-013-0806-x.
29. Nadrowski, B., Effertz, T., Senthilan, P. R., and Göpfert, M. C. (2011). Antennal hearing in insects-new findings, new questions. Hear. Res. 273, 7-13. doi: 10.1016/j.heares.2010.03.092.
30. Pelz, D., Roeske, T., Syed, Z., de Bruyne, M., and Galizia, C. G. (2006). The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a). J. Neurobiol. 66, 1544-1563. doi: 10.1002/neu.20333.
31. Riabinina, O., Dai, M., Duke, T., and Albert, J. T. (2011). Active process mediates species-specific tuning of Drosophila ears. Curr. Biol. 21, 658-664. doi: 10.1016/j.cub.2011.03.001.
32. Suh, G. S., Wong, A. M., Hergarden, A. C., Wang, J. W., Simon, A. F., Benzer, S., et al. (2004). A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854-859. doi: 10.1038/nature02980.
33. Tauber, E., and Eberl, D. F. (2003). Acoustic communication in Drosophila. Behav. Process. 64, 197-210. doi: 10.1016/S0376-6357(03)00135-9.
34. Tian, L., Hires, S. A., Mao, T., Huber, D., Chiappe, M. E., Chalasani, S. H., et al. (2009). Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881. doi: 10.1038/nmeth.1398.
35. Tuthill, J. C., Nern, A., Holtz, S. L., Rubin, G. M., and Reiser, M. B. (2013). Contributions of the 12 neuron classes in the fly lamina to motion vision. Neuron 79, 128-140. doi: 10.1016/j.neuron.2013.05.024.
36. Verkhusha, V. V., Otsuna, H., Awasaki, T., Oda, H., Tsukita, S., and Ito, K. (2001). An enhanced mutant of red fluorescent protein DsRed for double labeling and developmental timer of neural fiber bundle formation. J. Biol. Chem. 276, 29621-29624. doi: 10.1074/jbc.C100200200.
37. von Schilcher, F. (1977). A mutation which changes courtship song in Drosophila melanogaster. Behav. Genet. 7, 251-259. doi: 10.1007/BF01066278.
38. Wagh, D. A., Rasse, T. M., Asan, E., Hofbauer, A., Schwenkert, I., Durrbeck, H., 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, 833-844. doi: 10.1016/j.neuron.2006.02.008.
39. Wan, Y., Otsuna, H., Chien, C. B., and Hansen, C. (2009). An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research. IEEE T. Vis. Comput. Gr. 15, 1489-1496. doi: 10.1109/TVCG.2009.118.
40. Warmke, J., Yamakawa, M., Molloy, J., Falkenthal, S., and Maughan, D. (1992). Myosin light chain-2 mutation affects flight, wing beat frequency, and indirect flight muscle contraction kinetics in Drosophila. J. Cell Biol. 119, 1523-1539. doi: 10.1083/jcb.119.6.1523.
41. Wong, A. M., Wang, J. W., and Axel, R. (2002). Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109, 229-241. doi: 10.1016/S0092-8674(02)00707-9.
42. Wucherpfennig, T., Wilsch-Brauninger, M., and Gonzalez-Gaitan, M. (2003). Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161, 609-624. doi: 10.1083/jcb.200211087.
43. Yoon, J., Matsuo, E., Yamada, D., Mizuno, H., Morimoto, T., Miyakawa, H., et al. (2013). Selectivity and plasticity in a sound-evoked male-male interaction in Drosophila. PLoS ONE 8:e74289. doi: 10.1371/journal.pone.0074289.
44. Yorozu, S., Wong, A., Fischer, B. J., Dankert, H., Kernan, M. J., Kamikouchi, A., et al. (2009). Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 458, 201-205. doi: 10.1038/nature07843.