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Distinct sensory representations of wind and near-field sound in the Drosophila brain

Abstract

Behavioural responses to wind are thought to have a critical role in controlling the dispersal and population genetics of wild Drosophila species1,2, as well as their navigation in flight3, but their underlying neurobiological basis is unknown. We show that Drosophila melanogaster, like wild-caught Drosophila strains4, exhibits robust wind-induced suppression of locomotion in response to air currents delivered at speeds normally encountered in nature1,2. Here we identify wind-sensitive neurons in Johnston’s organ, an antennal mechanosensory structure previously implicated in near-field sound detection (reviewed in refs 5 and 6). Using enhancer trap lines targeted to different subsets of Johnston’s organ neurons7, and a genetically encoded calcium indicator8, we show that wind and near-field sound (courtship song) activate distinct populations of Johnston’s organ neurons, which project to different regions of the antennal and mechanosensory motor centre in the central brain. Selective genetic ablation of wind-sensitive Johnston’s organ neurons in the antenna abolishes wind-induced suppression of locomotion behaviour, without impairing hearing. Moreover, different neuronal subsets within the wind-sensitive population respond to different directions of arista deflection caused by air flow and project to different regions of the antennal and mechanosensory motor centre, providing a rudimentary map of wind direction in the brain. Importantly, sound- and wind-sensitive Johnston’s organ neurons exhibit different intrinsic response properties: the former are phasically activated by small, bi-directional, displacements of the aristae, whereas the latter are tonically activated by unidirectional, static deflections of larger magnitude. These different intrinsic properties are well suited to the detection of oscillatory pulses of near-field sound and laminar air flow, respectively. These data identify wind-sensitive neurons in Johnston’s organ, a structure that has been primarily associated with hearing, and reveal how the brain can distinguish different types of air particle movements using a common sensory organ.

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Figure 1: Behavioural and electrophysiological analyses of wind responses in Drosophila.
Figure 3: Ablation of wind-sensitive (C and E) neurons abolishes WISL behaviour.
Figure 2: Calcium imaging reveals distinct populations of wind- and sound-responsive JO neurons.
Figure 4: Wind-direction-sensitivity of zones C versus E.
Figure 5: Wind- and sound-sensitive JO neurons have different intrinsic response properties.

References

  1. Johnston, J. & Templeton, A. in Ecological Genetics and Evolution (eds Barker, J. S. F. & Starmer, W. T.) 241–256 (Academic, 1982)

    Google Scholar 

  2. Johnston, J. & Heed, W. Dispersal of desert-adapted Drosophila: the saguaro-breeding D. nigrospiracula. Am. Nat. 110, 629–651 (1976)

    Article  Google Scholar 

  3. Budick, S. A., Reiser, M. B. & Dickinson, M. H. The role of visual and mechanosensory cues in structuring forward flight in Drosophila melanogaster. J. Exp. Biol. 210, 4092–4103 (2007)

    Article  Google Scholar 

  4. Richardson, R. & Johnston, J. Behavioral components of dispersal in Drosophila mimica. Oecologia 20, 287–299 (1975)

    CAS  ADS  Article  Google Scholar 

  5. Caldwell, J. C. & Eberl, D. F. Towards a molecular understanding of Drosophila hearing. J. Neurobiol. 53, 172–189 (2002)

    CAS  Article  Google Scholar 

  6. Kernan, M. J. Mechanotransduction and auditory transduction in Drosophila. Pflügers Arch. 454, 703–720 (2007)

    CAS  Article  Google Scholar 

  7. Kamikouchi, A., Shimada, T. & Ito, K. Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J. Comp. Neurol. 499, 317–356 (2006)

    Article  Google Scholar 

  8. Nakai, J., Ohkura, M. & Imoto, K. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nature Biotechnol. 19, 137–141 (2001)

    CAS  Article  Google Scholar 

  9. Göpfert, M. C. & Robert, D. The mechanical basis of Drosophila audition. J. Exp. Biol. 205, 1199–1208 (2002)

    PubMed  Google Scholar 

  10. Mamiya, A. et al. Neural representations of airflow in Drosophila mushroom body. PLoS ONE 3, e4063 (2008)

    ADS  Article  Google Scholar 

  11. Manning, A. Antennae and sexual receptivity in Drosophila melanogaster females. Science 158, 136–137 (1967)

    CAS  ADS  Article  Google Scholar 

  12. Kim, J. et al. A TRPV family ion channel required for hearing in Drosophila. Nature 424, 81–84 (2003)

    CAS  ADS  Article  Google Scholar 

  13. Wang, S. L. et al. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 98, 453–463 (1999)

    CAS  Article  Google Scholar 

  14. Eberl, D. F., Hardy, R. W. & Kernan, M. J. Genetically similar transduction mechanisms for touch and hearing in Drosophila. J. Neurosci. 20, 5981–5988 (2000)

    CAS  Article  Google Scholar 

  15. Tanouye, M. A. & Wyman, R. J. Motor outputs of giant nerve fiber in Drosophila. J. Neurophysiol. 44, 405–421 (1980)

    CAS  Article  Google Scholar 

  16. Bennet-Clark, H. C. Acoustics of insect song. Nature 234, 255–259 (1971)

    ADS  Article  Google Scholar 

  17. Moffat, K. G. et al. Inducible cell ablation in Drosophila by cold-sensitive ricin A chain. Development 114, 681–687 (1992)

    CAS  PubMed  Google Scholar 

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

    CAS  Article  Google Scholar 

  19. Ewing, A. W. The antenna of Drosophila as a ‘love song’ receptor. Physiol. Entomol. 3, 33–36 (1978)

    Article  Google Scholar 

  20. Ikeda, I. et al. Selective phototoxic destruction of rat Merkel cells abolishes responses of slowly adapting type I mechanoreceptor units. J. Physiol. (Lond.) 479, 247–256 (1994)

    Article  Google Scholar 

  21. Hoffmann, J. N., Montag, A. G. & Dominy, N. J. Meissner corpuscles and somatosensory acuity: the prehensile appendages of primates and elephants. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 281, 1138–1147 (2004)

    Article  Google Scholar 

  22. Kamikouchi, A. et al. The neural basis of Drosophila gravity-sensing and hearing. Nature 1010.1038/nature07810 (this issue)

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

    CAS  Article  Google Scholar 

  24. Wang, Y. et al. Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent protein-based Ca2+ imaging. J. Neurosci. 24, 6507–6514 (2004)

    CAS  Article  Google Scholar 

  25. Berdnik, D., Chihara, T., Couto, A. & Luo, L. Wiring stability of the adult Drosophila olfactory circuit after lesion. J. Neurosci. 26, 3367–3376 (2006)

    CAS  Article  Google Scholar 

  26. Wheeler, D. A., Fields, W. L. & Hall, J. C. Spectral analysis of Drosophila courtship songs: D. melanogaster, D. simulans, and their interspecific hybrid. Behav. Genet. 18, 675–703 (1988)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank U. Heberlein and F. Wolf for hosting a sabbatical that led to the discovery of WISL; J. S. Johnson for helpful discussions; L. Zelnik, M. Reiser and P. Perona for creating locomotor tracking software; D. Eberl and J. Hall for D. melanogaster courtship song recordings; G. Maimon for making fly holders for imaging experiments; M. Roy for building behavioral chambers for WISL and female receptivity assays; H. Inagaki for JO-CE-GAL4;eyFLP flies; B. Hay for UAS-hid flies; D. Berdnik for UAS-FRT-STOP-FRT-Ricin flies; M. Dickinson for anemometers and discussions; J. L. Anderson for advice on fluid mechanics; M. Göpfert for providing a pressure gradient microphone; M. Konishi for advice and use of laboratory facilities; and G. Mosconi for laboratory management. D.J.A. is an Investigator of the Howard Hughes Medical Institute. This work was supported in part by NSF grant EF-0623527.

Author Contributions S.Y. and D.J.A. designed experiments, S.Y. carried out all experiments reported in this paper and D.J.A. and S.Y. wrote the manuscript. A.W. wrote Matlab programs for ΔF/F measurements and mechanical probe actuation, B.J.F. assisted with computational filtering of song stimuli, H.D. assisted with computational and statistical analysis of data, M.J.K. provided facilities and support for electrophysiological experiments, and A.K. and K.I. provided Gal4 lines.

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Correspondence to Suzuko Yorozu or David J. Anderson.

Supplementary information

Supplementary Information

This file contains Supplementary Figures S1-S4, Supplementary Notes S1-S4 and Supplementary Movie Legends. (PDF 3074 kb)

Supplementary Movie 1

This movie shows WISL behavior in Drosophila melanogaster (see file s1 for full legend). (MOV 877 kb)

Supplementary Movie 2a

This movie shows the responses of JO neurons to sound and wind stimuli in zones A, C and E, using the Gal4 line JO-ACE to drive expression of UAS-GCaMP (see file s1 for full legend). (MOV 1218 kb)

Supplementary Movie 2b

This movie shows the responses of JO neurons to sound and wind stimuli in zones A, C and E, using the Gal4 line JO-ACE to drive expression of UAS-GCaMP (see file s1 for full legend). (MOV 1228 kb)

Supplementary Movie 2c

This movie shows the responses of JO neurons to sound and wind stimuli in zones A, C and E, using the Gal4 line JO-ACE to drive expression of UAS-GCaMP (see file s1 for full legend). (MOV 1258 kb)

Supplementary Movie 2d

This movie shows the responses of JO neurons to sound and wind stimuli in zones A, C and E, using the Gal4 line JO-ACE to drive expression of UAS-GCaMP (see file s1 for full legend). (MOV 1252 kb)

Supplementary Movie 2e

This movie shows the responses of JO neurons to sound and wind stimuli in zones A, C and E, using the Gal4 line JO-ACE to drive expression of UAS-GCaMP (see file s1 for full legend). (MOV 1200 kb)

Supplementary Movie 3a

This movie shows the responses of zone C and E neurons to wind delivered from different directions, using the Gal4 line JO-CE to drive expression of GCaMP (see file s1 for full legend). (MOV 2694 kb)

Supplementary Movie 3b

This movie shows the responses of zone C and E neurons to wind delivered from different directions, using the Gal4 line JO-CE to drive expression of GCaMP (see file s1 for full legend). (MOV 2623 kb)

Supplementary Movie 3c

This movie shows the responses of zone C and E neurons to wind delivered from different directions, using the Gal4 line JO-CE to drive expression of GCaMP (see file s1 for full legend). (MOV 2727 kb)

Supplementary Movie 3d

This movie shows the responses of zone C and E neurons to wind delivered from different directions, using the Gal4 line JO-CE to drive expression of GCaMP (see file s1 for full legend). (MOV 2746 kb)

Supplementary Movie 3e

This movie shows the responses of zone C and E neurons to wind delivered from different directions, using the Gal4 line JO-CE to drive expression of GCaMP (see file s1 for full legend). (MOV 2668 kb)

Supplementary Movie 4a

This movie was made to show the direction of aristae deflection during the presentation of wind stimuli, under the same conditions used to obtain the data illustrated in Supplementary Movie 3 (see file s1 for full legend). (MOV 440 kb)

Supplementary Movie 4b

This movie was made to show the direction of aristae deflection during the presentation of wind stimuli, under the same conditions used to obtain the data illustrated in Supplementary Movie 3 (see file s1 for full legend). (MOV 415 kb)

Supplementary Movie 4c

This movie was made to show the direction of aristae deflection during the presentation of wind stimuli, under the same conditions used to obtain the data illustrated in Supplementary Movie 3 (see file s1 for full legend). (MOV 427 kb)

Supplementary Movie 4d

This movie was made to show the direction of aristae deflection during the presentation of wind stimuli, under the same conditions used to obtain the data illustrated in Supplementary Movie 3 (see file s1 for full legend). (MOV 446 kb)

Supplementary Movie 4e

This movie was made to show the direction of aristae deflection during the presentation of wind stimuli, under the same conditions used to obtain the data illustrated in Supplementary Movie 3 (see file s1 for full legend). (MOV 429 kb)

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Yorozu, S., Wong, A., Fischer, B. et al. Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 458, 201–205 (2009). https://doi.org/10.1038/nature07843

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