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

Nature volume 458, pages 201–205 (2009)Cite this article

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.

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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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Authors and Affiliations

  1. Division of Biology 216-76,,

    Suzuko Yorozu, Allan Wong, Brian J. Fischer, Heiko Dankert & David J. Anderson

  2. Howard Hughes Medical Institute,,

    Suzuko Yorozu, Allan Wong & David J. Anderson

  3. Division of Engineering and Applied Sciences 136-93, California Institute of Technology, Pasadena, California 91125, USA,

    Heiko Dankert

  4. Department of Neurobiology and Behavior, SUNY Stony Brook, Stony Brook, New York 11794-5239, USA,

    Maurice J. Kernan

  5. Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan,

    Azusa Kamikouchi & Kei Ito

  6. Sensory System Laboratory, Institute of Zoology, University of Cologne, 50923 Cologne, Germany

    Azusa Kamikouchi

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  1. Suzuko Yorozu
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Corresponding authors

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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