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

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Abstract
Mechanotransduction, the translation of mechanical forces into nerve impulses, is the basis of a number of senses including hearing, touch and awareness of gravity. Johnston's organ, a cluster of close to 500 sensory neurons in the Drosophila melanogaster antenna, is known to detect the vibrations of the antenna induced by the courtship song of a potential mate. Two laboratories have now identified additional senses mediating this system: Martin Göpfert and Kei Ito and colleagues show that it detects antennal deflections imposed by gravity, and Yorozu et al. find the same for deflections caused by wind. The behavioural responses to these stimuli are different, however, since different subsets of neurons are stimulated in each case. The way that these distinct mechanical senses are handled by separate neuronal pathways in a single organ is reminiscent of the vestibular division of the human inner ear that allows it to process sound and balance. These studies open the way to further genetic investigation in Drosophila as a broadly relevant model system for the detection of mechanosensory stimuli. One of two papers identifying distinct clusters of neurons in the Johnston's organ, a structure from the fruitfly antenna previously associated with courtship song detection, that specifically respond either to continuous deflections of the antenna, as provoked by wind or gravity, or to vibrating stimuli such as sounds. The segregation of different mechanosensation modalities through separate neuronal pathways in one organ is reminiscent of the hearing and vestibular system division of mammals. 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.