The voltage-gated potassium channelShal(Kv4) contributes to active hearing inDrosophila

Abstract

AbstractThe full complement of ion channels which influence insect auditory mechanotransduction, and the mechanisms by which their influence is exerted, remain unclear.Shal(Kv4), aShakerfamily member encoding voltage-gated potassium channels inDrosophila melanogaster, has been shown to localize to dendrites in some neuron types, suggesting a potential role forShalinDrosophilahearing, including mechanotransduction. A GFP-protein trap was used to visualize the localization of theShalchannel in Johnston’s organ neurons responsible for hearing in the antenna.Shalprotein was localized to the cell body and the proximal dendrite region of sensory neurons, suggesting its involvement not only in general auditory function, but specifically in mechanotransduction. Electrophysiological recordings conducted to assess neural responses to auditory stimuli in mutantShalflies revealed significant decreases in auditory responses. Laser Doppler Vibrometer recordings indicated abnormal antennal free fluctuation frequencies in mutant lines, indicating an effect on active antennal tuning, and thus active transduction mechanisms. This suggests thatShalparticipates in coordinating energy-dependent antennal movements inDrosophilathat are essential for tuning the antenna to courtship song frequencies.Significance StatementThe study of fruit fly hearing has revealed mechanosensitive ion channels that participate in mechanotransduction, and as in mammalian hearing, energy-dependent mechanisms actively amplify and tune auditory processes. Identifying distinct roles played by different ion channels is essential to better understand this process. Here, we explore the influence of a specific voltage-gated potassium channel,Shal, on fly hearing, and find that it affects specific parts of the mechanotransduction process. Our research uncoversShal’slocalization in sensory dendrite regions of auditory neurons, where it contributes to shaping mechanotransduction and active antennal tuning. UnderstandingShal’s involvement in auditory function and mechanotransduction deepens our knowledge of fly hearing and unveils a key player in the coordination of energy-dependent active antennal movements.