Distinct Roles of TRP Channels in Auditory Transduction and Amplification in Drosophila

Abstract

SUMMARY Auditory receptor cells rely on mechanically gated channels to transform sound stimuli into neural activity. Several TRP channels have been implicated in Drosophila auditory transduction, but mechanistic studies have been hampered by the inability to record subthreshold signals from receptor neurons. Here, we develop a non-invasive method for measuring these signals by recording from a central neuron that is electrically coupled to a genetically defined population of auditory receptor cells. We find that the TRPN family member NompC, which is necessary for the active amplification of sound-evoked motion by the auditory organ, is not required for transduction in auditory receptor cells. Instead, NompC sensitizes the transduction complex to movement and precisely regulates the static forces on the complex. In contrast, the TRPV channels Nanchung and Inactive are required for responses to sound, suggesting they are components of the transduction complex. Thus, transduction and active amplification are genetically separable processes in Drosophila hearing.

Responses ofDrosophilagiant descending neurons to visual and mechanical stimuli

“…In larger fly species, cobalt readily passes from antennal nerve afferents into the deutocerebral dendrites of the GDN. This observation is consistent with the recent physiological demonstration that sensory terminals from Johnston's organ make gap junctions with the dendrites of Drosophila GDN (Lehnert et al, 2013).…”

“…This is also seen in the Drosophila GDN, which additionally shows subthreshold responses to courtship song (Tootoonian et al, 2012) and to direct antennal displacement (Lehnert et al, 2013). Our results showed that an air puff to the antennae invariably elicited a large EPSP at the beginning of the stimulus (Fig.…”

“…Possible candidates are other members of the GDN cluster that comprise a system of at least eight parallel channels, which with the GDN likely share at least the same lobula-derived inputs (Strausfeld and Bacon, 1983;Milde and Strausfeld, 1990). More recent studies on the Drosophila GDN have shown that looming visual stimuli elicit subthreshold responses (Mu et al, 2012a), as do acoustic stimuli detected by the antenna's Johnston's organ (Tootoonian et al, 2012) or direct mechanical stimulation of the antenna (Lehnert et al, 2013). These subthreshold GDN responses were elicited in restrained flies, but in a preparation in which the mesothoracic legs were left free to elicit the escape jump, a looming stimulus did initiate single GDN spikes on some occasions (Von Reyn and Card, 2012).…”

Connecting Neural Codes with Behavior in the Auditory System of Drosophila

“…3H); however, this feature did not impact behavioral predictions (rank correlation between duration of the positive lobe and decoder performance ρ=−0.01, p=0.96). The range of filter durations may thus serve other aspects of song processing or other acousticallydriven behaviors (Lehnert et al, 2013;Vaughan et al, 2014). The relative homogeneity in response properties in our data set also makes it unlikely that females rely on any single neuron type when processing male song.…”

Separate TRP channels mediate amplification and transduction in drosophila

“…For detailed methods, see [12]. Briefly, trans-synaptic generator currents were recorded by making in vivo whole cell voltage-clamp recordings from the Giant Fiber Neuron (GFN).…”