Sound response mediated by the TRP channels NOMPC, NANCHUNG, and INACTIVE in chordotonal organs of Drosophila larvae

Abstract

Mechanical stimuli, including tactile and sound signals, convey a variety of information important for animals to navigate the environment and avoid predators. Recent studies have revealed that Drosophila larvae can sense harsh or gentle touch with dendritic arborization (da) neurons in the body wall and can detect vibration with chordotonal organs (Cho). Whether they can also detect and respond to vibration or sound from their predators remains an open question. Here we report that larvae respond to sound of wasps and yellow jackets, as well as to pure tones of frequencies that are represented in such natural sounds, with startle and burrowing behaviors. The larval response to sound/ vibration requires Cho neurons and, to a lesser extent, class IV da neurons. Our calcium imaging and electrophysiological experiments reveal that Cho neurons, but not class IV da neurons, are excited by natural sounds or pure tones, with tuning curves and intensity dependence appropriate for the behavioral responses. Furthermore, our study implicates the transient receptor potential (TRP) channels NOMPC, NANCHUNG, and INACTIVE, but not the dmPIEZO channel, in the mechanotransduction and/or signal amplification for the detection of sound by the larval Cho neurons. These findings indicate that larval Cho, like their counterparts in the adult fly, use some of the same mechanotransduction channels to detect sound waves and mediate the sensation akin to hearing in Drosophila larvae, allowing them to respond to the appearance of predators or other environmental cues at a distance with behaviors crucial for survival.

Intracellular lumen formation in Drosophila proceeds via a novel subcellular compartment

“…The Drosophila larva has become an important model for studying diverse aspects of physiology and behavior, including metabolism (Palanker et al, 2009), wound healing (Galko and Krasnow, 2004), locomotion and feeding (Schoofs et al, 2014), and sensory perception (Zhang et al, 2013). Studies of any of these processes could benefit from ultrastructural analysis.…”

Insect TRP channels as targets for insecticides and repellents

“…29) NompC is also essential in the transduction of cuticular deformation by campaniform sensillae, 30) in auditory transduction by Johnston's organ in adult Drosophila 31,32) and in vibration detection by the lateral (pentascolopidial) chordotonal organs in Drosophila larvae. 33) NOMPC is also present in the distal tip of the cilium of leg chordotonal organs, where it is likely to also be involved in sensory transduction for the proprioceptive sense. 34) Because of its widespread importance in sensitive mechanosensory processes of touch, hearing and proprioception and the importance of these senses in social interactions and behavior, NOMPC is likely to be a valid insecticidal target.…”

Drosophila Neurobiology: No Escape from ‘Big Data’ Science

“…As mentioned, it was already well established that class IV Md neurons are crucial in mediating nociception, and it was recently shown that larval chordotonal neurons respond preferentially to vibration signals [15,16] and are tuned to the vibration produced by predatory wasps [16]. The second key contribution of Ohyama et al [17] is to map several new components of the circuit, down to the command neurons that are sufficient to trigger larval rolling.…”

“…Dispatches chordotonal (Cho) neurons [15,16]. The responses to all these specific sensory cues depend not only on the type of neuron, but also on the molecular machineries involved [12,14,16].…”

“…The responses to all these specific sensory cues depend not only on the type of neuron, but also on the molecular machineries involved [12,14,16]. A new paper [17] aims at putting together these elements into a complete circuit controlling the rolling escape response that presumably evolved in fly larvae to escape from parasitoid wasp adversaries.…”