Auditory experience controls the maturation of song discrimination and sexual response in Drosophila.

Xiaodong Li,Hiroshi Ishimoto,Azusa Kamikouchi

doi:10.7554/elife.34348

Abstract

In birds and higher mammals, auditory experience during development is critical to discriminate sound patterns in adulthood. However, the neural and molecular nature of this acquired ability remains elusive. In fruit flies, acoustic perception has been thought to be innate. Here we report, surprisingly, that auditory experience of a species-specific courtship song in developing Drosophila shapes adult song perception and resultant sexual behavior. Preferences in the song-response behaviors of both males and females were tuned by social acoustic exposure during development. We examined the molecular and cellular determinants of this social acoustic learning and found that GABA signaling acting on the GABAA receptor Rdl in the pC1 neurons, the integration node for courtship stimuli, regulated auditory tuning and sexual behavior. These findings demonstrate that maturation of auditory perception in flies is unexpectedly plastic and is acquired socially, providing a model to investigate how song learning regulates mating preference in insects.

Highlights

Vocal learning in infants or juvenile birds relies heavily on the early experience of the adult conspecific sounds
We found that the experience of conspecific song, but not heterospecific song, tuned inter-pulse interval (IPI) perception in both males and female flies. We found that this experience-dependent IPI tuning relied on GABA synthesis, and that the ionotropic GABAA receptor of pC1 neurons gated IPI tuning in females
Because Drosophilids gather in groups in feeding sites (Powell, 1997), we reasoned that flies probably had experiences of the courtship songs of other males in social interactions, and tested how the auditory experience affected the IPI selectivity

Summary

Introduction

Vocal learning in infants or juvenile birds relies heavily on the early experience of the adult conspecific sounds. Because of the strong parallels between speech acquisition of humans and song learning of songbirds, and the difficulties to investigate the neural mechanisms of human early auditory memory at cellular resolution, songbirds have been used as a predominant model in studying memory formation during vocal learning. A small subset of neurons in the higher-order auditory cortex responded selectively to a song experienced in the early exposure, and were thought to be the neuronal substrate for song memory formation (Yanagihara and Yazaki-Sugiyama, 2016). The function of the sine song is not well understood, sound playback experiments have demonstrated that the pulse song promotes copulation in paired flies (Kyriacou and Hall, 1982; Ritchie et al, 1999). Receptivity of females is improved by playback of an artificial pulse song, which reduces female rejection responses and shortens the time to

Methods

Results

Conclusion