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

Elife. 2018 Mar 20:7:e34348. 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.

Keywords: D. melanogaster; acoustic perception; auditory experience; neuroscience; plasticity; song.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animal Communication*
  • Animals
  • Auditory Perception / physiology*
  • Courtship*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / physiology
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / physiology
  • Female
  • Hearing / genetics
  • Hearing / physiology
  • Male
  • Neurons / physiology
  • RNA Interference
  • Receptors, GABA-A / genetics
  • Receptors, GABA-A / physiology
  • Sexual Behavior, Animal / physiology*
  • Sound*
  • Vocalization, Animal / physiology*

Substances

  • Drosophila Proteins
  • Receptors, GABA-A

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.