A Bidirectional Circuit Switch Reroutes Pheromone Signals in Male and Female Brains

Cell. 2013 Dec 19;155(7):1610-23. doi: 10.1016/j.cell.2013.11.025.

Abstract

The Drosophila sex pheromone cVA elicits different behaviors in males and females. First- and second-order olfactory neurons show identical pheromone responses, suggesting that sex genes differentially wire circuits deeper in the brain. Using in vivo whole-cell electrophysiology, we now show that two clusters of third-order olfactory neurons have dimorphic pheromone responses. One cluster responds in females; the other responds in males. These clusters are present in both sexes and share a common input pathway, but sex-specific wiring reroutes pheromone information. Regulating dendritic position, the fruitless transcription factor both connects the male-responsive cluster and disconnects the female-responsive cluster from pheromone input. Selective masculinization of third-order neurons transforms their morphology and pheromone responses, demonstrating that circuits can be functionally rewired by the cell-autonomous action of a switch gene. This bidirectional switch, analogous to an electrical changeover switch, provides a simple circuit logic to activate different behaviors in males and females.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Behavior, Animal
  • Brain / metabolism
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / physiology*
  • Female
  • Male
  • Nerve Tissue Proteins / metabolism
  • Olfactory Receptor Neurons / metabolism*
  • Pheromones / metabolism*
  • Sex Characteristics
  • Signal Transduction
  • Transcription Factors / metabolism

Substances

  • Drosophila Proteins
  • Nerve Tissue Proteins
  • Pheromones
  • Transcription Factors
  • fru protein, Drosophila