Excitation and inhibition onto central courtship neurons biases Drosophila mate choice

Abstract

The ability to distinguish males from females is essential for productive mate selection and species propagation. Recent studies in Drosophila have identified different classes of contact chemosensory neurons that detect female or male pheromones and influence courtship decisions. Here, we examine central neural pathways in the male brain that process female and male pheromones using anatomical, calcium imaging, optogenetic, and behavioral studies. We find that sensory neurons that detect female pheromones, but not male pheromones, activate a novel class of neurons in the ventral nerve cord to cause activation of P1 neurons, male-specific command neurons that trigger courtship. In addition, sensory neurons that detect male pheromones, as well as those that detect female pheromones, activate central mAL neurons to inhibit P1. These studies demonstrate that the balance of excitatory and inhibitory drives onto central courtship-promoting neurons controls mating decisions.

DOI: http://dx.doi.org/10.7554/eLife.11188.001

eLife digest

Courtship displays are seen throughout the animal kingdom. For example, male birds-of-paradise are perhaps best known for the elaborate dances they use to attract a mate. Male fruit flies, belonging to the species Drosophila melanogaster, also perform courtship toward female flies. However, male flies do not court other males. Previous studies have shown that sex-specific chemical signals (or pheromones) are important cues that males use to direct courtship towards females. Researchers have previously identified two sets of sensory neurons that detect pheromones: one set detects female pheromones and promotes courtship, while the other detects male pheromones and inhibits courtship. However it was unclear how these sensory neurons controlled courtship behavior.

Now, Kallman et al. have studied the circuits of neurons in the fruit fly that promote or inhibit courtship when a fly detects a pheromone. The experiments identified several pathways of neurons in the brain of male Drosophila that respond to female and male pheromones. These pathways send signals that either excite or inhibit a central target, called P1 neurons. Female pheromones activated a pathway that activates the P1 neurons, whereas male pheromones activate another pathway that inhibits the P1 neurons. Kallman et al. suggest that the balance of these excitatory and inhibitory signals controls a fly’s decision to court.

Following on from this work one of the next challenges will be to identify the neural circuits that act downstream of the P1 neurons to control courtship. Future studies could also explore how P1 neurons integrate signals from different senses.

DOI: http://dx.doi.org/10.7554/eLife.11188.002