The neuropeptide tachykinin is essential for pheromone detection in a gustatory neural circuit

Abstract

Gustatory pheromones play an essential role in shaping the behavior of many organisms. However, little is known about the processing of taste pheromones in higher order brain centers. Here, we describe a male-specific gustatory circuit in Drosophila that underlies the detection of the anti-aphrodisiac pheromone (3R,11Z,19Z)-3-acetoxy-11,19-octacosadien-1-ol (CH503). Using behavioral analysis, genetic manipulation, and live calcium imaging, we show that Gr68a-expressing neurons on the forelegs of male flies exhibit a sexually dimorphic physiological response to the pheromone and relay information to the central brain via peptidergic neurons. The release of tachykinin from 8 to 10 cells within the subesophageal zone is required for the pheromone-triggered courtship suppression. Taken together, this work describes a neuropeptide-modulated central brain circuit that underlies the programmed behavioral response to a gustatory sex pheromone. These results will allow further examination of the molecular basis by which innate behaviors are modulated by gustatory cues and physiological state.In many species of animals, the male decides to pursue a potential female mate based on how she smells and tastes. Powerful chemical signals known as pheromones control this decision. When a male fruit fly mates with a female fruit fly, he often leaves behind an anti-aphrodisiac pheromone that, when males taste it, deters them from mating with the female. Until recently, however, little was known about how the brain processes information from such taste pheromones.Now, Shankar et al. have investigated this problem in a series of experiments with normal and genetically modified flies. In the first experiment normal male flies were exposed to the chemical on its own, to the chemical on a sample of female skin, and to the chemical on actual female flies. The male flies did not respond to the pheromone on its own, but they did respond to it in the other two scenarios.Next, Shankar et al. used genetic techniques to eliminate individual neurons in the male flies and then observed how the loss of specific neurons influenced the response of the fly to the pheromone. These experiments showed that male flies have a special group of sensory neurons in their legs that detect the chemical and then send an electrical signal to the brain. Shankar et al. then went on to identify a brain circuit consisting of 8–10 neurons that responds to this signal and to show that the release of a neurochemical called Tachykinin is essential in communicating the signal.In a final set of experiments, Shankar et al. introduced two sensors—one in the sensory neurons in the legs, the other in the 8–10 neurons in the brain—that light up when the neurons in that region are close enough to each other to form connections. The results suggest that the sensory neurons in the legs form connections with the 8–10 neurons in the brain.A challenge for the future is to understand how the nervous system combines different social cues and information about the physiological state of the animal, and how this influences the decision to mate.