Silenced gustatory inputs reveal new populations of pheromone detection cells involved in Drosophila courtship and support a non-associative basis for courtship conditioning

Male Drosophila suppress courtship toward virgin females after an unproductive sexual encounter with a mated female. This learned behavior is mediated by pheromones and has been formalized as associative learning in a paradigm called courtship conditioning. To identify the neural machinery responsible, four populations of gustatory receptor neurons (GRNs) were functionally silenced during the male\u27s initial training or subsequent test experience. While silencing all four populations reduced hard-wired courtship toward virgin females, behavioral differences arose when GRNs were silenced during training versus testing, or when males courted flies with different pheromone blends. Thus individual GRNs within a population control different aspects of behavior; a result which parallels the organization and drive of other gustatory behaviors like feeding and avoidance. To identify potential courtship circuits within the populations silenced, the behavioral results were compared across courtship contexts to generate courtship channels: hypothetical pathways connecting courtship behaviors to sub-sets of GRNs. One channel identified suggests courtship conditioning may not be associative in the classical formulation: males with this channel silenced during training suppress courtship selectively depending on the pheromones encountered during testing. An alternative theory, called the independent channel model, explains this and other long-standing anomalous results by proposing that courtship suppression is produced by experience modifying the efficacy of individual courtship channels to drive courtship