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Neural Circuits Underlying Mating Behavior in Drosophila

  • Author(s): Kallman, Benjamin Rory
  • Advisor(s): Scott, Kristin
  • et al.
Abstract

Reproduction is essential for the survival of animal species. Males and females exhibit innate sex-specific reproductive behaviors, which are established developmentally and do not require previous experience. Because mating can be energetically costly, animals have evolved mechanisms to distinguish between reproductively viable and futile conspecifics that rely largely on sex-specific pheromones. How these complex, often antagonistic cues are transmitted from the periphery to the higher brain, the neural circuits they activate, or the computational principles by which they are integrated remain unclear.

In the first part of this dissertation, I investigate the neural circuits underlying mating behavior in the fruit fly Drosophila melanogaster, leading to a novel model of decision-making. I employ anatomical, calcium-imaging, optogenetic, and behavioral studies to demonstrate 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, I show that sensory neurons that detect male pheromones, as well as those that detect female pheromones, activate GABAergic mAL neurons to inhibit P1 neurons. These data support a model in which the balance of excitatory and inhibitory inputs onto central courtship-promoting neurons regulates the decision to court.

In the second part of this dissertation, I develop methods to visualize the morphology of neurons in taste processing in the fly brain. I employ large-scale calcium imaging coupled to cell labeling to identify sweet- or bitter-responsive neurons in the subesophageal zone (SEZ), the primary taste relay in the fly brain. I successfully use this approach to label SEZ motor neurons and demonstrate that they are tuned to a single taste modality, arguing for labeled-line processing of taste from sensory input to motor output. Nonetheless, reliably labeling single, non-motor SEZ neurons using this strategy has been difficult. Using a modified approach incorporating a nuclear-localized calcium indicator, I reproducibly label a cluster of putative bitter-responsive SEZ neurons. Based on their morphology, these neurons appear to be inhibitory olfactory projection neurons (iPNs), which transmit information from the antennal lobe to the lateral horn, suggesting that taste inputs may modulate the processing of odors.

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