Neural circuit and molecular mechanisms underpinning mating state-dependent choice behavior in Drosophila females

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Every day our choices and decisions reflect our current internal state. Our immediate actions, but also how we remember a sensory experience strongly depends on our internal state. For instance, food not only smells and tastes better when we are hungry, our memory of such as meal is enhanced. It was previously proposed that neuromodulation of sensory neurons facilitates sensory processing and state-dependent long-term changes in animal behavior, by filtering sensory experiences. However, experimental evidence supporting this role and the mechanistic connection between organismic physiology and sensory processing remains insufficient. Here, I propose to use a model system based on female reproductive state-dependent behavior that we have recently developed to address two important questions using a combination of behavioral analysis, optical physiology, and genetics: (1) How do internal organs communicate internal states to modulate sensory neuron responses? (2), which concrete role does sensory neuromodulation play in long-term changes of animal behavior?Reproductive states including pregnancy influence a female s sensory perception of odors and tastes. Using the model organism Drosophila melanogaster, we recently showed that a G-protein coupled receptor (GPCR)-dependent neuromodulation of specific odor and taste sensory neurons was necessary and sufficient to change a female s choice behavior upon mating to match her changed internal state. Surprisingly, while this sensory neuron modulation lasted only for a few hours, mated females maintained the new choice behavior for several days. Furthermore, while we know the neuromodulator and its receptor in sensory neurons, the initial mating signal connecting internal organs or nerves and its role in initiating neuromodulation in sensory neurons remained elusive. Therefore, our previous work provides a great framework to address the above posed questions. In a first work package, we will characterize the role of candidate molecules from a genetic screen as signals from internal organs and nerves and unravel the underpinning molecular and neural circuit mechanisms. Furthermore, we will analyze the role of taste receptor neurons in the female gut as putative mediators of internal state and physiology. In a second work package, we will map the neural circuit that connects the identified odor and taste neurons to higher brain centers and address additional neuromodulation in higher neurons. Finally, we will test whether transient modulation of sensory neurons might facilitate memory formation and thereby long-term behavioral changes by sensory filtering. Both work packages therefore deal with questions of general interest and are embedded in a well-established experimental framework that our lab has developed in the recent years.