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The neural basis of acoustic communication in Drosophila

Subject Area Cognitive, Systems and Behavioural Neurobiology
Term from 2017 to 2024
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 329518246
 
Final Report Year 2024

Final Report Abstract

Social behaviors often rely on acoustic communication, yet the mechanisms behind signal production, coordination, processing, and behavioral transformation are largely unknown. We investigated these processes using Drosophila courtship as a model system, by combining behavioral experiments, genetic manipulations, calcium imaging, and computational modeling. Drosophila males use chemical cues to initiate courtship. Female chemical cues drive and male chemical cues suppress courtship. Interestingly, playback of song overrides to suppression of male chemical cues and drives male-directed courtship. Studying the integration of acoustic and chemical cues was the first objective of this project. By systematically manipulating chemical and acoustic cues during social interactions of a male with another male or a female, we find that gustatory and acoustic cues are integrated linearly to control social interactions. Statistical models reveal with male gustatory cues have a strong negative weight, suppress interactions and promote male-directed aggression. By contrast, female gustatory cues promote interactions and courtship. Olfactory cues have a secondary role. Having decided to court, the male chases the female and produces a song consisting of two modes - pulse and sine - by extending and fluttering one wing. In addition, males also produce substrate-borne vibrations. While the behavioral contexts and neural circuits that drive song are well-studied, when and how multimodal signals are produced is unclear. In the second part of this project, we identified the behavioral contexts and neural circuits that drive multimodal signaling in Drosophila. Computational models, tested using causal optogenetic manipulations of behavior reveal that stationarity drives vibrations. We then show that brain neurons that drive song also drive vibrations and set the locomotor state for vibrations. This implies that an single circuit controls multimodal signaling and coordinates it with ongoing behavior. One advantage of this integrated control is that signaling can be easily globally modulated by modifying only few circuit nodes. Females and males integrate acoustic, vibrational, visual, and chemical cues to inform their mating behavior. Using playback experiments we show that the sign or locomotor responses to song differs between sexes but that the feature selectivity is sex-shared. We then identified a shared set of neurons in both males and females that detect species-specific songs and drive sex-specific behavioral responses. These neurons exhibit similar feature selectivity but trigger distinct locomotor responses in each sex. By combining genetic tools and computational modeling, we have elucidated the neural mechanisms underlying social behavior in Drosophila. Our findings provide insights into how the brain controls the decision to engage in social interactions, the selection of appropriate signals, and the perception and interpretation of these signals.

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