Neuronal circuits for acoustic signals in Drosophila

Neuronal circuits are the functional units of the nervous system. Understanding their cellular composition, their connectivity and their principle of operation is a fundamental goal in neuroscience. Acoustic communication plays an important role in Drosophila courtship behavior. By vibrating one wing, the male fly generates a species specific pulse song with a precise pattern. Singing is innate and controlled by stereotyped neuronal classes expressing the putative transcription factor fruitless (fru). The "song neurons" identified so far are thought to be part of a sexually dimorphic circuit connecting action selection modules in the brain to a central pattern generator in the ventral nerve cord, which activates the motor neurons steering wing movements. The proposed project will explore and map this circuit for acoustic signals in Drosophila and aims to assemble a functional model of how signal generation is controlled by the nervous system. Major goals are the identification of a comprehensive set of neuronal classes involved in the generation of song by a combination of an anatomical and behavioral screen of neuronally expressed enhancer tile GAL4 lines. Further investigations are aimed to understand circuit features controlling the temporal patterns of the song, the difference in the neuronal control of song and flight and the role of sensory feedback during song production (sensory motor integration). Circuit connectivity (wiring diagram) and function will be addressed by Gfp reconstitution across synaptic partners (GRASP), neuronal epistasis experiments, functional imaging and electrophysiology. In addition, I intend to study sexual differentiation and the modulatory role of fru in the song circuit. Sexual differences in circuit architecture and their functional implications for singing behavior will be explored by cell specific sex change experiments. Using Drosophila acoustic signaling as a model system, the main objective of the project is the dissection of a potentially stereotyped and hard wired neuronal circuit dedicated to a specific innate behavior at a cellular resolution. The computational rules and the basic principles of action selection and pattern generation which orchestrate Drosophila song are expected to be of general relevance for circuit neuroscience.

In this project, it was investigated how the nervous system generates acoustic signals and which genes and nerve cells influence and control innate behaviour. The nervous system consists of functional units, so called neuronal circuits. It is a fundamental task of neuroscience to understand the cellular architecture, the connectivity and the function of these neuronal circuits. The building-up and organizational principles, the physiological characteristics of nerve cells and the gene expression in the nervous system are conserved in evolution. The fruitfly Drosophila melanogaster is thus a suitable model organism gain insight in nervous system function which is relevant for human medicine. Acoustic communications plays an important role in the courtship and mating behaviour of Drosophila. The male fly generates a species-specific courtship song by vibrating one wing in a controlled fashion. Many different genes, which are turned on in specifically interconnected nerve cells, are essential for the generation of this behaviour.In the course of this project, nerve cells for fine-tuned motor control and motor pattern generation were identified. When these nerve cells are silenced the fly either fails to generate courtship song or generates courtship song with different classes of characteristic structural defects. Some of the identified nerve cells are bifunctional, i.e. their function is also essential for flight behaviour. Moreover, significant insight was gained into how three different splice variants of the gene fruitless, which are only produced in male flies, lead to the development of sex-specific differences in the nervous system and, by doing so, influence song behaviour. All three variants of the gene are needed for correct courtship song and the respective mutants show an aberrant motor pattern during song production. One variant stands out in such that its lack in the male nervous system causes certain sex-specific nerve cells to develop a female-like morphology. These changed nerve cells fail to correctly process sensory stimuli important for song behaviour. This work in the model organism Drosophila contributed to the understanding how genes and gene variants act in circuits of defined nerve cells in order to generate and control fine-tuned motor behaviour.