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New fruit fly resource reveals nerve circuits that control flight and courtship

A team of researchers have created a new resource for studying motor control of wing movements in fruit flies.

The study, recently as a Reviewed Preprint in eLife, is described by the editors as an important resource paper presenting a library of cell-type-specific genetic driver lines that label wing-related motor and premotor neurons in the ventral nerve cord (VNC) of the fruit fly, Drosophila melanogaster.

The toolkit is systematically validated with compelling anatomical and behavioral evidence and will provide a resource for future studies of Drosophila flight and courtship.

All animals must perform precisely controlled movements enabling them to survive and reproduce. In the fruit fly, these motor functions are controlled by the VNC, which receives and processes sensory information and generates the movements required for functions such as walking, flight and courtship.

"Wing behaviors comprise some of the most fascinating examples of motor control," says lead author Erica Ehrhardt, a former postdoctoral researcher at HHMI's Janelia Research Campus, Virginia, U.S. "In flight, subtle adjustments can have large aerodynamic consequences, whereas on the ground male flies' tightly patterned and subtle wing vibrations create a species-specific courtship song."

These different behaviors use the same limited set of motor neurons and muscles, but how the pre-movement VNC circuits generate these distinct context-dependent movements through the same set of neurons is not well understood.

To address this, the team used state-of-the-art genetic engineering methods to produce a large set of transgenic fly "driver" lines that could then be used to identify the constituent neurons in the pre-movement VNC circuits. They identified 196 unique dorsal VNC cell types targeted by 195 stabilized fly driver lines in the library. This included different types of neurons in the dorsal region of the VNC that connect to wing muscles or other regions and can now be studied and manipulated experimentally.

To demonstrate the library's utility, the researchers performed a series of behavioral and anatomical tests. First, they used reagents targeting the wing motor neurons and mapped the manipulation of individual motor neurons to specific flight and courtship behaviors. They found activation of specific neurons during tethered flight that caused measurable changes in wing motion, consistent with previous studies.

But, they also found some subtle differences. For example, while activation of a steering muscle motor neuron called i2 decreases wing stroke amplitude, activation of a related motor neuron, i1, did not—even though previous studies predicted the two motor neurons would have similar effects.

For courtship behaviors, they found that silencing a specific motor neuron called tp2 affected all aspects of courtship song, whereas silencing of other neurons only affected specific components of the wing action during song—either pulsing or a continuous tone.

Next, they worked out the developmental origins of the 196 target cells and the sites (muscles and/or brain) to which they send and receive neurological signals. This information was then matched with data from the published VNC connectome, providing a useful resource for future investigations of these neurons.

"This suggests there might be discrete populations of neurons involved in the control of wing behaviors," says Ehrhardt. "Future studies using this new resource can probe the functional importance of this subset of cells."

"Together the results lay the groundwork for a basic functional architecture of the neuronal circuitry controlling wing movements and provide an important resource for future investigations of the neurons underlying motor behavior," says senior author Wyatt Korff, Senior Director of Team Projects at HHMI's Janelia Research Campus.

"The library should enable researchers to probe the premotor circuits controlling the rich set of behaviors that require wing, neck or haltere coordination, such as flight or courtship."