Abstract

We describe the anatomy of all the primary motor neurons in the fly proboscis and characterize their contributions to its diverse reaching movements. Pairing this behavior with the wealth of Drosophila's genetic tools offers the possibility to study motor control at single-neuron resolution, and soon throughout entire circuits. As an entry to these circuits, we provide detailed anatomy of proboscis motor neurons, muscles, and joints. We create a collection of fly strains to individually manipulate every proboscis muscle through control of its motor neurons, the first such collection for an appendage. We generate a model of the action of each proboscis joint, and find that only a small number of motor neurons are needed to produce proboscis reaching. Comprehensive control of each motor element in this numerically simple system paves the way for future study of both reflexive and flexible movements of this appendage.

Highlights

  • To interact with the world, many organisms rely on an ability to reach an appendage towards a target, yet much remains to be discovered about how neural circuits control this prototypical goaldirected behavior

  • The haustellum extends and flexes from its joint with the rostrum. These movements were confirmed in live flies by filming proboscis extension in a synchrotron particle accelerator, using x-rays to render flies partly transparent and show the movement of the segments inside the head capsule (Video 1)

  • The present work describes the anatomy and function of motor neurons controlling each muscle of the fly proboscis

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Summary

Introduction

To interact with the world, many organisms rely on an ability to reach an appendage towards a target, yet much remains to be discovered about how neural circuits control this prototypical goaldirected behavior. Previous efforts using GAL4 lines with broader expression patterns, or stochastic techniques to refine GAL4 lines, identified some of the critical motor neurons (Gordon and Scott, 2009; Schwarz et al, 2017). We use the split GAL4 technique, which intersects two expression patterns to genetically target only the cells in common between the two (Luan et al, 2006), to provide more precise and reproducible targeting of particular neurons. We create a collection of split GAL4 fly strains to identify and separately target the primary motor neurons for every proboscis muscle

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