Review
Making an escape: Development and function of the Drosophila giant fibre system

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Abstract

Flies escape danger by jumping into the air and flying away. The giant fibre system (GFS) is the neural circuit that mediates this simple behavioural response to visual stimuli. The sensory signal is received by the giant fibre and relayed to the leg and wing muscle motorneurons. Many of the neurons in the Drosophila GFS are uniquely identifiable and amenable to cell biological, electrophysiological and genetic studies. Here we review the anatomy and development of this system and highlight its utility for studying many aspects of nervous system biology ranging from neural development and synaptic plasticity to the aetiology of neural disorder.

Section snippets

From single cell to neural pathway: brief history of the Drosophila giant fibre system

Giant nerve fibres are a feature of the nervous system of many invertebrates and lower vertebrates and typically are associated with escape responses. The giants of giant fibres are the 0.5–1 mm diameter axons in the stellate ganglion of the squid. First described by Young in 1936 [1], this classical preparation was used by Hodgkin and Huxley [2] for their Nobel Prize winning experiments on the ionic basis of the action potential and ever since has served as a model for understanding nerve cell

The GFS is the neural basis of escape behaviour

Flight initiation in Drosophila involves a stereotyped sequence of events [9]. Voluntary flight begins with elevation of the wings from their resting position and is followed by a jump into the air brought about by extension of the middle legs. In the face of a threatening visual stimulus the pre-flight stage is dispensed with, saving at least 3 ms. The fly executes an escape jump with the wings still folded in the resting position and is airborne before they have unfolded fully into the lateral

The GFS: a model central neural pathway

Several features of the GF pathway make it an attractive model system. Many of the neurons can be identified by their size, position and distinctive morphology (Fig. 1; Supplementary material) and the development of individual neurons has been mapped (Fig. 2; Section 5). Identification and morphological analyses are facilitated by the fact that several of the GFS neurons form electrical synapses with their neighbours. Such synapses are assemblies of intercellular channels (gap junctions) that

Pattern of synaptic connections

Relatively little is known about the sensory pathways of the GFS. By contrast, the motor circuitry is very well defined; the GF–TTM and GF–DLM pathways, in particular, have been the focus of considerable attention since first described by King and Wyman [5] (Section 1). They observed, in light and electron micrographs, that the GF established close membrane contacts in T2 with the ipsilateral TTMn and PSI neurons. The PSI, in turn, formed conventional chemical synapses in the peripheral nerve

Birth of the GFS neurons

Both the GF and TTMn appear to be born during embryonic stages. These cells do not incorporate the thymidine analogue, bromodeoxyuridine, during larval and pupal stages nor can they be visualised in MARCM labelled clones generated at these stages indicating that they undergo their final division earlier in development [23], [41]. Moreover, no degenerating larval dendrites are seen at early pupal stages, which would be indicative of remodelling of persistent functional embryonic neurons [25],

Genetic regulation of GFS development

A large number of genes have been identified to play a role in the development of the GF circuit. Interestingly, while some genes have been found to function at a particular stage of development, others have functions during multiple stages.

The GFS in the study of normal and abnormal neural function

The GFS is a valuable model for examining normal and abnormal neural function within the context of an experimentally accessible central circuit in the fly. Historically, important contributions were made in characterising paralyzed (para) Na+ channel mutants [67], Shaker (Sh) K+ channel mutants [68], and shibire (shi) dynamin mutants [69]. More recently, the GFS has provided opportunities for studying physiological parameters of synaptic plasticity [70], [71], [72] and seizure disorder [73],

Summary

‘Escape’ neural circuits have long been attractive models because of their relative simplicity and known behavioural function. Typically, such circuits feature ‘giant’ neurons and synapses that lend themselves to cell biological and electrophysiological studies. Uniquely, in the Drosophila giant fibre system the tools of cell biology and physiology can be combined with sophisticated genetic techniques.

The GFS is one the most fully elucidated central neural circuits in the fly. Studies over the

Acknowledgements

We thank Robin Konieczny for the artwork in Fig. 1. M.J.A.'s research is supported by The Wellcome Trust (069710/Z/02/Z); T.A.G. is supported by NIH (RO1-NS044609 to R.K. Murphey).

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