Abstract

Coordinated walking in vertebrates and multi-legged invertebrates [corrected] such as Drosophila melanogaster requires a complex neural network coupled to sensory feedback. An understanding of this network will benefit from systems such as Drosophila that have the ability to genetically manipulate neural activities. However, the fly's small size makes it challenging to analyze walking in this system. In order to overcome this limitation, we developed an optical method coupled with high-speed imaging that allows the tracking and quantification of gait parameters in freely walking flies with high temporal and spatial resolution. Using this method, we present a comprehensive description of many locomotion parameters, such as gait, tarsal positioning, and intersegmental and left-right coordination for wild type fruit flies. Surprisingly, we find that inactivation of sensory neurons in the fly's legs, to block proprioceptive feedback, led to deficient step precision, but interleg coordination and the ability to execute a tripod gait were unaffected.DOI:http://dx.doi.org/10.7554/eLife.00231.001.

Highlights

  • Ever since life became terrestrial ∼360 million years ago, animals have developed increasingly sophisticated methods to navigate their environments (Dickinson et al, 2000)

  • To measure the biomechanical features underlying walking in Drosophila we turned to an optical effect known as frustrated Total Internal Reflection (Zhu et al, 1986)

  • The frustrated Total Internal Reflection (fTIR) method and FlyWalker software provides a robust suite of tools for analyzing walking in Drosophila

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Summary

Introduction

Ever since life became terrestrial ∼360 million years ago, animals have developed increasingly sophisticated methods to navigate their environments (Dickinson et al, 2000). One of the most common forms of terrestrial locomotion depends on the movement of multi-jointed legs For this to occur, animal nervous systems face two main computational challenges. Multiple leg joints must move rhythmically and in a precisely coordinated fashion to allow the stereotyped movements that occurs during the swing and stance phases of each step cycle These movements must be coordinated between legs, which number four in a typical tetrapod and six in a hexapod. Leg movement coordination is assisted by proprioceptive sensory inputs that report the load and position of leg joints (Bässler, 1977; Borgmann et al, 2009) Other sensory modalities, such as visual, olfactory and gravitational, modulate the activity of locomotor CPGs to allow animals to readily change their motor behavior in response to their environment (Frye, 2010)

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