Abstract

The precise coordination of body parts is essential for survival and behavior of higher organisms. While progress has been made towards the identification of central mechanisms coordinating limb movement, only limited knowledge exists regarding the generation and execution of sequential motor action patterns at the level of individual motoneurons. Here we use Drosophila proboscis extension as a model system for a reaching-like behavior. We first provide a neuroanatomical description of the motoneurons and muscles contributing to proboscis motion. Using genetic targeting in combination with artificial activation and silencing assays we identify the individual motoneurons controlling the five major sequential steps of proboscis extension and retraction. Activity-manipulations during naturally evoked proboscis extension show that orchestration of serial motoneuron activation does not rely on feed-forward mechanisms. Our data support a model in which central command circuits recruit individual motoneurons to generate task-specific proboscis extension sequences.

Highlights

  • Locomotion and behavioral motor sequences are generated by a precise movement of selected body parts

  • central pattern generators (CPGs) are involved in the generation and coordination of stereotyped motion patterns of limb or appendage segments depending on alternating extensor-flexor muscle activation (Grillner, 2003; Talpalar et al, 2011; Tripodi et al, 2011; Zhang et al, 2014)

  • Our analysis revealed that the proboscis extension response (PER) program consists of four major extension steps prior to food ingestion

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Summary

Introduction

Locomotion and behavioral motor sequences are generated by a precise movement of selected body parts. Significant progress has been made towards the identification of central neuronal circuitries mediating and controlling the alternation of limb movement necessary for walking or swimming in both invertebrate and vertebrate model systems (Berkowitz et al, 2010; Guertin, 2009; Marder et al, 2005; Talpalar et al, 2013) These studies demonstrated that in many cases local central pattern generators (CPGs) and reciprocal inhibitory interneuron networks coordinate the alternating activation of limb motor units (Berkowitz et al, 2010; Borgmann and Buschges, 2015; Buschges et al, 2011; Crone et al, 2008; Guertin, 2009; Lanuza et al, 2004; Marder et al, 2005; Talpalar et al, 2013).

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