Abstract

The organisational principles of locomotor networks are less well understood than those of many sensory systems, where in-growing axon terminals form a central map of peripheral characteristics. Using the neuromuscular system of the Drosophila embryo as a model and retrograde tracing and genetic methods, we have uncovered principles underlying the organisation of the motor system. We find that dendritic arbors of motor neurons, rather than their cell bodies, are partitioned into domains to form a myotopic map, which represents centrally the distribution of body wall muscles peripherally. While muscles are segmental, the myotopic map is parasegmental in organisation. It forms by an active process of dendritic growth independent of the presence of target muscles, proper differentiation of glial cells, or (in its initial partitioning) competitive interactions between adjacent dendritic domains. The arrangement of motor neuron dendrites into a myotopic map represents a first layer of organisation in the motor system. This is likely to be mirrored, at least in part, by endings of higher-order neurons from central pattern-generating circuits, which converge onto the motor neuron dendrites. These findings will greatly simplify the task of understanding how a locomotor system is assembled. Our results suggest that the cues that organise the myotopic map may be laid down early in development as the embryo subdivides into parasegmental units.

Highlights

  • The way in which neural networks underlying locomotion are specified and assembled is less well understood than the development of other parts of the nervous system, the sensory nervous system

  • Because our interest lies in the mechanisms that underlie the assembly of the motor system, we focused on stages when each motor neuron first establishes a characteristic domain of arborisation within the neuropile

  • The cell bodies of segmental nerve (SN) motor neurons are located in the same segment as the muscles that they innervate, whereas intersegmental nerve (ISN) motor neuron somata are located in the segment anterior

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Summary

Introduction

The way in which neural networks underlying locomotion are specified and assembled is less well understood than the development of other parts of the nervous system, the sensory nervous system. Motor pools (and columns) reflect the locations of motor neuron cell bodies, but not the regions of the spinal cord where their dendritic arbors receive synaptic connections. It is not clear whether motor columns are a consequence of the process by which motor neurons are generated and specified or whether they reveal an underlying functional organisation in the motor system (Landmesser 1978). The task of understanding how the system is assembled would be greatly simplified if an underlying principle to the organisation of connectivity in a motor system could be demonstrated

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