Date Published: November 17, 2003
Publisher: Public Library of Science
Author(s): Matthias Landgraf, Victoria Jeffrey, Miki Fujioka, James B Jaynes, Michael Bate
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.
Partial Text: 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, particularly the sensory nervous system. One of the reasons for this is that, in many sensory systems, in-growing sensory axons are marshalled to form a clear anatomical map of peripheral characteristics in the central nervous system (CNS) (for reviews, see Knudsen 2002; Keller and Vosshall 2003; McLaughlin et al. 2003). This straightforward anatomical outcome of the developmental process, which rather explicitly reflects the function of the neurons concerned, means that developmental observations and experiments can readily be interpreted in terms of axon growth and targeting within the orderly framework of the map. For motor systems, on the other hand, there appears to be no such simplifying anatomical correlate of function, at least insofar as the underlying patterns of neuronal connectivity are concerned. Nonetheless, there are some regularities on the motor side. In the vertebrate spinal cord, motor neurons are organised into pools and columns that form a neural correlate of the anatomy of the body musculature they innervate. Motor neurons innervating the same muscles are clustered into pools, and motor pools are grouped into columns, each supplying a different muscle set (Landmesser 1978; Tsuchida et al. 1994). The organisation of motor pools is highly conserved among different species and, to a degree, reflects the distribution of the muscles that they supply (Romanes 1951; Cruce 1974; Landmesser 1978). However, 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. Thus, it is not clear whether motor columns are simply a consequence of the process by which motor neurons are generated and specified or whether they actually 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.