Figures
Citation: (2003) Underlying Principles of Motor System Organization Revealed. PLoS Biol 1(2): e56. https://doi.org/10.1371/journal.pbio.0000056
Published: November 17, 2003
Copyright: © 2003 Public Library of Science. This is an open-access article distributed under the terms of the Public Library of Science Open-Access License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Time after time in biology, revelations about structure lead to insights about corresponding functional mechanisms. While evolution throws in the occasional spandrel, more often organizational structure serves a practical purpose. So naturally, neuroscientists wonder, does the architectural organization of the motor system reveal an underlying functional organization?
Progress on this question has been complicated by the fact that there appears to be no clear correspondence between the development of motor neurons centrally and their target muscles in the periphery. In the visual system, for example, retinal ganglion cells send axons in an ordered manner into the brain, where they form connections with neurons of the primary visual center in the brain responsible for detecting visual targets. The arrangement of these connections mirrors the neighboring relationships of the neurons in the retina, and so the neural map of connections in the brain is an “anatomical correlate” of the arrangements in the retina. The origin of these anatomical relationships can be traced through the process of development, allowing scientists to link the assembly of this sensory system with the function of the neurons involved. Matthias Landgraf and colleagues now report that in the fruitfly Drosophila the arrangement of motor neurons corresponds to the distribution of their target muscles. Thus, anatomical correlates also exist in the motor system, in the form of a “myotopic map,” where the arrangement of motor neuron dendritic branches in the central nervous system reflects the distribution of their target body wall muscles in the periphery.
Starting with the larger question of how the neural networks governing locomotion are specified and assembled during development, the researchers decided to see if they could identify an elementary principle of motor system organization. Working in Drosophila, they examined motor neurons and the body wall muscles they innervate. With an eye toward understanding the mechanisms directing the assembly of the motor system, the researchers concentrated on the early stages of development, when the motor neurons first establish their characteristic dendritic territories. They found that the dendrites of motor neurons innervating internal muscles and that those innervating external muscles do in fact project into distinct regions, corresponding to the distinct mapping of the muscles themselves. Surprisingly, the arrangement of the dendrites in the myotopic map forms independently of the muscles they innervate. It may be, the researchers suggest, that the initial signals charting the location of the dendrites are set very early in development, when the coordinates for other structural elements are established. But that question requires further investigation.
The researchers are among the first to reveal such an orderly connection between patterns of motor neuron dendrites and patterns of muscles. This organization, in the form of the myotopic map, may be mirrored by the patterning of processes of higher-order neurons, which form connections with the motor neuron dendrites themselves. In vertebrates, studies have shown that motor neurons are grouped into “pools” and “columns” that correlate with the muscles they innervate. But because these pools and columns represent the location of the cell bodies and not the areas of the spinal cord where the neurons receive most of their inputs, that is, their dendritic branches, scientists could not say whether the pools and columns are simply spandrels— an incidental result of the way motor neurons are generated—or mirror a functional organization of the motor system. This novel finding in Drosophila will pave the way for future studies on the relationship between anatomy and physiology during development. It will be particularly interesting to discover whether such myotopic arrangements of motor neuron dendrites are unique to insects or whether this organizational principle occurs in other motor systems, including vertebrates.