Repeating patterns of motoneurons in nematodes: the origin of segmentation?

Abstract

Evolutionarily diverse groups of animals share numerous similarities as individual neurons are assembled into functional neural circuits. One example is the hierarchical sequence of events that individual nerve cells follow during morphological development. In the initial step a presumptive neuron is generated and positioned appropriately. Second, the undifferentiated cell elaborates a growth cone capable of interacting with extrinsic cues and leading the presumptive axonal process as it is guided into areas where potential synaptic targets reside. Finally, the differentiating nerve cell selects among appropriate and inappropriate target cells as it completes the process of selective synaptogenesis. The extracellular matrix molecule laminin provides a second example, this time at the molecular level. Biochemical and genetic studies have shown that this molecule directs process guidance of neurons in vertebrates, annelids, and nematodes. In both examples an interest in neural development has provided a window through which evolutionarily processes have been revealed. The free-living soil nematode Caenorhabditis elegans possesses several features that collectively place it in a rather unique position among metazoans and has allowed genetic and cellular studies to be integrated at the level of identified neurons and neural circuits. This review will focus on developmental studies of C. elegans locomotory neural circuits. General issues that will be addressed are the similarities and differences among different taxa regarding: the relationship between cell lineage and cell fate determination in generating reiterative neural patterns; pioneer cells and the molecular basis for process guidance and finally genetic epigenetic events involved in sculpting highly specific synaptic patterns.