Normal segmentation and size of the primary sympathetic ganglia depend upon the alternation of rostrocaudal properties of the somites

Abstract

Metameric organization of the dorsal root ganglia (DRG) and ventral roots depends on the alternation of rostrocaudal properties within the somites. In addition, the size of DRG is likely to be regulated by the adjacent mesoderm, because unilateral creation of a paraxial mesoderm with only rostral somitic (RS) halves, leads to the development of non-segmented DRG that are larger and contain more cells than the sum of the contralateral, control DRG. We have now extended our studies of the role of the paraxial mesoderm in the morphogenesis of the peripheral nervous system (PNS) to another metameric PNS component, the sympathetic ganglia (SG). The development of the primary sympathetic chain was studied in chick-quail chimeras with multiple half-somite grafts using quantitative morphometric analysis. In the presence of an exclusively rostral or caudal somitic mesoderm, segmentation of the initially homogeneous primary sympathetic chain into ganglia is prevented. Therefore, the SG, like the DRG and ventral roots, require the normal rostrocaudal alternation of the somitic mesoderm for segmental morphogenesis. On embryonic day 4 (E4), there is a 38% average decrease in the volume of the primary sympathetic chain opposite a RS mesoderm, compared with the primary chain on the unoperated side. This is in contrast to the average increase of 27% in the volume of the DRG opposite the grafted mesoderm in the same embryos. Our results, and classical observations, have led us to propose a model in which the mesoderm controls DRG and SG size by modulating the partition of migrating NC precursors between the anlage of these two ganglion types. According to this model, the reduction in SG volume and concomitant increase in DRG volume observed opposite RS grafts, results from the arrest in the DRG anlage of neural crest cells that normally migrate to the SG.