Quantitative lineage analysis of the origin of frog primary motor and sensory neurons from cleavage stage blastomeres.

The average number of primary motoneurons and Rohon-Beard neurons that descend from each "identified" blastomere of the 16- and 32-cell stages of the frog Xenopus laevis was determined. The dorsal, animal blastomeres are the major motoneuron progenitors, and the ventral, animal blastomeres are the major Rohon-Beard progenitors. Cells along the midline primarily give rise to only one of these phenotypes, whereas cells along the frontal plane, which separates dorsal from ventral, give rise to both phenotypes. Each blastomere produces a characteristic number of each type of neuron, with only small variations between embryos. The mean values were used to construct quantitative retrospective lineage diagrams for the first 5 cell cycles after fertilization. These diagrams illustrate that the fate to become a major neuronal progenitor is segregated as early as the 4-cell stage. The lineage patterns of which sister cell makes the majority of primary neurons at each cleavage after the 4-cell stage are quite similar for both neurons in the D lineage but only moderately similar for both neurons in the V lineage. The pattern of predominant Rohon-Beard neuron fate is very similar in the D and V lineages. Analysis of the axial distribution of the primary motoneurons and Rohon-Beard neurons that descend from each blastomere indicates that the major progenitors contribute neuronal descendants periodically, to nearly every segmental bin, but the minor progenitors distribute neuronal descendants randomly along the axis. These data demonstrate that primary neuronal phenotype, cell number, predominant lineal pattern, and in some cases segmental distribution are highly regular across a large population of embryos. This population consistency suggests that several features of neuronal fate may be influenced either by cell position or lineage.