Oligodendrocytes are the myelin-forming cells in the central nervous system of vertebrates. In the rodent embryo, these cells have been shown to emerge from restricted territories of the neuroepithelium. However, a comprehensive view of the development of oligodendroglial populations from their ventricular sources remains to be established. As a first step toward this aim, we have examined in vivo the spatiotemporal emergence of oligodendrocytes in the chick embryonic brain. We have detailed the patterns of expression of three early markers of the oligodendroglial lineage: the plp/dm-20 and PDGFRalpha transcripts and the O4-reactive antigen. During embryonic development, these molecules showed a similar segmental pattern of expression. However, plp/dm-20(+) cells were already observed, in the ventricular layer, at E2.5, i.e., 2 days before the appearance of O4(+) and PDGFRalpha(+) cells, suggesting that oligodendrocyte precursors arise nearly simultaneously with neurons. In the chick embryonic brain, the onset of expression of plp/dm-20 appears therefore to be the earliest event indicative of oligodendroglial specification and we propose, based on the expression of plp/dm-20 transcript, a ventricular map of the foci at which oligodendrocytes originate. In addition, we document the precocious segregation, from E5, of plp/dm-20(+) and PDGFRalpha(+) oligodendroglial cells in the subventricular and mantle layers of the brain.

In the central nervous system (CNS), oligodendrocytes have long been considered to be the last cell type to be generated during development. In rodents, the progenitor cells that give rise to oligodendrocytes have been reported to originate in the subventricular zone. Here, we review recent data demonstrating the existence of oligodendrocyte precursor cells in the ventricular layer of the neural tube that emerge prior to the progenitor stage. Oligodendrocyte precursors arise in restricted foci that are distributed along the rostrocaudal axis of the neural tube, for the most part ventrally. The generation of oligodendrocyte precursor cells occurs either simultaneously with, or follows closely upon the emergence of the first neurons. Experiments with quail-chick chimeras provide evidence that oligodendrocyte progenitors derived from ventricular precursors migrate either tangentially or radially to colonize extensive or segmentally restricted territories of the brain. The choice depends on their site of origin. Finally, we discuss the possibility that oligodendrocytes could be a mosaic population that originates from at least two types of precursor cells.

Oligodendrocytes are the myelin-forming cells in the central nervous system. In the brain, oligodendrocyte precursors arise in multiple restricted foci, distributed along the caudorostral axis of the ventricular neuroepithelium. In chick embryonic hind-, mid- and caudal forebrain, oligodendrocytes have a basoventral origin, while in the rostral fore-brain oligodendrocytes emerge from alar territories (Perez Villegas, E. M., Olivier, C., Spassky, N., Poncet, C., Cochard, P., Zalc, B., Thomas, J. L. and Martinez, S. (1999) Dev. Biol. 216, 98–113). To investigate the respective territories colonized by oligodendrocyte progenitor cells that originate from either the basoventral or alar foci, we have created a series of quail-chick chimeras. Homotopic chimeras demonstrate clearly that, during embryonic development, oligodendrocyte progenitors that emerge from the alar anterior entopeduncular area migrate tangentially to invade the entire telencephalon, whereas those from the basal rhombomeric foci show a restricted rostrocaudal distribution and colonize only their rhombomere of origin. Heterotopic chimeras indicate that differences in the migratory properties of oligodendroglial cells do not depend on their basoventral or alar ventricular origin. Irrespective of their origin (basal or alar), oligodendrocytes migrate only short distances in the hindbrain and long distances in the prosencephalon. Furthermore, we provide evidence that, in the developing chick brain, all telencephalic oligodendrocytes originate from the anterior entopeduncular area and that the prominent role of anterior entopeduncular area in telencephalic oligodendrogenesis is conserved between birds and mammals.