A new approach to the development of the cerebellum provided by the quail-chick marker system

Abstract

We have used the quail-chick chimera system to reveal the cell migrations and settling pattern involved in the construction of the cerebellum. Three types of orthotopic transplantations were carried out, between quail and chick embryos, at the 12-somite stage: exchanges of (i) the whole metencephalic vesicle, (ii) the lateral half of this vesicle and (iii) the diencephalic plus the mesencephalic vesicles. Histological study of chimeric embryos and young chicks provided the following results: longitudinal morphogenetic movements distort the embryonic neural tube as early as the fifth embryonic day, so that the dorsal limit of the mes-, met- and myelencephalic vesicles are displaced caudad and their ventral limits rostrad. This leads to a participation of mesencephalic vesicular material in the construction of the cerebellum. Cells originating in the mesencephalic vesicle are found in a rostromedial V-shaped region, in all the cerebellar cellular layers, except the external granular layer, the presumptive territory of which is entirely located in the metencephalic vesicle. The chimerism of the rostromedial part of the cerebellum allows the analysis of the origin of the various cerebellar cell types. We find (i) that the Purkinje cells always have the same cellular marker as the ventricular epithelium radially beneath them. This strongly suggests that these cells reach their final localization following strictly radial migrations. (ii) Most of the small cells surrounding the Purkinje neurons and most of the neurons and glial cells of the molecular layer are also of the same type as the ventricular epithelium they surmount, i.e. different from the type of the external granular layer cells. Therefore, they are not derived from the external granular layer and are not of the same origin as the granule cells as previously believed. Unilateral substitutions of the metencephalic vesicle revealed that transverse cell migrations occur across the sagittal plane. They have been observed mainly in the inner and external granular layers, but also, though to a lesser extent, in the molecular layer and in the cell layer located at the level of the Purkinje neurons. These observations show that the position of cerebellar cells is determined by both morphogenetic movements and cell type-specific active radial and tangential migrations. The quail-chick chimera system is thus able to provide new information both on the origin of cerebellar cells and how each cell type assumes its final position.