The differentiation of the olfactory placode in Xenopus laevis: A light and electron microscope study

Abstract

AbstractThe origin and development of the olfactory neuroepithelium of Xeno‐pus laevis has been investigated with light microscopy and scanning and transmission electron microscopy.The cranial ectoderm of the Xenopus laevis embryo consists of two layers: The inner layer is called the sensory or nervous layer (NL) and the outer layer is called the nonnervous layer of the ectoderm (NNE). Between stages 23 and 26, the presumptive olfactory region consists of two discretely arranged cellular populations: the cells of the olfactory placode proper derived from the NL and the cells of the overlying NNE. After stage 26 the placodal cells begin to move toward the body surface by migrating between the NNE cells. As the placodai cells migrate they sprout an apical process which reaches the body surface at approximately stage 28. The apical process contains free and membrane‐bound ribosomes, elongated mitochondria, and microtubules oriented parallel to the process. Centrioles and basal bodies are present in the apical cytoplasm and microvilli and cilia project from the process's surface. The structure and ultrastructure of the apical process identify it as the dendrite of an olfactory neuron. As the apical process reaches the epithelial free surface, a second process sprouts from the base of the cell. This process pierces the basal lamina at stage 29/30 to reach the underlying telencephalon. The basal process is considerably thinner than the apical one and contains only free ribosomes and mitochondria. Between the stages 29/30 and 32+ it elongates and displays at its distal end the characteristics of a growth cone. The structural and ultrastructural morphology of the basal process identifies it as the axon of the olfactory neuron. Thus the placodai cells which migrate superficially differentiate into the olfactory neurons. Many placodai cells do not migrate, however, butremain at the epi‐thelial base as basal cells.As the placodal cells migrate to the body surface the NNE cells, originally confined to the surface layer (NNE), elongate and project processes toward the basal lamina. Beginning at stage 27 the apical surface of these cells becomes domed; the dome is filled with dense‐core vesicles and is covered with microvilli and globular material. The supranuclear cytoplasm of these cells contains free and membrane‐bound ribosomes, microtubules, and bundles of filaments. These cells can be characterized as the supporting cells of the olfactory neuroepithelium.The results indicate that (1) the olfactory neurons and basal cells are derived from the cells of the nervous layer, (2) the supporting cells are derived from the cells of the nonnervous ectoderm, (3) the olfactory nerve emerges from the olfactory neuroepithelium at stage 29/30, and (4) the placodai cells begin to display the morphological features of the mature olfactory neurons before their axons reach their target, the olfactory bulb.