In order to meet the requirements for myelin biogenesis, the processes of oligodendrocytes must differentiate into specialized cellular compartments. For translation of myelin basic protein mRNA to occur in the oligodendrocyte processes or the myelin membrane, these structures must contain ribosomes and other components of the protein translation machinery. Light microscopy and electron microscopy (EM) were used to explore this possibility by analyzing the cytoskeletal organization and the organelle population of the processes of oligodendrocytes during development in vivo and in culture. Microtubules (MTs) were few and bundled in the younger processes of oligodendrocytes in culture. Some of these processes were characterized by the additional presence of serpentine MTs. EM revealed the presence of clusters of ribosomes in both immature and mature oligodendrocyte processes. In the former these clusters were frequently found at regular intervals along the processes. A similar interval characterized the distribution of myelin-like figures along the processes of mature cells in culture. Both in vivo and in culture, the processes became enriched in endoplasmic reticulum cisternae and mitochondria as the cells matured. The spatial arrangement of cellular organelles is compatible with protein and lipid synthesis occurring in the processes, at or near the site of myelin assembly.