Short-survival thymidine radiograms from rat embryos aged 13-19 days were analyzed to delineate the precerebellar neuroepithelium of the rhombencephalon. The original definition of the term "rhombencephalon" was modified to refer only to the unique dorsal portion (surface plate) of the medulla and pons where the neural groove fails to fuse and, instead, the medullary velum covers the rhomboid lumen of the fourth ventricle. Initially, the neuroepithelial tissue of the rhombencephalon consists of a pair of rostral and caudal bridgeheads: the former the primary neuroepithelium of the cerebellum and the latter the primary neuroepithelium of the octavo-precerebellar system. The spatial relationship between the cerebellar and precerebellar neuroepithelia soon changes as a result of ongoing morphogenetic events, such that the cerebellar primordium assumes a dorsal position and the precerebellar primordium a ventral position, and the distance between the two decreases. Concurrently the tela choroidea invaginates into the fourth ventricle and a secondary precerebellar neuroepithelium develops. The rostral portion of the secondary precerebellar neuroepithelium grows forward along the choroid plexus and forms the medial recess of the anterior fourth ventricle, while its caudal portion grows in the opposite direction beneath the medullary velum and forms the rostral wall of the posterior fourth ventricle. Evidence will be presented in the succeeding papers that the primary precerebellar neuroepithelium first generates the neurons of the inferior olive that migrate by a circumferential intramural (parenchymal) route to their destination. Next, the neurons of the lateral reticular and external cuneate nuclei are generated. These migrate by a posterior extramural (superficial) route and settle contralaterally. Subsequently, the primary precerebellar neuroepithelium produces the neurons of the nucleus reticularis tegmenti pontis and these form the anterior extramural migratory stream and settle ipsilaterally. Finally, the secondary precerebellar neuroepithelium produces the latest generated neurons of the basal pontine gray that follow the anterior extramural stream and settle ipsilaterally.