Orderly migration of neurons to the principal sensory nucleus of the trigeminal nerve of the rat

Abstract

As nuclei in the central nervous system develop, neurons actively migrate from their site of generation to their permanent residence. This study examines the spatiotemporal sequence of the migration of neurons to the principal sensory nucleus of the trigeminal nerve (PSN) of the rat. Tritiated thymidine autoradiography and bromodeoxyuridine immunohistochemistry were used to examine the spatiotemporal patterns of migration of PSN neurons born on gestational day (G) 12 (early-generated neurons) and of those born on G14 (late-generated neurons). The final residence of early- and late-generated neurons was determined by injecting a thymidine analog into a pregnant rat on G12 or G14 and sacrificing the pups on postnatal day (P) 30. Early- and late-generated neurons were distributed medially and laterally, respectively. The schedule of the migration of PSN neurons was also determined. A few pioneer neurons born on G12 reached the PSN by G14; however, the last of the neurons born on G12 arrived in the PSN by G18. The migration of neurons born on G14 was completed 2–6 days later than that of the early-generated neurons. The path followed by migrating neurons was delineated by radial glial fibers. These processes were identified in the developing metencephalon by RAT-401 immunohistochemistry. Radial glial fibers extended from the lateral part of the ventricular zone through the tegmentum and the PSN to the surface of the metencephalon external to the sensory tract of the trigeminal nerve. RAT-401-immunoreactive processes were detected during the period of neuronal migration, but disappeared by P5. Thus, the migration of PSN neurons follows an inside-to-outside sequence, which apparently is organized by radial glial fibers. The inside-to-outside sequence of neuronal migration directly opposes the outside-to-inside gradient of synaptogenesis.