Evidences for tangential migrations in Xenopus telencephalon: Developmental patterns and cell tracking experiments

Abstract

Extensive tangential cell migrations have been described in the developing mammalian, avian, and reptilian forebrain, and they are viewed as a powerful developmental mechanism to increase neuronal complexity in a given brain structure. Here, we report for the first time anatomical and cell tracking evidence for the presence of important migratory processes in the developing forebrain of the anamniote Xenopus laevis. Combining developmental gene expression patterns (Pax6, Nkx2.1, Isl1, Lhx5, Lhx9, and Dll3), neurotransmitter identity (GABA, NOS, ChAT), and connectivity information, several types of putative migratory cell populations and migration routes originating in the ventral pallium and the subpallium are proposed. By means of in vivo cell tracking experiments, pallio-subpallial and subpallio-pallial migrating neurons are visualized. Among them, populations of Nkx2.1(+) striatal interneurons and pallial GABAergic interneurons, which also express the migratory marker doublecortin, are identified. Finally, we find that these tangentially migrating pallial interneurons travel through an "isl1-free channel" that may guide their course through the subpallium. Our findings strongly suggest that the developing Xenopus telencephalon shares many similarities with amniotes in terms of neuronal specification and migrations. However, some differences are discussed, particularly with regard to the evolution of the pallium.