Conserved pattern of tangential neuronal migration during forebrain development

Abstract

Origin, timing and direction of neuronal migration during brain development determine the distinct organization of adult structures. Changes in these processes might have driven the evolution of the forebrain in vertebrates. GABAergic neurons originate from the ganglionic eminence in mammals and migrate tangentially to the cortex. We are interested in differences and similarities in tangential migration patterns across corresponding telencephalic territories in mammals and reptiles. Using morphological criteria and expression patterns of Darpp-32, Tbr1, Nkx2.1 and Pax6 genes, we show in slice cultures of turtle embryos that early cohorts of tangentially migrating cells are released from the medial ganglionic eminence between stages 14 and 18. Additional populations migrate tangentially from the dorsal subpallium. Large cohorts of tangentially migrating neurons originate ventral to the dorsal ventricular ridge at stage 14 and from the lateral ganglionic eminence from stage 15. Release of GABAergic cells from these regions was investigated further in explant cultures. Tangential migration in turtle proceeds in a fashion similar to mammals. In chimeric slice culture and in ovo graft experiments, the tangentially migrating cells behaved according to the host environment -turtle cells responded to the available cues in mouse slices and mouse cells assumed characteristic migratory routes in turtle brains, indicating highly conserved embryonic signals between these distant species. Our study contributes to the evaluation of theories on the origin of the dorsal cortex and indicates that tangential migration is universal in mammals and sauropsids.

Changes in cortical interneuron migration contribute to the evolution of the neocortex

“…Consistent with the previous finding that turtle MGE cells were able to migrate into the mouse neocortex in vitro (25), MGE cells from both chicken and turtle have the competency to migrate tangentially through the neocortical SVZ/IZ, and they have weak competency to enter neocortical layers 5 and 6 (Fig. S8B).…”

“…This proposal is reasonable, but it may not be sufficient to fully explain the functional establishment of the neocortex, because it does not take into account the other essential component of the neocortex, interneurons, which invade from outside the pallium. Although the overall ratio of interneurons to the total number of neurons in the dorsal pallium varies among amniotes (20)(21)(22)(23), the tangential migration of interneurons from the MGE to the dorsal pallium is highly conserved across gnathostomes, including amniotes (24)(25)(26)(27)(28), and ∼75% of interneurons in the chicken pallium originate from the MGE (24). Interestingly, the mechanism of the tangential migration seems to be conserved across amniotes (25), suggesting that the common mechanism of tangential migration from the MGE to the dorsal pallium was already established in the ancestor of amniotes.…”

“…We used a combination of the strategy of interspecies transplantation of MGE cells (25) and a technique of MGE cell transplantation in mice in utero (12,29) to examine the migratory behavior of chicken, turtle, and marmoset MGE cells within the mouse neocortex in vivo. The results suggested that, although the phylogenetic origin of the MGE cell competencies to enter the neocortical SVZ is the ancestor of amniotes, the competencies of MGE cells to enter the neocortical CP, especially layers 2-4, were acquired in the ancestor of mammals.…”

A Novel Transient Glutamatergic Population Migrating from the Pallial–Subpallial Boundary Contributes to Neocortical Development

“…Based on analogy of connectivity, Karten (1997) suggested that the redistribution by tangential migration of cells generated by the DVR (dorsal ventricular ridge) domain, a derivative of the VP/LP in birds and reptiles, contributed to form the neocortex. However, until recently, tangential migration of glutamatergic cells from the VP/PSB toward the dorsal pallium was not demonstrated in mammals and was further excluded to occur in sauropsids (Métin et al, 2007).…”

The Embryonic Preoptic Area Is a Novel Source of Cortical GABAergic Interneurons

“…With the possible exception of human and nonhuman primates (Letinic et al, 2002), cortical GABAergic interneurons seem to derive almost exclusively from the subpallium in all vertebrates studied so far (Anderson et al, 1997(Anderson et al, , 2002Cobos et al, 2001a;González et al, 2002;Stühmer et al, 2002;Brox et al, 2003;Tuorto et al, 2003;Mueller et al, 2006;Fogarty et al, 2007;Métin et al, 2007;Xu et al, 2008) and reach the cortex through a long tangential migration (Corbin et al, 2001;Rubenstein, 2001, 2003;Métin et al, 2006). In particular, the medial ganglionic eminence (MGE) and the caudal aspect of the lateral ganglionic eminence (cLGE) [also known as the dorsal aspect of the caudal ganglionic eminence (dCGE)] have been suggested to generate most cortical GABAergic interneurons (Xu et al, 2004).…”