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

The establishment of the mammalian neocortex is often explained phylogenetically by an evolutionary change in the pallial neuronal progenitors of excitatory projection neurons. It remains unclear, however, whether and how the evolutionary change in inhibitory interneurons, which originate outside the neocortex, has been involved in the establishment of the neocortex. In this study, we transplanted chicken, turtle, mouse, and marmoset medial ganglionic eminence (MGE) cells into the embryonic mouse MGE in utero and compared their migratory behaviors. We found that the MGE cells from all of the species were able to migrate through the mouse neocortical subventricular zone and that both the mouse and marmoset cells subsequently invaded the neocortical cortical plate (CP). However, regardless of their birthdates and interneuron subtypes, most of the chicken and turtle cells ignored the neocortical CP and passed beneath it, although they were able to invade the archicortex and paleocortex, suggesting that the proper responsiveness of MGE cells to guidance cues to enter the neocortical CP is unique to mammals. When chicken MGE cells were transplanted directly into the neocortical CP, they were able to survive and mature, suggesting that the neocortical CP itself is essentially permissive for postmigratory development of chicken MGE cells. These results suggest that an evolutionary change in the migratory ability of inhibitory interneurons, which originate outside the neocortex, was involved in the establishment of the neocortex by supplying inhibitory components to the network.