Evolutionary origin of Tbr2‐expressing precursor cells and the subventricular zone in the developing cortex

Abstract

The subventricular zone (SVZ) is greatly expanded in primates with gyrencephalic cortices, and is thought to be absent from vertebrates with three-layered, lissencephalic cortices, such as the turtle. Recent work in rodents has shown that Tbr2-expressing neural precursor cells in the SVZ produce excitatory neurons for each cortical layer in the neocortex. Many excitatory neurons are generated through a two-step process in which Pax6-expressing radial glial cells divide in the VZ to produce Tbr2-expressing intermediate progenitor cells, which divide in the SVZ to produce cortical neurons. We investigated the evolutionary origin of SVZ neural precursor cells in the prenatal cerebral cortex by testing for the presence and distribution of Tbr2-expressing cells in the prenatal cortex of reptilian and avian species. We found that mitotic Tbr2+ cells are present in the prenatal cortex of lizard, turtle, chicken and dove. Furthermore, Tbr2+ cells are organized into a distinct SVZ in the DVR of turtle forebrain, and in the cortices of chicken and dove. Our results are consistent with the concept that Tbr2+ neural precursor cells were present in the common ancestor of mammals and reptiles. Our data also suggest that the organizing principle guiding the assembly of Tbr2+ cells into an anatomically distinct SVZ, both developmentally and evolutionarily, may be shared across vertebrates. Finally, our results indicate that Tbr2 expression can be used to test for the presence of a distinct SVZ, and to define the boundaries of the SVZ in developing cortices.

Pattern of Neurogenesis and Identification of Neuronal Progenitor Subtypes during Pallial Development in Xenopus laevis

“…One of the focuses in the study of the evolutionary differences of this region has been its neurogenesis, that is, the mechanisms of development by which neurons are generated from neural progenitor cells. This process includes many aspects such as proliferative capacity, number of progenitors and their cell division types, proliferation rates, cell cycle length or the lineage relationships of different types of progenitors, which vary in the different vertebrate models (Kornack and Rakic, 1998; Nomura et al, 2013a, 2016; Florio and Huttner, 2014; Martínez-Cerdeño et al, 2016; Montiel et al, 2016). …”

“…The analysis of the pallium throughout development in the anuran amphibian Xenopus laevis (anamniote tetrapod) serves to shed light on the anamniote-amniote transition, since particular attention has been given only to reptiles and birds in recent years (Nomura et al, 2013a,b, 2015, 2016; Suzuki and Hirata, 2014; Martínez-Cerdeño et al, 2016; Montiel et al, 2016). Although general patterns of cell proliferation in the anuran brain have been studied (Wullimann et al, 2005; Chapman et al, 2006; Raucci et al, 2006; Simmons et al, 2006; Coen et al, 2007; Denver et al, 2009; Tao et al, 2015; Thuret et al, 2015), no detailed analysis of the pallium has been performed.…”

“…In the search for the ontogenetic mechanisms underlying the expansion of the neocortex, many recent studies have shed light on the differences between species in major neurogenetic events (Clinton et al, 2014; Martínez-Cerdeño et al, 2016). Pallial neurogenesis is understood as the process of generation of post-mitotic cells, neurons and glia, from the neural progenitors that divide and produce all the cells of the pallium.…”

“…In an evolutionary context, previous studies have suggested that pallial neurogenetic cells, and especially the IPs, evolved independently in mammalian and sauropsid lineages. For example, in some reptiles such as crocodiles or geckos, no IPs were detected (Charvet et al, 2009; Martínez-Cerdeño et al, 2016), but they were described in turtles (Cheung et al, 2007; Clinton et al, 2014; Martínez-Cerdeño et al, 2016). Therefore, this feature opens a very interesting question about evolutionary relationships, because the presence of IPs may be a derived feature of the turtle lineage that evolved independently, or they may had been already present in ancestral amniotes or even in anamniotes.…”

“…Pax6 and Lhx2, have been used to label pallial precursors, because throughout cortical neurogenesis they have been described as markers of neocortical progenitors within the vz, and both are involved in cortical cell fate determination (reviewed in von Bohlen und Halbach, 2011; Chou and O’Leary, 2013). Finally, the staining with Tbr2 as marker of IPs was attempted (Noctor et al, 2004; Martínez-Cerdeño et al, 2016). …”