The evolution of cortical development: the synapsid-diapsid divergence

Abstract

The cerebral cortex covers the rostral part of the brain and, in higher mammals and particularly humans, plays a key role in cognition and consciousness. It is populated with neuronal cell bodies distributed in radially organized layers. Understanding the common and lineage-specific molecular mechanisms that orchestrate cortical development and evolution are key issues in neurobiology. During evolution, the cortex appeared in stem amniotes and evolved divergently in two main branches of the phylogenetic tree: the synapsids (which led to present day mammals) and the diapsids (reptiles and birds). Comparative studies in organisms that belong to those two branches have identified some common principles of cortical development and organization that are possibly inherited from stem amniotes and regulated by similar molecular mechanisms. These comparisons have also highlighted certain essential features of mammalian cortices that are absent or different in diapsids and that probably evolved after the synapsid-diapsid divergence. Chief among these is the size and multi-laminar organization of the mammalian cortex, and the propensity to increase its area by folding. Here, I review recent data on cortical neurogenesis, neuronal migration and cortical layer formation and folding in this evolutionary perspective, and highlight important unanswered questions for future investigation.

BuMPing Into Neurogenesis: How the Canonical BMP Pathway Regulates Neural Stem Cell Divisions Throughout Space and Time

“…Emerging from the pallium, which itself represents the dorsal part of the telencephalon, the cerebral cortex represents the most evolutionarily divergent region of the mammalian CNS, with comparable structures being only found in the amniote clade (Goffinet, 2017;Briscoe and Ragsdale, 2018;García-Moreno and Molnár, 2020). During early mammalian brain development, various BMP ligands (BMP2/4/5/6/7) are expressed and secreted by discrete regions of the dorsal telencephalon, the cortical hem and the choroid plaque, from where they act as morphogens to pattern the dorsal telencephalic midline (Furuta et al, 1997;Grove et al, 1998;Hebert et al, 2002;Hébert and Fishell, 2008).…”

The multiple facets of Cajal-Retzius neurons

“…In sauropsids, only a handful of studies have addressed the matter and the issue is not as clear. As noted above, Reln expression has been described in the telencephalic MZ of turtles, lizards and birds (Bar et al, 2000;Goffinet, 2017). By contrast, expression of p73 was reported to be very limited in lizards (Cabrera-Socorro et al, 2007), whereas in crocodiles most subpial Reln + cells were also found to be p73 + (Tissir et al, 2003).…”

“…In humans, analysis of p73 expression (which labels all but VPderived CRs) suggests that the hem, septum and TE are conserved sources among mammals (Meyer et al, 2002). In sauropsids (birds, turtles and lizards), Reln-positive cells have been observed at the pallial surface, but little is known regarding the origins and migratory behaviour of these putative CRs (Bar et al, 2000;Goffinet, 2017). The pattern of p73 expression in lizards suggests that most CRs are located in the ventral telencephalon and derive from the septum and TE, whereas only few hem-derived CR invade the pallium dorsally (Cabrera-Socorro et al, 2007).…”

Mercury Toxicity and Neurogenesis in the Mammalian Brain

“…Eventually, NECs give rise to pluripotent neural stem cells (NSCs) and apical radial glial cells (aRGs; Figure 1 C) [ 3 ]. The aRGs undergo further symmetrical cell divisions to produce additional aRGs or asymmetrical division to give rise to additional cell types, including basal radial glia, intermediate progenitor cells, and neurons ( Figure 1 D) [ 6 , 7 , 8 ].…”