Primate neocortex development and evolution: Conserved versus evolved folding

Abstract

The neocortex, the seat of higher cognitive functions, exhibits a key feature across mammalian species—a highly variable degree of folding. Within the neocortex, two distinct subtypes of cortical areas can be distinguished, the isocortex and the proisocortex. Here, we have compared specific spatiotemporal aspects of folding between the proisocortex and the isocortex in 13 primates, including human, chimpanzee, and various Old World and New World monkeys. We find that folding at the boundaries of the dorsal isocortex and the proisocortex, which gives rise to the cingulate sulcus (CiS) and the lateral fissure (LF), is conserved across the primates studied and is therefore referred to as conserved folding. In contrast, the degree of folding within the dorsal isocortex exhibits huge variation across these primates, indicating that this folding, which gives rise to gyri and sulci, is subject to major changes during primate evolution. We therefore refer to the folding within the dorsal isocortex as evolved folding. Comparison of fetal neocortex development in long‐tailed macaque and human reveals that the onset of conserved folding precedes the onset of evolved folding. Moreover, the analysis of infant human neocortex exhibiting lissencephaly, a developmental malformation thought to be mainly due to abnormal neuronal migration, shows that the evolved folding is perturbed more than the conserved folding. Taken together, our study presents a two‐step model of folding that pertains to primate neocortex development and evolution. Specifically, our data imply that the conserved folding and the evolved folding constitute two distinct, sequential events.

Length of the Neurogenic Period—A Key Determinant for the Generation of Upper-Layer Neurons During Neocortex Development and Evolution

“…Although smaller mammals tend to have less folded neocortices, with the GI close to 1.0, the relationship between overall brain size and folding is not universal, with examples of large mammals such as the manatee having a lissencephalic cortex (Welker, 1990;Pillay and Manger, 2007;Lewitus et al, 2014;Vaid et al, 2018). Similarly, phylogenetic lineage relationships are also not determinative of cortex folding as exemplified by marmosets, which are lissencephalic, in contrast to most other primates, which possess gyrencephalic neocortices (Zilles et al, 1989;Kelava et al, 2012;Lewitus et al, 2014;Mitchell and Leopold, 2015;Vaid et al, 2018;Namba et al, 2019). Humans, next to cetaceans and elephants, are among the species with the highest GI (Zilles et al, 1988(Zilles et al, , 1989Kelava et al, 2012;Lewitus et al, 2014;Namba et al, 2019).…”

Xenopus leads the way: Frogs as a pioneering model to understand the human brain

“…Many “higher order” behaviors displayed by mammals, including primates, and humans specifically, have been proposed to be supported by uniquely evolved neurodevelopmental programs executed during forebrain development in these lineages (Kriegstein et al, 2006; Namba & Huttner, 2017; Namba, Vaid, & Huttner, 2019; Nowakowski, Pollen, Sandoval‐Espinosa, & Kriegstein, 2016). This suggestion is intuitively appealing for humans, particularly when trying to frame knowledge about complex psychological processes (including multisensory, cognitive, and emotional processes) associated with human brain function and human behavior.…”

Malformations of Human Neocortex in Development – Their Progenitor Cell Basis and Experimental Model Systems

“…However, although ferrets are a superior model organism in this regard, they present several limitations, as follows. First, although the ferret brain is bigger than that of mouse and gyrified, it does not exhibit a prominent temporal lobe and lateral fissure (Hutchinson et al, 2017), two specific macroscopic features found in primate brains (Bryant and Preuss, 2018; Namba et al, 2019). Second, the available ferrets are outbred animals, and hence their genetic background is not homogeneous, in contrast to that of the inbred mouse lines.…”