Abstract
The neocortex, a six-layer neuronal brain structure that arose during the evolution of, and is unique to, mammals, is the seat of higher order brain functions responsible for human cognitive abilities. Despite its recent evolutionary origin, it shows a striking variability in size and folding complexity even among closely related mammalian species. In most mammals, cortical neurogenesis occurs prenatally, and its length correlates with the length of gestation. The evolutionary expansion of the neocortex, notably in human, is associated with an increase in the number of neurons, particularly within its upper layers. Various mechanisms have been proposed and investigated to explain the evolutionary enlargement of the human neocortex, focussing in particular on changes pertaining to neural progenitor types and their division modes, driven in part by the emergence of human-specific genes with novel functions. These led to an amplification of the progenitor pool size, which affects the rate and timing of neuron production. In addition, in early theoretical studies, another mechanism of neocortex expansion was proposed—the lengthening of the neurogenic period. A critical role of neurogenic period length in determining neocortical neuron number was subsequently supported by mathematical modeling studies. Recently, we have provided experimental evidence in rodents directly supporting the mechanism of extending neurogenesis to specifically increase the number of upper-layer cortical neurons. Moreover, our study examined the relationship between cortical neurogenesis and gestation, linking the extension of the neurogenic period to the maternal environment. As the exact nature of factors promoting neurogenic period prolongation, as well as the generalization of this mechanism for evolutionary distinct lineages, remain elusive, the directions for future studies are outlined and discussed.
Highlights
The neocortex is the largest structure in the mammalian brain, covering most of its surface and being responsible for a substantial part of its computing capacity (Van Essen et al, 2018)
The outer SVZ (oSVZ) expands substantially during neurogenesis due to the presence of highly proliferative basal progenitors (BPs) (Smart et al, 2002; Fietz et al, 2010; Hansen et al, 2010; Reillo et al, 2011). This expansion of the germinal zones allows for the substantial increase in the cell clone size originating from a single VZresident apical radial glia (aRG) (Noctor et al, 2001; Reillo et al, 2011), and leads to the lateral spread of the daughter neurons over a larger surface area in gyrencephalic, as opposed to lissencephalic, species (Reillo et al, 2011; Kalebic et al, 2018)
Some of the more informative studies addressing this question include comparative studies that examine the evolutionary changes in the dynamics of cortical neurogenesis in vitro, as the culture systems allow for easier tracking of developmental events over a wide time window with frequent sampling
Summary
The neocortex is the largest structure in the mammalian brain, covering most of its surface and being responsible for a substantial part of its computing capacity (Van Essen et al, 2018). The characteristic structure of the neocortex with its six cytoarchitecturally distinct layers forms during the process of cortical neurogenesis, which in most placental mammals is completed prenatally (Clancy et al, 2001; Lewitus et al, 2014), with the exception of certain species such as ferret, where it continues for a short time after birth (Jackson et al, 1989) The length of this neurogenic period differs widely among mammalian species, e.g., in mouse, a small-brained lissencephalic mammal, the neurogenic period lasts only about 9–10 days (from embryonic day E10.5 to E18–E19.5) (Stepien et al, 2020), while in human, a large-brained gyrencephalic species, it lasts for around 110 days (from gestation week 10–25) (Clancy et al, 2001; Lewitus et al, 2014). We will review the experimental evidence demonstrating the crucial role of the length of the neurogenic period in neocortical expansion, and propose directions for future studies, which should further explore and mechanistically explain the role of this mechanism in evolution
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