Comparative aspects of cortical neurogenesis in vertebrates

Abstract

The mammalian neocortex consists of six layers. By contrast, the reptilian and avian cortices have only three, which are believed to be equivalent to layers I, V and VI of mammals. In mammals, the majority of cortical cell proliferation occurs in the ventricular and subventricular zones, but there are a small number of scattered individual divisions throughout the cortex. Neurogenesis in the cortical subventricular zone is believed to contribute to the supragranular layers. To estimate the proportions of different forms of divisions in reptiles and birds, we examined the site of proliferation in embryonic turtle (stages 18-25) and chick (embryonic days 8-15) brains using phospho-histone H3 (a G2 and M phase marker) immunohistochemistry. In turtle, only few scattered abventricular H3-immunoreactive cells were found outside the ventricular zone; the majority of the H3-immunoreactive cells were located in the ventricular zone throughout the entire turtle brain. Ventricular zone cell proliferation peaks at stages 18 and 20, before an increase of abventricular proliferation at stages 23 and 25. In turtle cortex, however, abventricular proliferation at any given stage never exceeded 17.5 ± 2.47% of the total division and the mitotic profiles did not align parallel to the ventricular zone. Phospho-histone H3 immunoreactivity in embryonic chick brains suggests the lack of subventricular zone in the dorsal cortex, but the presence of subventricular zone in the ventral telencephalon. We were able to demonstrate that the avian subventricular zone is present in both pallial and subpallial regions of the ventral telencephalon during embryonic development, and we characterize the spatial and temporal organization of the subventricular zone. Comparative studies suggest that the subventricular zone was involved in the laminar expansion of the cortex to six layers in mammals from the three-layered cortex found in reptiles and birds. Within mammals, the number of neurons in a cortical column appears to be largely constant; nevertheless, there are considerable differences between the germinal zones in mammalian species. It is yet to be determined whether these elaborations of the subventricular zone may have contributed to cell diversity, tangential expansion or gyrus formation of the neocortex and whether it might have been the major driving force behind the evolution of the six-layered neocortex in mammals.

Coevolution of radial glial cells and the cerebral cortex

“…The occurrence of basal progenitors in the dorsal pallium and their coalescence in the SVZ, which allows indirect neurogenesis and increased neuron production, has been widely recognized as the critical milestone in the evolutionary expansion of the cerebral cortex leading to mammals, particularly in its radial dimension and the formation of six layers (Cheung et al, 2010; Cheung et al, 2007; Molnar, 2011; Molnar et al, 2006; Puzzolo and Mallamaci, 2010), as originally proposed by Smart (1972a, 1972b). However, even with the occurrence of indirect neurogenesis, the persistence of aRGCs undergoing direct neurogenesis continues to limit neuron production because each neurogenic aRGC will generate, at most, half as many neurons compared with aRGCs generating basal progenitors; the difference will be even greater if basal progenitors can self‐amplify to any extent.…”

From sauropsids to mammals and back: New approaches to comparative cortical development

“…In comparison with mammals, the rudimentary 3‐layered reptilian cortices lack an SVZ despite the presence of a small population of scattered abventricular mitoses (Martínez‐Cerdeño et al, 2006; Cheung et al, 2007) and expression of Tbr2 (Clinton et al, 2014). Progenitor cells in the proliferative dorsal pallial compartment of reptiles cycle more slowly than mammalian progenitors that have a corresponding location (Nomura et al, 2013).…”

“…This is not due to the absence of subventricular and scattered abventricular mitoses (which are regularly observed in the hyper, meso, and nido‐pallium), but due to absence of a “zone”‐like clustering of these mitoses (Cheung et al, 2007). However, some species (such as parakeets and zebra finches) do show aggregation of abventricular mitoses as a thin band above the VZ (Charvet et al, 2009).…”

“…However, some species (such as parakeets and zebra finches) do show aggregation of abventricular mitoses as a thin band above the VZ (Charvet et al, 2009). However, the proportion of abventricular mitoses in the hyperpallium (proposed to be homologous to the dorsal cortex of mammals (Molnár and Butler, 2002)) is negligible compared to the proportions observed in the meso and nido‐pallium (Cheung et al, 2007). Even more relevant is that chickens and quails belong to a basal avian order (Galliformes) and zebra finch and parakeets to evolutionarily distant avian groups, the songbirds (order Passeriformes and Psittaciformes, respectively) (Zelenitsky et al, 2011).…”

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

“…In many mammalian species, this area is progressively subdivided into two subregions, the inner subventricular zone (ISVZ) and the outer subventricular zone (OSVZ), which appears later in development and is greatly expanded in gyrencephalic species (Cheung et al, 2007; Fish et al, 2008; Franco and Muller, 2013; Kriegstein et al, 2006; Lui et al, 2011; Martinez‐Cerdeno et al, 2012; Smart et al, 2002). The SVZ harbors a variety of neural progenitors, collectively referred to as basal progenitors, which eventually become the main source of neocortical neurons.…”