The Subventricular Zone Is the Developmental Milestone of a 6-Layered Neocortex: Comparisons in Metatherian and Eutherian Mammals

Abstract

The major lineages of mammals (Eutheria, Metatheria, and Monotremata) diverged more than 100 million years ago and have undergone independent changes in the neocortex. We found that adult South American gray short-tailed opossum (Monodelphis domestica) and tammar wallaby (Macropus eugenii) possess a significantly lower number of cerebral cortical neurons compared with the mouse (Mus musculus). To determine whether the difference is reflected in the development of the cortical germinal zones, the location of progenitor cell divisions was examined in opossum, tammar wallaby, and rat. The basic pattern of the cell divisions was conserved, but the emergence of a distinctive band of dividing cells in the subventricular zone (SVZ) occurred relatively later in the opossum (postnatal day [P14]) and the tammar wallaby (P40) than in rodents. The planes of cell divisions in the ventricular zone (VZ) were similar in all species, with comparable mRNA expression patterns of Brn2, Cux2, NeuroD6, Tbr2, and Pax6 in opossum (P12 and P20) and mouse (embryonic day 15 and P0). In conclusion, the marsupial neurodevelopmental program utilizes an organized SVZ, as indicated by the presence of intermediate (or basal) progenitor cell divisions and gene expression patterns, suggesting that the SVZ emerged prior to the Eutherian-Metatherian split.

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

“…Quantification of the number of neurons in the primary somatosensory cortex of the adult mouse and Monodelphis domestica (picture) in a cresyl violet‐stained coronal section (Cheung et al, 2010). An arbitrary “unit column” (a 100‐μm wide, 40‐μm thick region spanning from layer 1 to 6) was marked in the primary somatosensory area (boxed areas in left panels).…”

“…The structure and function of a given brain area is determined during ontogeny by the regulation of cell proliferation and migration (Cheung et al, 2010; Lui et al, 2011; Borrell and Calegari, 2014; Florio and Huttner, 2014; Taverna et al, 2014). Recent investigations have tried to establish links between the organization of the germinal zones and telencephalic structures in various species.…”

“…Reptiles possess a cortex with a sparse density of neurons at all levels of the cortex relative to mammalian values (Cheung et al, 2010). These reptilian cells are mostly comparable to infragranular early‐generated neocortical neuronal populations, mammalian layers 5 and 6 (Reiner, 1991, 2000).…”

“…These reptilian cells are mostly comparable to infragranular early‐generated neocortical neuronal populations, mammalian layers 5 and 6 (Reiner, 1991, 2000). In our neurodevelopmental comparative studies of the turtle we found that in the telencephalon most neuronal divisions occur in the ventricular zone (VZ) of the lateral ventricle and in abventricular positions at various distances from the VZ (Abdel‐Mannan et al, 2008; Cheung et al, 2010). However, divisions outside of the VZ are infrequent and scattered in the turtle dorsal cortex, suggesting the absence or very rudimentary existence of an SVZ (Cheung et al, 2010).…”