Neural Progenitors in the Developing Neocortex of the Northern Tree Shrew (Tupaia belangeri) Show a Closer Relationship to Gyrencephalic Primates Than to Lissencephalic Rodents

Abstract

The neocortex is the most complex part of the mammalian brain and as such it has undergone tremendous expansion during evolution, especially in primates. The majority of neocortical neurons originate from distinct neural stem and progenitor cells (NPCs) located in the ventricular and subventricular zone (SVZ). Previous studies revealed that the SVZ thickness as well as the abundance and distribution of NPCs, especially that of basal radial glia (bRG), differ markedly between the lissencephalic rodent and gyrencephalic primate neocortex. The northern tree shrew (Tupaia belangeri) is a rat-sized mammal with a high brain to body mass ratio, which stands phylogenetically mid-way between rodents and primates. Our study provides – for the first time – detailed data on the presence, abundance and distribution of bRG and other distinct NPCs in the developing neocortex of the northern tree shrew (Tupaia belangeri). We show that the developing tree shrew neocortex is characterized by an expanded SVZ, a high abundance of Pax6+ NPCs in the SVZ, and a relatively high percentage of bRG at peak of upper-layer neurogenesis. We further demonstrate that key features of tree shrew neocortex development, e.g., the presence, abundance and distribution of distinct NPCs, are closer related to those of gyrencephalic primates than to those of ferret and lissencephalic rodents. Together, our study provides novel insight into the evolution of bRG and other distinct NPCs in the neocortex development of Euarchontoglires and introduces the tree shrew as a potential novel model organism in the area of human brain development and developmental disorders.

Developmental Differences in Neocortex Neurogenesis and Maturation Between the Altricial Dwarf Rabbit and Precocial Guinea Pig

“…We first concentrated on APs as the primary NPCs. As observed in most mammalian species (Götz et al, 1998;Englund et al, 2005;Osumi et al, 2008;Fietz et al, 2010;Hansen et al, 2010;Reillo et al, 2011;Romer et al, 2018;Sauerland et al, 2018), NPCs of the dwarf rabbit and guinea pig VZ were Pax6+ and largely Tbr2-(Figures 1, 2, 3A,B). The highest abundance of Pax6+ NPCs in the VZ of the dwarf rabbit was observed at day 15 p.c.…”

Ginsenoside Rg1 improves cognitive capability and affects the microbiota of large intestine of tree shrew model for Alzheimer's disease

“…The tree shrew model of AD has been successfully constructed in our study ( 26 ). A recent study has suggested that the neocortex development of the tree shrew is closer to primates than to rodents ( 27 ). This makes the tree shrew a good experimental animal in neurological diseases.…”

Characteristics of the tree shrew gut virome

“…belangeri chinensis [3]. Previous studies [4–5] showed that the tree shrew has a closer relationship with humans than did rodents in terms of physiological function, biochemical metabolism and genomic signatures. Due to its unique characteristics, such as small body size, low cost of maintenance, life span and short reproductive cycle, the tree shrew has been increasingly used in laboratory analyses in recent years.…”