Development of Deep and Upper Neuronal Layers in the Domestic Cat, Sheep and Pig Neocortex

Abstract

The neocortex plays a key role in cognition, volitional motor control and sensory perception and has undergone tremendous expansion during evolution. The mature neocortex consists of radially aligned neurons that are arranged in six layers. Layers II-VI are often split into two groups: deep and upper layers, both building up the so-called cortical plate during embryonic and foetal development. So far cortical neurogenesis, including the generation of deep and upper layers, has mostly been studied in laboratory rodents and primates. However, precise data for most companion animals are lacking. This study determined the main period of neurogenesis, specifically the timing of deep and upper layer generation, in the developing domestic cat, pig and sheep neocortex using immunohistochemistry for specific neuronal markers, that is Tbr1 and Brn2. We found that the general sequence of neural events is preserved among cat, pig, sheep and other mammalian species. However, we observed differences in the timing of the overall cortical neurogenic period and occurrence of distinct neural events when these three species were compared. Moreover, our data provide further evidence that the cortical neurogenic period and gestation length might be tightly related. Together, these data expand our current understanding of neocortex development and are important for future studies investigating neocortex development and expansion especially in companion animals.

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

“…Quantification of the CP thickness revealed that corticogenesis in the tree shrew starts before E32 and is largely completed at the time of birth, with E32 representing the stage at which mainly Tbr1+ deep-layers are being produced and E37 the stage at which largely Tbr2– upper-layers are being produced ( Figure 3E ). Double-immunofluorescence for Brn2, characteristically expressed by upper-layer neurons, and Tbr1 revealed that a major fraction of Tbr1– cells in the E37–P1 CP belong to the population of upper-layer neurons, thus corroborating E32 to represent the peak of deep-layer and E37 the peak of upper-layer production (Supplementary Figures 4E–H ) ( McEvilly et al, 2002 ; Sugitani et al, 2002 ; Britanova et al, 2008 ; Glatzle et al, 2017 ). Together, this indicates that – similar to other mammalian species – the SVZ of the developing tree shrew neocortex is an important site of neurogenesis, being largest at developmental stages when upper layers of the CP are being produced ( Kriegstein et al, 2006 ; Kriegstein and Alvarez-Buylla, 2009 ).…”

Loss of interneurons and disruption of perineuronal nets in the cerebral cortex following hypoxia-ischaemia in near-term fetal sheep

“…The initial appearance of PNNs in cortical layer 6 in the present study likely reflects the earlier formation of this layer compared with other cortical lamina, as during cortical development, the deeper layers (5 and 6) form first, followed by superficial layers (2–4) 57 . In sheep, neurogenesis and formation of cortical layers 5 and 6 occur from approximately 30 d gestation, and are largely complete by 60 d 88 .…”

Signs of Reduced Basal Progenitor Levels and Cortical Neurogenesis in Human Fetuses with Open Spina Bifida at 11–15 Weeks of Gestation

“…(He et al, 1989;Bulfone et al, 1995;Hevner, 2007;Molyneaux et al, 2007;Toma and Hanashima, 2015;Glatzle et al, 2017). This revealed that, in…”