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. 2017 Aug 30;284(1861):20171169.
doi: 10.1098/rspb.2017.1169.

Coevolution in the Timing of GABAergic and Pyramidal Neuron Maturation in Primates

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Free PMC article

Coevolution in the Timing of GABAergic and Pyramidal Neuron Maturation in Primates

Christine J Charvet et al. Proc Biol Sci. .
Free PMC article

Abstract

The cortex of primates is relatively expanded compared with many other mammals, yet little is known about what developmental processes account for the expansion of cortical subtype numbers in primates, including humans. We asked whether GABAergic and pyramidal neuron production occurs for longer than expected in primates than in mice in a sample of 86 developing primate and rodent brains. We use high-resolution structural, diffusion MR scans and histological material to compare the timing of the ganglionic eminences (GE) and cortical proliferative pool (CPP) maturation between humans, macaques, rats, and mice. We also compare the timing of post-neurogenetic maturation of GABAergic and pyramidal neurons in primates (i.e. humans, macaques) relative to rats and mice to identify whether delays in neurogenesis are concomitant with delayed post-neurogenetic maturation. We found that the growth of the GE and CPP are both selectively delayed compared with other events in primates. By contrast, the timing of post-neurogenetic GABAergic and pyramidal events (e.g. synaptogenesis) are predictable from the timing of other events in primates and in studied rodents. The extended duration of GABAergic and pyramidal neuron production is associated with the amplification of GABAerigc and pyramidal neuron numbers in the human and non-human primate cortex.

Keywords: development; evolution; human.

Conflict of interest statement

The authors declare that we have no competing interests.

Figures

Figure 1.
Figure 1.
The timing of modelled events in humans and macaques are plotted against the timing of modelled events in mice. We use the timing of neural events to find equivalent maturational time points across humans, macaques, and mice [29]. Events that occur late in development occur progressively later in longer developing species such as humans. Isocortical neurogenesis timing, which is protracted in primates relative to studied rodents, is not included. (Online version in colour.)
Figure 2.
Figure 2.
Three-dimensional reconstruction of the GE in a human fetus at gestational week (GW) 17. Arrowheads point to the approximate coronal planes shown for each fetus (bj). Coronal slices of structural MRI scans of fetal humans at GW 17 (bd) and GW 20 (eg). The GE as well as the CPP (e.g. SVZ) are defined as a bright or dense region abutting the lateral ventricles. (Online version in colour.)
Figure 3.
Figure 3.
Growth of the GE in humans (a), macaques (b), and mice (c). Age in days after conception (embryonic days) of humans and macaques were translated to the age of mice [29]. A Gaussian function was fitted to the data. The peak size of the GE and CPP occur later than expected in humans and macaques compared with mice. (Online version in colour.)
Figure 4.
Figure 4.
Growth of the CPP in humans (a), macaques (b), and mice (c). Age in days after conception (embryonic days) of humans and macaques were translated to the age of mice [29]. We fitted a Gaussian function to the data. The peak size of the GE and CPP occur later than expected in humans and macaques compared with mice. (Online version in colour.)
Figure 5.
Figure 5.
(a) Diffusion MR tractography of a human fetus at gestational week (GW) 20. The anisotropy of the GE is aligned along the anterior to posterior axis. (b) The GE expands at GW 21 and declines between the ages of GW 21–31. (c) MR tractography shows that the GE wanes between GW 21–31. Scale bar is 10 mm. (Online version in colour.)
Figure 6.
Figure 6.
The timing of neural events expressed in days post-conception in humans (a) and macaques (b) are plotted against an event scale generated from the timing of events in rats and mice. Boxplots show the distribution of residuals derived from the linear regression for humans (a,b) and macaques (c,d). These data show that the timing of GABAergic and pyramidal events are similar to those of other events. These findings demonstrate that the timing of GABAergic and pyramidal post-neurogenetic events conform to the timing of other events in humans, macaques, rats, and mice. Dpc, days post-conception. (Online version in colour.)

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