Coevolution in the timing of GABAergic and pyramidal neuron maturation in primates

Author:

Charvet Christine J.12ORCID,Šimić Goran3,Kostović Ivica3,Knezović Vinka3,Vukšić Mario3,Babić Leko Mirjana3,Takahashi Emi14,Sherwood Chet C.2,Wolfe Marnin D.5,Finlay Barbara L.6

Affiliation:

1. Division of Newborn Medicine, Department of Medicine, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA

2. Department of Anthropology and Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC, USA

3. Department of Neuroscience, Croatian Institute for Brain Research, University of Zagreb School of Medicine, Zagreb, Croatia

4. Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA, USA

5. School of Integrative Plant Science, Department of Psychology, Cornell University, Ithaca, NY, USA

6. Evolutionary Neuroscience Group, Department of Psychology, Cornell University, Ithaca, NY, USA

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.

Funder

James S. McDonnell Foundation

National Institute of Health

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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