Subcortical origins of human and monkey neocortical interneurons

Nat Neurosci. 2013 Nov;16(11):1588-97. doi: 10.1038/nn.3536. Epub 2013 Oct 6.

Abstract

Cortical GABAergic inhibitory interneurons have crucial roles in the development and function of the cerebral cortex. In rodents, nearly all neocortical interneurons are generated from the subcortical ganglionic eminences. In humans and nonhuman primates, however, the developmental origin of neocortical GABAergic interneurons remains unclear. Here we show that the expression patterns of several key transcription factors in the developing primate telencephalon are very similar to those in rodents, delineating the three main subcortical progenitor domains (the medial, lateral and caudal ganglionic eminences) and the interneurons tangentially migrating from them. On the basis of the continuity of Sox6, COUP-TFII and Sp8 transcription factor expression and evidence from cell migration and cell fate analyses, we propose that the majority of primate neocortical GABAergic interneurons originate from ganglionic eminences of the ventral telencephalon. Our findings reveal that the mammalian neocortex shares basic rules for interneuron development, substantially reshaping our understanding of the origin and classification of primate neocortical interneurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Age Factors
  • Animals
  • Animals, Newborn
  • Bromodeoxyuridine / metabolism
  • Cell Count
  • Cell Movement / physiology*
  • Cells, Cultured
  • Embryo, Mammalian
  • Gene Expression Regulation, Developmental / physiology*
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Interneurons / classification
  • Interneurons / physiology*
  • Macaca mulatta
  • Male
  • Mice
  • Neocortex / cytology*
  • Neocortex / embryology*
  • Nerve Tissue Proteins / metabolism
  • Organ Culture Techniques
  • Transcription Factors / metabolism
  • Transfection
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Nerve Tissue Proteins
  • Transcription Factors
  • Green Fluorescent Proteins
  • gamma-Aminobutyric Acid
  • Bromodeoxyuridine