Extended Production of Cortical Interneurons into the Third Trimester of Human Gestation

Cereb Cortex. 2016 May;26(5):2242-2256. doi: 10.1093/cercor/bhv074. Epub 2015 Apr 16.

Abstract

In humans, the developmental origins of interneurons in the third trimester of pregnancy and the timing of completion of interneuron neurogenesis have remained unknown. Here, we show that the total and cycling Nkx2.1(+)and Dlx2(+)interneuron progenitors as well as Sox2(+)precursor cells were higher in density in the medial ganglionic eminence (MGE) compared with the lateral ganglionic eminence and cortical ventricular/subventricular zone (VZ/SVZ) of 16-35 gw subjects. The proliferation of these progenitors reduced as a function of gestational age, almost terminating by 35 gw. Proliferating Dlx2(+)cells were higher in density in the caudal ganglionic eminence (CGE) compared with the MGE, and persisted beyond 35 gw. Consistent with these findings, Sox2, Nkx2.1, Dlx2, and Mash1 protein levels were higher in the ganglionic eminences relative to the cortical VZ/SVZ. The density of gamma-aminobutyric acid-positive (GABA(+)) interneurons was higher in the cortical VZ/SVZ relative to MGE, but Nkx2.1 or Dlx2-expressing GABA(+)cells were more dense in the MGE compared with the cortical VZ/SVZ. The data suggest that the MGE and CGE are the primary source of cortical interneurons. Moreover, their generation continues nearly to the end of pregnancy, which may predispose premature infants to neurobehavioral disorders.

Keywords: Dlx2; GABAergic; Nkx2.1; Sox2; ganglionic eminence; interneuron; subventricular zone.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Brain / embryology*
  • Brain / metabolism
  • Brain / physiology*
  • Cell Count
  • Cerebral Cortex / embryology
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / physiology
  • Female
  • Fetal Development*
  • GABAergic Neurons / metabolism
  • GABAergic Neurons / physiology*
  • Gestational Age
  • Homeodomain Proteins / metabolism
  • Humans
  • Interneurons / metabolism
  • Interneurons / physiology*
  • Lateral Ventricles / embryology
  • Lateral Ventricles / metabolism
  • Lateral Ventricles / physiology
  • Male
  • Median Eminence / embryology
  • Median Eminence / physiology
  • Neural Stem Cells / metabolism
  • Neural Stem Cells / physiology*
  • Neurogenesis
  • Nuclear Proteins / metabolism
  • Pregnancy
  • Pregnancy Trimester, Third
  • Thyroid Nuclear Factor 1
  • Transcription Factors / metabolism

Substances

  • Distal-less homeobox proteins
  • Homeodomain Proteins
  • Nuclear Proteins
  • Thyroid Nuclear Factor 1
  • Transcription Factors