Ferret brain possesses young interneuron collections equivalent to human postnatal migratory streams

J Comp Neurol. 2019 Dec 1;527(17):2843-2859. doi: 10.1002/cne.24711. Epub 2019 May 15.

Abstract

The human early postnatal brain contains late migratory streams of immature interneurons that are directed to cortex and other focal brain regions. However, such migration is not observed in rodent brain, and whether other small animal models capture this aspect of human brain development is unclear. Here, we investigated whether the gyrencephalic ferret cortex possesses human-equivalent postnatal streams of doublecortin positive (DCX+) young neurons. We mapped DCX+ cells in the brains of ferrets at P20 (analogous to human term gestation), P40, P65, and P90. In addition to the rostral migratory stream, we identified three populations of young neurons with migratory morphology at P20 oriented toward: (a) prefrontal cortex, (b) dorsal posterior sigmoid gyrus, and (c) occipital lobe. These three neuronal collections were all present at P20 and became extinguished by P90 (equivalent to human postnatal age 2 years). DCX+ cells in such collections all expressed GAD67, identifying them as interneurons, and they variously expressed the subtype markers SP8 and secretagogin (SCGN). SCGN+ interneurons appeared in thick sections to be oriented from white matter toward multiple cortical regions, and persistent SCGN-expressing cells were observed in cortex. These findings indicate that ferret is a suitable animal model to study the human-relevant process of late postnatal cortical interneuron integration into multiple regions of cortex.

Keywords: RRID: AB839504; RRID: AB_1640532; RRID:AB_10000320; RRID:AB_10615497; RRID:AB_1079874; RRID:AB_1586992; RRID:AB_2069869; RRID:AB_2194626; RRID:AB_2195374; RRID:AB_2298772; RRID:AB_305869; RRID:AB_477010; RRID:AB_561007; RRID:AB_882455; cortical interneurons; dorsal migratory stream; doublecortin; ferret; medial migratory stream; posterior migratory stream; postnatal migration; prefrontal cortex; secretagogin.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain / cytology*
  • Brain / growth & development*
  • Brain / metabolism
  • Caspase 3 / metabolism
  • Cell Movement
  • Doublecortin Domain Proteins
  • Doublecortin Protein
  • Ferrets / anatomy & histology*
  • Ferrets / metabolism
  • Humans
  • Interneurons / cytology*
  • Interneurons / metabolism
  • Microtubule-Associated Proteins / metabolism
  • Neuropeptides / metabolism
  • Secretagogins / metabolism
  • White Matter / cytology
  • White Matter / growth & development
  • White Matter / metabolism

Substances

  • DCX protein, human
  • Doublecortin Domain Proteins
  • Doublecortin Protein
  • Microtubule-Associated Proteins
  • Neuropeptides
  • Secretagogins
  • Caspase 3