Both excitatory and inhibitory neurons transiently form clusters at the outermost region of the developing mammalian cerebral neocortex

Minkyung Shin, Ayako Kitazawa, Satoshi Yoshinaga, Kanehiro Hayashi, Yukio Hirata, Colette Dehay, Kenichiro Kubo, Kazunori Nakajima

Research output: Contribution to journalArticle

Abstract

During development of the mammalian cerebral neocortex, postmitotic excitatory neurons migrate toward the outermost region of the neocortex. We previously reported that this outermost region is composed of densely packed relatively immature neurons; we named this region, which is observed during the late stage of mouse neocortical development, the “primitive cortical zone (PCZ).” Here, we report that postmigratory immature neurons spend about 1–1.5 days in the PCZ. An electron microscopic analysis showed that the neurons in the PCZ tend to be in direct contact with each other, mostly in a radial direction, forming “primitive neuronal clusters” with a height of 3–7 cells and a width of 1–2 cells. A time-course analysis of fluorescently labeled neurons revealed that the neurons took their positions within the primitive clusters in an inside-out manner. The neurons initially participated in the superficial part of the clusters, gradually shifted their relative positions downward, and then left the clusters at the bottom of this structure. GABAergic inhibitory interneurons were also found within the primitive clusters in the developing mouse neocortex, suggesting that some clusters are composed of both excitatory neurons and inhibitory interneurons. Similar clusters were also observed in the outermost region of embryonic day (E) 78 cynomolgus monkey occipital cortex and 23 gestational week (GW) human neocortices. In the primate neocortices, including human, the presumptive primitive clusters seemed to expand in the radial direction more than that observed in mice, which might contribute to the functional integrity of the primate neocortex.

Original languageEnglish
JournalJournal of Comparative Neurology
DOIs
Publication statusPublished - 2019 Jan 1

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Neocortex
Neurons
Interneurons
Primates
Occipital Lobe
Macaca fascicularis
Electrons

Keywords

  • excitatory neuron
  • in utero electroporation (IUE)
  • inhibitory interneuron
  • mammalian neocortical development
  • neuronal migration
  • primate neocortical development
  • primitive cortical zone (PCZ)
  • primitive neuronal clusters
  • RRID:AB_10712211, AB_141607, AB_141708, AB_141709, AB_162542, AB_162543, AB_2068506, AB_2298772, AB_2340375, AB_2491093, AB_2535853, AB_2536180, AB_2539796, AB_300798, AB_305426, AB_634520

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Both excitatory and inhibitory neurons transiently form clusters at the outermost region of the developing mammalian cerebral neocortex. / Shin, Minkyung; Kitazawa, Ayako; Yoshinaga, Satoshi; Hayashi, Kanehiro; Hirata, Yukio; Dehay, Colette; Kubo, Kenichiro; Nakajima, Kazunori.

In: Journal of Comparative Neurology, 01.01.2019.

Research output: Contribution to journalArticle

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AU - Shin, Minkyung

AU - Kitazawa, Ayako

AU - Yoshinaga, Satoshi

AU - Hayashi, Kanehiro

AU - Hirata, Yukio

AU - Dehay, Colette

AU - Kubo, Kenichiro

AU - Nakajima, Kazunori

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