Robo1 regulates the migration and laminar distribution of upper-layer pyramidal neurons of the cerebral cortex

Yuko Gonda, William D. Andrews, Hidenori Tabata, Takashi Namba, John G. Parnavelas, Kazunori Nakajima, Shinichi Kohsaka, Carina Hanashima, Shigeo Uchino

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

Laminar organization is a key feature of the mammalian cerebral cortex, but the mechanisms by which final positioning and "inside-out" distribution of neurons are determined remain largely unknown. Here, we demonstrate that Robo1, a member of the family of Roundabout receptors, regulates the correct positioning of layers II/III pyramidal neurons in the neocortex. Specifically, we used RNA interference in mice to suppress the expression of Robo1 in a subset of layers II/III neurons, and observed the positions of these cells at distinct developmental stages. In contrast to control neurons that migrated toward the pial surface by P1, Robo1-suppressed neurons exhibited a delay in entering the cortical plate at respective stages. Unexpectedly, after the first postnatal week, these neurons were predominantly located in the upper part of layers II/III, in contrast to control cells that were distributed throughout these layers. Sequential electroporation studies revealed that Robo1-suppressed cells failed to establish the characteristic inside-out neuronal distribution and, instead, they accumulated beneath the marginal zone regardless of their birthdate. These results demonstrate that Robo receptors play a crucial role in neocortical lamination and particularly in the positioning of layers II/III pyramidal neurons.

Original languageEnglish
Pages (from-to)1495-1508
Number of pages14
JournalCerebral Cortex
Volume23
Issue number6
DOIs
Publication statusPublished - 2013 Jun

Fingerprint

Pyramidal Cells
Cerebral Cortex
Neurons
Electroporation
Neocortex
RNA Interference

Keywords

  • lamination
  • layers II/III
  • neocortex
  • neuronal positioning
  • Roundabout

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Cellular and Molecular Neuroscience

Cite this

Robo1 regulates the migration and laminar distribution of upper-layer pyramidal neurons of the cerebral cortex. / Gonda, Yuko; Andrews, William D.; Tabata, Hidenori; Namba, Takashi; Parnavelas, John G.; Nakajima, Kazunori; Kohsaka, Shinichi; Hanashima, Carina; Uchino, Shigeo.

In: Cerebral Cortex, Vol. 23, No. 6, 06.2013, p. 1495-1508.

Research output: Contribution to journalArticle

Gonda, Y, Andrews, WD, Tabata, H, Namba, T, Parnavelas, JG, Nakajima, K, Kohsaka, S, Hanashima, C & Uchino, S 2013, 'Robo1 regulates the migration and laminar distribution of upper-layer pyramidal neurons of the cerebral cortex', Cerebral Cortex, vol. 23, no. 6, pp. 1495-1508. https://doi.org/10.1093/cercor/bhs141
Gonda, Yuko ; Andrews, William D. ; Tabata, Hidenori ; Namba, Takashi ; Parnavelas, John G. ; Nakajima, Kazunori ; Kohsaka, Shinichi ; Hanashima, Carina ; Uchino, Shigeo. / Robo1 regulates the migration and laminar distribution of upper-layer pyramidal neurons of the cerebral cortex. In: Cerebral Cortex. 2013 ; Vol. 23, No. 6. pp. 1495-1508.
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