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
Externally publishedYes

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

Gonda, Y., Andrews, W. D., Tabata, H., Namba, T., Parnavelas, J. G., Nakajima, K., ... Uchino, S. (2013). Robo1 regulates the migration and laminar distribution of upper-layer pyramidal neurons of the cerebral cortex. Cerebral Cortex, 23(6), 1495-1508. https://doi.org/10.1093/cercor/bhs141

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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