The fully linked HTML version of this article has now been published.
Development ePress online publication date 8 Oct 2003
doi: 10.1242/dev.00825
Research article
Multimodal tangential migration of neocortical GABAergic neurons independent of GPI-anchored proteins
Daisuke Tanaka,
Yohei Nakaya,
Yuchio Yanagawa,
Kunihiko Obata,
and
Fujio Murakami*
* Author for correspondence (e-mail: murakami{at}fbs.osaka-u.ac.jp)
Neuronal migration is crucial for the construction of neuronal architecture such as layers and nuclei. Most inhibitory interneurons in the neocortex derive from the basal forebrain and migrate tangentially; however, little is known about the mode of migration of these neurons in the cortex. We used glutamate decarboxylase (Gad)67-green fluorescent protein (GFP) knock-in embryonic mice with expression of GFP in gamma-aminobutyric acid (GABA)-ergic neurons and performed time-lapse analysis. In coronal slices, many GFP-positive neurons in the lower intermediate zone (IZ) and subventricular zone (SVZ) showed robust tangential migration from lateral to medial cortex, while others showed radial and non-radial migration mostly towards the pial surface. In flat-mount preparations, GFP-positive neurons of the marginal zone (MZ) showed multidirectional tangential migration. Some of these neurons descended toward the cortical plate (CP). Intracortical migration of these neurons was largely unaffected by a treatment that cleaves glycosylphosphatidylinositol (GPI) anchors. These findings suggest that tangential migration of cortical interneurons from lateral to medial cortex predominantly occurs in the IZ/SVZ and raise the possibility that a part of the pial surface-directed neurons in the IZ/SVZ reach the MZ, whereby they spread into the whole area of the cortex. At least a part of these neurons may descend toward the CP. Our results also suggest that intracortical migration of GABAergic neurons occurs independent of GPI-anchored proteins.
This article has been cited by other articles:

|
 |

|
 |
 
P. P. Gopal and J. A. Golden
Pax6-/- Mice Have a Cell Nonautonomous Defect in Nonradial Interneuron Migration
Cereb Cortex,
April 1, 2008;
18(4):
752 - 762.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Lopez-Bendito, J. A. Sanchez-Alcaniz, R. Pla, V. Borrell, E. Pico, M. Valdeolmillos, and O. Marin
Chemokine Signaling Controls Intracortical Migration and Final Distribution of GABAergic Interneurons
J. Neurosci.,
February 13, 2008;
28(7):
1613 - 1624.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Li, H. Adesnik, J. Li, J. Long, R. A. Nicoll, J. L. R. Rubenstein, and S. J. Pleasure
Regional Distribution of Cortical Interneurons and Development of Inhibitory Tone Are Regulated by Cxcl12/Cxcr4 Signaling
J. Neurosci.,
January 30, 2008;
28(5):
1085 - 1098.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Poluch, B. Jablonska, and S. L. Juliano
Alteration of Interneuron Migration in a Ferret Model of Cortical Dysplasia
Cereb Cortex,
January 1, 2008;
18(1):
78 - 92.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Metin, C. Alvarez, D. Moudoux, T. Vitalis, C. Pieau, and Z. Molnar
Conserved pattern of tangential neuronal migration during forebrain development
Development,
August 1, 2007;
134(15):
2815 - 2827.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-B. Manent and A. Represa
Neurotransmitters and Brain Maturation: Early Paracrine Actions of GABA and Glutamate Modulate Neuronal Migration
Neuroscientist,
June 1, 2007;
13(3):
268 - 279.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Liodis, M. Denaxa, M. Grigoriou, C. Akufo-Addo, Y. Yanagawa, and V. Pachnis
Lhx6 Activity Is Required for the Normal Migration and Specification of Cortical Interneuron Subtypes
J. Neurosci.,
March 21, 2007;
27(12):
3078 - 3089.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Pla, V. Borrell, N. Flames, and O. Marin
Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling.
J. Neurosci.,
June 28, 2006;
26(26):
6924 - 6934.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Andrews, A. Liapi, C. Plachez, L. Camurri, J. Zhang, S. Mori, F. Murakami, J. G. Parnavelas, V. Sundaresan, and L. J. Richards
Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain
Development,
June 1, 2006;
133(11):
2243 - 2252.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. H. Tanaka, K. Maekawa, Y. Yanagawa, K. Obata, and F. Murakami
Multidirectional and multizonal tangential migration of GABAergic interneurons in the developing cerebral cortex
Development,
June 1, 2006;
133(11):
2167 - 2176.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-B. Manent, I. Jorquera, Y. Ben-Ari, L. Aniksztejn, and A. Represa
Glutamate acting on AMPA but not NMDA receptors modulates the migration of hippocampal interneurons.
J. Neurosci.,
May 31, 2006;
26(22):
5901 - 5909.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. M. Morozov, A. E. Ayoub, and P. Rakic
Translocation of Synaptically Connected Interneurons across the Dentate Gyrus of the Early Postnatal Rat Hippocampus.
J. Neurosci.,
May 10, 2006;
26(19):
5017 - 5027.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Alcantara, E. Pozas, C. F. Ibanez, and E. Soriano
BDNF-modulated Spatial Organization of Cajal-Retzius and GABAergic Neurons in the Marginal Zone Plays a Role in the Development of Cortical Organization
Cereb Cortex,
April 1, 2006;
16(4):
487 - 499.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Nomura, J. Holmberg, J. Frisen, and N. Osumi
Pax6-dependent boundary defines alignment of migrating olfactory cortex neurons via the repulsive activity of ephrin A5
Development,
April 1, 2006;
133(7):
1335 - 1345.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Hammond, E. So, J. Gunnersen, H. Valcanis, M. Kalloniatis, and S.-S. Tan
Layer Positioning of Late-Born Cortical Interneurons Is Dependent on Reelin But Not p35 Signaling
J. Neurosci.,
February 1, 2006;
26(5):
1646 - 1655.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. J. Barkovich, R. I. Kuzniecky, G. D. Jackson, R. Guerrini, and W. B. Dobyns
A developmental and genetic classification for malformations of cortical development
Neurology,
December 27, 2005;
65(12):
1873 - 1887.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Abe, Y. Yanagawa, K. Kanbara, K. Maemura, H. Hayasaki, H. Azuma, K. Obata, Y. Katsuoka, M. Yabumoto, and M. Watanabe
Epithelial Localization of Green Fluorescent Protein-Positive Cells in Epididymis of the GAD67-GFP Knock-in Mouse
J Androl,
September 1, 2005;
26(5):
568 - 577.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Yozu, H. Tabata, and K. Nakajima
The Caudal Migratory Stream: A Novel Migratory Stream of Interneurons Derived from the Caudal Ganglionic Eminence in the Developing Mouse Forebrain
J. Neurosci.,
August 3, 2005;
25(31):
7268 - 7277.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Bellion, J.-P. Baudoin, C. Alvarez, M. Bornens, and C. Metin
Nucleokinesis in Tangentially Migrating Neurons Comprises Two Alternating Phases: Forward Migration of the Golgi/Centrosome Associated with Centrosome Splitting and Myosin Contraction at the Rear
J. Neurosci.,
June 15, 2005;
25(24):
5691 - 5699.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Kanatani, H. Tabata, and K. Nakajima
Topical Review: Neuronal Migration in Cortical Development
J Child Neurol,
April 1, 2005;
20(4):
274 - 279.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Tripodi, A. Filosa, M. Armentano, and M. Studer
The COUP-TF nuclear receptors regulate cell migration in the mammalian basal forebrain
Development,
December 15, 2004;
131(24):
6119 - 6129.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Lopez-Bendito, K. Sturgess, F. Erdelyi, G. Szabo, Z. Molnar, and O. Paulsen
Preferential Origin and Layer Destination of GAD65-GFP Cortical Interneurons
Cereb Cortex,
October 1, 2004;
14(10):
1122 - 1133.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Kanatani, H. Tabata, and K. Nakajima
Topical Review: Neuronal Migration in Cortical Development
J Child Neurol,
March 1, 2004;
19(3):
274 - 279.
[Abstract]
[PDF]
|
 |
|
© The Company of Biologists Ltd 2003