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The Journal of Neuroscience, March 17, 2004, 24(11):2612-2622; doi:10.1523/JNEUROSCI.5667-03.2004
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Development/Plasticity/Repair
Origins of Cortical Interneuron Subtypes
Qing Xu,1
Inma Cobos,2
Estanislao De La Cruz,1
John L. Rubenstein,2 and
Stewart A. Anderson1
1Department of Psychiatry, Weill Medical College of Cornell University, New York, New York 10021, and 2Department of Psychiatry, University of California, San Francisco, San Francisco, California 94143
Cerebral cortical functions are conducted by two general classes of neurons: glutamatergic projection neurons and GABAergic interneurons. Distinct interneuron subtypes serve distinct roles in modulating cortical activity and can be differentially affected in cortical diseases, but little is known about the mechanisms for generating their diversity. Recent evidence suggests that many cortical interneurons originate within the subcortical telencephalon and then migrate tangentially into the overlying cortex. To test the hypothesis that distinct interneuron subtypes are derived from distinct telencephalic subdivisions, we have used an in vitro assay to assess the developmental potential of subregions of the telencephalic proliferative zone (PZ) to give rise to neurochemically defined interneuron subgroups. PZ cells from GFP+ donor mouse embryos were transplanted onto neonatal cortical feeder cells and assessed for their ability to generate specific interneuron subtypes. Our results suggest that the parvalbumin- and the somatostatin-expressing interneuron subgroups originate primarily within the medial ganglionic eminence (MGE) of the subcortical telencephalon, whereas the calretinin-expressing interneurons appear to derive mainly from the caudal ganglionic eminence (CGE). These results are supported by findings from primary cultures of cortex from Nkx2.1 mutants, in which normal MGE fails to form but in which the CGE is less affected. In these cultures, parvalbumin- and somatostatin-expressing cells are absent, although calretinin-expressing interneurons are present. Interestingly, calretinin-expressing bipolar interneurons were nearly absent from cortical cultures of Dlx1/2 mutants. By establishing spatial differences in the origins of interneuron subtypes, these studies lay the groundwork for elucidating the molecular bases for their distinct differentiation pathways.
Key words: interneuron; cortex; Nkx2.1; parvalbumin; somatostatin; calretinin
Received Oct 20, 2003;
revised January 26, 2004;
accepted January 27, 2004.
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|

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|
 |
|

|
 |

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|
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|
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|
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|
 |
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|
 |

|
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|
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|
 |

|
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|
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|
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 |
|

|
 |

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 |
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|
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|
 |
|

|
 |

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|
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 |
|

|
 |

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|
 |
|

|
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|
 |
|

|
 |

|
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|
 |
|

|
 |

|
 |
 
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5012 - 5022.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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J. Neurosci.,
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[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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J. Neurosci.,
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3078 - 3089.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. B. Glickstein, S. Alexander, and M. E. Ross
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Cereb Cortex,
March 1, 2007;
17(3):
632 - 642.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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Electrophysiological Differences Between Neurogliaform Cells From Monkey and Rat Prefrontal Cortex
J Neurophysiol,
February 1, 2007;
97(2):
1030 - 1039.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. S. E. Carney, T. B. Alfonso, D. Cohen, H. Dai, S. Nery, B. Stoica, J. Slotkin, B. S. Bregman, G. Fishell, and J. G. Corbin
Cell Migration along the Lateral Cortical Stream to the Developing Basal Telencephalic Limbic System.
J. Neurosci.,
November 8, 2006;
26(45):
11562 - 11574.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Trotter, J. Kapur, M. J. Anzivino, and K. S. Lee
GABAergic Synaptic Inhibition Is Reduced before Seizure Onset in a Genetic Model of Cortical Malformation.
J. Neurosci.,
October 18, 2006;
26(42):
10756 - 10767.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. C. Cuzon, P. W. Yeh, Q. Cheng, and H. H. Yeh
Ambient GABA Promotes Cortical Entry of Tangentially Migrating Cells Derived from the Medial Ganglionic Eminence
Cereb Cortex,
October 1, 2006;
16(10):
1377 - 1388.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. L. Ramos, J. Bai, and J. J. LoTurco
Heterotopia Formation in Rat but Not Mouse Neocortex after RNA Interference Knockdown of DCX
Cereb Cortex,
September 1, 2006;
16(9):
1323 - 1331.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Yano, T. Subkhankulova, F. J. Livesey, and H. P. C. Robinson
Electrophysiological and gene expression profiling of neuronal cell types in mammalian neocortex
J. Physiol.,
September 1, 2006;
575(2):
361 - 365.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Alvarez-Dolado, M. E. Calcagnotto, K. M. Karkar, D. G. Southwell, D. M. Jones-Davis, R. C. Estrada, J. L. R. Rubenstein, A. Alvarez-Buylla, and S. C. Baraban
Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain.
J. Neurosci.,
July 12, 2006;
26(28):
7380 - 7389.
[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]
|
 |
|

|
 |

|
 |
 
Y. Ma, H. Hu, A. S. Berrebi, P. H. Mathers, and A. Agmon
Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice.
J. Neurosci.,
May 10, 2006;
26(19):
5069 - 5082.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Kawaguchi, F. Karube, and Y. Kubota
Dendritic Branch Typing and Spine Expression Patterns in Cortical Nonpyramidal Cells
Cereb Cortex,
May 1, 2006;
16(5):
696 - 711.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N.V. Povysheva, G. Gonzalez-Burgos, A.V. Zaitsev, S. Kroner, G. Barrionuevo, D.A. Lewis, and L.S. Krimer
Properties of Excitatory Synaptic Responses in Fast-spiking Interneurons and Pyramidal Cells from Monkey and Rat Prefrontal Cortex
Cereb Cortex,
April 1, 2006;
16(4):
541 - 552.
[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]
|
 |
|

|
 |

|
 |
 
Q. Xu, C. P. Wonders, and S. A. Anderson
Sonic hedgehog maintains the identity of cortical interneuron progenitors in the ventral telencephalon
Development,
November 15, 2005;
132(22):
4987 - 4998.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. S. Krimer, A. V. Zaitsev, G. Czanner, S. Kroner, G. Gonzalez-Burgos, N. V. Povysheva, S. Iyengar, G. Barrionuevo, and D. A. Lewis
Cluster Analysis-Based Physiological Classification and Morphological Properties of Inhibitory Neurons in Layers 2-3 of Monkey Dorsolateral Prefrontal Cortex
J Neurophysiol,
November 1, 2005;
94(5):
3009 - 3022.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. C. Moe, M. Varghese, A. I. Danilov, U. Westerlund, J. Ramm-Pettersen, L. Brundin, M. Svensson, J. Berg-Johnsen, and I. A. Langmoen
Multipotent progenitor cells from the adult human brain: neurophysiological differentiation to mature neurons
Brain,
September 1, 2005;
128(9):
2189 - 2199.
[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.V. Zaitsev, G. Gonzalez-Burgos, N.V. Povysheva, S. Kroner, D.A. Lewis, and L.S. Krimer
Localization of Calcium-binding Proteins in Physiologically and Morphologically Characterized Interneurons of Monkey Dorsolateral Prefrontal Cortex
Cereb Cortex,
August 1, 2005;
15(8):
1178 - 1186.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Wonders and S. A. Anderson
Cortical Interneurons and Their Origins
Neuroscientist,
June 1, 2005;
11(3):
199 - 205.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Narasimhaiah, A. Tuchman, S. L. Lin, and J. R. Naegele
Oxidative Damage and Defective DNA Repair is Linked to Apoptosis of Migrating Neurons and Progenitors During Cerebral Cortex Development in Ku70-Deficient Mice
Cereb Cortex,
June 1, 2005;
15(6):
696 - 707.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Englund, A. Fink, C. Lau, D. Pham, R. A. M. Daza, A. Bulfone, T. Kowalczyk, and R. F. Hevner
Pax6, Tbr2, and Tbr1 Are Expressed Sequentially by Radial Glia, Intermediate Progenitor Cells, and Postmitotic Neurons in Developing Neocortex
J. Neurosci.,
January 5, 2005;
25(1):
247 - 251.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Foldy, J. Dyhrfjeld-Johnsen, and I. Soltesz
Structure of cortical microcircuit theory
J. Physiol.,
January 1, 2005;
562(1):
47 - 54.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. F. McManus, I. M. Nasrallah, M. M. Pancoast, A. Wynshaw-Boris, and J. A. Golden
Lis1 Is Necessary for Normal Non-Radial Migration of Inhibitory Interneurons
Am. J. Pathol.,
September 1, 2004;
165(3):
775 - 784.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Alifragis, A. Liapi, and J. G. Parnavelas
Lhx6 Regulates the Migration of Cortical Interneurons from the Ventral Telencephalon But Does Not Specify their GABA Phenotype
J. Neurosci.,
June 16, 2004;
24(24):
5643 - 5648.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|