Neuronal activity is required for the development of specific cortical interneuron subtypes

被引:195
作者
Garcia, Natalia V. De Marco [1 ,2 ]
Karayannis, Theofanis [1 ,2 ]
Fishell, Gord [1 ,2 ]
机构
[1] NYU, Langone Med Ctr, Smilow Neurosci Program, Dept Cell Biol, New York, NY 10016 USA
[2] NYU, Langone Med Ctr, Dept Neural Sci, New York, NY 10016 USA
基金
美国国家卫生研究院;
关键词
ELECTRICAL-ACTIVITY; IN-VIVO; GANGLIONIC EMINENCE; APOPTOTIC CELLS; CEREBRAL-CORTEX; MIGRATION; NETWORKS; MOUSE; PROJECTIONS; ENGULFMENT;
D O I
10.1038/nature09865
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Electrical activity has been shown to regulate development in a variety of species and in various structures(1), including the retina(2-4), spinal cord(5,6) and cortex(5). Within the mammalian cortex specifically, the development of dendrites and commissural axons in pyramidal cells is activity-dependent(7,8). However, little is known about the developmental role of activity in the other major cortical population of neurons, the GABA-producing interneurons. These neurons are morphologically and functionally heterogeneous and efforts over the past decade have focused on determining the mechanisms that contribute to this diversity(9-11). It was recently discovered that 30% of all cortical interneurons arise from a relatively novel source within the ventral telencephalon, the caudal ganglionic eminence (CGE)(11,12). Owing to their late birth date, these interneurons populate the cortex only after the majority of other interneurons and pyramidal cells are already in place and have started to functionally integrate. Here we demonstrate in mice that for CGE-derived reelin (Re)-positive and calretinin (Cr)-positive (but not vasoactive intestinal peptide (VIP)-positive) interneurons(12,13), activity is essential before postnatal day 3 for correct migration, and that after postnatal day 3, glutamate-mediated activity controls the development of their axons and dendrites. Furthermore, we show that the engulfment and cell motility 1 gene (Elmo1)(14), a target of the transcription factor distal-less homeobox 1 (Dlx1)(15), is selectively expressed in Re+ and Cr+ interneurons and is both necessary and sufficient for activity-dependent interneuron migration. Our findings reveal a selective requirement for activity in shaping the cortical integration of specific neuronal subtypes.
引用
收藏
页码:351 / U116
页数:6
相关论文
共 34 条
[1]   Early NMDA receptor-driven waves of activity in the developing neocortex: physiological or pathological network oscillations? [J].
Allene, Camille ;
Cossart, Rosa .
JOURNAL OF PHYSIOLOGY-LONDON, 2010, 588 (01) :83-91
[2]   Interneuron migration from basal forebrain to neocortex: Dependence on Dlx genes [J].
Anderson, SA ;
Eisenstat, DD ;
Shi, L ;
Rubenstein, JLR .
SCIENCE, 1997, 278 (5337) :474-476
[3]   Petilla terminology:: nomenclature of features of GABAergic interneurons of the cerebral cortex [J].
Ascoli, Giorgio A. ;
Alonso-Nanclares, Lidia ;
Anderson, Stewart A. ;
Barrionuevo, German ;
Benavides-Piccione, Ruth ;
Burkhalter, Andreas ;
Buzsaki, Gyoergy ;
Cauli, Bruno ;
DeFelipe, Javier ;
Fairen, Alfonso ;
Feldmeyer, Dirk ;
Fishell, Gord ;
Fregnac, Yves ;
Freund, Tamas F. ;
Gardner, Daniel ;
Gardner, Esther P. ;
Goldberg, Jesse H. ;
Helmstaedter, Moritz ;
Hestrin, Shaul ;
Karube, Fuyuki ;
Kisvarday, Zoltan F. ;
Lambolez, Bertrand ;
Lewis, David A. ;
Marin, Oscar ;
Markram, Henry ;
Munoz, Alberto ;
Packer, Adam ;
Petersen, Carl C. H. ;
Rockland, Kathleen S. ;
Rossier, Jean ;
Rudy, Bernardo ;
Somogyi, Peter ;
Staiger, Jochen F. ;
Tamas, Gabor ;
Thomson, Alex M. ;
Toledo-Rodriguez, Maria ;
Wang, Yun ;
West, David C. ;
Yuste, Rafael .
NATURE REVIEWS NEUROSCIENCE, 2008, 9 (07) :557-568
[4]   THE DEVELOPMENTAL INTEGRATION OF CORTICAL INTERNEURONS INTO A FUNCTIONAL NETWORK [J].
Batista-Brito, Renata ;
Fishell, Gord .
DEVELOPMENT OF NEURAL CIRCUITRY, 2009, 87 :81-+
[5]   Mechanisms underlying spontaneous patterned activity in developing neural circuits [J].
Blankenship, Aaron G. ;
Feller, Marla B. .
NATURE REVIEWS NEUROSCIENCE, 2010, 11 (01) :18-29
[6]   KCC2 Expression Promotes the Termination of Cortical Interneuron Migration in a Voltage-Sensitive Calcium-Dependent Manner [J].
Bortone, Dante ;
Polleux, Franck .
NEURON, 2009, 62 (01) :53-71
[7]   The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes [J].
Butt, Simon J. B. ;
Sousa, Vitor H. ;
Fuccillo, Marc V. ;
Hjerling-Leffler, Jens ;
Miyoshi, Goichi ;
Kimura, Shioko ;
Fishell, Gord .
NEURON, 2008, 59 (05) :722-732
[8]   Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo [J].
Cancedda, Laura ;
Fiumelli, Hubert ;
Chen, Karen ;
Poo, Mu-ming .
JOURNAL OF NEUROSCIENCE, 2007, 27 (19) :5224-5235
[9]   Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy [J].
Cobos, I ;
Calcagnotto, ME ;
Vilaythong, AJ ;
Thwin, MT ;
Noebels, JL ;
Baraban, SC ;
Rubenstein, JLR .
NATURE NEUROSCIENCE, 2005, 8 (08) :1059-1068
[10]   Dlx transcription factors promote migration through repression of axon and dendrite growth [J].
Cobos, Inma ;
Borello, Ugo ;
Rubenstein, John L. R. .
NEURON, 2007, 54 (06) :873-888