 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, December 1, 1999, 19(23):10372-10382
The Establishment of GABAergic and Glutamatergic Synapses on CA1 Pyramidal Neurons is Sequential and Correlates with the Development of the Apical Dendrite
Roman Tyzio, Alfonso Represa, Isabel Jorquera, Yehezkel Ben-Ari, Henri Gozlan, and Laurent Aniksztejn Institut de Neurobiologie de la Méditérranée, Institut National de la Santé, et de la Recherche Médicale, 13273 Marseille Cedex 09, France
We have performed a morphofunctional analysis of CA1 pyramidal neurons at birth to examine the sequence of formation of GABAergic and glutamatergic postsynaptic currents (PSCs) and to determine their relation to the dendritic arborization of pyramidal neurons. We report that at birth pyramidal neurons are heterogeneous. Three stages of development can be identified: (1) the majority of the neurons (80%) have small somata, an anlage of apical dendrite, and neither spontaneous nor evoked PSCs; (2) 10% of the neurons have a small apical dendrite restricted to the stratum radiatum and PSCs mediated only by GABAA receptors; and (3) 10% of the neurons have an apical dendrite that reaches the stratum lacunosum moleculare and PSCs mediated both by GABAA and glutamate receptors. These three groups of pyramidal neurons can be differentiated by their capacitance (Cm = 17.9 ± 0.8; 30.2 ± 1.6; 43.2 ± 3.0 pF, respectively). At birth, the synaptic markers synapsin-1 and synaptophysin labeling are present in dendritic layers but not in the stratum pyramidale, suggesting that GABAergic peridendritic synapses are established before perisomatic ones. The present observations demonstrate that GABAergic and glutamatergic synapses are established sequentially with GABAergic synapses being established first most likely on the apical dendrites of the principal neurons. We propose that different sets of conditions are required for the establishment of functional GABA and glutamate synapses, the latter necessitating more developed neurons that have apical dendrites that reach the lacunosum moleculare region.
Key words: CA1 pyramidal cells; development; GABAA receptors; AMPA receptors; NMDA receptors; synaptic transmission
Copyright © 1999 Society for Neuroscience 0270-6474/99/192310372-11$05.00/0
This article has been cited by other articles:
D. D. Wang and A. R. Kriegstein
GABA Regulates Excitatory Synapse Formation in the Neocortex via NMDA Receptor Activation
J. Neurosci., May 21, 2008; 28(21): 5547 - 5558.
[Abstract] [Full Text] [PDF]
Y. Kang, X. Zhang, F. Dobie, H. Wu, and A. M. Craig
Induction of GABAergic Postsynaptic Differentiation by {alpha}-Neurexins
J. Biol. Chem., January 25, 2008; 283(4): 2323 - 2334.
[Abstract] [Full Text] [PDF]
L. Deng, J. Yao, C. Fang, N. Dong, B. Luscher, and G. Chen
Sequential Postsynaptic Maturation Governs the Temporal Order of GABAergic and Glutamatergic Synaptogenesis in Rat Embryonic Cultures
J. Neurosci., October 3, 2007; 27(40): 10860 - 10869.
[Abstract] [Full Text] [PDF]
A. A. Cattani, V. D. Bonfardin, A. Represa, Y. Ben-Ari, and L. Aniksztejn
Generation of Slow Network Oscillations in the Developing Rat Hippocampus After Blockade of Glutamate Uptake
J Neurophysiol, October 1, 2007; 98(4): 2324 - 2336.
[Abstract] [Full Text] [PDF]
Y. Ben-Ari, J.-L. Gaiarsa, R. Tyzio, and R. Khazipov
GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations
Physiol Rev, October 1, 2007; 87(4): 1215 - 1284.
[Abstract] [Full Text] [PDF]
I. Marchionni, A. Omrani, and E. Cherubini
In the developing rat hippocampus a tonic GABAA-mediated conductance selectively enhances the glutamatergic drive of principal cells
J. Physiol., June 1, 2007; 581(2): 515 - 528.
[Abstract] [Full Text] [PDF]
J. Huupponen, S. M. Molchanova, T. Taira, and S. E. Lauri
Susceptibility for homeostatic plasticity is down-regulated in parallel with maturation of the rat hippocampal synaptic circuitry
J. Physiol., June 1, 2007; 581(2): 505 - 514.
[Abstract] [Full Text] [PDF]
Y. Liu, L. I. Zhang, and H. W. Tao
Heterosynaptic Scaling of Developing GABAergic Synapses: Dependence on Glutamatergic Input and Developmental Stage
J. Neurosci., May 16, 2007; 27(20): 5301 - 5312.
[Abstract] [Full Text] [PDF]
A. L. Brewster, Y. Chen, R. A. Bender, A. Yeh, R. Shigemoto, and T. Z. Baram
Quantitative Analysis and Subcellular Distribution of mRNA and Protein Expression of the Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels throughout Development in Rat Hippocampus
Cereb Cortex, March 1, 2007; 17(3): 702 - 712.
[Abstract] [Full Text] [PDF]
R. Tyzio, R. Cossart, I. Khalilov, M. Minlebaev, C. A. Hubner, A. Represa, Y. Ben-Ari, and R. Khazipov
Maternal Oxytocin Triggers a Transient Inhibitory Switch in GABA Signaling in the Fetal Brain During Delivery
Science, December 15, 2006; 314(5806): 1788 - 1792.
[Abstract] [Full Text] [PDF]
V. F. Safiulina, R. Afzalov, L. Khiroug, E. Cherubini, and R. Giniatullin
Reactive Oxygen Species Mediate the Potentiating Effects of ATP on GABAergic Synaptic Transmission in the Immature Hippocampus
J. Biol. Chem., August 18, 2006; 281(33): 23464 - 23470.
[Abstract] [Full Text] [PDF]
G. D. Hilton, L. L. Bambrick, S. M. Thompson, and M. M. McCarthy
Estradiol Modulation of Kainic Acid-Induced Calcium Elevation in Neonatal Hippocampal Neurons
Endocrinology, March 1, 2006; 147(3): 1246 - 1255.
[Abstract] [Full Text] [PDF]
L. O. Wadiche, D. A. Bromberg, A. L. Bensen, and G. L. Westbrook
GABAergic Signaling to Newborn Neurons in Dentate Gyrus
J Neurophysiol, December 1, 2005; 94(6): 4528 - 4532.
[Abstract] [Full Text] [PDF]
M. S. Esposito, V. C. Piatti, D. A. Laplagne, N. A. Morgenstern, C. C. Ferrari, F. J. Pitossi, and A. F. Schinder
Neuronal Differentiation in the Adult Hippocampus Recapitulates Embryonic Development
J. Neurosci., November 2, 2005; 25(44): 10074 - 10086.
[Abstract] [Full Text] [PDF]
V. F. Safiulina, A. M. Kasyanov, R. Giniatullin, and E. Cherubini
Adenosine Down-Regulates Giant Depolarizing Potentials in the Developing Rat Hippocampus by Exerting a Negative Control on Glutamatergic Inputs
J Neurophysiol, October 1, 2005; 94(4): 2797 - 2804.
[Abstract] [Full Text] [PDF]
V. F Safiulina, A. M Kasyanov, E. Sokolova, E. Cherubini, and R. Giniatullin
ATP contributes to the generation of network-driven giant depolarizing potentials in the neonatal rat hippocampus
J. Physiol., June 15, 2005; 565(3): 981 - 992.
[Abstract] [Full Text] [PDF]
S. T. Sipila, K. Huttu, I. Soltesz, J. Voipio, and K. Kaila
Depolarizing GABA Acts on Intrinsically Bursting Pyramidal Neurons to Drive Giant Depolarizing Potentials in the Immature Hippocampus
J. Neurosci., June 1, 2005; 25(22): 5280 - 5289.
[Abstract] [Full Text] [PDF]
A. F. Schinder and F. H. Gage
A Hypothesis About the Role of Adult Neurogenesis in Hippocampal Function
Physiology, October 1, 2004; 19(5): 253 - 261.
[Abstract] [Full Text] [PDF]
I. Colin-Le Brun, N. Ferrand, O. Caillard, P. Tosetti, Y. Ben-Ari, and J.-L. Gaiarsa
Spontaneous synaptic activity is required for the formation of functional GABAergic synapses in the developing rat hippocampus
J. Physiol., August 15, 2004; 559(1): 129 - 139.
[Abstract] [Full Text] [PDF]
Q. Li, S. Guo-Ross, D. V. Lewis, D. Turner, A. M. White, W. A. Wilson, and H. S. Swartzwelder
Dietary Prenatal Choline Supplementation Alters Postnatal Hippocampal Structure and Function
J Neurophysiol, April 1, 2004; 91(4): 1545 - 1555.
[Abstract] [Full Text] [PDF]
L. S. Overstreet, S. T. Hentges, V. F. Bumaschny, F. S. J. de Souza, J. L. Smart, A. M. Santangelo, M. J. Low, G. L. Westbrook, and M. Rubinstein
A Transgenic Marker for Newly Born Granule Cells in Dentate Gyrus
J. Neurosci., March 31, 2004; 24(13): 3251 - 3259.
[Abstract] [Full Text] [PDF]
H. Golan, T. Levav, A. Mendelsohn, and M. Huleihel
Involvement of Tumor Necrosis Factor Alpha in Hippocampal Development and Function
Cereb Cortex, January 1, 2004; 14(1): 97 - 105.
[Abstract] [Full Text] [PDF]
O. Belluzzi, M. Benedusi, J. Ackman, and J. J. LoTurco
Electrophysiological Differentiation of New Neurons in the Olfactory Bulb
J. Neurosci., November 12, 2003; 23(32): 10411 - 10418.
[Abstract] [Full Text] [PDF]
H. Gozlan and Y. Ben-Ari
Interneurons are the Source and the Targets of the First Synapses Formed in the Rat Developing Hippocampal Circuit
Cereb Cortex, June 1, 2003; 13(6): 684 - 692.
[Abstract] [Full Text] [PDF]
V. I. Dzhala and K. J. Staley
Excitatory Actions of Endogenously Released GABA Contribute to Initiation of Ictal Epileptiform Activity in the Developing Hippocampus
J. Neurosci., March 1, 2003; 23(5): 1840 - 1846.
[Abstract] [Full Text] [PDF]
L. Maggi, C. Le Magueresse, J.-P. Changeux, and E. Cherubini
Nicotine activates immature "silent" connections in the developing hippocampus
PNAS, February 18, 2003; 100(4): 2059 - 2064.
[Abstract] [Full Text] [PDF]
L. Groc, B. Gustafsson, and E. Hanse
Spontaneous Unitary Synaptic Activity in CA1 Pyramidal Neurons during Early Postnatal Development: Constant Contribution of AMPA and NMDA Receptors
J. Neurosci., July 1, 2002; 22(13): 5552 - 5562.
[Abstract] [Full Text] [PDF]
I. Brunig, A. Suter, I. Knuesel, B. Luscher, and J.-M. Fritschy
GABAergic Terminals Are Required for Postsynaptic Clustering of Dystrophin But Not of GABAA Receptors and Gephyrin
J. Neurosci., June 15, 2002; 22(12): 4805 - 4813.
[Abstract] [Full Text] [PDF]
R. Khazipov, M. Esclapez, O. Caillard, C. Bernard, I. Khalilov, R. Tyzio, J. Hirsch, V. Dzhala, B. Berger, and Y. Ben-Ari
Early Development of Neuronal Activity in the Primate Hippocampus In Utero
J. Neurosci., December 15, 2001; 21(24): 9770 - 9781.
[Abstract] [Full Text] [PDF]
M. Martina, S. Royer, and D. Pare
Cell-Type-Specific GABA Responses and Chloride Homeostasis in the Cortex and Amygdala
J Neurophysiol, December 1, 2001; 86(6): 2887 - 2895.
[Abstract] [Full Text] [PDF]
A. F. Keller, J. A. M. Coull, N. Chery, P. Poisbeau, and Y. De Koninck
Region-Specific Developmental Specialization of GABA-Glycine Cosynapses in Laminas I-II of the Rat Spinal Dorsal Horn
J. Neurosci., October 15, 2001; 21(20): 7871 - 7880.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|