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Volume 16, Number 20, Issue of October 15, 1996 pp. 6414-6423
Copyright ©1996 Society for Neuroscience

Excitatory GABA Responses in Embryonic and Neonatal Cortical Slices Demonstrated by Gramicidin Perforated-Patch Recordings and Calcium Imaging

Received May 17, 1996; revised July 18, 1996; accepted July 24, 1996.

David F. Owens, Leslie H. Boyce, Marion B. E. Davis, and Arnold R. Kriegstein

Department of Neurology and The Center for Neurobiology and Behavior, College of Physicians and Surgeons of Columbia University, New York, New York 10025

Gramicidin perforated-patch-clamp recordings in brain slices were used to obtain an accurate assessment of the developmental change in the GABAA receptor reversal potential (EGABAA) in embryonic and early postnatal rat neocortical cells including neuroepithelial precursor cells, cortical plate neurons, and postnatal neocortical neurons. Our results demonstrate that there is a progressive negative shift in EGABAA, with the most positive values found in the youngest cortical precursor cells. At the early stages of neocortical development, EGABAA is determined by the chloride (Cl-) gradient, and the internal chloride concentration ([Cl-]i) decreases with development. EGABAA is positive to the resting potential, indicating that GABA serves to depolarize developing neocortical cells. Consistent with this conclusion, GABAA receptor activation with muscimol was found to increase the internal calcium concentration ([Ca2+]i) in both embryonic and early postnatal neocortical cells through the activation of voltage-gated calcium channels (VGCCs). Postnatal cells exhibit spontaneous postsynaptic synaptic currents, which are eliminated by bicuculline methiodide (BMI) but not glutamate receptor antagonists and reverse at the Cl- equilibrium potential. Likewise, brief spontaneous increases in [Ca2+]i, sensitive to BMI and TTX, are observed at the same ages, suggesting that endogenous synaptic GABAA receptor activation can depolarize cells and activate VGCCs. These results suggest that GABAA receptor-mediated depolarization may influence early neocortical developmental events, including neurogenesis and synaptogenesis, through the activation of Ca2+-dependent signal transduction pathways.

Key words: cortical development; GABA; intracellular calcium; perforated-patch recording; neocortex; synaptogenesis




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Induction of NMDA and GABAA Receptor-Mediated Ca2+ Oscillations With KCC2 mRNA Downregulation in Injured Facial Motoneurons
J Neurophysiol, March 1, 2003; 89(3): 1353 - 1362.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
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]


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J. Neurosci.Home page
M. G. Hanson and L. T. Landmesser
Characterization of the Circuits That Generate Spontaneous Episodes of Activity in the Early Embryonic Mouse Spinal Cord
J. Neurosci., January 15, 2003; 23(2): 587 - 600.
[Abstract] [Full Text] [PDF]


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J Child NeurolHome page
T. A. Simeone, S. D. Donevan, and J. M. Rho
Molecular Biology and Ontogeny of {gamma}-Aminobutyric Acid (GABA) Receptors in the Mammalian Central Nervous System
J Child Neurol, January 1, 2003; 18(1): 39 - 48.
[Abstract] [PDF]


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Mol. Endocrinol.Home page
R. A. DeFazio, S. Heger, S. R. Ojeda, and S. M. Moenter
Activation of A-Type {gamma}-Aminobutyric Acid Receptors Excites Gonadotropin-Releasing Hormone Neurons
Mol. Endocrinol., December 1, 2002; 16(12): 2872 - 2891.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
T. Opitz, A. D. De Lima, and T. Voigt
Spontaneous Development of Synchronous Oscillatory Activity During Maturation of Cortical Networks In Vitro
J Neurophysiol, November 1, 2002; 88(5): 2196 - 2206.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
M. Luo and D. J. Perkel
Intrinsic and Synaptic Properties of Neurons in an Avian Thalamic Nucleus During Song Learning
J Neurophysiol, October 1, 2002; 88(4): 1903 - 1914.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
R. C. Foehring, J. F. M. van Brederode, G. A. Kinney, and W. J. Spain
Serotonergic Modulation of Supragranular Neurons in Rat Sensorimotor Cortex
J. Neurosci., September 15, 2002; 22(18): 8238 - 8250.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
G. Radnikow, D. Feldmeyer, and J. Lubke
Axonal Projection, Input and Output Synapses, and Synaptic Physiology of Cajal-Retzius Cells in the Developing Rat Neocortex
J. Neurosci., August 15, 2002; 22(16): 6908 - 6919.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
I. L. Hanganu, W. Kilb, and H. J. Luhmann
Functional Synaptic Projections onto Subplate Neurons in Neonatal Rat Somatosensory Cortex
J. Neurosci., August 15, 2002; 22(16): 7165 - 7176.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
I.-S. Jang, H.-J. Jeong, S. Katsurabayashi, and N. Akaike
Functional roles of presynaptic GABAA receptors on glycinergic nerve terminals in the rat spinal cord
J. Physiol., June 1, 2002; 541(2): 423 - 434.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
S.-K. Han, I. M. Abraham, and A. E. Herbison
Effect of GABA on GnRH Neurons Switches from Depolarization to Hyperpolarization at Puberty in the Female Mouse
Endocrinology, April 1, 2002; 143(4): 1459 - 1466.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
P. Branchereau, J. Chapron, and P. Meyrand
Descending 5-Hydroxytryptamine Raphe Inputs Repress the Expression of Serotonergic Neurons and Slow the Maturation of Inhibitory Systems in Mouse Embryonic Spinal Cord
J. Neurosci., April 1, 2002; 22(7): 2598 - 2606.
[Abstract] [Full Text] [PDF]


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Physiol. Rev.Home page
T. J. Jentsch, V. Stein, F. Weinreich, and A. A. Zdebik
Molecular Structure and Physiological Function of Chloride Channels
Physiol Rev, April 1, 2002; 82(2): 503 - 568.
[Abstract] [Full Text] [PDF]


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Pharmacol. Rev.Home page
S. Boehm and H. Kubista
Fine Tuning of Sympathetic Transmitter Release via Ionotropic and Metabotropic Presynaptic Receptors
Pharmacol. Rev., March 1, 2002; 54(1): 43 - 99.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
T. Numakawa, S. Yamagishi, N. Adachi, T. Matsumoto, D. Yokomaku, M. Yamada, and H. Hatanaka
Brain-derived Neurotrophic Factor-induced Potentiation of Ca2+ Oscillations in Developing Cortical Neurons
J. Biol. Chem., February 15, 2002; 277(8): 6520 - 6529.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Cell Physiol.Home page
M. Shimura, N. Akaike, and N. Harata
Circadian rhythm in intracellular Cl- activity of acutely dissociated neurons of suprachiasmatic nucleus
Am J Physiol Cell Physiol, February 1, 2002; 282(2): C366 - C373.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
F. Miskevich, W. Lu, S.-Y. Lin, and M. Constantine-Paton
Interaction between Metabotropic and NMDA Subtypes of Glutamate Receptors in Sprout Suppression at Young Synapses
J. Neurosci., January 1, 2002; 22(1): 226 - 238.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
T. Voigt, T. Opitz, and A. D. de Lima
Synchronous Oscillatory Activity in Immature Cortical Network Is Driven by GABAergic Preplate Neurons
J. Neurosci., November 15, 2001; 21(22): 8895 - 8905.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
M. Neunlist, K. Michel, D. Reiche, G. Dobreva, K. Huber, and M. Schemann
Glycine activates myenteric neurones in adult guinea-pigs
J. Physiol., November 1, 2001; 536(3): 727 - 739.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
J. Eilers, T. D Plant, N. Marandi, and A. Konnerth
GABA-mediated Ca2+ signalling in developing rat cerebellar Purkinje neurones
J. Physiol., October 15, 2001; 536(2): 429 - 437.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
P. Monsivais and E. W Rubel
Accommodation Enhances Depolarizing Inhibition in Central Neurons
J. Neurosci., October 1, 2001; 21(19): 7823 - 7830.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
L. Maggi, E. Sher, and E. Cherubini
Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus
J. Physiol., October 1, 2001; 536(1): 89 - 100.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
I.-S. Jang, H.-J. Jeong, and N. Akaike
Contribution of the Na-K-Cl Cotransporter on GABAA Receptor-Mediated Presynaptic Depolarization in Excitatory Nerve Terminals
J. Neurosci., August 15, 2001; 21(16): 5962 - 5972.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
G. Grabauskas and R. M. Bradley
Postnatal Development of Inhibitory Synaptic Transmission in the Rostral Nucleus of the Solitary Tract
J Neurophysiol, May 1, 2001; 85(5): 2203 - 2212.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
A. Peinado
Immature Neocortical Neurons Exist as Extensive Syncitial Networks Linked by Dendrodendritic Electrical Connections
J Neurophysiol, February 1, 2001; 85(2): 620 - 629.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
M. F. Karadsheh and E. Delpire
Neuronal Restrictive Silencing Element Is Found in the KCC2 Gene: Molecular Basis for KCC2-Specific Expression in Neurons
J Neurophysiol, February 1, 2001; 85(2): 995 - 997.
[Abstract] [Full Text] [PDF]


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Endocr. Rev.Home page
E. Terasawa and D. L. Fernandez
Neurobiological Mechanisms of the Onset of Puberty in Primates
Endocr. Rev., February 1, 2001; 22(1): 111 - 151.
[Abstract] [Full Text]


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J. Neurophysiol.Home page
X.-B. Gao and A. N. Van Den Pol
GABA, Not Glutamate, a Primary Transmitter Driving Action Potentials in Developing Hypothalamic Neurons
J Neurophysiol, January 1, 2001; 85(1): 425 - 434.
[Abstract] [Full Text] [PDF]



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