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

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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 GABA_A receptor reversal potential (E_{GABA_A}) 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 E_{GABA_A}, with the most positive values found in the youngest cortical precursor cells. At the early stages of neocortical development, E_{GABA_A} is determined by the chloride (Cl) gradient, and the internal chloride concentration ([Cl]_i) decreases with development. E_{GABA_A} is positive to the resting potential, indicating that GABA serves to depolarize developing neocortical cells. Consistent with this conclusion, GABA_A 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 GABA_A receptor activation can depolarize cells and activate VGCCs. These results suggest that GABA_A 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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J. Neurosci., April 1, 2002; 22(7): 2598 - 2606.
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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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]

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]