Regulation of intracellular Cl- levels by Na(+)-dependent Cl- cotransport distinguishes depolarizing from hyperpolarizing GABAA receptor-mediated responses in spinal neurons

QUICK SEARCH:

[advanced]

	Author:		Keyword(s):
Year:		Vol:		Page:

HOME | SEARCH | ARCHIVE | SUBSCRIBE | CONTACT | HELP

This Article

Full Text (PDF)

Submit an eLetter

Alert me when this article is cited

Alert me when eLetters are posted

Alert me if a correction is posted

Citation Map

Services

Email this article to a friend

Similar articles in this journal

Similar articles in PubMed

Alert me to new issues of the journal

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via Google Scholar

Google Scholar

Articles by Rohrbough, J.

Articles by Spitzer, N. C.

Search for Related Content

PubMed

PubMed Citation

Articles by Rohrbough, J.

Articles by Spitzer, N. C.

Pubmed/NCBI databases
Compound via MeSH
Substance via MeSH
Hazardous Substances DB
SODIUM

Previous Article | Next Article

Journal of Neuroscience, Vol 16, 82-91, Copyright © 1996 by Society for Neuroscience

ARTICLE

Regulation of intracellular Cl- levels by Na(+)-dependent Cl- cotransport distinguishes depolarizing from hyperpolarizing GABAA receptor-mediated responses in spinal neurons

J Rohrbough and NC Spitzer
Department of Biology, University of California at San Diego, La Jolla 92093-0357, USA.
Rohon-Beard (RB) spinal neurons of Xenopus larvae are depolarized by GABA. To study the mechanisms underlying this distinctive response, intracellular and patch-clamp recordings were made from RB neurons in situ. The intracellularly recorded GABA reversal potential (EREV) was near -30 mV in normal saline and was approximately 25 mV more negative in Na(+)-free saline. Whole-cell recordings from RB neurons and from neighboring dorsolateral interneurons (DLi) revealed that GABA responses of both cells were mediated by GABAA receptors. Currents elicited by GABA were mimicked by muscimol and reversibly blocked by bicuculline, and EREV shifted with changes in Cl- concentration ([Cl]) in agreement with Cl- selectivity. In perforated patch recordings, EREV for RB cells was significantly more positive than for DLi cells (-38 vs -63 mV), indicating that intact RB cells maintain higher levels of intracellular Cl-. Replacement of external Na+ or exposure to the Cl- transport inhibitor bumetanide (100 microM) shifted RB cell EREV to move negative values, consistent with Na+(-)dependent Cl cotransport contributing to higher internal [Cl]. In contrast, these treatments did not change DLi cell EREV. The results indicate that a Na+(-)dependent Cl- transport mechanism underlies GABAA receptor-mediated depolarizing Cl- conductances in RB neurons. Thus, both inhibitory and excitatory GABA responses appear to be present during the same developmental period in vivo. GABA may stimulate Ca2+ influx in RB neurons because the intracellular GABA EREV is above the threshold for low voltage- activated Ca2+ channels.

This article has been cited by other articles:

C. Wang and W. Slikker Jr
Strategies and Experimental Models for Evaluating Anesthetics: Effects on the Developing Nervous System
Anesth. Analg., June 1, 2008; 106(6): 1643 - 1658.
[Abstract] [Full Text] [PDF]

A. Delpy, A.-E. Allain, P. Meyrand, and P. Branchereau
NKCC1 cotransporter inactivation underlies embryonic development of chloride-mediated inhibition in mouse spinal motoneuron
J. Physiol., February 15, 2008; 586(4): 1059 - 1075.
[Abstract] [Full Text] [PDF]

M. Derchansky, S. S. Jahromi, M. Mamani, D. S. Shin, A. Sik, and P. L. Carlen
Transition to seizures in the isolated immature mouse hippocampus: a switch from dominant phasic inhibition to dominant phasic excitation
J. Physiol., January 15, 2008; 586(2): 477 - 494.
[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]

K. Achilles, A. Okabe, M. Ikeda, C. Shimizu-Okabe, J. Yamada, A. Fukuda, H. J. Luhmann, and W. Kilb
Kinetic Properties of Cl Uptake Mediated by Na+-Dependent K+-2Cl Cotransport in Immature Rat Neocortical Neurons
J. Neurosci., August 8, 2007; 27(32): 8616 - 8627.
[Abstract] [Full Text] [PDF]

L.-L. Zhang, E. Delpire, and N. Vardi
NKCC1 Does Not Accumulate Chloride in Developing Retinal Neurons
J Neurophysiol, July 1, 2007; 98(1): 266 - 277.
[Abstract] [Full Text] [PDF]

S. Duvarci and D. Pare
Glucocorticoids Enhance the Excitability of Principal Basolateral Amygdala Neurons
J. Neurosci., April 18, 2007; 27(16): 4482 - 4491.
[Abstract] [Full Text] [PDF]

Z. Xie, B. E. Herring, and A. P. Fox
Excitatory and Inhibitory Actions of Isoflurane in Bovine Chromaffin Cells
J Neurophysiol, December 1, 2006; 96(6): 3042 - 3050.
[Abstract] [Full Text] [PDF]

A. K. McCabe, S. L. Chisholm, H. L. Picken-Bahrey, and W. J. Moody
The self-regulating nature of spontaneous synchronized activity in developing mouse cortical neurones
J. Physiol., November 15, 2006; 577(1): 155 - 167.
[Abstract] [Full Text] [PDF]

S. T. Sipila, S. Schuchmann, J. Voipio, J. Yamada, and K. Kaila
The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus
J. Physiol., June 15, 2006; 573(3): 765 - 773.
[Abstract] [Full Text] [PDF]

C. J. Akerman and H. T. Cline
Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo.
J. Neurosci., May 10, 2006; 26(19): 5117 - 5130.
[Abstract] [Full Text] [PDF]

J. Ren and J. J. Greer
Modulation of respiratory rhythmogenesis by chloride-mediated conductances during the perinatal period.
J. Neurosci., April 5, 2006; 26(14): 3721 - 3730.
[Abstract] [Full Text] [PDF]

N. Chub, G. Z. Mentis, and M. J. O'Donovan
Chloride-Sensitive MEQ Fluorescence in Chick Embryo Motoneurons Following Manipulations of Chloride and During Spontaneous Network Activity
J Neurophysiol, January 1, 2006; 95(1): 323 - 330.
[Abstract] [Full Text] [PDF]

J. Ren, Y. Momose-Sato, K. Sato, and J. J. Greer
Rhythmic Neuronal Discharge in the Medulla and Spinal Cord of Fetal Rats in the Absence of Synaptic Transmission
J Neurophysiol, January 1, 2006; 95(1): 527 - 534.
[Abstract] [Full Text] [PDF]

S. M. Moenter and R. A. DeFazio
Endogenous {gamma}-Aminobutyric Acid Can Excite Gonadotropin-Releasing Hormone Neurons
Endocrinology, December 1, 2005; 146(12): 5374 - 5379.
[Abstract] [Full Text] [PDF]

E. Brustein and P. Drapeau
Serotoninergic Modulation of Chloride Homeostasis during Maturation of the Locomotor Network in Zebrafish
J. Neurosci., November 16, 2005; 25(46): 10607 - 10616.
[Abstract] [Full Text] [PDF]

W. J. Moody and M. M. Bosma
Ion Channel Development, Spontaneous Activity, and Activity-Dependent Development in Nerve and Muscle Cells
Physiol Rev, July 1, 2005; 85(3): 883 - 941.
[Abstract] [Full Text] [PDF]

M.-G. Lee, D. W MacGlashan Jr, and B. J Undem
Role of chloride channels in bradykinin-induced guinea pig airway vagal C-fibre activation
J. Physiol., July 1, 2005; 566(1): 205 - 212.
[Abstract] [Full Text] [PDF]

Z. Chu and S. M. Moenter
Endogenous Activation of Metabotropic Glutamate Receptors Modulates GABAergic Transmission to Gonadotropin-Releasing Hormone Neurons and Alters Their Firing Rate: A Possible Local Feedback Circuit
J. Neurosci., June 15, 2005; 25(24): 5740 - 5749.
[Abstract] [Full Text] [PDF]

L. Zhu, D. Lovinger, and E. Delpire
Cortical Neurons Lacking KCC2 Expression Show Impaired Regulation of Intracellular Chloride
J Neurophysiol, March 1, 2005; 93(3): 1557 - 1568.
[Abstract] [Full Text] [PDF]

Z Xie, K. P. M Currie, and A. P Fox
Etomidate elevates intracellular calcium levels and promotes catecholamine secretion in bovine chromaffin cells
J. Physiol., November 1, 2004; 560(3): 677 - 690.
[Abstract] [Full Text] [PDF]

M. L. Baccei and M. Fitzgerald
Development of GABAergic and Glycinergic Transmission in the Neonatal Rat Dorsal Horn
J. Neurosci., May 19, 2004; 24(20): 4749 - 4757.
[Abstract] [Full Text] [PDF]

L. G. Costa, L. Steardo, and V. Cuomo
Structural Effects and Neurofunctional Sequelae of Developmental Exposure to Psychotherapeutic Drugs: Experimental and Clinical Aspects
Pharmacol. Rev., March 1, 2004; 56(1): 103 - 147.
[Abstract] [Full Text] [PDF]

Z. Xie, K.P.M. Currie, A. L. Cahill, and A. P. Fox
Role of Cl- Co-Transporters in the Excitation Produced by GABAA Receptors in Juvenile Bovine Adrenal Chromaffin Cells
J Neurophysiol, December 1, 2003; 90(6): 3828 - 3837.
[Abstract] [Full Text] [PDF]

O. Sacchi, M. L. Rossi, R. Canella, and R. Fesce
Voltage- and Activity-Dependent Chloride Conductance Controls the Resting Status of the Intact Rat Sympathetic Neuron
J Neurophysiol, August 1, 2003; 90(2): 712 - 722.
[Abstract] [Full Text] [PDF]

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]

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]

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]

K. L. Myhr, P. D. Lukasiewicz, and R. O. L. Wong
Mechanisms Underlying Developmental Changes in the Firing Patterns of ON and OFF Retinal Ganglion Cells during Refinement of their Central Projections
J. Neurosci., November 1, 2001; 21(21): 8664 - 8671.
[Abstract] [Full Text] [PDF]

A. Wenning, C. F. J. Erxleben, and R. L. Calabrese
Indirectly Gated Cl--Dependent Cl- Channels Sense Physiological Changes of Extracellular Chloride in the Leech
J Neurophysiol, October 1, 2001; 86(4): 1826 - 1838.
[Abstract] [Full Text] [PDF]

Z. J. Zhou
A Critical Role of the Strychnine-Sensitive Glycinergic System in Spontaneous Retinal Waves of the Developing Rabbit
J. Neurosci., July 15, 2001; 21(14): 5158 - 5168.
[Abstract] [Full Text] [PDF]

T. S. Perrot-Sinal, A. M. Davis, K. A. Gregerson, J. P. Y. Kao, and M. M. McCarthy
Estradiol Enhances Excitatory Gammabutyric Acid-Mediated Calcium Signaling in Neonatal Hypothalamic Neurons
Endocrinology, June 1, 2001; 142(6): 2238 - 2243.
[Abstract] [Full Text] [PDF]

N. Chub and M. J. O'Donovan
Post-Episode Depression of GABAergic Transmission in Spinal Neurons of the Chick Embryo
J Neurophysiol, May 1, 2001; 85(5): 2166 - 2176.
[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]

P. A. Nunez-Abades, J. M. Pattillo, T. M. Hodgson, and W. E. Cameron
Role of Synaptic Inputs in Determining Input Resistance of Developing Brain Stem Motoneurons
J Neurophysiol, November 1, 2000; 84(5): 2317 - 2329.
[Abstract] [Full Text] [PDF]

A. Kulik, H. Nishimaru, and K. Ballanyi
Role of Bicarbonate and Chloride in GABA- and Glycine-Induced Depolarization and [Ca2+]i Rise in Fetal Rat Motoneurons In Situ
J. Neurosci., November 1, 2000; 20(21): 7905 - 7913.
[Abstract] [Full Text] [PDF]

R. A. DeFazio, S. Keros, M. W. Quick, and J. J. Hablitz
Potassium-Coupled Chloride Cotransport Controls Intracellular Chloride in Rat Neocortical Pyramidal Neurons
J. Neurosci., November 1, 2000; 20(21): 8069 - 8076.
[Abstract] [Full Text] [PDF]

K.-W. Sung, M. Kirby, M. P. McDonald, D. M. Lovinger, and E. Delpire
Abnormal GABAA Receptor-Mediated Currents in Dorsal Root Ganglion Neurons Isolated from Na-K-2Cl Cotransporter Null Mice
J. Neurosci., October 15, 2000; 20(20): 7531 - 7538.
[Abstract] [Full Text] [PDF]

N. Vardi, L.-L. Zhang, J. A. Payne, and P. Sterling
Evidence That Different Cation Chloride Cotransporters in Retinal Neurons Allow Opposite Responses to GABA
J. Neurosci., October 15, 2000; 20(20): 7657 - 7663.
[Abstract] [Full Text] [PDF]

T. Q. Vu, J. A. Payne, and D. R. Copenhagen
Localization and Developmental Expression Patterns of the Neuronal K-Cl Cotransporter (KCC2) in the Rat Retina
J. Neurosci., February 15, 2000; 20(4): 1414 - 1423.
[Abstract] [Full Text] [PDF]

R. Enz, B. J. Ross, and G. R. Cutting
Expression of the Voltage-Gated Chloride Channel ClC-2 in Rod Bipolar Cells of the Rat Retina
J. Neurosci., November 15, 1999; 19(22): 9841 - 9847.
[Abstract] [Full Text] [PDF]

J. Rohrbough and N. C. Spitzer
Ca2+-Permeable AMPA Receptors and Spontaneous Presynaptic Transmitter Release at Developing Excitatory Spinal Synapses
J. Neurosci., October 1, 1999; 19(19): 8528 - 8541.
[Abstract] [Full Text] [PDF]

M. F. Usiak and L. T. Landmesser
Neuromuscular Activity Blockade Induced by Muscimol and d-Tubocurarine Differentially Affects the Survival of Embryonic Chick Motoneurons
J. Neurosci., September 15, 1999; 19(18): 7925 - 7939.
[Abstract] [Full Text] [PDF]

D. F. Owens, X. Liu, and A. R. Kriegstein
Changing Properties of GABAA Receptor-Mediated Signaling During Early Neocortical Development
J Neurophysiol, August 1, 1999; 82(2): 570 - 583.
[Abstract] [Full Text] [PDF]

S. Bolea, E. Avignone, N. Berretta, J. V. Sanchez-Andres, and E. Cherubini
Glutamate Controls the Induction of GABA-Mediated Giant Depolarizing Potentials Through AMPA Receptors in Neonatal Rat Hippocampal Slices
J Neurophysiol, May 1, 1999; 81(5): 2095 - 2102.
[Abstract] [Full Text] [PDF]

J. R. Williams, J. W. Sharp, V. G. Kumari, M. Wilson, and J. A. Payne
The Neuron-specific K-Cl Cotransporter, KCC2. ANTIBODY DEVELOPMENT AND INITIAL CHARACTERIZATION OF THE PROTEIN
J. Biol. Chem., April 30, 1999; 274(18): 12656 - 12664.
[Abstract] [Full Text] [PDF]

Y. Kakazu, N. Akaike, S. Komiyama, and J. Nabekura
Regulation of Intracellular Chloride by Cotransporters in Developing Lateral Superior Olive Neurons
J. Neurosci., April 15, 1999; 19(8): 2843 - 2851.
[Abstract] [Full Text] [PDF]

L. D. Milner and L. T. Landmesser
Cholinergic and GABAergic Inputs Drive Patterned Spontaneous Motoneuron Activity before Target Contact
J. Neurosci., April 15, 1999; 19(8): 3007 - 3022.
[Abstract] [Full Text] [PDF]

M. Martin-Caraballo and J. J. Greer
Electrophysiological Properties of Rat Phrenic Motoneurons During Perinatal Development
J Neurophysiol, March 1, 1999; 81(3): 1365 - 1378.
[Abstract] [Full Text] [PDF]

M. J. O'Donovan
Review : Robustness and Self-regulation in the Production of Neural Activity by Developing Networks
Neuroscientist, January 1, 1999; 5(1): 41 - 47.
[Abstract] [PDF]

N. KUDO and H. NISHIMARU
Reorganization of Locomotor Activity during Development in the Prenatal Rat
Ann. N.Y. Acad. Sci., November 16, 1998; 860(1): 306 - 317.
[Abstract] [Full Text] [PDF]

A. B. Ribera and C. Nusslein-Volhard
Zebrafish Touch-Insensitive Mutants Reveal an Essential Role for the Developmental Regulation of Sodium Current
J. Neurosci., November 15, 1998; 18(22): 9181 - 9191.
[Abstract] [Full Text] [PDF]

G. S. Hollrigel, S. T. Ross, and I. Soltesz
Temporal Patterns and Depolarizing Actions of Spontaneous GABAA Receptor Activation in Granule Cells of the Early Postnatal Dentate Gyrus
J Neurophysiol, November 1, 1998; 80(5): 2340 - 2351.
[Abstract] [Full Text] [PDF]

S.-Y. Lin and M. Constantine-Paton
Suppression of Sprouting: An Early Function of NMDA Receptors in the Absence of AMPA/Kainate Receptor Activity
J. Neurosci., May 15, 1998; 18(10): 3725 - 3737.
[Abstract] [Full Text] [PDF]

K. F. Fischer, P. D. Lukasiewicz, and R. O.�L. Wong
Age-Dependent and Cell Class-Specific Modulation of Retinal Ganglion Cell Bursting Activity by GABA
J. Neurosci., May 15, 1998; 18(10): 3767 - 3778.
[Abstract] [Full Text] [PDF]

X.-B. Gao, G. Chen, and A. N. van den Pol
GABA-Dependent Firing of Glutamate-Evoked Action Potentials at AMPA/Kainate Receptors in Developing Hypothalamic Neurons
J Neurophysiol, February 1, 1998; 79(2): 716 - 726.
[Abstract] [Full Text] [PDF]

N. Chub and M. J. O'Donovan
Blockade and Recovery of Spontaneous Rhythmic Activity after Application of Neurotransmitter Antagonists to Spinal Networks of the Chick Embryo
J. Neurosci., January 1, 1998; 18(1): 294 - 306.
[Abstract] [Full Text] [PDF]

G. S. Hollrigel and I. Soltesz
Slow Kinetics of Miniature IPSCs during Early Postnatal Development in Granule Cells of the Dentate Gyrus
J. Neurosci., July 1, 1997; 17(13): 5119 - 5128.
[Abstract] [Full Text] [PDF]

D. F. Owens, L. H. Boyce, M. B.�E