 |
Previous Article | Next Article 
The Journal of Neuroscience, April 1, 1999, 19(7):2693-2705
Choline and Selective Antagonists Identify Two Subtypes of
Nicotinic Acetylcholine Receptors that Modulate GABA Release from CA1
Interneurons in Rat Hippocampal Slices
Manickavasagom
Alkondon1,
Edna F. R.
Pereira1,
Howard
M.
Eisenberg2, and
Edson X.
Albuquerque1, 3
1 Department of Pharmacology and Experimental
Therapeutics, 2 Department of Neurosurgery, University of
Maryland School of Medicine, Baltimore, Maryland 21201, and
3 Departamento de Farmacologia Básica e
Clínica, ICB, CCS, Universidade Federal do Rio de Janeiro, Rio de
Janeiro, RJ 21944, Brazil
Neuronal nicotinic receptors (nAChR) are known to control
transmitter release in the CNS. Thus, this study was aimed at exploring the diversity and localization of nAChRs present in CA1 interneurons in
rat hippocampal slices. The use of a U-tube as the agonist delivery
system was critical for the reliable detection of nicotinic responses
induced by brief exposure of the neurons to ACh or to the 7
nAChR-selective agonist choline. The present study demonstrated that
CA1 interneurons, in addition to expressing functional 7 nAChRs,
also express functional 4 2-like nAChRs and that activation of
both receptors facilitates an action potential-dependent release of
GABA. Depending on the experimental condition, one of the following nicotinic responses was recorded from the interneurons by means of the
patch-clamp technique: a nicotinic whole-cell current, depolarization
accompanied by action potentials, or GABA-mediated postsynaptic
currents (PSCs). Responses mediated by 7 nAChRs were short-lasting,
whereas those mediated by 4 2 nAChRs were long-lasting. Thus,
phasic or tonic inhibition of CA1 interneurons may be achieved by
selective activation of 7 or 4 2 nAChRs, respectively. It can
also be suggested that synaptic levels of choline generated by
hydrolysis of ACh in vivo may be sufficient to control
the activity of the 7 nAChRs. The finding that methyllycaconitine and dihydro- -erythroidine (antagonists of 7 and 4 2 nAChRs, respectively) increased the frequency and amplitude of GABAergic PSCs
suggests that there is an intrinsic cholinergic activity that sustains
a basal level of nAChR activity in these interneurons.
Key words:
hippocampus; GABA; choline; methyllycaconitine; -bungarotoxin; dihydro- -erythroidine
Copyright © 1999 Society for Neuroscience 0270-6474/99/1972693-13$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
C. C. Fernandes, A. Pinto-Duarte, J. A. Ribeiro, and A. M. Sebastiao
Postsynaptic Action of Brain-Derived Neurotrophic Factor Attenuates {alpha}7 Nicotinic Acetylcholine Receptor-Mediated Responses in Hippocampal Interneurons
J. Neurosci.,
May 21, 2008;
28(21):
5611 - 5618.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Lendvai and E. S. Vizi
Nonsynaptic Chemical Transmission Through Nicotinic Acetylcholine Receptors
Physiol Rev,
April 1, 2008;
88(2):
333 - 349.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Davis, J. W. Kenney, and T. J. Gould
Hippocampal {alpha}4{beta}2 Nicotinic Acetylcholine Receptor Involvement in the Enhancing Effect of Acute Nicotine on Contextual Fear Conditioning
J. Neurosci.,
October 3, 2007;
27(40):
10870 - 10877.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Liu, Y. Otsu, C. Vasuta, H. Nawa, and T. H. Murphy
Action-Potential-Independent GABAergic Tone Mediated by Nicotinic Stimulation of Immature Striatal Miniature Synaptic Transmission
J Neurophysiol,
August 1, 2007;
98(2):
581 - 593.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. A. Dmitrieva, C. E. Strang, and K. T. Keyser
Expression of Alpha 7 Nicotinic Acetylcholine Receptors by Bipolar, Amacrine, and Ganglion Cells of the Rabbit Retina
J. Histochem. Cytochem.,
May 1, 2007;
55(5):
461 - 476.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Zhang and D. K. Berg
Reversible inhibition of GABAA receptors by {alpha}7-containing nicotinic receptors on the vertebrate postsynaptic neurons
J. Physiol.,
March 15, 2007;
579(3):
753 - 763.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Liu, R. A. Neff, and D. K. Berg
Sequential Interplay of Nicotinic and GABAergic Signaling Guides Neuronal Development
Science,
December 8, 2006;
314(5805):
1610 - 1613.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Xu, Y. Zhu, and S. F. Heinemann
Identification of sequence motifs that target neuronal nicotinic receptors to dendrites and axons.
J. Neurosci.,
September 20, 2006;
26(38):
9780 - 9793.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. H. Selina Mok and J. N. C. Kew
Excitation of rat hippocampal interneurons via modulation of endogenous agonist activity at the {alpha}7 nicotinic ACh receptor
J. Physiol.,
August 1, 2006;
574(3):
699 - 710.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Alkondon and E. X. Albuquerque
Subtype-Specific Inhibition of Nicotinic Acetylcholine Receptors by Choline: A Regulatory Pathway
J. Pharmacol. Exp. Ther.,
July 1, 2006;
318(1):
268 - 275.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Bandyopadhyay, B. Sutor, and J. J. Hablitz
Endogenous Acetylcholine Enhances Synchronized Interneuron Activity in Rat Neocortex
J Neurophysiol,
March 1, 2006;
95(3):
1908 - 1916.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R.-K. Cheng, W. H. Meck, and C. L. Williams
{alpha}7 Nicotinic acetylcholine receptors and temporal memory: Synergistic effects of combining prenatal choline and nicotine on reinforcement-induced resetting of an interval clock
Learn. Mem.,
March 1, 2006;
13(2):
127 - 134.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Zhu, R. R. Stewart, J. M. McIntosh, and F. F. Weight
Activation of Nicotinic Acetylcholine Receptors Increases the Frequency of Spontaneous GABAergic IPSCs in Rat Basolateral Amygdala Neurons
J Neurophysiol,
November 1, 2005;
94(5):
3081 - 3091.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. E. Strang, M. E. Andison, F. R. Amthor, and K. T. Keyser
Rabbit retinal ganglion cells express functional {alpha}7 nicotinic acetylcholine receptors
Am J Physiol Cell Physiol,
September 1, 2005;
289(3):
C644 - C655.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. L. Obaid, M. E. Nelson, J. Lindstrom, and B. M. Salzberg
Optical studies of nicotinic acetylcholine receptor subtypes in the guinea-pig enteric nervous system
J. Exp. Biol.,
August 1, 2005;
208(15):
2981 - 3001.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. S. Hurst, M. Hajos, M. Raggenbass, T. M. Wall, N. R. Higdon, J. A. Lawson, K. L. Rutherford-Root, M. B. Berkenpas, W. E. Hoffmann, D. W. Piotrowski, et al.
A Novel Positive Allosteric Modulator of the {alpha}7 Neuronal Nicotinic Acetylcholine Receptor: In Vitro and In Vivo Characterization
J. Neurosci.,
April 27, 2005;
25(17):
4396 - 4405.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. F. M. Braga, E. F. R. Pereira, A. Mike, and E. X. Albuquerque
Pb2+ via Protein Kinase C Inhibits Nicotinic Cholinergic Modulation of Synaptic Transmission in the Hippocampus
J. Pharmacol. Exp. Ther.,
November 1, 2004;
311(2):
700 - 710.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Maggi, E. Sola, F. Minneci, C. Le Magueresse, J. P. Changeux, and E. Cherubini
Persistent decrease in synaptic efficacy induced by nicotine at Schaffer collateral-CA1 synapses in the immature rat hippocampus
J. Physiol.,
September 15, 2004;
559(3):
863 - 874.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. L. Hanganu and H. J. Luhmann
Functional Nicotinic Acetylcholine Receptors on Subplate Neurons in Neonatal Rat Somatosensory Cortex
J Neurophysiol,
July 1, 2004;
92(1):
189 - 198.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X. D. Li and J. J. Buccafusco
Role of {alpha}7 Nicotinic Acetylcholine Receptors in the Pressor Response to Intracerebroventricular Injection of Choline: Blockade by Amyloid Peptide A{beta}1-42
J. Pharmacol. Exp. Ther.,
June 1, 2004;
309(3):
1206 - 1212.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Alkondon, E. F. R. Pereira, P. Yu, E. Z. Arruda, L. E. F. Almeida, P. Guidetti, W. P. Fawcett, M. T. Sapko, W. R. Randall, R. Schwarcz, et al.
Targeted Deletion of the Kynurenine Aminotransferase II Gene Reveals a Critical Role of Endogenous Kynurenic Acid in the Regulation of Synaptic Transmission via {alpha}7 Nicotinic Receptors in the Hippocampus
J. Neurosci.,
May 12, 2004;
24(19):
4635 - 4648.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Alkondon, E. F.R. Pereira, and E. X. Albuquerque
NMDA and AMPA Receptors Contribute to the Nicotinic Cholinergic Excitation of CA1 Interneurons in the Rat Hippocampus
J Neurophysiol,
September 1, 2003;
90(3):
1613 - 1625.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. A. Ferchmin, D. Perez, V. A. Eterovic, and J. de Vellis
Nicotinic Receptors Differentially Regulate N-Methyl-D-aspartate Damage in Acute Hippocampal Slices
J. Pharmacol. Exp. Ther.,
June 1, 2003;
305(3):
1071 - 1078.
[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]
|
 |
|

|
 |

|
 |
 
M. D. Santos, E. F. R. Pereira, Y. Aracava, N. G. Castro, W. P. Fawcett, W. R. Randall, and E. X. Albuquerque
Low Concentrations of Pyridostigmine Prevent Soman-Induced Inhibition of GABAergic Transmission in the Central Nervous System: Involvement of Muscarinic Receptors
J. Pharmacol. Exp. Ther.,
January 1, 2003;
304(1):
254 - 265.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Christophe, A. Roebuck, J. F. Staiger, D. J. Lavery, S. Charpak, and E. Audinat
Two Types of Nicotinic Receptors Mediate an Excitation of Neocortical Layer I Interneurons
J Neurophysiol,
September 1, 2002;
88(3):
1318 - 1327.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. D. Santos, M. Alkondon, E. F. R. Pereira, Y. Aracava, H. M. Eisenberg, A. Maelicke, and E. X. Albuquerque
The Nicotinic Allosteric Potentiating Ligand Galantamine Facilitates Synaptic Transmission in the Mammalian Central Nervous System
Mol. Pharmacol.,
May 1, 2002;
61(5):
1222 - 1234.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. V. Buhler and T. V. Dunwiddie
alpha 7 Nicotinic Acetylcholine Receptors on GABAergic Interneurons Evoke Dendritic and Somatic Inhibition of Hippocampal Neurons
J Neurophysiol,
January 1, 2002;
87(1):
548 - 557.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. I. Hatton and Q. Z. Yang
Synaptic Potentials Mediated by alpha 7 Nicotinic Acetylcholine Receptors in Supraoptic Nucleus
J. Neurosci.,
January 1, 2002;
22(1):
29 - 37.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Alkondon and E. X. Albuquerque
Nicotinic Acetylcholine Receptor alpha 7 and alpha 4beta 2 Subtypes Differentially Control GABAergic Input to CA1 Neurons in Rat Hippocampus
J Neurophysiol,
December 1, 2001;
86(6):
3043 - 3055.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Wang, E. F. R. Pereira, A. D. J. Maus, N. S. Ostlie, D. Navaneetham, S. Lei, E. X. Albuquerque, and B. M. Conti-Fine
Human Bronchial Epithelial and Endothelial Cells Express alpha 7 Nicotinic Acetylcholine Receptors
Mol. Pharmacol.,
December 1, 2001;
60(6):
1201 - 1209.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Hilmas, E. F. R. Pereira, M. Alkondon, A. Rassoulpour, R. Schwarcz, and E. X. Albuquerque
The Brain Metabolite Kynurenic Acid Inhibits {alpha}7 Nicotinic Receptor Activity and Increases Non-{alpha}7 Nicotinic Receptor Expression: Physiopathological Implications
J. Neurosci.,
October 1, 2001;
21(19):
7463 - 7473.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Liu, B. Ford, M. A. Mann, and G. D. Fischbach
Neuregulins Increase {alpha}7 Nicotinic Acetylcholine Receptors and Enhance Excitatory Synaptic Transmission in GABAergic Interneurons of the Hippocampus
J. Neurosci.,
August 1, 2001;
21(15):
5660 - 5669.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Barazangi and L. W. Role
Nicotine-Induced Enhancement of Glutamatergic and GABAergic Synaptic Transmission in the Mouse Amygdala
J Neurophysiol,
July 1, 2001;
86(1):
463 - 474.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Mori, X. Zhao, Y. Zuo, G. L. Aistrup, K. Nishikawa, W. Marszalec, J. Z. Yeh, and T. Narahashi
Modulation of Neuronal Nicotinic Acetylcholine Receptors by Halothane in Rat Cortical Neurons
Mol. Pharmacol.,
April 1, 2001;
59(4):
732 - 743.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
K. M. Coates, L. E. Mather, R. Johnson, and P. Flood
Thiopental is a Competitive Inhibitor at the Human {{alpha}}7 Nicotinic Acetylcholine Receptor
Anesth. Analg.,
April 1, 2001;
92(4):
930 - 933.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Q.-s. Liu, H. Kawai, and D. K. Berg
beta -Amyloid peptide blocks the response of alpha 7-containing nicotinic receptors on hippocampal neurons
PNAS,
March 22, 2001;
(2001)
81553598.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
A. Köfalvi, B. Sperlágh, T. Zelles, and E. S. Vizi
Long-Lasting Facilitation of 4-Amino-n-[2,3-3H]butyric Acid ([3H]GABA) Release from Rat Hippocampal Slices by Nicotinic Receptor Activation
J. Pharmacol. Exp. Ther.,
November 1, 2000;
295(2):
453 - 462.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
T. P. George, C. D. Verrico, M. R. Picciotto, and R. H. Roth
Nicotinic Modulation of Mesoprefrontal Dopamine Neurons: Pharmacologic and Neuroanatomic Characterization
J. Pharmacol. Exp. Ther.,
October 1, 2000;
295(1):
58 - 66.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
S. Kaiser and S. Wonnacott
alpha -Bungarotoxin-Sensitive Nicotinic Receptors Indirectly Modulate [3H]Dopamine Release in Rat Striatal Slices via Glutamate Release
Mol. Pharmacol.,
August 1, 2000;
58(2):
312 - 318.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
T. Narahashi
Neuroreceptors and Ion Channels as the Basis for Drug Action: Past, Present, and Future
J. Pharmacol. Exp. Ther.,
July 1, 2000;
294(1):
1 - 26.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
D. Ji and J. A. Dani
Inhibition and Disinhibition of Pyramidal Neurons by Activation of Nicotinic Receptors on Hippocampal Interneurons
J Neurophysiol,
May 1, 2000;
83(5):
2682 - 2690.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Stitzel, M. Jimenez, M. J. Marks, T. Tritto, and A. C. Collins
Potential Role of the alpha 4 and alpha 6 Nicotinic Receptor Subunits in Regulating Nicotine-Induced Seizures
J. Pharmacol. Exp. Ther.,
April 1, 2000;
293(1):
67 - 74.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
M. Alkondon, E. F. R. Pereira, H. M. Eisenberg, and E. X. Albuquerque
Nicotinic Receptor Activation in Human Cerebral Cortical Interneurons: a Mechanism for Inhibition and Disinhibition of Neuronal Networks
J. Neurosci.,
January 1, 2000;
20(1):
66 - 75.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Zhu and V. A. Chiappinelli
Nicotine Modulates Evoked GABAergic Transmission in the Brain
J Neurophysiol,
December 1, 1999;
82(6):
3041 - 3045.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. E. Castillo, A. Carleton, J.-D. Vincent, and P.-M. Lledo
Multiple and Opposing Roles of Cholinergic Transmission in the Main Olfactory Bulb
J. Neurosci.,
November 1, 1999;
19(21):
9180 - 9191.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Zhou, A. G. Engel, and A. Auerbach
Serum choline activates mutant acetylcholine receptors that cause slow channel congenital myasthenic syndromes
PNAS,
August 31, 1999;
96(18):
10466 - 10471.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Q.-s. Liu, H. Kawai, and D. K. Berg
beta -Amyloid peptide blocks the response of alpha 7-containing nicotinic receptors on hippocampal neurons
PNAS,
April 10, 2001;
98(8):
4734 - 4739.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|