 |
 Previous Article | Next Article 
The Journal of Neuroscience, September 15, 1998, 18(18):7075-7083
Nicotinic Stimulation Produces Multiple Forms of Increased
Glutamatergic Synaptic Transmission
Kristofer A.
Radcliffe and
John A.
Dani
Division of Neuroscience, Baylor College of Medicine, Houston,
Texas 77030-3498
Synaptic modulation and long-term synaptic changes are thought to
be the cellular correlates for learning and memory (; ; ). The hippocampus is a
center for learning and memory that receives abundant cholinergic
innervation and has a high density of nicotinic acetylcholine receptors
(nAChRs) (; ). We report that strong, brief
stimulation of nAChRs enhanced hippocampal glutamatergic synaptic
transmission on two independent time scales and altered the
relationship between consecutively evoked synaptic currents. The
nicotinic synaptic enhancement required extracellular calcium and was
produced by the activation of presynaptic  7-containing nAChRs.
Although one form of glutamatergic enhancement lasted only for seconds,
another form lasted for minutes after the nicotinic stimulation had
ceased and the nicotinic agonist had been washed away. The synaptic
enhancement lasting minutes suggests that nAChR activity can initiate
calcium-dependent mechanisms that are known to induce glutamatergic
synaptic plasticity. The results with evoked synaptic currents showed
that nAChR activity can alter the relationship between the incoming
presynaptic activity and outgoing postsynaptic signaling along
glutamatergic fibers. Thus, the same information arriving along the
same glutamatergic afferents will be processed differently when
properly timed nicotinic activity converges onto the glutamatergic
presynaptic terminals. Influencing information processing at
glutamatergic synapses may be one way in which nicotinic cholinergic
activity influences cognitive processes. Disruption of these nicotinic
cholinergic mechanisms may contribute to the deficits associated with
the degeneration of cholinergic functions during Alzheimer's
disease.
Key words:
glutamate synaptic transmission; nicotinic acetylcholine
receptors; hippocampal cultures; synaptic modulation; learning; memory
Copyright © 1998 Society for Neuroscience 0270-6474/98/18187075-09$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]
|
|
|
|
|
|
|
V. Parikh, K. Man, M. W. Decker, and M. Sarter
Glutamatergic Contributions to Nicotinic Acetylcholine Receptor Agonist-Evoked Cholinergic Transients in the Prefrontal Cortex
J. Neurosci.,
April 2, 2008;
28(14):
3769 - 3780.
[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. H. Chin, L. Ma, D. MacTavish, and J. H. Jhamandas
Amyloid {beta} Protein Modulates Glutamate-Mediated Neurotransmission in the Rat Basal Forebrain: Involvement of Presynaptic Neuronal Nicotinic Acetylcholine and Metabotropic Glutamate Receptors
J. Neurosci.,
August 29, 2007;
27(35):
9262 - 9269.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. G. Farias, A. S. Valles, M. Colombres, J. A. Godoy, E. M. Toledo, R. J. Lukas, F. J. Barrantes, and N. C. Inestrosa
Wnt-7a Induces Presynaptic Colocalization of {alpha}7-Nicotinic Acetylcholine Receptors and Adenomatous Polyposis Coli in Hippocampal Neurons
J. Neurosci.,
May 16, 2007;
27(20):
5313 - 5325.
[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]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
H. Geerts and G. T. Grossberg
Pharmacology of Acetylcholinesterase Inhibitors and N-methyl-D-aspartate Receptors for Combination Therapy in the Treatment of Alzheimer's Disease
J. Clin. Pharmacol.,
July 1, 2006;
46(suppl_1):
8S - 16S.
[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]
|
|
|
|
|
|
|
S. Ge and J. A. Dani
Nicotinic Acetylcholine Receptors at Glutamate Synapses Facilitate Long-Term Depression or Potentiation
J. Neurosci.,
June 29, 2005;
25(26):
6084 - 6091.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. J. Turner
Nicotine Enhancement of Dopamine Release by a Calcium-Dependent Increase in the Size of the Readily Releasable Pool of Synaptic Vesicles
J. Neurosci.,
December 15, 2004;
24(50):
11328 - 11336.
[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]
|
|
|
|
|
|
|
R. Lape and J. A. Dani
Complex Response to Afferent Excitatory Bursts by Nucleus Accumbens Medium Spiny Projection Neurons
J Neurophysiol,
September 1, 2004;
92(3):
1276 - 1284.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. G. Severance, H. Zhang, Y. Cruz, S. Pakhlevaniants, S. H. Hadley, J. Amin, L. Wecker, C. Reed, and J. Cuevas
The {alpha}7 Nicotinic Acetylcholine Receptor Subunit Exists in Two Isoforms that Contribute to Functional Ligand-Gated Ion Channels
Mol. Pharmacol.,
September 1, 2004;
66(3):
420 - 429.
[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]
|
|
|
|
|
|
|
R. Metherate
Nicotinic Acetylcholine Receptors in Sensory Cortex
Learn. Mem.,
January 1, 2004;
11(1):
50 - 59.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. I. Pidoplichko, J. Noguchi, O. O. Areola, Y. Liang, J. Peterson, T. Zhang, and J. A. Dani
Nicotinic Cholinergic Synaptic Mechanisms in the Ventral Tegmental Area Contribute to Nicotine Addiction
Learn. Mem.,
January 1, 2004;
11(1):
60 - 69.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. A. Dajas-Bailador, K. Heimala, and S. Wonnacott
The Allosteric Potentiation of Nicotinic Acetylcholine Receptors by Galantamine Is Transduced into Cellular Responses in Neurons: Ca2+ Signals and Neurotransmitter Release.
Mol. Pharmacol.,
November 1, 2003;
64(5):
1217 - 1226.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. V. Uteshev, E. M. Meyer, and R. L. Papke
Regulation of Neuronal Function by Choline and 4OH-GTS-21 Through alpha 7 Nicotinic Receptors
J Neurophysiol,
April 1, 2003;
89(4):
1797 - 1806.
[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. Zhang and R. A. Warren
Muscarinic and Nicotinic Presynaptic Modulation of EPSCs in the Nucleus Accumbens During Postnatal Development
J Neurophysiol,
December 1, 2002;
88(6):
3315 - 3330.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Kawai, W. Zago, and D. K. Berg
Nicotinic alpha 7 Receptor Clusters on Hippocampal GABAergic Neurons: Regulation by Synaptic Activity and Neurotrophins
J. Neurosci.,
September 15, 2002;
22(18):
7903 - 7912.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. S. Broide, R. Salas, D. Ji, R. Paylor, J. W. Patrick, J. A. Dani, and M. De Biasi
Increased Sensitivity to Nicotine-Induced Seizures in Mice Expressing the L250T alpha 7 Nicotinic Acetylcholine Receptor Mutation
Mol. Pharmacol.,
March 1, 2002;
61(3):
695 - 705.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Fabian-Fine, P. Skehel, M. L. Errington, H. A. Davies, E. Sher, M. G. Stewart, and A. Fine
Ultrastructural Distribution of the {alpha}7 Nicotinic Acetylcholine Receptor Subunit in Rat Hippocampus
J. Neurosci.,
October 15, 2001;
21(20):
7993 - 8003.
[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]
|
|
|
|
|
|
|
R. Girod and L. W. Role
Long-Lasting Enhancement of Glutamatergic Synaptic Transmission by Acetylcholine Contrasts with Response Adaptation after Exposure to Low-Level Nicotine
J. Neurosci.,
July 15, 2001;
21(14):
5182 - 5190.
[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]
|
|
|
|
|
|
|
J. P. Hodgkiss and J. S. Kelly
Effect of FK960, a Putative Cognitive Enhancer, on Synaptic Transmission in CA1 Neurons of Rat Hippocampus
J. Pharmacol. Exp. Ther.,
April 12, 2001;
297(2):
620 - 628.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
V. B. Aramakis, C. Y. Hsieh, F. M. Leslie, and R. Metherate
A Critical Period for Nicotine-Induced Disruption of Synaptic Development in Rat Auditory Cortex
J. Neurosci.,
August 15, 2000;
20(16):
6106 - 6116.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
K. T. Dineley and J. W. Patrick
Amino Acid Determinants of alpha 7 Nicotinic Acetylcholine Receptor Surface Expression
J. Biol. Chem.,
April 28, 2000;
275(18):
13974 - 13985.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
Q.-S. Liu and D. K. Berg
Extracellular Calcium Regulates Responses of Both alpha 3- and alpha 7-Containing Nicotinic Receptors on Chick Ciliary Ganglion Neurons
J Neurophysiol,
September 1, 1999;
82(3):
1124 - 1132.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. L. Obaid, T. Koyano, J. Lindstrom, T. Sakai, and B. M. Salzberg
Spatiotemporal Patterns of Activity in an Intact Mammalian Network with Single-Cell Resolution: Optical Studies of Nicotinic Activity in an Enteric Plexus
J. Neurosci.,
April 15, 1999;
19(8):
3073 - 3093.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
