 |
Previous Article | Next Article 
The Journal of Neuroscience, October 15, 1998, 18(20):8485-8495
Nicotine Selectively Enhances NMDA Receptor-Mediated Synaptic
Transmission during Postnatal Development in Sensory Neocortex
V. Bess
Aramakis and
Raju
Metherate
Department of Psychobiology, University of California, Irvine,
California 92697-4550
The neurotransmitters acetylcholine (ACh) and glutamate have been
separately implicated in synaptic plasticity during development of
sensory neocortex. Here we show that these neurotransmitters can, in
fact, act synergistically via their actions at nicotinic ACh receptors
(nAChRs) and NMDA receptors, respectively. To determine how
activation of nAChRs modifies glutamatergic EPSPs, we made whole-cell recordings from visualized pyramidal neurons in slices of
rat auditory cortex. Pulsed (pressure) ejection of nicotine onto apical
dendrites selectively enhanced EPSPs mediated by NMDA receptors without
affecting AMPA/kainate (AMPA/KA) receptor-mediated EPSPs. The
enhancement occurred during a transient, postnatal period of heightened
cholinergic function [neurons tested on postnatal day 8-16
(P8-16)], and not in the mature cortex (>P19). Three related
findings indicated the mechanism of action: (1) The specific 7 nAChR
antagonist methyllycaconitine citrate (MLA) blocked the effect of
nicotine; (2) pulsed nicotine did not enhance postsynaptic depolarizations induced by iontophoretically applied NMDA; and (3) bath
exposure to nicotine for several minutes produced apparent nAChR
desensitization and precluded enhancement of EPSPs by pulsed nicotine.
Together, the data suggest that nicotine acts at rapidly desensitizing,
presynaptic 7 nAChRs to increase glutamate release onto postsynaptic
NMDA receptors. The synergistic actions mediated by 7 nAChRs and
NMDA receptors may contribute to experience-dependent synaptic
plasticity in sensory neocortex during early postnatal life.
Key words:
acetylcholine; acetylcholinesterase; auditory
cortex; development; enhancement; EPSP; glutamate; nicotine; NMDA
Copyright © 1998 Society for Neuroscience 0270-6474/98/18208485-11$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
S. Yamamoto, J. Yamada, S. Ueno, H. Kubota, T. Furukawa, S. Yamamoto, and A. Fukuda
Insertion of {alpha}7 Nicotinic Receptors at Neocortical Layer V GABAergic Synapses Is Induced by a Benzodiazepine, Midazolam
Cereb Cortex,
March 1, 2007;
17(3):
653 - 660.
[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]
|
 |
|

|
 |

|
 |
 
R. B. Levy, A. D. Reyes, and C. Aoki
Nicotinic and Muscarinic Reduction of Unitary Excitatory Postsynaptic Potentials in Sensory Cortex; Dual Intracellular Recording In Vitro
J Neurophysiol,
April 1, 2006;
95(4):
2155 - 2166.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. J. Gould and M. C. Lewis
Coantagonism of glutamate receptors and nicotinic acetylcholinergic receptors disrupts fear conditioning and latent inhibition of fear conditioning
Learn. Mem.,
July 1, 2005;
12(4):
389 - 398.
[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]
|
 |
|

|
 |

|
 |
 
M. Alkondon and E. X. Albuquerque
Nicotinic Receptor Subtypes in Rat Hippocampal Slices Are Differentially Sensitive to Desensitization and Early in Vivo Functional Up-Regulation by Nicotine and to Block by Bupropion
J. Pharmacol. Exp. Ther.,
May 1, 2005;
313(2):
740 - 750.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. W. Jones and S. Wonnacott
Precise Localization of {alpha}7 Nicotinic Acetylcholine Receptors on Glutamatergic Axon Terminals in the Rat Ventral Tegmental Area
J. Neurosci.,
December 15, 2004;
24(50):
11244 - 11252.
[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]
|
 |
|

|
 |

|
 |
 
F. M. LESLIE, S. E. LOUGHLIN, R. WANG, L. PEREZ, S. LOTFIPOUR, and J. D. BELLUZZIA
Adolescent Development of Forebrain Stimulant Responsiveness: Insights from Animal Studies
Ann. N.Y. Acad. Sci.,
June 1, 2004;
1021(1):
148 - 159.
[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]
|
 |
|

|
 |

|
 |
 
M. ATZORI, P. KANOLD, J. C. PINEDA, and J. FLORES-HERNANDEZ
Dopamine-Acetylcholine Interactions in the Modulation of Glutamate Release
Ann. N.Y. Acad. Sci.,
November 1, 2003;
1003(1):
346 - 348.
[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. Dobelis, S. Hutton, Y. Lu, and A. C. Collins
GABAergic Systems Modulate Nicotinic Receptor-Mediated Seizures in Mice
J. Pharmacol. Exp. Ther.,
September 1, 2003;
306(3):
1159 - 1166.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. I. O. Myme, K. Sugino, G. G. Turrigiano, and S. B. Nelson
The NMDA-to-AMPA Ratio at Synapses Onto Layer 2/3 Pyramidal Neurons Is Conserved Across Prefrontal and Visual Cortices
J Neurophysiol,
August 1, 2003;
90(2):
771 - 779.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. J. Frazier, B. W. Strowbridge, and R. L. Papke
Nicotinic Receptors on Local Circuit Neurons in Dentate Gyrus: A Potential Role in Regulation of Granule Cell Excitability
J Neurophysiol,
June 1, 2003;
89(6):
3018 - 3028.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. L. King, M. J. Marks, S. R. Grady, B. J. Caldarone, A. O. Koren, A. G. Mukhin, A. C. Collins, and M. R. Picciotto
Conditional Expression in Corticothalamic Efferents Reveals a Developmental Role for Nicotinic Acetylcholine Receptors in Modulation of Passive Avoidance Behavior
J. Neurosci.,
May 1, 2003;
23(9):
3837 - 3843.
[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]
|
 |
|

|
 |

|
 |
 
Y.-H. Jo and L. W. Role
Cholinergic Modulation of Purinergic and GABAergic Co-Transmission at In Vitro Hypothalamic Synapses
J Neurophysiol,
November 1, 2002;
88(5):
2501 - 2508.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. B. Levy and C. Aoki
alpha 7 Nicotinic Acetylcholine Receptors Occur at Postsynaptic Densities of AMPA Receptor-Positive and -Negative Excitatory Synapses in Rat Sensory Cortex
J. Neurosci.,
June 15, 2002;
22(12):
5001 - 5015.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Alkondon and E. X. Albuquerque
A Non-alpha 7 Nicotinic Acetylcholine Receptor Modulates Excitatory Input to Hippocampal CA1 Interneurons
J Neurophysiol,
March 1, 2002;
87(3):
1651 - 1654.
[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]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|
|