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Journal of Neuroscience, Vol 15, 4395-4407, Copyright © 1995 by Society for Neuroscience
Activation of a nonselective cationic conductance by metabotropic glutamatergic and muscarinic agonists in CA3 pyramidal neurons of the rat hippocampus
NC Guerineau, JL Bossu, BH Gahwiler and U Gerber
Brain Research Institute, University of Zurich, Switzerland.
We have characterized a cationic membrane conductance activated by
metabotropic glutamatergic and muscarinic cholinergic agonists in CA3
neurons in hippocampal slice cultures using the patch-clamp technique. When
the potassium concentration in the superfusing fluid was raised above 5 mM,
a biphasic current was observed in cells held at -60 mV in response to
stimulation of postsynaptic metabotropic glutamate receptors (mGluRs) with
1S,3R-ACPD (50 microM) or muscarinic receptors with methacholine (MCh, 5
microM). The initial inward component was due to an increase in a cationic
membrane conductance as determined by its reversal potential and its
sensitivity to changes in extracellular K+ or Na+. The conductance
underlying this current displayed no apparent voltage sensitivity over the
range -120 to -50 mV. The response was reduced by extracellular application
of Ba2+, Cd2+, Mg2+, or TEA, whereas extracellular Cs+ or loading cells
with BAPTA or Cs+ did not affect the current. The effects of 1S,3R-ACPD
were reversibly inhibited by bath-applied MCPG, an antagonist at mGluRs.
Experiments with atropine and pirenzepine indicated that non-M1 muscarinic
receptors mediated the MCh-induced current. A decrease in a resting leak
potassium conductance (IK,leak) was responsible for the late component of
the 1S,3R-ACPD- and MCh-induced response, seen as an outward current in the
bathing solution with high K+ concentration. Loading cells with GDP beta S,
GTP gamma S, or GTP did not alter the cationic current, while, in the same
cells, the reduction in IKleak was abolished or irreversibly activated.
Single-channel recordings of cationic channel activity in the cell-attached
configuration provided evidence for the requirement of second messengers in
coupling these receptors to the cationic channels. The data indicate that
in addition to the previously described reduction of IK,leak, IM, and IAHP,
both 1S,3R-ACPD and MCh activate a nonselective cationic conductance that
is clearly revealed upon elevating external K+ concentration. This current
is mediated by activation of metabotropic receptors, although no evidence
could be obtained to show an involvement of G-proteins.
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|
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|
|
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|
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79(4):
2003 - 2012.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Martin, Z. Nie, and G. R. Siggins
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78(6):
3028 - 3038.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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78(5):
2287 - 2295.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
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17(19):
7503 - 7522.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
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17(14):
5366 - 5379.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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J Neurophysiol,
June 1, 1997;
77(6):
3021 - 3034.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Klink and A. Alonso
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J Neurophysiol,
April 1, 1997;
77(4):
1829 - 1843.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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77(1):
221 - 228.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
X.-W. Dong, D. Morin, and J. L. Feldman
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J. Neurosci.,
August 15, 1996;
16(16):
4971 - 4982.
[Abstract]
[Full Text]
[PDF]
|
|
|
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K. Ito and D. Dulon
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Am J Physiol Cell Physiol,
May 1, 2002;
282(5):
C1121 - C1135.
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