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Volume 16, Number 10,
Issue of May 15, 1996
pp. 3189-3198
Copyright ©1996 Society for Neuroscience
A Macromolecular Synthesis-Dependent Late Phase of Long-Term
Potentiation Requiring cAMP in the Medial Perforant Pathway of Rat
Hippocampal Slices
Received Nov. 27, 1995; revised Feb. 23, 1996; accepted Feb. 26, 1996.
Peter V. Nguyen and
Eric R. Kandel
The Howard Hughes Medical Institute and Center for Neurobiology and
Behavior, College of Physicians and Surgeons of Columbia University,
New York, New York 10032
Memory storage consists of a short-term phase that is independent
of new protein synthesis and a long-term phase that requires the
synthesis of new proteins and RNA. A cellular representation of these
two phases has been demonstrated recently for long-term potentiation
(LTP) in both the Schaffer collateral and the mossy fibers of the
hippocampus, a structure widely thought to contribute to memory
consolidation. By contrast, much less information is available about
the medial perforant pathway (MPP), one of the major inputs to the
hippocampus. We found that both a short-lasting and a long-lasting
potentiation (L-LTP) can be induced in the MPP of rat hippocampal
slices by applying repeated tetanization in reduced levels of
magnesium. This potentiation was dependent on the activation of NMDA
receptors. The early, transient phase of LTP in the MPP did not require
either protein or RNA synthesis, and it was independent of protein
kinase A activation. By contrast, L-LTP required the synthesis of
proteins and RNA, and was selectively blocked by inhibitors of
cAMP-dependent protein kinase (PKA). Forskolin, an adenylate cyclase
activator, also induced a L-LTP that was attenuated by inhibition of
transcription. Our results demonstrate that, like LTP in the Schaffer
collateral and mossy fiber pathways, MPP LTP also consists of a late
phase that is dependent on protein and RNA synthesis and PKA activity.
Thus, cAMP-mediated transcription appears to be a common mechanism for
the late form of LTP in all three pathways within the hippocampus.
Key words:
LTP;
hippocampus;
synaptic plasticity;
gene expression;
cAMP;
protein kinase A
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|
|
|
|
|
|
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|
|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
|
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273(47):
31345 - 31351.
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[Full Text]
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|
|
|
|
|
|
|
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J. Biol. Chem.,
September 11, 1998;
273(37):
23969 - 23975.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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J Neurophysiol,
January 1, 1998;
79(1):
496 - 499.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R R Ramirez, C C Gandhi, I A Muzzio, and L D Matzel
Protein synthesis-dependent memory and neuronal enhancement in Hermissenda are contingent on parameters of training and retention.
Learn. Mem.,
January 1, 1998;
4(6):
462 - 477.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R. M. FITZSIMONDS and M.-M. POO
Retrograde Signaling in the Development and Modification of Synapses
Physiol Rev,
January 1, 1998;
78(1):
143 - 170.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Bernabeu, L. Bevilaqua, P. Ardenghi, E. Bromberg, P. Schmitz, M. Bianchin, I. Izquierdo, and J. H. Medina
Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats
PNAS,
June 24, 1997;
94(13):
7041 - 7046.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. D. Murphy and M. Segal
Morphological plasticity of dendritic spines in central neurons is mediated by activation of cAMP response element binding protein
PNAS,
February 18, 1997;
94(4):
1482 - 1487.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P V Nguyen and E R Kandel
Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus.
Learn. Mem.,
January 1, 1997;
4(2):
230 - 243.
[Abstract]
[PDF]
|
|
|
|
|
|
|
E D Roberson, J D English, and J D Sweatt
A biochemist's view of long-term potentiation.
Learn. Mem.,
January 1, 1996;
3(1):
1 - 24.
[Abstract]
[PDF]
|
|
|
|
|
|
|
Y Y Huang, P V Nguyen, T Abel, and E R Kandel
Long-lasting forms of synaptic potentiation in the mammalian hippocampus.
Learn. Mem.,
January 1, 1996;
3(2-3):
74 - 85.
[PDF]
|
|
|
|
|
|
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G. E. Schafe and J. E. LeDoux
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September 15, 2000;
20(18):
RC96 - RC96.
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|
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