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Journal of Neuroscience, Vol 11, 2795-2803, Copyright © 1991 by Society for Neuroscience
Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence
JE Cavazos, G Golarai and TP Sutula
Neuroscience Training Program, University of Wisconsin, Madison 53792.
Recent studies have revealed that mossy fiber axons of granule cells in the
dentate gyrus undergo reorganization of their terminal projections in both
animal models of epilepsy and human epilepsy. This synaptic reorganization
has been demonstrated by the Timm method, a histochemical technique that
selectively labels synaptic terminals of mossy fibers because of their high
zinc content. It has been generally presumed that the reorganization of the
terminal projections of the mossy fiber pathway is a consequence of axonal
sprouting and synaptogenesis by mossy fibers. To evaluate this possibility
further, the time course for development of Timm granules, which correspond
ultrastructurally to mossy fiber synaptic terminals, was examined in the
supragranular layer of the dentate gyrus at the initiation of kindling
stimulation with an improved scoring method for assessment of alterations
in Timm histochemistry. The progression and permanence of this histological
alteration were similarly evaluated during the behavioral and
electrographic evolution of kindling evoked by perforant path, amygdala, or
olfactory bulb stimulation. Mossy fiber synaptic terminals developed in the
supragranular region of the dentate gyrus by 4 d after initiation of
kindling stimulation in a time course compatible with axon sprouting. The
induced alterations in the terminal projections of the mossy fiber pathway
progressed with the evolution of behavioral kindled seizures, became
permanent in parallel with the development of longlasting susceptibility to
evoked seizures, and were observed as long as 8 months after the last
evoked kindled seizure. The results demonstrated a strong correlation
between mossy fiber synaptic reorganization and the development,
progression, and permanence of the kindling phenomenon.
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|
|
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|
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|
|
|
|
|
|
|
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|
|
|
|
|
|
|
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|
|
|
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|
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|
|
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|
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[Full Text]
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|
|
|
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|
|
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|
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|
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[Full Text]
[PDF]
|
|
|
|
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16(22):
7398 - 7406.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
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J. Neurosci.,
July 1, 1996;
16(13):
4250 - 4260.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Watanabe, R. S. Johnson, L. S. Butler, D. K. Binder, B. M. Spiegelman, V. E. Papaioannou, and J. O. McNamara
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J. Neurosci.,
June 15, 1996;
16(12):
3827 - 3836.
[Abstract]
[Full Text]
[PDF]
|
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