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The Journal of Neuroscience, May 1, 2000, 20(9):3434-3441

Metaplasticity of Mossy Fiber Synaptic Transmission Involves Altered Release Probability

Ivan V. Goussakov¹, Klaus Fink², Christian E. Elger¹, and Heinz Beck¹

¹ Department of Epileptology, University of Bonn, 53105 Bonn, Germany, and ² Department of Pharmacology, University of Bonn, 53113 Bonn, Germany

Activity-dependent synaptic plasticity is a fundamental feature of CNS synapses. Intriguingly, the capacity of synapses to express plastic changes is itself subject to considerable activity-dependent variation, or metaplasticity. These forms of higher order plasticity are important because they may be crucial to maintain synapses within a dynamic functional range. In this study, we asked whether neuronal activity induced in vivo by application of kainate can induce lasting changes in mossy fiber short- and long-term plasticity.

Several weeks after kainate-induced status epilepticus, the mossy fiber, but not the associational-commissural pathway, exhibits a marked loss of paired-pulse facilitation, augmentation, and long-term potentiation (LTP). Because the adenylyl cyclase-protein kinase A cascade is involved in mossy fiber LTP induction, we have tested the integrity of this key pathway by pharmacological activation of either adenylyl cyclase or protein kinase A. These treatments resulted in LTP in control, but not in kainate-treated animals, indicating that status-induced changes occur downstream of protein kinase A. To test whether altered neurotransmitter release might account for these changes, we measured the size of the releasable pool of glutamate in mossy fiber terminals. We find that the size of the releasable pool of glutamate was significantly increased in kainate-treated rats, indicating an increased release probability at the mossy fiber-CA3 synapse.

Therefore, we suggest that lasting changes in neurotransmitter release probability caused by neuronal activity may be a powerful mechanism for metaplasticity that modulates both short- and long-term plasticity in the mossy fiber-CA3 synapse after status epilepticus.

Key words: synaptic plasticity; paired-pulse facilitation; mossy fiber pathway; long-term potentiation; status epilepticus; release probability

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Copyright © 2000 Society for Neuroscience  0270-6474/00/2093434-08$05.00/0

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