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Received April 10, 2006
Revised April 27, 2006
Accepted after revision May 16, 2006
1 Neurobiology, UAB; Mol Cell Biol, Harvard University
2 Cell Biology & Anatomy and Neurology, New York Medical College
3 Mol Cell Biol, Harvard University
4 Psychiatry, Neuroscience Research Institute, Charité, Humboldt University
5 Neurosci Res Instit, Charité, Humboldt Univ; Neurosurg, Neurol, and Neurosci, Univ New Mexico
6 Neurobiology, University of Alabama at Birmingham
* To whom correspondence should be addressed. E-mail: lucaspm{at}uab.edu.
Exerting its actions pre-, post-, and peri-synaptically, brain-derived neurotrophic factor (BDNF) is one of the most potent modulators of hippocampal synaptic function. Here, we examined the effects of BDNF on a rapidly recycling pool (RRP) of vesicles within excitatory synapses. First, we estimated vesicular release in hippocampal cultures by performing FM4-64 imaging in terminals impinging on eGFP-labeled dendritic spines - a hallmark of excitatory synapses. Consistent with a modulation of the RRP, BDNF increased the evoked destaining rate of FM4-64 only during the initial phase of field stimulation. Multiphoton microscopy in acute hippocampal slices confirmed these observations by selectively imaging the RRP, which was loaded with FM1-43 by hyperosmotic shock. Slices exposed to BDNF showed an increase in the evoked and spontaneous rates of FM1-43 destaining from terminals in CA1 stratum radiatum, mostly representing excitatory terminals of Schaffer collaterals. Variance-mean analysis of evoked EPSCs in CA1 pyramidal neurons further confirmed that release probability is increased in BDNF-treated slices, without changes in the number of independent release sites or average postsynaptic quantal amplitude. Because BDNF was absent during dye loading, imaging, destaining, and whole-cell recordings, these results demonstrate that BDNF induces a long-lasting enhancement in the probability of transmitter release at hippocampal excitatory synapses by modulating the RRP. Since the endogenous BDNF scavenger TrkB-IgG prevented the enhancement of FM1-43 destaining rate caused by induction of long-term potentiation in acute hippocampal slices, the modulation of a rapidly recycling vesicle pool may underlie BDNF's role in hippocampal long-term synaptic plasticity.
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