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NEUROSCIENCE |
1 Department of Neurobiology and Civitan International Research Center, University of Alabama at Birmingham, Birmingham, AL 35294, USA
2 Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138, USA
3 Departments of Cell Biology and Anatomy, and Neurology, New York Medical College, Valhalla, NY 10595, USA
4 Neuroscience Research Institute, Charité, Humboldt University, Berlin, D-10117, Germany
5 Department of Psychiatry, Charité, Humboldt University, Berlin, D-10117, Germany
6 Departments of Neurosurgery, Neurology, and Neuroscience, University of New Mexico School of Medicine, Albuquerque, NM 87131, USA
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 enhanced green fluorescent protein (eGFP)-labelled 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 the role of BDNF in hippocampal long-term synaptic plasticity.
(Received 10 April 2006;
accepted after revision 16 May 2006;
first published online 18 May 2006)
Corresponding author L. Pozzo-Miller: Department of Neurobiology, SHEL-1002, University of Alabama at Birmingham, 1825 University Blvd, Birmingham, AL 35294-2182, USA. Email: lucaspm{at}uab.edu
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