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The Journal of Neuroscience, September 1, 1998, 18(17):6830-6839
Presynaptic Modulation of Synaptic Transmission and Plasticity by
Brain-Derived Neurotrophic Factor in the Developing Hippocampus
Wolfram
Gottschalk1,
Lucas D.
Pozzo-Miller2,
Alexander
Figurov1, and
Bai
Lu1
1 Unit on Synapse Development and Plasticity,
Laboratory of Developmental Neurobiology, National Institute of Child
Health and Human Development, and 2 Laboratory of
Neurobiology, National Institute of Neurological Diseases and Stroke,
National Institutes of Health, Bethesda, Maryland 20892
In addition to the regulation of neuronal survival and
differentiation, neurotrophins may play a role in synapse development and plasticity. Application of brain-derived neurotrophic factor (BDNF)
promotes long-term potentiation (LTP) in CA1 synapses of neonatal
hippocampus, which otherwise exhibit only short-term potentiation. This
is attributable, at least in part, to an attenuation of the synaptic
fatigue induced by high-frequency stimulation (HFS). However, the
prevention of synaptic fatigue by BDNF could be mediated by an
attenuation of synaptic vesicle depletion from presynaptic terminals
and/or a reduction of the desensitization of postsynaptic receptors.
Here we provide evidence supporting a presynaptic effect of BDNF. The
effect of BDNF on synaptic fatigue depended on the stimulation
frequency, not on the stimulus duration nor on the number of
stimulation pulses. BDNF was only effective when the synapses were
stimulated at frequencies >50 Hz. Treatment with BDNF also potentiated
paired-pulse facilitation (PPF), a parameter reflecting changes in the
properties of presynaptic terminals. This effect of BDNF was restricted
only to PPF elicited with interpulse intervals  20 msec. Changes in
the extracellular calcium concentration altered the magnitude of the
BDNF effect on PPF and synaptic responses to HFS, suggesting that BDNF
regulates neurotransmitter release. When the desensitization of
glutamate receptors was blocked by cyclothiazide or aniracetam, the
BDNF potentiation of the synaptic responses to HFS was unaltered. Taken together, these results suggest that BDNF acts presynaptically. When
two pathways in the same slice were monitored simultaneously, BDNF
treatment potentiated the tetanized pathway without affecting the
synaptic efficacy of the untetanized pathway. The selective potentiation of high-frequency transmission by BDNF appears to contribute directly to the effect of BDNF on LTP rather than indirectly by inducing the release of additional diffusible factors. The preferential potentiation of highly active synapses by BDNF may have
implications in the Hebbian mechanism of synaptic plasticity.
Key words:
BDNF; presynaptic; hippocampus; LTP; synaptic fatigue; plasticity
Copyright © 1998 Society for Neuroscience 0270-6474/98/18176830-10$05.00/0
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