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The Journal of Neuroscience, September 1, 2002, 22(17):7453-7461
Brain-Derived Neurotrophic Factor Triggers
Transcription-Dependent, Late Phase Long-Term Potentiation In
Vivo
Elhoucine
Messaoudi1,
Shui-Wang
Ying1,
Tambudzai
Kanhema1,
Susan D.
Croll2, and
Clive R.
Bramham1
1 Department of Physiology and Locus on Neuroscience,
University of Bergen, N-5009 Bergen, Norway, and
2 Regeneron Pharmaceuticals, Tarrytown, New York 10591
Acute intrahippocampal infusion of brain-derived neurotrophic
factor (BDNF) leads to long-term potentiation (BDNF-LTP) of synaptic
transmission at medial perforant path granule cell synapses in
the rat dentate gyrus. Endogenous BDNF is implicated in the maintenance
of high-frequency stimulation-induced LTP (HFS-LTP). However, the
relationship between exogenous BDNF-LTP and HFS-LTP is unclear. First,
we found that BDNF-LTP, like HFS-LTP, is associated with enhancement in
both synaptic strength and granule cell excitability (EPSP-spike
coupling). Second, treatment with a competitive NMDA receptor (NMDAR)
antagonist blocked HFS-LTP but had no effect on the development or
magnitude of BDNF-LTP. Thus, NMDAR activation is not required for the
induction or expression of BDNF-LTP. Formation of stable, late phase
HFS-LTP requires mRNA synthesis and is coupled to upregulation of the
immediate early gene activity-regulated cytoskeleton-associated protein
(Arc). Local infusion of the transcription inhibitor actinomycin D
(ACD) 1 hr before or immediately before BDNF infusion inhibited
BDNF-LTP and upregulation of Arc protein expression. ACD applied 2 hr
after BDNF infusion had no effect, defining a critical time window of
transcription-dependent synaptic strengthening. Finally, the functional
role of BDNF-LTP was assessed in occlusion experiments with HFS-LTP.
HFS-LTP was induced, and BDNF was infused at time points corresponding
to early phase (1 hr) or late phase (4 hr) HFS-LTP. BDNF applied during
the early phase led to normal BDNF-LTP. In contrast, BDNF-LTP was
completely occluded during the late phase. The results strongly support
a role for BDNF in triggering transcription-dependent, late phase LTP
in the intact adult brain.
Key words:
long-term potentiation (LTP); synaptic plasticity; neurotrophin; brain-derived neurotrophic factor (BDNF); dentate gyrus; hippocampus; activity-regulated cytoskeleton-associated protein (Arc); gene expression
Copyright © 2002 Society for Neuroscience 0270-6474/02/22177453-09$05.00/0
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