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The Journal of Neuroscience, March 28, 2007, 27(13):3408-3415; doi:10.1523/JNEUROSCI.4831-06.2007

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Behavioral/Systems/Cognitive
An NMDA Receptor/Nitric Oxide Cascade in Presynaptic Parallel Fiber–Purkinje Neuron Long-Term Potentiation

De-lai Qiu and Thomas Knöpfel

Laboratory for Neuronal Circuit Dynamics, RIKEN Brain Science Institute, Saitama 351-0198, Japan

Correspondence should be addressed to Dr. Thomas Knöpfel, RIKEN Brain Science Institute, Laboratory for Neuronal Circuit Dynamics, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan. Email: tknopfel{at}brain.riken.jp

Plasticity of synaptic transmission between parallel fiber (PF) and Purkinje neurons (PNs) is widely accepted as a cellular model for certain forms of cerebellar learning. Whereas the signaling cascades involved in postsynaptically expressed bidirectional long-term changes at PF–PN synapses are well investigated, data on presynaptically expressed long-term potentiation (LTP) are incomplete and controversial. Here we used transgenic mice that express a fluorescent protein Ca²⁺ sensor in PFs to demonstrate LTP of PF presynaptic Ca²⁺ transients after PF stimulation with 120 pulses at 4 Hz. Potentiation of the presynaptic Ca²⁺ transients correlated with the expression of simultaneously recorded LTP of PF–PN synaptic transmission and was suppressed by a protein kinase A inhibitor. Moreover, this presynaptically expressed form of LTP clearly required activation of an NMDA receptor/nitric oxide pathway, in contrast with the majority of previous reports. Blockade of NMDA receptors did not affect the PF Ca²⁺ transients induced during 4 Hz stimulation, indicating that the NMDA receptors required for the induction of presynaptic PF LTP are not localized in PFs.

Key words: calcium (Ca); cerebellum; nitric oxide; NMDA; presynaptic mechanisms; synaptic plasticity

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Received Aug. 18, 2006; revised Jan. 27, 2007; accepted Feb. 19, 2007.

Correspondence should be addressed to Dr. Thomas Knöpfel, RIKEN Brain Science Institute, Laboratory for Neuronal Circuit Dynamics, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan. Email: tknopfel{at}brain.riken.jp

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