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J Neurophysiol (September 12, 2007). doi:10.1152/jn.00376.2007
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Submitted on April 2, 2007
Accepted on September 7, 2007

Developmental Changes in Agonist-induced Retrograde Signaling at Parallel Fiber-Purkinje Cell Synapses; Role of Calcium Induced Calcium Release

Francis Roger Crepel1* and Herve Daniel1

1 I.B.B.M.C, University Paris XI, Orsay, Essonne, France

* To whom correspondence should be addressed. E-mail: francis.crepel{at}u-psud.fr.

In cerebellar Purkinje cells (PCs), activation of post-synaptic mGluR1 receptors inhibits parallel fiber (PF) to PC synaptic transmission by retrograde signaling. However, results were conflicting with respect to whether endocannabinoids (Maejima et al., 2001) or glutamate (Glu) (Levenes et al., 2001) is the retrograde messenger involved. Experiments in cerebellar slices from 10 to 12 day-old rats and mice confirmed that suppression of PF-EPSCs by mGluR1 agonists was entirely blocked by cannabinoid receptor antagonists at this early developmental stage. In contrast, suppression of PF-EPSCs by mGluR1 agonists was only partly blocked by cannabinoid receptor antagonists in 18 to 22 day-old rats, and the remaining suppression was accompanied by an increase in paired-pulse facilitation. This endocannnabinoid-independent suppression of PF-EPSCs was potentiated by the Glu uptake inhibitor DL-TBOA and blocked by the desensitizing kainate (KA) receptors agonist SYM 2081, by non saturing concentrations of CNQX (but not by GYKI), and by dialyzing PCs with GDP-{beta}S. An endocannnabinoid-independent suppression of PF-EPSCs was also present in nearly mature wild type mice but was absent in GluR6 -/- mice. The endocannnabinoid-independent suppression of PF-EPSCs induced by mGluR1 agonists as well as the KA-dependent component of depolarization-induced suppression of excitation (DSE) (Crepel, 2007) were blocked by ryanodine acting at a pre-synaptic level. We conclude that retrograde release of Glu by PCs participates in mGluR1 agonist-induced suppression of PF-EPSCs at nearly mature PF-PC synapses, and that Glu operates through activation of pre-synaptic KA receptors located on PFs and prolonged release of calcium from pre-synaptic internal calcium stores.




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