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The Journal of Neuroscience, March 1, 2002, 22(5):1690-1697
The Cannabinoid CB1 Receptor Mediates Retrograde Signals for
Depolarization-Induced Suppression of Inhibition in Cerebellar Purkinje
Cells
Takayuki
Yoshida1,
Kouichi
Hashimoto1,
Andreas
Zimmer2,
Takashi
Maejima1,
Kenji
Araishi1, and
Masanobu
Kano1
1 Department of Cellular Neurophysiology, Graduate
School of Medical Science, Kanazawa University, Kanazawa 920-8640, Japan, and 2 Department of Psychiatry, University of Bonn,
53105 Bonn, Germany
Action potential firing or depolarization of the postsynaptic
neuron can induce a transient suppression of inhibitory synaptic inputs
to the depolarized neuron in the cerebellum and hippocampus. This
phenomenon, termed depolarization-induced suppression of inhibition
(DSI), is initiated postsynaptically by an elevation of intracellular
Ca2+ concentration
([Ca2+]i) and is expressed
presynaptically as a suppression of the transmitter release. It is,
therefore, thought that some retrograde signal must exist from the
depolarized postsynaptic neurons to the presynaptic terminals. Recent
studies on hippocampal neurons have revealed that endogenous
cannabinoids (endocannabinoids) play a key role as a retrograde
messenger. There are, however, conflicting reports that glutamate may
be a candidate retrograde messenger for cerebellar DSI that acts on
presynaptic group II metabotropic glutamate receptors (mGluRs). In this
study, we examined whether endocannabinoids mediate retrograde signal
for cerebellar DSI. We recorded IPSCs from Purkinje cells by
stimulating putative basket cell axons in mouse cerebellar slices. DSI
was readily induced in evoked IPSCs by a depolarizing pulse train. We
found that DSI was completely occluded by a cannabinoid agonist,
WIN55,212-2, was totally eliminated by a specific antagonist of the
type 1 cannabinoid (CB1) receptor, SR141716A, and was deficient in the
CB1 knock-out mouse. In contrast, a group II mGluR-specific agonist,
(2S,2'R,3'R)-2-(2',3'-dicarboxycyclopropyl)glycine, did not completely occlude DSI, and an mGluR antagonist,
(RS)- -methyl-4-carboxyphenylglycine, had no
depressant effect on DSI. These results clearly indicate that the CB1
receptor mediates retrograde signal for DSI in cerebellar Purkinje cells.
Key words:
inhibitory transmission; cerebellum; Purkinje cell; retrograde signal; synaptic modulation; cannabinoid receptor
Copyright © 2002 Society for Neuroscience 0270-6474/02/2251690-08$05.00/0
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