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The Journal of Neuroscience, June 1, 1999, 19(11):4544-4558
Presynaptically Located CB1 Cannabinoid Receptors Regulate GABA
Release from Axon Terminals of Specific Hippocampal
Interneurons
István
Katona1,
Beáta
Sperlágh1,
Attila
Sík1,
Attila
Käfalvi1,
E. Sylvester
Vizi1,
Ken
Mackie2, and
Tamás F.
Freund1
1 Institute of Experimental Medicine, Hungarian Academy
of Sciences, Budapest, H-1450, Hungary, and 2 Departments
of Anesthesiology, and Physiology and Biophysics, University of
Washington, Seattle, Washington 98195
To understand the functional significance and mechanisms of action
in the CNS of endogenous and exogenous cannabinoids, it is crucial to
identify the neural elements that serve as the structural substrate of
these actions. We used a recently developed antibody against the CB1
cannabinoid receptor to study this question in hippocampal networks.
Interneurons with features typical of basket cells showed a selective,
intense staining for CB1 in all hippocampal subfields and layers. Most
of them (85.6%) contained cholecystokinin (CCK), which corresponded to
96.9% of all CCK-positive interneurons, whereas only 4.6% of the
parvalbumin (PV)-containing basket cells expressed CB1. Accordingly,
electron microscopy revealed that CB1-immunoreactive axon terminals of
CCK-containing basket cells surrounded the somata and proximal
dendrites of pyramidal neurons, whereas PV-positive basket cell
terminals in similar locations were negative for CB1. The synthetic
cannabinoid agonist WIN 55,212-2 (0.01-3 µM) reduced
dose-dependently the electrical field stimulation-induced [3H]GABA release from superfused hippocampal
slices, with an EC50 value of 0.041 µM.
Inhibition of GABA release by WIN 55,212-2 was not mediated by
inhibition of glutamatergic transmission because the WIN 55,212-2 effect was not reduced by the glutamate blockers AP5 and CNQX. In
contrast, the CB1 cannabinoid receptor antagonist SR 141716A (1 µM) prevented this effect, whereas by itself it did not
change the outflow of [3H]GABA.
These results suggest that cannabinoid-mediated modulation of
hippocampal interneuron networks operate largely via presynaptic receptors on CCK-immunoreactive basket cell terminals. Reduction of
GABA release from these terminals is the likely mechanism by which both
endogenous and exogenous CB1 ligands interfere with hippocampal network
oscillations and associated cognitive functions.
Key words:
interneurons; cannabinoids; GABA; inhibition; cholecystokinin; parvalbumin; hippocampus, anxiety
Copyright © 1999 Society for Neuroscience 0270-6474/99/19114544-15$05.00/0
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