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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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J. Trettel, D. A. Fortin, and E. S. Levine
Endocannabinoid signalling selectively targets perisomatic inhibitory inputs to pyramidal neurones in juvenile mouse neocortex
J. Physiol., April 1, 2004; 556(1): 95 - 107.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
A. Losonczy, A. A. Biro, and Z. Nusser
Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons
PNAS, February 3, 2004; 101(5): 1362 - 1367.
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J. Lipid Res.Home page
N. G. Bazan
Synaptic lipid signaling: significance of polyunsaturated fatty acids and platelet-activating factor
J. Lipid Res., December 1, 2003; 44(12): 2221 - 2233.
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Proc. Natl. Acad. Sci. USAHome page
L. Yao, P. Fan, Z. Jiang, W. S. Mailliard, A. S. Gordon, and I. Diamond
Addicting drugs utilize a synergistic molecular mechanism in common requiring adenosine and Gi-{beta}{gamma} dimers
PNAS, November 25, 2003; 100(24): 14379 - 14384.
[Abstract] [Full Text] [PDF]


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ScienceHome page
G. Marsicano, S. Goodenough, K. Monory, H. Hermann, M. Eder, A. Cannich, S. C. Azad, M. G. Cascio, S. O. Gutierrez, M. van der Stelt, et al.
CB1 Cannabinoid Receptors and On-Demand Defense Against Excitotoxicity
Science, October 3, 2003; 302(5642): 84 - 88.
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Mol. Pharmacol.Home page
H. Andersson, A. M. D'Antona, D. A. Kendall, G. Von Heijne, and C.-N. Chin
Membrane Assembly of the Cannabinoid Receptor 1: Impact of a Long N-Terminal Tail
Mol. Pharmacol., September 1, 2003; 64(3): 570 - 577.
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J. Neurosci.Home page
M. A. Diana and A. Marty
Characterization of Depolarization-Induced Suppression of Inhibition Using Paired Interneuron-Purkinje Cell Recordings
J. Neurosci., July 2, 2003; 23(13): 5906 - 5918.
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J. Neurophysiol.Home page
R. E. Hampson, S.-y. Zhuang, J. L. Weiner, and S. A. Deadwyler
Functional Significance of Cannabinoid-Mediated, Depolarization-Induced Suppression of Inhibition (DSI) in the Hippocampus
J Neurophysiol, July 1, 2003; 90(1): 55 - 64.
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Physiol. Rev.Home page
T. F. FREUND, I. KATONA, and D. PIOMELLI
Role of Endogenous Cannabinoids in Synaptic Signaling
Physiol Rev, July 1, 2003; 83(3): 1017 - 1066.
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BrainHome page
L. Iversen
Cannabis and the brain
Brain, June 1, 2003; 126(6): 1252 - 1270.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
A. B. Clement, E. G. Hawkins, A. H. Lichtman, and B. F. Cravatt
Increased Seizure Susceptibility and Proconvulsant Activity of Anandamide in Mice Lacking Fatty Acid Amide Hydrolase
J. Neurosci., May 1, 2003; 23(9): 3916 - 3923.
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J. Neurosci.Home page
P. Derkinderen, E. Valjent, M. Toutant, J.-C. Corvol, H. Enslen, C. Ledent, J. Trzaskos, J. Caboche, and J.-A. Girault
Regulation of Extracellular Signal-Regulated Kinase by Cannabinoids in Hippocampus
J. Neurosci., March 15, 2003; 23(6): 2371 - 2382.
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J. Neurosci.Home page
J. Kim, M. Isokawa, C. Ledent, and B. E. Alger
Activation of Muscarinic Acetylcholine Receptors Enhances the Release of Endogenous Cannabinoids in the Hippocampus
J. Neurosci., December 1, 2002; 22(23): 10182 - 10191.
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J. Neurosci.Home page
C.-S. Chiu, K. Jensen, I. Sokolova, D. Wang, M. Li, P. Deshpande, N. Davidson, I. Mody, M. W. Quick, S. R. Quake, et al.
Number, Density, and Surface/Cytoplasmic Distribution of GABA Transporters at Presynaptic Structures of Knock-In Mice Carrying GABA Transporter Subtype 1-Green Fluorescent Protein Fusions
J. Neurosci., December 1, 2002; 22(23): 10251 - 10266.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
D. Rueda, B. Navarro, A. Martinez-Serrano, M. Guzman, and I. Galve-Roperh
The Endocannabinoid Anandamide Inhibits Neuronal Progenitor Cell Differentiation through Attenuation of the Rap1/B-Raf/ERK Pathway
J. Biol. Chem., November 22, 2002; 277(48): 46645 - 46650.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
T. P. Dinh, D. Carpenter, F. M. Leslie, T. F. Freund, I. Katona, S. L. Sensi, S. Kathuria, and D. Piomelli
Brain monoglyceride lipase participating in endocannabinoid inactivation
PNAS, August 6, 2002; 99(16): 10819 - 10824.
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Pharmacol. Rev.Home page
A. C. Howlett, F. Barth, T. I. Bonner, G. Cabral, P. Casellas, W. A. Devane, C. C. Felder, M. Herkenham, K. Mackie, B. R. Martin, et al.
International Union of Pharmacology. XXVII. Classification of Cannabinoid Receptors
Pharmacol. Rev., June 1, 2002; 54(2): 161 - 202.
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J. Neurosci.Home page
T. Ohno-Shosaku, H. Tsubokawa, I. Mizushima, N. Yoneda, A. Zimmer, and M. Kano
Presynaptic Cannabinoid Sensitivity Is a Major Determinant of Depolarization-Induced Retrograde Suppression at Hippocampal Synapses
J. Neurosci., May 15, 2002; 22(10): 3864 - 3872.
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J. Neurosci.Home page
T. Klausberger, J. D. B. Roberts, and P. Somogyi
Cell Type- and Input-Specific Differences in the Number and Subtypes of Synaptic GABAA Receptors in the Hippocampus
J. Neurosci., April 1, 2002; 22(7): 2513 - 2521.
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Mol. Pharmacol.Home page
M. Kouznetsova, B. Kelley, M. Shen, and S. A. Thayer
Desensitization of Cannabinoid-Mediated Presynaptic Inhibition of Neurotransmission Between Rat Hippocampal Neurons in Culture
Mol. Pharmacol., March 1, 2002; 61(3): 477 - 485.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
M. A. Diana, C. Levenes, K. Mackie, and A. Marty
Short-Term Retrograde Inhibition of GABAergic Synaptic Currents in Rat Purkinje Cells Is Mediated by Endogenous Cannabinoids
J. Neurosci., January 1, 2002; 22(1): 200 - 208.
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J. Neurosci.Home page
I. Katona, E. A. Rancz, L. Acsady, C. Ledent, K. Mackie, N. Hajos, and T. F. Freund
Distribution of CB1 Cannabinoid Receptors in the Amygdala and their Role in the Control of GABAergic Transmission
J. Neurosci., December 1, 2001; 21(23): 9506 - 9518.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
J. Nie and D. L. Lewis
Structural Domains of the CB1 Cannabinoid Receptor That Contribute to Constitutive Activity and G-Protein Sequestration
J. Neurosci., November 15, 2001; 21(22): 8758 - 8764.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
E A Jennings, C W Vaughan, and M J Christie
Cannabinoid actions on rat superficial medullary dorsal horn neurons in vitro
J. Physiol., August 1, 2001; 534(3): 805 - 812.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
V. Morisset and L. Urban
Cannabinoid-Induced Presynaptic Inhibition of Glutamatergic EPSCs in Substantia Gelatinosa Neurons of the Rat Spinal Cord
J Neurophysiol, July 1, 2001; 86(1): 40 - 48.
[Abstract] [Full Text] [PDF]


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J. Pharmacol. Exp. Ther.Home page
K. Soderstrom and F. Johnson
Zebra Finch CB1 Cannabinoid Receptor: Pharmacology and in Vivo and in Vitro Effects of Activation
J. Pharmacol. Exp. Ther., April 1, 2001; 297(1): 189 - 197.
[Abstract] [Full Text]


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J. Neurosci.Home page
A. A. Coutts, S. Anavi-Goffer, R. A. Ross, D. J. MacEwan, K. Mackie, R. G. Pertwee, and A. J. Irving
Agonist-Induced Internalization and Trafficking of Cannabinoid CB1 Receptors in Hippocampal Neurons
J. Neurosci., April 1, 2001; 21(7): 2425 - 2433.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
J. J. Rodriguez, K. Mackie, and V. M. Pickel
Ultrastructural Localization of the CB1 Cannabinoid Receptor in {micro}-Opioid Receptor Patches of the Rat Caudate Putamen Nucleus
J. Neurosci., February 1, 2001; 21(3): 823 - 833.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
A. F. Hoffman and C. R. Lupica
Direct Actions of Cannabinoids on Synaptic Transmission in the Nucleus Accumbens: A Comparison With Opioids
J Neurophysiol, January 1, 2001; 85(1): 72 - 83.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
R. E. Hampson and S. A. Deadwyler
Cannabinoids Reveal the Necessity of Hippocampal Neural Encoding for Short-Term Memory in Rats
J. Neurosci., December 1, 2000; 20(23): 8932 - 8942.
[Abstract] [Full Text] [PDF]


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J. Pharmacol. Exp. Ther.Home page
A. Köfalvi, B. Sperlágh, T. Zelles, and E. S. Vizi
Long-Lasting Facilitation of 4-Amino-n-[2,3-3H]butyric Acid ([3H]GABA) Release from Rat Hippocampal Slices by Nicotinic Receptor Activation
J. Pharmacol. Exp. Ther., November 1, 2000; 295(2): 453 - 462.
[Abstract] [Full Text]


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J. Neurosci.Home page
L. Acsady, I. Katona, F. J. Martinez-Guijarro, G. Buzsaki, and T. F. Freund
Unusual Target Selectivity of Perisomatic Inhibitory Cells in the Hilar Region of the Rat Hippocampus
J. Neurosci., September 15, 2000; 20(18): 6907 - 6919.
[Abstract] [Full Text] [PDF]


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Learn. Mem.Home page
J. M. Sullivan
Cellular and Molecular Mechanisms Underlying Learning and Memory Impairments Produced by Cannabinoids
Learn. Mem., May 1, 2000; 7(3): 132 - 139.
[Abstract] [Full Text]



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