 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, January 1, 2002, 22(1):200-208
Short-Term Retrograde Inhibition of GABAergic Synaptic Currents in Rat Purkinje Cells Is Mediated by Endogenous Cannabinoids
Marco A. Diana1, Carole Levenes1, Ken Mackie2, and Alain Marty1 1 Laboratoire de Physiologie Cérébrale, Université Paris 5, 75006 Paris, France, and 2 Department of Anesthesiology, Physiology, and Biophysics, University of Washington, Seattle, Washington 98195
Depolarization-induced suppression of inhibition (DSI) is a form of short-term plasticity of GABAergic synaptic transmission that is found in cerebellar Purkinje cells and hippocampal CA1 pyramidal cells. DSI involves the release of a calcium-dependent retrograde messenger by the somatodendritic compartment of the postsynaptic cell. Both glutamate and endogenous cannabinoids have been proposed as retrograde messenger.
Here we show that, in cerebellar parasagittal slices, type 1 cannabinoid receptors (CB1Rs) are expressed at high levels in axons of GABAergic interneurons and in presynaptic terminals onto Purkinje cells. Application of the cannabinoid antagonist AM-251 (500 nM) leads to the abolition of the DSI of evoked currents (eIPSCs) recorded in paired recordings and to a strong reduction of the DSI of TTX-insensitive miniature events (mIPSCs) recorded from Purkinje cells. Furthermore, the CB1R agonist WIN 55-212,2 (5 µM) induces a presynaptic inhibition of synaptic currents similar to that occurring during DSI, as well as an occlusion of DSI after stimulation of Purkinje cells. Moreover, WIN 55-212,2 reduces the calcium transients evoked in presumed presynaptic varicosities by short trains of action potentials.
Our results indicate that DSI is mediated by the activation of presynaptic CB1Rs and that an endogenous cannabinoid is a likely candidate retrograde messenger in this preparation. They further suggest that DSI involves distinct presynaptic modifications for eIPSCs and mIPSCs, including an inhibition of action potential-evoked calcium rises.
Key words: depolarization-induced suppression of inhibition; endogenous cannabinoids; CB1 receptors; retrograde messengers; synaptic transmission; synaptic plasticity; cerebellum; interneurons
Copyright © 2002 Society for Neuroscience 0270-6474/02/221200-09$05.00/0
This article has been cited by other articles:
Y. S. Kim, J. H. Shin, F. S. Hall, and D. J. Linden
Dopamine Signaling Is Required for Depolarization-Induced Slow Current in Cerebellar Purkinje Cells
J. Neurosci., July 1, 2009; 29(26): 8530 - 8538.
[Abstract] [Full Text] [PDF]
M. Kano, T. Ohno-Shosaku, Y. Hashimotodani, M. Uchigashima, and M. Watanabe
Endocannabinoid-Mediated Control of Synaptic Transmission
Physiol Rev, January 1, 2009; 89(1): 309 - 380.
[Abstract] [Full Text] [PDF]
P. J. Sjostrom, E. A. Rancz, A. Roth, and M. Hausser
Dendritic Excitability and Synaptic Plasticity
Physiol Rev, April 1, 2008; 88(2): 769 - 840.
[Abstract] [Full Text] [PDF]
I. C. Duguid, Y. Pankratov, G. W. J. Moss, and T. G. Smart
Somatodendritic Release of Glutamate Regulates Synaptic Inhibition in Cerebellar Purkinje Cells via Autocrine mGluR1 Activation
J. Neurosci., November 14, 2007; 27(46): 12464 - 12474.
[Abstract] [Full Text] [PDF]
F. Crepel and H. Daniel
Developmental Changes in Agonist-Induced Retrograde Signaling at Parallel Fiber Purkinje Cell Synapses: Role of Calcium-Induced Calcium Release
J Neurophysiol, November 1, 2007; 98(5): 2550 - 2565.
[Abstract] [Full Text] [PDF]
J. Torres-Reveron and M. J. Friedlander
Properties of Persistent Postnatal Cortical Subplate Neurons
J. Neurosci., September 12, 2007; 27(37): 9962 - 9974.
[Abstract] [Full Text] [PDF]
S.-y. Kawaguchi and T. Hirano
Sustained Structural Change of GABAA Receptor-Associated Protein Underlies Long-Term Potentiation at Inhibitory Synapses on a Cerebellar Purkinje Neuron
J. Neurosci., June 20, 2007; 27(25): 6788 - 6799.
[Abstract] [Full Text] [PDF]
F. Crepel
Developmental Changes in Retrograde Messengers Involved in Depolarization-Induced Suppression of Excitation at Parallel Fiber-Purkinje Cell Synapses in Rodents
J Neurophysiol, January 1, 2007; 97(1): 824 - 836.
[Abstract] [Full Text] [PDF]
B. Szabo, M. J. Urbanski, T. Bisogno, V. D. Marzo, A. Mendiguren, W. U. Baer, and I. Freiman
Depolarization-induced retrograde synaptic inhibition in the mouse cerebellar cortex is mediated by 2-arachidonoylglycerol
J. Physiol., November 15, 2006; 577(1): 263 - 280.
[Abstract] [Full Text] [PDF]
M. E. Hofmann, B. Nahir, and C. J. Frazier
Endocannabinoid-Mediated Depolarization-Induced Suppression of Inhibition in Hilar Mossy Cells of the Rat Dentate Gyrus
J Neurophysiol, November 1, 2006; 96(5): 2501 - 2512.
[Abstract] [Full Text] [PDF]
A. Fisyunov, V. Tsintsadze, R. Min, N. Burnashev, and N. Lozovaya
Cannabinoids Modulate the P-Type High-Voltage-Activated Calcium Currents in Purkinje Neurons
J Neurophysiol, September 1, 2006; 96(3): 1267 - 1277.
[Abstract] [Full Text] [PDF]
Y. Kishimoto and M. Kano
Endogenous Cannabinoid Signaling through the CB1 Receptor Is Essential for Cerebellum-Dependent Discrete Motor Learning.
J. Neurosci., August 23, 2006; 26(34): 8829 - 8837.
[Abstract] [Full Text] [PDF]
B. J. van Beugen, R. Y. Nagaraja, and C. Hansel
Climbing fiber-evoked endocannabinoid signaling heterosynaptically suppresses presynaptic cerebellar long-term potentiation.
J. Neurosci., August 9, 2006; 26(32): 8289 - 8294.
[Abstract] [Full Text] [PDF]
N. Wettschureck, M. van der Stelt, H. Tsubokawa, H. Krestel, A. Moers, S. Petrosino, G. Schutz, V. Di Marzo, and S. Offermanns
Forebrain-Specific Inactivation of Gq/G11 Family G Proteins Results in Age-Dependent Epilepsy and Impaired Endocannabinoid Formation
Mol. Cell. Biol., August 1, 2006; 26(15): 5888 - 5894.
[Abstract] [Full Text] [PDF]
T. Yoshida, M. Fukaya, M. Uchigashima, E. Miura, H. Kamiya, M. Kano, and M. Watanabe
Localization of diacylglycerol lipase-alpha around postsynaptic spine suggests close proximity between production site of an endocannabinoid, 2-arachidonoyl-glycerol, and presynaptic cannabinoid CB1 receptor.
J. Neurosci., May 3, 2006; 26(18): 4740 - 4751.
[Abstract] [Full Text] [PDF]
Y. Kawamura, M. Fukaya, T. Maejima, T. Yoshida, E. Miura, M. Watanabe, T. Ohno-Shosaku, and M. Kano
The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum.
J. Neurosci., March 15, 2006; 26(11): 2991 - 3001.
[Abstract] [Full Text] [PDF]
M. Hirono and K. Obata
{alpha}-Adrenoceptive Dual Modulation of Inhibitory GABAergic Inputs to Purkinje Cells in the Mouse Cerebellum
J Neurophysiol, February 1, 2006; 95(2): 700 - 708.
[Abstract] [Full Text] [PDF]
B. Engler, I. Freiman, M. Urbanski, and B. Szabo
Effects of Exogenous and Endogenous Cannabinoids on GABAergic Neurotransmission between the Caudate-Putamen and the Globus Pallidus in the Mouse
J. Pharmacol. Exp. Ther., February 1, 2006; 316(2): 608 - 617.
[Abstract] [Full Text] [PDF]
M. Yamasaki, K. Hashimoto, and M. Kano
Miniature Synaptic Events Elicited by Presynaptic Ca2+ Rise Are Selectively Suppressed by Cannabinoid Receptor Activation in Cerebellar Purkinje Cells
J. Neurosci., January 4, 2006; 26(1): 86 - 95.
[Abstract] [Full Text] [PDF]
M. Mukhtarov, D. Ragozzino, and P. Bregestovski
Dual Ca2+ modulation of glycinergic synaptic currents in rodent hypoglossal motoneurones
J. Physiol., December 15, 2005; 569(3): 817 - 831.
[Abstract] [Full Text] [PDF]
N. Lozovaya, N. Yatsenko, A. Beketov, T. Tsintsadze, and N. Burnashev
Glycine Receptors in CNS Neurons as a Target for Nonretrograde Action of Cannabinoids
J. Neurosci., August 17, 2005; 25(33): 7499 - 7506.
[Abstract] [Full Text] [PDF]
T. Maejima, S. Oka, Y. Hashimotodani, T. Ohno-Shosaku, A. Aiba, D. Wu, K. Waku, T. Sugiura, and M. Kano
Synaptically Driven Endocannabinoid Release Requires Ca2+-Assisted Metabotropic Glutamate Receptor Subtype 1 to Phospholipase C {beta}4 Signaling Cascade in the Cerebellum
J. Neurosci., July 20, 2005; 25(29): 6826 - 6835.
[Abstract] [Full Text] [PDF]
D. A. Rusakov, F. Saitow, K. P. Lehre, and S. Konishi
Modulation of Presynaptic Ca2+ Entry by AMPA Receptors at Individual GABAergic Synapses in the Cerebellum
J. Neurosci., May 18, 2005; 25(20): 4930 - 4940.
[Abstract] [Full Text] [PDF]
F. RODRIGUEZ de FONSECA, I. DEL ARCO, F. J. BERMUDEZ-SILVA, A. BILBAO, A. CIPPITELLI, and M. NAVARRO
THE ENDOCANNABINOID SYSTEM: PHYSIOLOGY AND PHARMACOLOGY
Alcohol Alcohol., January 1, 2005; 40(1): 2 - 14.
[Abstract] [Full Text] [PDF]
B. Szabo, M. Than, D. Thorn, and I. Wallmichrath
Analysis of the Effects of Cannabinoids on Synaptic Transmission between Basket and Purkinje Cells in the Cerebellar Cortex of the Rat
J. Pharmacol. Exp. Ther., September 1, 2004; 310(3): 915 - 925.
[Abstract] [Full Text] [PDF]
M. Hirasawa, Y. Schwab, S. Natah, C. J. Hillard, K. Mackie, K. A. Sharkey, and Q. J. Pittman
Dendritically released transmitters cooperate via autocrine and retrograde actions to inhibit afferent excitation in rat brain
J. Physiol., September 1, 2004; 559(2): 611 - 624.
[Abstract] [Full Text] [PDF]
C. Kushmerick, G. D. Price, H. Taschenberger, N. Puente, R. Renden, J. I. Wadiche, R. M. Duvoisin, P. Grandes, and H. von Gersdorff
Retroinhibition of Presynaptic Ca2+ Currents by Endocannabinoids Released via Postsynaptic mGluR Activation at a Calyx Synapse
J. Neurosci., June 30, 2004; 24(26): 5955 - 5965.
[Abstract] [Full Text] [PDF]
H. Huang and A. Bordey
Glial Glutamate Transporters Limit Spillover Activation of Presynaptic NMDA Receptors and Influence Synaptic Inhibition of Purkinje Neurons
J. Neurosci., June 23, 2004; 24(25): 5659 - 5669.
[Abstract] [Full Text] [PDF]
S. P. Brown, P. K. Safo, and W. G. Regehr
Endocannabinoids Inhibit Transmission at Granule Cell to Purkinje Cell Synapses by Modulating Three Types of Presynaptic Calcium Channels
J. Neurosci., June 16, 2004; 24(24): 5623 - 5631.
[Abstract] [Full Text] [PDF]
M. Galante and M. A. Diana
Group I Metabotropic Glutamate Receptors Inhibit GABA Release at Interneuron-Purkinje Cell Synapses through Endocannabinoid Production
J. Neurosci., May 19, 2004; 24(20): 4865 - 4874.
[Abstract] [Full Text] [PDF]
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]
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.
[Abstract] [Full Text] [PDF]
M. Galante and A. Marty
Presynaptic Ryanodine-Sensitive Calcium Stores Contribute to Evoked Neurotransmitter Release at the Basket Cell-Purkinje Cell Synapse
J. Neurosci., December 3, 2003; 23(35): 11229 - 11234.
[Abstract] [Full Text] [PDF]
T. Bisogno, F. Howell, G. Williams, A. Minassi, M. G. Cascio, A. Ligresti, I. Matias, A. Schiano-Moriello, P. Paul, E.-J. Williams, et al.
Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain
J. Cell Biol., November 10, 2003; 163(3): 463 - 468.
[Abstract] [Full Text] [PDF]
S. D. Brenowitz and W. G. Regehr
Calcium Dependence of Retrograde Inhibition by Endocannabinoids at Synapses onto Purkinje Cells
J. Neurosci., July 16, 2003; 23(15): 6373 - 6384.
[Abstract] [Full Text] [PDF]
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.
[Abstract] [Full Text] [PDF]
T. F. FREUND, I. KATONA, and D. PIOMELLI
Role of Endogenous Cannabinoids in Synaptic Signaling
Physiol Rev, July 1, 2003; 83(3): 1017 - 1066.
[Abstract] [Full Text] [PDF]
J. Brockhaus and J. W Deitmer
Long-lasting modulation of synaptic input to Purkinje neurons by Bergmann glia stimulation in rat brain slices
J. Physiol., December 1, 2002; 545(2): 581 - 593.
[Abstract] [Full Text] [PDF]
D. Robbe, M. Kopf, A. Remaury, J. Bockaert, and O. J. Manzoni
Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens
PNAS, June 11, 2002; 99(12): 8384 - 8388.
[Abstract] [Full Text] [PDF]
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.
[Abstract] [Full Text] [PDF]
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.
[Abstract] [Full Text] [PDF]
R. I. Wilson and R. A. Nicoll
Endocannabinoid Signaling in the Brain
Science, April 26, 2002; 296(5568): 678 - 682.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|