Group I metabotropic glutamate receptors inhibit GABA release at interneuron-Purkinje cell synapses through endocannabinoid production

Journal of Neuroscience

Volumn 24, Issue 20, 2004, Pages 4865-4874

  Galante, Micaela ^a,b   Diana, Marco A ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b PSL RESEARCH UNIVERSITY   (France)

Author keywords

2 AG; 2 arachidonyl glycerol; Cerebellar Purkinje cell; Endocannabinoids; GABAergic transmission; Group I metabotropic glutamate receptors; Paired recordings

Indexed keywords

2 ARACHIDONOYLGLYCEROL; 3,5 DIHYDROXYPHENYLGLYCINE; 4 AMINOBUTYRIC ACID; CALCIUM; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; GUANOSINE TRIPHOSPHATE DERIVATIVE; LIPOPROTEIN LIPASE; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR AGONIST; PHOSPHOLIPASE C;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CEREBELLUM; CONTROLLED STUDY; DEPOLARIZATION; GABAERGIC SYSTEM; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; NERVE CELL STIMULATION; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PURKINJE CELL; RAT; RECEPTOR UPREGULATION; SYNAPSE;

ANIMALS; CEREBELLUM; ENDOCANNABINOIDS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GTP-BINDING PROTEINS; INTERNEURONS; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 2442691616     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0403-04.2004     Document Type: Article

References (53)

1. Alger BE (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247-286.
2. Baude A, Nusser Z, Roberts JDB, Mulvihill E, McIlhinney RAJ, Somogyi P (1993) The Metabotropic glutamate receptor (mGluR1α) is concentrated at perysynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-787.
3. Batchelor AM, Madge DJ, Garthwaite J (1994) Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience 63:911-915.
4. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A, Matias I, Schiano-Moriello A, Paul P, Williams EJ, Gangadharan U, Hobbs C, Di Marzo V, Doherty P (2003) Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signalling in the brain. J Cell Biol 163:463-468.
5. BoxallA (2000) GABAergic mIPSCs in rat cerebellar Purkinje cells are modulated by TrkB and mGluR1-mediated stimulation of Src. J Physiol (Lond) 524:677-684.
6. Brown SP, Brenowitz SD, Regehr WG (2003) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048-1057.
7. Canepari M, Ogden D (2003) Evidence for protein tyrosine phosphatase, tyrosine kinase, and G-protein regulation of the parallel fiber metabotropic slow EPSC of rat cerebellar Purkinje neurons. J Neurosci 23:4066-4071.
8. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472.
9. Choi S, Lovinger DM (1997) Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc Natl Acad Sci USA 94:2665-2670.
10. Diana MA, Marty A (2003) Characterization of depolarization-induced suppression of inhibition using paired interneuron-Purkinje cell recordings. J Neurosci 23:5906-5918.
11. Diana MA, Levenes C, Mackie K, Marty A (2002) Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22:200-208.
12. Di Marzo V, Melck D, Bisogno T, De Petrocellis L (1998) Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends in Neurosci 21:521-528.
13. Dzubay JA, Otis TS (2002) Climbing fiber activation of metabotropic glutamate receptors on cerebellar purkinje neurons. Neuron 36:1159-1167.
14. Egertova M, Elphick MR (2000) Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422:159-171.
15. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066.
16. Galante M, Marty A (2003) Presynaptic ryanodine-sensitive calcium stores contribute to evoked neurotransmitter release at the basket cell-Purkinje cell synapse. J Neurosci 23:11229-11234.
17. Gee CE, Benquet P, Gerber U (2003) Group I metabotropic glutamate receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J Physiol (Lond) 546:655-664.
18. Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5:446-451.
19. 2+. Eur J Neurosci 12:987-993.
20. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, Freund TF (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544-4558.
21. Kim J, Isokawa M, Ledent C, Alger BE (2002) Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 22:10182-10191.
22. Kim SJ, Kim YS, Yuan JP, Petralia RS, Worley PF, Linden DJ (2003) Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 426:285-291.
23. Kreitzer AC, Regebr WG (2001a) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
24. Kreitzer AC, Regehr WG (2001b) Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21 [RC174]:1-5.
25. Kreitzer AC, Carter AG, Regehr WG (2002) Inhibition of interneuron firing extends the spread of endocannabinoid signalling in the cerebellum. Neuron 34:787-796.
26. Levenes C, Daniel H, Crepel F (2001) Retrograde modulation of transmitter release by postsynaptic subtype 1 metabotropic glutamate receptors in the rat cerebellum. J Physiol (Lond) 537:125-140.
27. Llano I, Marty A (1995) Presynaptic metabotropic glutamatergic regulation of inhibitory synapses in rat cerebellar slices. J Physiol (Lond) 486:163-176.
28. Llano I, Leresche N, Marty A (1991) Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6:565-574.
29. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475.
30. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H,Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534.
31. Martin LA, Alger BE (1999) Muscarinic facilitation of the occurrence of depolarization-induced suppression of inhibition in rat hippocampus. Neuroscience 92:61-71.
32. Neale SA, Garthwaite J, Batchelor AM (2001) mGlu1 receptors mediate a post-tetanic depression at parallel fibre-Purkinje cell synapses in rat cerebellum. Eur J Neurosci 14:1313-1319.
33. Negyessy L, Vidnyanszky Z, Kuhn R, Knopfel T, Gorcs TJ, Hamori J (1997) Light and electron microscopic demonstration of mGluR5 metabotropic glutamate receptor immunoreactive neuronal elements in the rat cerebellar cortex. J Comp Neurol 385:641-650.
34. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729-738.
35. Ohno-Shosaku T, Shosaku J, Tsubokawa H, Kano M (2002a) Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur J Neurosci 15:953-961.
36. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M (2002b) Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22:3864-3872.
37. Ohno-Shosaku T, Matsui M, Fukudome Y, Shosaku J, Tsubokawa H, Taketo MM, Manabe T, Kano M (2003) Postsynaptic M1 and M3 receptors are responsible for the muscarinic enhancement of retrograde endocannabinoid signalling in the hippocampns. Eur J Neurosci 18:109-116.
38. Palay SL, Chan Palay V (1974) Cerebellar cortex: cytology and organization. New York: Springer.
39. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873-884.
40. Pitler TA, Alger BE (1992) Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci 12:4122-4132.
41. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ (2002) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci USA 99:8384-8388.
42. Sjöström PJ, Turrigiano GG, Nelson SB (2003) Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641-654.
43. Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773-778.
44. Takahashi KA, Linden DJ (2000) Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. J Neurophysiol 83:1167-1180.
45. Tempia F, Miniaci MC, Anchisi D, Strata P (1998) Postsynaptic current mediated by metabotropic glutamate receptors in cerebellar Purkinje cells. J Neurophysiol 80:520-528.
46. Trettel J, Levine ES (2003) Endocannabinoids mediate rapid retrograde signalling at interneuron right-arrow pyramidal neuron synapses of the neocortex. J Neurophysiol 89:2334-2338.
47. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393-411.
48. Varma N, Carlson GC, Ledent C, Alger BE (2001) Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21:RC188.
49. Vincent P, Marty A (1993) Neighboring cerebellar Purkinje cells communicate via retrograde inhibition of common presynaptic interneurons. Neuron 11:885-893.
50. Vincent P, Marty A (1996) Fluctuations of inhibitory postsynaptic currents in Purkinje cells from rat cerebellar slices. J Physiol (Lond) 494:183-199.
51. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32:301-313.
52. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.
53. Xu-Friedman MA, Harris KM, Regehr WG (2001) Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells. J Neurosci 21:6666-6672.