Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells

Journal of Neurophysiology

Volumn 83, Issue 3, 2000, Pages 1167-1180

  Takahashi, Kanji A ^a   Linden, David J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CALCIUM ION; CANNABINOID; CANNABINOID RECEPTOR; RIMONABANT;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CEREBELLUM; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; KINETICS; MALE; NERVE FIBER; NEUROTRANSMITTER RELEASE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PURKINJE CELL; RAT; SYNAPTIC TRANSMISSION; VELOCITY;

EID: 0034063313     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.3.1167     Document Type: Article

References (72)

1. ADAMS, I. B. AND MARTIN, B. R. Cannabis: pharmacology and toxicology in animals and humans. Addiction 91: 1585-1614, 1996.
2. BARBOUR, B. Synaptic currents evoked in Purkinje cells by stimulating individual granule cells. Neuron 11: 759-769, 1993.
3. BELUE, R. C., HOWLETT, A. C., WESTLAKE, T. M., AND HUTCHINGS, D. E. The ontogeny of cannabinoid receptors in the brain of postnatal and aging rats. Neurotoxicol. Teratol. 17: 25-30, 1994.
4. BIDAUT-RUSSELL, M., DEVANE, W. A., AND HOWLETT, A. C. Cannabinoid receptors and modulation of cyclic AMP accumulation in the rat brain. J. Neurochem. 55: 21-26, 1990.
5. CAULFIELD, M. P. AND BROWN, D. A. Cannabinoid receptor agonists inhibit Ca current in NG108-14 neuroblastoma cells via a pertussis toxin-sensitive mechanism. Br. J. Pharmacol. 106: 231-232, 1992.
6. CHAN, P. K., CHAN, S. C., AND YUNG, W. H. Presynaptic inhibition of GABAergic inputs to rat substantia nigra pars reticulata neurones by a cannabinoid agonist. Neuroreport 9: 671-675, 1998.
7. CHAVEZ-NORIEGA, L. E. AND STEVENS, C. F. Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J. Neurosci. 14: 310-317, 1994.
8. CHAVIS, P., MOLLARD, P., BOCKAERT, J., AND MANZONI, O. Visualization of cyclic AMP-regulated presynaptic activity at cerebellar granule cells. Neuron 20: 773-781, 1998.
9. CHEN, C. AND REGEHR, W. G. The mechanism of cAMP-mediated enhancement at a cerebellar synapse. J. Neurosci. 17: 8687-8694, 1997.
10. A receptor-activated current by norepinephrine in cerebellar Purkinje cells. Neuroscience 51: 951-960, 1992.
11. CHILDERS, S. R. AND DEADWYLER, S. A. Role of cyclic AMP in the actions of cannabinoid receptors. Biochem. Pharmacol. 52: 819-827, 1996.
12. DEADWYLER, S. A., HAMPSON, R. E., BENNETT, B. A., EDWARDS, T. A., MU, J., PACHECO, M. A., WARD, S. J., AND CHILDERS, S. R. Cannabinoids modulate potassium current in cultured hippocampal neurons. Receptors Channels 1: 121-134, 1993.
13. DEADWYLER, S. A., HAMPSON, R. E., MU, J., WHYTE, A., AND CHILDERS, S. Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. J. Pharmacol. Exp. Ther. 273: 734-743, 1995.
14. DITTMAN, J. S. AND REGEHR, W. G. Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J. Neurosci. 16: 1623-1633, 1996.
15. DITTMAN, J. S. AND REGEHR, W. G. Mechanism and kinetics of heterosynaptic depression at a cerebellar synapse. J. Neurosci. 17: 9048-9059, 1997.
16. FARRANT, M. AND CULL-CANDY, S. G. Excitatory amino acid receptor-channels in Purkinje cells in thin cerebellar slices. Proc. R. Soc. Lond. B Biol. Sci. 244: 179-184, 1991.
17. GAONI, Y. AND MECHOULAM, R. Isolation, structure, and partial synthesis of an active constituent of hashish. J. Am. Chem. Soc. 86: 1646-1647, 1964.
18. GARCIA, D. E., BROWN, S., HILLE, B., AND MACKIE, K. Protein kinase C disrupts cannabanoid actions by phosphorylation of the CB1 cannabinoid receptor. J. Neurosci. 18: 2834-2841, 1998.
19. s linkage to the CB1 receptor. J. Neurosci. 17: 5327-5333, 1997.
20. GODA, Y. AND STEVENS, C. F. Two components of transmitter release at a central synapse. Proc. Natl. Acad Sci. USA 91: 12942-12946, 1994.
21. HAMPSON, R. E., EVANS, G.J.O., MU, J., ZHUANG, S., KING, V. C., CHILDERS, S. R., AND DEADWYLER, S. A. Role of cyclic AMP dependent protein kinase in cannabinoid receptor modulation of potassium "A-current" in cultured rat hippocampal neurons. Life Sci. 56: 2081-2088, 1995.
22. HENRY, D. J. AND CHAVKIN, C. Activation of inwardly rectifying potassium channels (GIRK1) by co-expressed rat brain cannabinoid receptors in Xenopus oocytes. Neurosci. Lett. 186: 91-94, 1995.
23. HERKENHAM, M. Cannabinoid receptor localization in brain: relationship to motor and reward systems. Ann. NY Acad. Sci. 654: 19-32, 1992.
24. HERKENHAM, M., LYNN, A. B., JOHNSON, M. R., MELVIN, L. S., COSTA, B. R., AND RICE, K. C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci. 11: 563-583, 1991.
25. HOWLETT, A. C. Inhibition of neuroblastoma adenylate cyclase by cannabinoid and nantradol compounds. Life Sci. 35: 1803-1810, 1984.
26. HOWLETT, A. C. AND FLEMING, R. M. Cannabinoid inhibition of adenylate cyclase: pharmacology of the response in neuroblastoma cell membranes. Mol. Pharmacol. 26: 532-538, 1984.
27. ITO, M. The Cerebellum and Neural Control. New York: Raven, 1984, p. 36, 77, 84, 108, 112.
28. KANO, M. Synaptic excitation produces a long-lasting rebound potentiation of inhibitory synaptic signals in cerebellar Purkinje cells. Nature 356: 601-604, 1992.
29. KATONA, I., SPERLAGH, B., SIK, A., KÄFALVI, A., VIZI, E. S., MACKIE, K., AND FREUND, T. F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19: 4544-4558, 1999.
30. 1A receptor in the cat's cerebellar cortex. Brain Res. 591: 253-260, 1992.
31. KONISHI, S., MITOMA, H., ISHIDA, M., AND SHINOZAKI, H. Cerebellar GABAergic transmission reciprocally regulated by monoaminergic receptor-operated facilitation and metabotropic glutamate receptor-operated inhibition. Pharmacol. Rev. Comm. 8: 169-172, 1996.
32. KONNERTH, A., LLANO, I., AND ARMSTRONG, C. Synaptic currents in cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA 87: 2662-2665, 1990.
33. LEFKOWITZ, R. J. G Protein-coupled receptors. III. New roles for receptor kinases and β-arrestins in receptor signaling and desensitization. J. Biol. Chem. 273: 18677-18680, 1998.
34. LéVéNèS, C., DANIEL, H., SOUBRIÉ, P., AND CRÉPEL, F. Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J. Physiol. (Lond.) 510: 867-879, 1998.
35. LLANO, I. AND GERSHENFELD, H. M. Inhibitory synaptic currents in stellate cells of rat cerebellar slices. J. Physiol. (Lond.) 468: 177-200, 1993.
36. LLANO, I., MARTY, A., ARMSTRONG, C. M., AND KONNERTH, A. Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J. Physiol. (Lond.) 434: 183-213, 1991.
37. LLINÁS, R. AND SUGIMORI, M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J. Physiol. (Lond.) 305: 171-195, 1980.
38. LOEWE, S. Studies on the pharmacology and acute toxicity of compounds with marihuana activity. J. Pharmacol. Exp. Ther. 88: 154-161, 1946.
39. MACKIE, K. AND HILLE, B. Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc. Natl. Acad. Sci. USA 1992: 3825-3829, 1992.
40. MACKIE, K., LAI, Y., WESTENBROEK, R., AND MITCHEL, R. Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in Att20 cells transfected with rat brain cannabinoid receptor. J. Neurosci. 15: 6552-6561, 1995.
41. MAILLEUX, P. AND VANDERHAEGHEN, J. J. Distribution of neuronal cannabinoid receptor in the adult rat brain: a comparative receptor binding autoradiography and in situ hybridization histochemistry. Neuroscience 48: 655-668, 1992.
42. MATSUDA, L. A., BONNER, T. I., AND LOLIAT, S. J. Localization of cannabinoid receptor mRNA in rat brain. J. Comp. Neural 327: 535-550, 1993.
43. MATSUDA, L. A., LOLAIT, S. J., BROWNSTEIN, M. H., YOUNG, A. C., AND BONNER, T. I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346: 561-564, 1990.
44. MILLER, A. S. AND WALKER, J. M. Effects of cannabinoid on spontaneous and evoked neuronal activity in the substantia nigra pars reticulata. Eur. J. Pharmacol. 279: 179-185, 1995.
45. MILLER, A. S. AND WALKER, J. M. Electrophysiological effects of a cannabinoid on neural activity in the globus pallidus. Eur. J. Pharmacol. 304: 29-35, 1996.
46. MILLER, R. J. Presynaptic receptors. Annu. Rev. Pharmacol. Toxicol. 38: 201-227, 1998.
47. MISNER, D. L. AND SULLIVAN, J. M. Mechanism of cannabinoid effects on long-term potentiation and depression in hippocampal CA1 neurons. J. Neurosci. 19: 6793-6805, 1999.
48. MITOMA, H., KOBAYASHI, T., SONG, S., AND KONISHI, S. Enhancement by serotonin of GABA-mediated inhibitory synaptic currents in rat cerebellar Purkinje cells. Neurosci. Lett. 173: 127-130, 1994.
49. MITOMA, H. AND KONISHI, S. Long-lasting facilitation of inhibitory transmission by monoaminergic and cAMP-dependent mechanism in rat cerebellar GABAergic synapses. Neurosci. Lett. 217: 141-144, 1996
50. MUNRO, S., THOMAS, K., AND ABU-SHAAR, M. Molecular characterization of a peripheral receptor for Cannabinoids. Nature 365: 61-65, 1993.
51. PACHECO, M. A., WARD, S. J., AND CHILDERS, S. R. Identification of cannabinoid receptors in cultures of rat cerebellar granule cells. Brain Res. 603: 102-110, 1993.
52. PALAY, S. L. AND CHAN-PALAY, V. Cerebellar Cortex: Cytology and Organization. Heidelberg: Springer-Verlag Berlin, 1974, p. 199-215.
53. PAULA-BARBOSA, M. M., TAVARES, M. A., RUELA, C., AND BARROCA, H. The distribution of stellate cell descending axons in the rat cerebellum: a Golgi and a combined Golgi-electron microscopical study. J. Anat. 137: 757-764, 1983.
54. PEKHLETSKI, R., GERLAI, R., OVERSTREET, L. S., HUANG, X., AGOPYAN, N., SLATER, N. T., ABRAMOW-NEWERLY, W., RODER, J. C., AND HAMPSON, D. R. Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. J. Neurosci. 16: 6364-6373, 1996.
55. PERKEL, D. J., HESTRIN, S., SAH, P., AND NICOLL, R. Excitatory synaptic currents in Purkinje cells. Proc. R. Soc. Lond. B Biol. Sci. 241: 116-121, 1990.
56. PETTIT, D.A.D., HARRISON, M. P., OLSON, J. M., SPENCER, R. F., AND CABRAL, G. A. Immunohistochemical localization of the neural cannabinoid receptor in rat brain. J. Neurosci. Res. 51: 391-402, 1998.
57. POUZAT, C. AND HESTRIN, S. Developmental regulation of basket/stellate cell → Purkinje cell synapses in the cerebellum. J. Neurosci. 17: 9104-9112, 1997.
58. SESSLER, F. M., MOURADIAN, R. D., CHENG, J., YEH, H. H., LIU, W., AND WATERHOUSE, B. D. Noradrenergic potentiation of cerebellar Purkinje cell responses to GABA: evidence for mediation through the β-adrenoreceptor-coupled cyclic AMP system. Brain Res. 499: 27-38, 1989.
59. SHEN, M. AND THAYER, S. A. The cannabinoid agonist Win55,212-2 inhibits calcium channels by receptor-mediated and direct pathways in cultured rat hippocampal neurons. Brain Res. 783: 77-84, 1998.
60. SHEN, M., PISER, T. M., SEYBOLD, V. S., AND THAYER, S. A. Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J. Neurosci. 16: 4322-4334, 1996.
61. SILVER, R. A., MOMIYAMA, A., AND CULL-CANDY, S. G. Locus of frequency-dependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses. J. Physiol. (Lond.) 510: 881-902, 1998.
62. STRAHLENDORF, J. C., LEE, M., AND STRAHLENDORF, H. K. Serotonin modulates muscimol- and baclofen-elicited inhibition of cerebellar Purkinje cells. Eur. J. Pharmacol. 201: 239-242, 1991.
63. STRATA, P. AND ROSSI, F. Plasticity of the olivocerebellar pathway. Trends Neurosci. 21: 407-413, 1998.
64. SULLIVAN, J. M. Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J. Neurophysiol. 82: 1286-1294, 1999.
65. SZABO, B., DÖRNER, L., PFREUNDTNER, C., NÖRENBERG, W., AND STARKE, K. Inhibition of GABAergic inhibitory postsynaptic currents by cannabinoids in rat corpus striatum. Neuroscience 85: 395-403, 1998.
66. TAKAHASHI, M., KOVALCHUK, Y., AND ATTWELL, D. Pre- and postsynaptic determinants of EPSC waveform at cerebellar climbing fiber and parallel fiber to Purkinje cell synapses. J. Neurosci. 15: 5693-5702, 1995.
67. TERRANOVA, J. P., STORME, J. J., LAFOU, N., PÉRIO, A., RINALDI-CARMONA, M., FUR, G. L., AND SOUBRIÉ, P. Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology (Berl.). 126: 165-172, 1996.
68. TSOU, K., BROWN, S., SAN̄UDO-PEN̄A, J. C., MACKIE, K., AND WALKER, J. M. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83: 393-411, 1998.
69. TWITCHELL, W., BROWN, S., AND MACKIE, K. Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J. Neurophysiol. 78: 43-50, 1997.
70. VAUGHAN, C. W., MCGREGOR, I. S., AND CHRISTIE, M. J. Cannabinoid receptor activation inhibits GABAergic neurotransmission in rostral ventromedial medulla neurons in vitro. Br. J. Pharmacol. 127: 935-940, 1999.
71. VINCENT, P., ARMSTRONG, C. M., AND MARTY, A. Inhibitory synaptic currents in rat cerebellar Purkinje cells: modulation by postsynaptic depolarization. J. Physiol. (Lond.) 456: 453-471, 1992.
72. WU, L. AND SAGGAU, P. Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci. 20: 204-212, 1997.