Retrograde endocannabinoid signaling in the cerebellar cortex

Cerebellum

Volumn 5, Issue 2, 2006, Pages 134-145

  Safo, Patrick ^a   Cravatt, Benjamin ^a   Regehr, Wade ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cerebellar cortex; Endocannabinoid signalling; Parallel fibers

Indexed keywords

ENDOCANNABINOID;

BRAIN FUNCTION; CELL MEMBRANE DEPOLARIZATION; CEREBELLUM CORTEX; CLIMBING FIBER; LONG TERM DEPRESSION; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; REGULATORY MECHANISM; REVIEW; SYNAPSE; SYNAPTIC INHIBITION;

ANIMALS; CEREBELLAR CORTEX; ENDOCANNABINOIDS; HUMANS; INTERNEURONS; NEURAL PATHWAYS; PRESYNAPTIC TERMINALS; PURKINJE CELLS; RECEPTOR, CANNABINOID, CB1; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 33745813913     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1080/14734220600791477     Document Type: Review

References (84)

1. Raymond JL, Lisberger SG, Mauk MD. The cerebellum: A neuronal learning machine? Science. 1996;272(5265):1126-31.
2. Palay SL, Chan-Palay V. Cerebellar cortex. New York: Springer-Verlag; 1974.
3. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol. 2002;64:355-405.
4. Carey M, Lisberger S. Embarrassed, but not depressed: Eye opening lessons for cerebellar learning. Neuron. 2002;35:223-6.
5. Kreitzer AC, Regehr WG. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron. 2001;29:717-27.
6. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron. 2001;31:463-75.
7. Brown SP, Safo PK, Regehr WG. Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci. 2004;24:5623-31.
8. Diana MA, Levenes C, Mackie K, Marty A. Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci. 2002;22:200-8.
9. Egertova M, Elphick MR. Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol. 2000;422:159-71.
10. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci. 1991;11:563-83.
11. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience. 1998;83:393-411.
12. Chevaleyre V, Takahashi KA, Castillo PE. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci. 2006;29:37-75.
13. Llano I, Leresche N, Marty A. Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron. 1991;6:565-74.
14. Vincent P, Armstrong CM, Marty A. Inhibitory synaptic currents in rat cerebellar Purkinje cells: modulation by postsynaptic depolarization. J Physiol. 1992;456:453-71.
15. Pitler TA, Alger BE. Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci. 1992;12:4122-32.
16. Ohno-Shosaku T, Maejima T, Kano M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron. 2001;29:729-38.
17. Wilson RI, Nicoll RA. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature. 2001;410(6828):588-92.
18. Diana MA, Marty A. Endocannabinoid-mediated short-term synaptic plasticity: Depolarization-induced suppression of inhibition (DSI) and depolarization-induced suppression of excitation (DSE). Br J Pharmacol. 2004;142:9-19.
19. Safo PK, Regehr WG. Endocannabinoids control the induction of cerebellar LTD. Neuron. 2005;48:647-59.
20. 2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature. 1995;373(6510):155-8.
21. Neale SA, Garthwaite J, Batchelor AM. mGlu1 receptors mediate a post-tetanic depression at parallel fibre-Purkinje cell synapses in rat cerebellum. Eur J Neurosci. 2001;14:1313-9.
22. Galante M, Diana MA. Group I metabotropic glutamate receptors inhibit GABA release at interneuron-Purkinje cell synapses through endocannabinoid production. J Neurosci. 2004;24(20):4865-74.
23. Maejima T, Oka S, Hashimotodani Y, Ohno-Shosaku T, Aiba A, Wu D, et al. Synaptically driven endocannabinoid release requires Ca2+-assisted metabotropic glutamate receptor subtype 1 to phospholipase Cbeta4 signaling cascade in the cerebellum. J Neurosci. 2005;25(29):6826-35.
24. Knopfel T, Grandes P. Metabotropic glutamate receptors in the cerebellum with a focus on their function in Purkinje cells. Cerebellum. 2002;1:19-26.
25. Freund TF, Katona I, Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev. 2003;83:1017-66.
26. Brown SP, Brenowitz SD, Regehr WG. Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci. 2003;6:1048-57.
27. Batchelor AM, Madge DJ, Garthwaite J. Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience. 1994;63:911-5.
28. Tempia F, Alojado ME, Strata P, Knopfel T. Characterization of the mGluR(1)-mediated electrical and calcium signaling in Purkinje cells of mouse cerebellar slices. J Neurophysiol. 2001;86:1389-97.
29. Marcaggi P, Attwell D. Endocannabinoid signaling depends on the spatial pattern of synapse activation. Nat Neurosci. 2005;8:776-81.
30. Wadiche JI, Jahr CE. Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nat Neurosci. 2005;8:1329-34.
31. Wang SS, Denk W, Hausser M. Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci. 2000;3:1266-73.
32. Denk W, Sugimori M, Llinas R. Two types of calcium response limited to single spines in cerebellar purkinje cells. Proc Natl Acad Sci USA. 1995;92:8279-82.
33. Kreitzer AC, Carter AG, Regehr WG. Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron. 2002;34:787-96.
34. Brenowitz SD, Regehr WG. Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron. 2005;45:419-31.
35. Pertwee RG. The therapeutic potential of drugs that target cannabinoid receptors or modulate the tissue levels or actions of endocannabinoids. Aaps J. 2005;7:E625-54.
36. Stella N, Schweitzer P, Piomelli D. A second endogenous cannabinoid that modulates long-term potentiation. Nature. 1997;388(6644):773-8.
37. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science. 1992;258 (5090):1946-9.
38. Piomelli D. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci. 2003;4:873-84.
39. Ueda N, Okamoto Y, Morishita J. N-acylphosphatidylethanolamine- hydrolyzing phospholipase D: a novel enzyme of the beta-lactamase fold family releasing anandamide and other N-acylethanolamines. Life Sci. 2005;77:1750-8.
40. McKinney MK, Cravatt BF. Structure and function of fatty acid amide hydrolase. Annu Rev Biochem. 2005;74:411-32.
41. Gulyas AI, Cravatt BF, Bracey MH, Dinh TP, Piomelli D, Boscia F, et al. Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci. 2004;20:441-58.
42. Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, et al. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA. 2002;99:10819-24.
43. Breivogel CS, Walker JM, Huang SM, Roy MB, Childers SR. Cannabinoid signaling in rat cerebellar granule cells: G-protein activation, inhibition of glutamate release and endogenous cannabinoids. Neuropharmacology. 2004;47:81-91.
44. Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, et al. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci USA. 2001;98:9371-6.
45. Hohmann AG, Suplita RL, Bolton NM, Neely MH, Fegley D, Mangieri R, et al. An endocannabinoid mechanism for stress-induced analgesia. Nature. 2005;435(7045):1108-12.
46. Brenowitz SD, Regehr WG. Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci. 2003;23:6373-84.
47. Diana MA, Marty A. Characterization of depolarization-induced suppression of inhibition using paired interneuron - Purkinje cell recordings. J Neurosci. 2003;23:5906-18.
48. Chadderton P, Margrie TW, Hausser M. Integration of quanta in cerebellar granule cells during sensory processing. Nature. 2004;428(6985):856-60.
49. Kitazawa S, Kimura T, Yin PB. Cerebellar complex spikes encode both destinations and errors in arm movements. Nature. 1998;392(6675):494-7.
50. Schultz W, Dickinson A. Neuronal coding of prediction errors. Annu Rev Neurosci. 2000;23:473-500.
51. 2+ kinetics in rodent Purkinje cells: role of parvalbumin and calbindin D28k. J Physiol. 2003;551(Pt 1):13-32.
52. Tank DW, Sugimori M, Connor JA, Llinas RR. Spatially resolved calcium dynamics of mammalian Purkinje cells in cerebellar slice. Science. 1988;242(4879):773-7.
53. Ito M. Cerebellar long-term depression: Characterization, signal transduction, and functional roles. Physiol Rev. 2001;81:1143-95.
54. Levenes C, Daniel H, Soubrie P, Crepel F. Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J Physiol. 1998;510(Pt 3):867-79.
55. Daniel H, Levenes C, Crepel F. Cellular mechanisms of cerebellar LTD. Trends Neurosci. 1998;21:401-7.
56. Sakurai M. Calcium is an intracellular mediator of the climbing fiber in induction of cerebellar long-term depression. Proc Nad Acad Sci USA. 1990;87:3383-5.
57. Ito M. Long-term depression. Annu Rev Neurosci. 1989;12:85-102.
58. Kano M, Kato M. Quisqualate receptors are specifically involved in cerebellar synaptic plasticity. Nature. 1987;325(6101):276-9.
59. Ekerot CF, Kano M. Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res. 1985;342:357-60.
60. Wang SS, Khiroug L, Augustine GJ. Quantification of spread of cerebellar long-term depression with chemical two-photon uncaging of glutamate. Proc Nad Acad Sci USA. 2000;97:8635-40.
61. Reynolds T, , Hartell NA. An evaluation of the synapse specificity of long-term depression induced in rat cerebellar slices. J Physiol. 2000;527 Pt 3:563-77.
62. Hartell NA. Strong activation of parallel fibers produces localized calcium transients and a form of LTD that spreads to distant synapses. Neuron. 1996;16:601-10.
63. Gerdeman GL, Ronesi J, Lovinger DM. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci. 2002;5:446-51.
64. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Nad Acad Sci USA. 2002;99:8384-8.
65. Sjostrom PJ, Turrigiano GG, Nelson SB. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron. 2003;39:641-54.
66. Chevaleyre V, Castillo PE. Heterosynaptic LTD of hippocampal GABAergic synapses: A novel role of endocannabinoids in regulating excitability. Neuron. 2003;38:461-72.
67. Kreitzer AC, Malenka RC. Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J Neurosci. 2005;25:10537-45.
68. Shibuki K, Okada D. Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature. 1991;349(6307):326-8.
69. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, et al. Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell. 1994;79:377-88.
70. 2+ in the induction of cerebellar long-term depression. Neuron. 1997;18:1025-38.
71. Stefano GB, Esch T, Cadet P, Zhu W, Mantione K, Benson H. Endocannabinoids as autoregulatory signaling molecules: Coupling to nitric oxide and a possible association with the relaxation response. Med Sci Monit. 2003;9:RA63-75.
72. Deutsch DG, Goligorsky MS, Schmid PC, Krebsbach RJ, Schmid HH, Das SK, et al. Production and physiological actions of anandamide in the vasculature of the rat kidney. J Clin Invest. 1997;100:1538-46.
73. Hillard CJ, Muthian S, Kearn CS. Effects of CB (1) cannabinoid receptor activation on cerebellar granule cell nitric oxide synthase activity. FEBS Lett. 1999;459:277-81.
74. Shin JH, Linden DJ. An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. J Neurophysiol. 2005;94:4281-9.
75. Kreitzer AC, Regehr WG. Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci. 2001;21:RC174.
76. Takahashi KA, Linden DJ. Cannabinoid receptor modulation of synapses received by cerebellar Purkinje cells. J Neurophysiol. 2000;83:1167-80.
77. 2+ rise are selectively suppressed by cannabinoid receptor activation in cerebellar Purkinje cells. J Neurosci. 2006;26:86-95.
78. Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci USA. 1999;96:5780-5.
79. Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, et al. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science., 1999;283(5400):401-4.
80. Kawato M, Gomi H. The cerebellum and VOR/OKR learning models. Trends Neurosci. 1992;15:445-53.
81. Ito M. The cerebellum and neural control. New York: Raven Press; 1984.
82. Nakamura M, Sato K, Fukaya M, Araishi K, Aiba A, Kano M, et al. Signaling complex formation of phospholipase Cbeta4 with metabotropic glutamate receptor type 1alpha and 1,4,5-trisphosphate receptor at the perisynapse and endoplasmic reticulum in the mouse brain. Eur J Neurosci. 2004;20:2929-44.
83. Miyata M, Kim HT, Hashimoto K, Lee TK, Cho SY, Jiang H, et al. Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C beta4 mutant mice. Eur J Neurosci. 2001;13:1945-54.
84. Turrigiano GG, Nelson SB. Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol. 2000;10:358-64.