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Cannabinoids and Synaptic Transmission in the Cerebellum

  • Michael H. Myoga
  • Wade G. Regehr
Reference work entry

Abstract

Endocannabinoids (eCBs) are retrograde messengers that regulate the strength of synapses throughout the brain. eCB signaling is prominent within the cerebellar cortex, where multiple types of neurons release eCBs in a calcium-dependent manner. Liberated eCBs suppress synaptic strength on both short and long timescales by retrogradely activating CB1 cannabinoid receptors (CB1Rs) on presynaptic terminals. The chapter will discuss mechanisms that control eCB release, the consequences of eCB signaling in the cerebellar cortex and the role of the eCB system in cerebellar function.

Keywords

Cerebellar Cortex Inferior Olive Deep Cerebellar Nucleus Eyeblink Conditioning Cerebellar Function 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377–388PubMedCrossRefGoogle Scholar
  2. Bacci A, Huguenard JR, Prince DA (2004) Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431:312–316PubMedCrossRefGoogle Scholar
  3. Beierlein M, Regehr WG (2006) Local interneurons regulate synaptic strength by retrograde release of endocannabinoids. J Neurosci 26:9935–9943PubMedCrossRefGoogle Scholar
  4. Beierlein M, Fioravante D, Regehr WG (2007) Differential expression of posttetanic potentiation and retrograde signaling mediate target-dependent short-term synaptic plasticity. Neuron 54:949–959PubMedCrossRefGoogle Scholar
  5. Best AR, Regehr WG (2008) Serotonin evokes endocannabinoid release and retrogradely suppresses excitatory synapses. J Neurosci 28:6508–6515PubMedCrossRefGoogle Scholar
  6. Bouaboula M, Poinot-Chazel C, Bourrie B, Canat X, Calandra B, Rinaldi-Carmona M, Le Fur G, Casellas P (1995) Activation of mitogen-activated protein kinases by stimulation of the central cannabinoid receptor CB1. Biochem J 312(Pt 2):637–641PubMedGoogle Scholar
  7. Brenowitz SD, Regehr WG (2003) Calcium dependence of retrograde inhibition by endocannabinoids at synapses onto Purkinje cells. J Neurosci 23:6373–6384PubMedGoogle Scholar
  8. Brenowitz SD, Regehr WG (2005) Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 45:419–431PubMedCrossRefGoogle Scholar
  9. Brenowitz SD, Best AR, Regehr WG (2006) Sustained elevation of dendritic calcium evokes widespread endocannabinoid release and suppression of synapses onto cerebellar Purkinje cells. J Neurosci 26:6841–6850PubMedCrossRefGoogle Scholar
  10. Brown SP, Brenowitz SD, Regehr WG (2003) Brief presynaptic bursts evoke synapse-specific retrograde inhibition mediated by endogenous cannabinoids. Nat Neurosci 6:1048–1057PubMedCrossRefGoogle Scholar
  11. Brown SP, Safo PK, Regehr WG (2004) Endocannabinoids inhibit transmission at granule cell to Purkinje cell synapses by modulating three types of presynaptic calcium channels. J Neurosci 24:5623–5631PubMedCrossRefGoogle Scholar
  12. Cadas H, di Tomaso E, Piomelli D (1997) Occurrence and biosynthesis of endogenous cannabinoid precursor, N-arachidonoyl phosphatidylethanolamine, in rat brain. J Neurosci 17:1226–1242PubMedGoogle Scholar
  13. Carey MR, Myoga MH, McDaniels KR, Marsicano G, Lutz B, Mackie K, Regehr WG (2010) Presynaptic CB1 receptors regulate synaptic plasticity at cerebellar parallel fiber synapses. J Neurophysiol 105:958–963PubMedCrossRefGoogle Scholar
  14. Chavez AE, Chiu CQ, Castillo PE (2010) TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Nat Neurosci 13:1511–1518PubMedCrossRefGoogle Scholar
  15. Chen C, Regehr WG (1997) The mechanism of cAMP-mediated enhancement at a cerebellar synapse. J Neurosci 17:8687–8694PubMedGoogle Scholar
  16. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461–472PubMedCrossRefGoogle Scholar
  17. Chevaleyre V, Takahashi KA, Castillo PE (2006) Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 29:37–76PubMedCrossRefGoogle Scholar
  18. Colleran K, Pai H (2007) Rimonabant: a novel approach for the treatment of obesity and cardiometabolic risk by blockade of the endocannabinoid system. Future Cardiol 3:497–505PubMedCrossRefGoogle Scholar
  19. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384:83–87PubMedCrossRefGoogle Scholar
  20. Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, Lichtman AH (2001) Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci USA 98:9371–9376PubMedCrossRefGoogle Scholar
  21. Cristino L, Starowicz K, De Petrocellis L, Morishita J, Ueda N, Guglielmotti V, Di Marzo V (2008) Immunohistochemical localization of anabolic and catabolic enzymes for anandamide and other putative endovanilloids in the hippocampus and cerebellar cortex of the mouse brain. Neuroscience 151:955–968PubMedCrossRefGoogle Scholar
  22. Daniel H, Levenes C, Crepel F (1998) Cellular mechanisms of cerebellar LTD. Trends Neurosci 21:401–407PubMedCrossRefGoogle Scholar
  23. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946–1949PubMedCrossRefGoogle Scholar
  24. Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 99:10819–10824PubMedCrossRefGoogle Scholar
  25. Dittman JS, Regehr WG (1996) Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J Neurosci 16:1623–1633PubMedGoogle Scholar
  26. 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 422:159–171PubMedCrossRefGoogle Scholar
  27. Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5:446–451PubMedGoogle Scholar
  28. Grueter BA, Brasnjo G, Malenka RC (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat Neurosci 13:1519–1525PubMedCrossRefGoogle Scholar
  29. Gulyas AI, Cravatt BF, Bracey MH, Dinh TP, Piomelli D, Boscia F, Freund TF (2004) Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci 20:441–458PubMedCrossRefGoogle Scholar
  30. Hanus L, Gopher A, Almog S, Mechoulam R (1993) Two new unsaturated fatty acid ethanolamides in brain that bind to the cannabinoid receptor. J Med Chem 36:3032–3034PubMedCrossRefGoogle Scholar
  31. Hanus L, Abu-Lafi S, Fride E, Breuer A, Vogel Z, Shalev DE, Kustanovich I, Mechoulam R (2001) 2-arachidonyl glyceryl ether, an endogenous agonist of the cannabinoid CB1 receptor. Proc Natl Acad Sci USA 98:3662–3665PubMedCrossRefGoogle Scholar
  32. Hashimotodani Y, Ohno-Shosaku T, Tsubokawa H, Ogata H, Emoto K, Maejima T, Araishi K, Shin HS, Kano M (2005) Phospholipase Cbeta serves as a coincidence detector through its Ca2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45:257–268PubMedCrossRefGoogle Scholar
  33. Heishman SJ, Huestis MA, Henningfield JE, Cone EJ (1990) Acute and residual effects of marijuana: profiles of plasma THC levels, physiological, subjective, and performance measures. Pharmacol Biochem Behav 37:561–565PubMedCrossRefGoogle Scholar
  34. Henry DJ, Chavkin C (1995) Activation of inwardly rectifying potassium channels (GIRK1) by co-expressed rat brain cannabinoid receptors in Xenopus oocytes. Neurosci Lett 186:91–94PubMedCrossRefGoogle Scholar
  35. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci 11:563–583PubMedGoogle Scholar
  36. Hillard CJ, Muthian S, Kearn CS (1999) Effects of CB(1) cannabinoid receptor activation on cerebellar granule cell nitric oxide synthase activity. FEBS Lett 459:277–281PubMedCrossRefGoogle Scholar
  37. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International union of pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161–202PubMedCrossRefGoogle Scholar
  38. Ito M (1989) Long-term depression. Annu Rev Neurosci 12:85–102PubMedCrossRefGoogle Scholar
  39. Ito M (2001) Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev 81:1143–1195PubMedGoogle Scholar
  40. Janowsky DS, Meacham MP, Blaine JD, Schoor M, Bozzetti LP (1976) Marijuana effects on simulated flying ability. Am J Psychiatry 133:384–388PubMedGoogle Scholar
  41. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309–380PubMedCrossRefGoogle Scholar
  42. Kishimoto Y, Kano M (2006) Endogenous cannabinoid signaling through the CB1 receptor is essential for cerebellum-dependent discrete motor learning. J Neurosci 26:8829–8837PubMedCrossRefGoogle Scholar
  43. Kreitzer AC, Malenka RC (2005) Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J Neurosci 25:10537–10545PubMedCrossRefGoogle Scholar
  44. Kreitzer AC, Regehr WG (2001a) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717–727PubMedCrossRefGoogle Scholar
  45. Kreitzer AC, Regehr WG (2001b) Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21:RC174PubMedGoogle Scholar
  46. Kreitzer AC, Carter AG, Regehr WG (2002) Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum. Neuron 34:787–796PubMedCrossRefGoogle Scholar
  47. Lev-Ram V, Jiang T, Wood J, Lawrence DS, Tsien RY (1997) Synergies and coincidence requirements between NO, cGMP, and Ca2+ in the induction of cerebellar long-term depression. Neuron 18:1025–1038PubMedCrossRefGoogle Scholar
  48. Liguori A, Gatto CP, Robinson JH (1998) Effects of marijuana on equilibrium, psychomotor performance, and simulated driving. Behav Pharmacol 9:599–609PubMedCrossRefGoogle Scholar
  49. 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 6:565–574PubMedCrossRefGoogle Scholar
  50. Mackie K (2005) Distribution of cannabinoid receptors in the central and peripheral nervous system. Handb Exp Pharmacol 168:299–325PubMedCrossRefGoogle Scholar
  51. Mackie K (2008) Cannabinoid receptors: where they are and what they do. J Neuroendocrinol 20(Suppl 1):10–14PubMedCrossRefGoogle Scholar
  52. Mackie K, Hille B (1992) Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci USA 89:3825–3829PubMedCrossRefGoogle Scholar
  53. Mackie K, Lai Y, Westenbroek R, Mitchell R (1995) Cannabinoids activate an inwardly rectifying potassium conductance and inhibit Q-type calcium currents in AtT20 cells transfected with rat brain cannabinoid receptor. J Neurosci 15:6552–6561PubMedGoogle Scholar
  54. Maeda H, Ellis-Davies GC, Ito K, Miyashita Y, Kasai H (1999) Supralinear Ca2+ signaling by cooperative and mobile Ca2+ buffering in Purkinje neurons. Neuron 24:989–1002PubMedCrossRefGoogle Scholar
  55. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463–475PubMedCrossRefGoogle Scholar
  56. Maejima T, Oka S, Hashimotodani Y, Ohno-Shosaku T, Aiba A, Wu D, Waku K, Sugiura T, Kano M (2005) Synaptically driven endocannabinoid release requires Ca2+ −assisted metabotropic glutamate receptor subtype 1 to phospholipase Cbeta4 signaling cascade in the cerebellum. J Neurosci 25:6826–6835PubMedCrossRefGoogle Scholar
  57. Marinelli S, Pacioni S, Bisogno T, Di Marzo V, Prince DA, Huguenard JR, Bacci A (2008) The endocannabinoid 2-arachidonoylglycerol is responsible for the slow self-inhibition in neocortical interneurons. J Neurosci 28:13532–13541PubMedCrossRefGoogle Scholar
  58. Martina M, Metz AE, Bean BP (2007) Voltage-dependent potassium currents during fast spikes of rat cerebellar Purkinje neurons: inhibition by BDS-I toxin. J Neurophysiol 97:563–571PubMedCrossRefGoogle Scholar
  59. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561–564PubMedCrossRefGoogle Scholar
  60. Mechoulam R, Gaoni Y (1965) A total synthesis of DL-delta-1-tetrahydrocannabinol, the active constituent of hashish. J Am Chem Soc 87:3273–3275PubMedCrossRefGoogle Scholar
  61. Mechoulam R, Ben-Shabat S, Hanus L, Ligumsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR et al (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50:83–90PubMedCrossRefGoogle Scholar
  62. Miyata M, Kim HT, Hashimoto K, Lee TK, Cho SY, Jiang H, Wu Y, Jun K, Wu D, Kano M, Shin HS (2001) Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C beta4 mutant mice. Eur J Neurosci 13:1945–1954PubMedCrossRefGoogle Scholar
  63. Moreira FA, Crippa JA (2009) The psychiatric side-effects of rimonabant. Rev Bras Psiquiatr 31:145–153PubMedCrossRefGoogle Scholar
  64. Myoga MH, Beierlein M, Regehr WG (2009) Somatic spikes regulate dendritic signaling in small neurons in the absence of backpropagating action potentials. J Neurosci 29:7803–7814PubMedCrossRefGoogle Scholar
  65. Myoga MH, Regehr WG (2011) Calcium microdomains near R-type calcium channels control the induction of presynaptic long-term potentiation at parallel fiber to purkinje cell synapses. J Neurosci 31:5235–5243PubMedCrossRefGoogle Scholar
  66. Nakamura M, Sato K, Fukaya M, Araishi K, Aiba A, Kano M, Watanabe M (2004) 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 20:2929–2944PubMedCrossRefGoogle Scholar
  67. Neher E, Sakaba T (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59:861–872PubMedCrossRefGoogle Scholar
  68. Offermanns S, Hashimoto K, Watanabe M, Sun W, Kurihara H, Thompson RF, Inoue Y, Kano M, Simon MI (1997) Impaired motor coordination and persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking Galphaq. Proc Natl Acad Sci USA 94:14089–14094PubMedCrossRefGoogle Scholar
  69. Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:729–738PubMedCrossRefGoogle Scholar
  70. Ohno-Shosaku T, Shosaku J, Tsubokawa H, Kano M (2002) Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur J Neurosci 15:953–961PubMedCrossRefGoogle Scholar
  71. Palay SL, Chan-Palay V (1974) Cerebellar cortex. Springer, New YorkCrossRefGoogle Scholar
  72. Pang DS, Robledo CJ, Carr DR, Gent TC, Vyssotski AL, Caley A, Zecharia AY, Wisden W, Brickley SG, Franks NP (2009) An unexpected role for TASK-3 potassium channels in network oscillations with implications for sleep mechanisms and anesthetic action. Proc Natl Acad Sci USA 106:17546–17551PubMedCrossRefGoogle Scholar
  73. Pertwee RG (2007) GPR55: a new member of the cannabinoid receptor clan? Br J Pharmacol 152:984–986PubMedCrossRefGoogle Scholar
  74. Pitler TA, Alger BE (1992) Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci 12:4122–4132PubMedGoogle Scholar
  75. Raymond JL, Lisberger SG, Mauk MD (1996) The cerebellum: a neuronal learning machine? Science 272:1126–1131PubMedCrossRefGoogle Scholar
  76. Rebecchi MJ, Pentyala SN (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80:1291–1335PubMedGoogle Scholar
  77. 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 99:8384–8388PubMedCrossRefGoogle Scholar
  78. Ronesi J, Gerdeman GL, Lovinger DM (2004) Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J Neurosci 24:1673–1679PubMedCrossRefGoogle Scholar
  79. Safo PK, Regehr WG (2005) Endocannabinoids control the induction of cerebellar LTD. Neuron 48:647–659PubMedCrossRefGoogle Scholar
  80. Safo PK, Cravatt BF, Regehr WG (2006) Retrograde endocannabinoid signaling in the cerebellar cortex. Cerebellum 5:134–145PubMedCrossRefGoogle Scholar
  81. Salin PA, Malenka RC, Nicoll RA (1996) Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16:797–803PubMedCrossRefGoogle Scholar
  82. Sawzdargo M, Nguyen T, Lee DK, Lynch KR, Cheng R, Heng HH, George SR, O’Dowd BF (1999) Identification and cloning of three novel human G protein-coupled receptor genes GPR52, PsiGPR53 and GPR55: GPR55 is extensively expressed in human brain. Brain Res Mol Brain Res 64:193–198PubMedCrossRefGoogle Scholar
  83. Schlicker E, Kathmann M (2001) Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol Sci 22:565–572PubMedCrossRefGoogle Scholar
  84. Schonewille M, Belmeguenai A, Koekkoek SK, Houtman SH, Boele HJ, van Beugen BJ, Gao Z, Badura A, Ohtsuki G, Amerika WE, Hosy E, Hoebeek FE, Elgersma Y, Hansel C, De Zeeuw CI (2010) Purkinje cell-specific knockout of the protein phosphatase PP2B impairs potentiation and cerebellar motor learning. Neuron 67:618–628PubMedCrossRefGoogle Scholar
  85. Shibuki K, Okada D (1991) Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349:326–328PubMedCrossRefGoogle Scholar
  86. Sjostrom PJ, Turrigiano GG, Nelson SB (2003) Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641–654PubMedCrossRefGoogle Scholar
  87. Skosnik PD, Edwards CR, O’Donnell BF, Steffen A, Steinmetz JE, Hetrick WP (2008) Cannabis use disrupts eyeblink conditioning: evidence for cannabinoid modulation of cerebellar-dependent learning. Neuropsychopharmacology 33:1432–1440PubMedCrossRefGoogle Scholar
  88. Soler-Llavina GJ, Sabatini BL (2006) Synapse-specific plasticity and compartmentalized signaling in cerebellar stellate cells. Nat Neurosci 9:798–806PubMedCrossRefGoogle Scholar
  89. Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388:773–778PubMedCrossRefGoogle Scholar
  90. Storm DR, Hansel C, Hacker B, Parent A, Linden DJ (1998) Impaired cerebellar long-term potentiation in type I adenylyl cyclase mutant mice. Neuron 20:1199–1210PubMedCrossRefGoogle Scholar
  91. Suarez J, Bermudez-Silva FJ, Mackie K, Ledent C, Zimmer A, Cravatt BF, de Fonseca FR (2008) Immunohistochemical description of the endogenous cannabinoid system in the rat cerebellum and functionally related nuclei. J Comp Neurol 509:400–421PubMedCrossRefGoogle Scholar
  92. Suhara Y, Takayama H, Nakane S, Miyashita T, Waku K, Sugiura T (2000) Synthesis and biological activities of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand, and its metabolically stable ether-linked analogues. Chem Pharm Bull 48:903–907PubMedCrossRefGoogle Scholar
  93. Tanimura A, Yamazaki M, Hashimotodani Y, Uchigashima M, Kawata S, Abe M, Kita Y, Hashimoto K, Shimizu T, Watanabe M, Sakimura K, Kano M (2010) The endocannabinoid 2-arachidonoylglycerol produced by diacylglycerol lipase alpha mediates retrograde suppression of synaptic transmission. Neuron 65:320–327PubMedCrossRefGoogle Scholar
  94. van Beugen BJ, Nagaraja RY, Hansel C (2006) Climbing fiber-evoked endocannabinoid signaling heterosynaptically suppresses presynaptic cerebellar long-term potentiation. J Neurosci 26:8289–8294PubMedCrossRefGoogle Scholar
  95. Vincent P, Marty A (1993) Neighboring cerebellar Purkinje cells communicate via retrograde inhibition of common presynaptic interneurons. Neuron 11:885–893PubMedCrossRefGoogle Scholar
  96. Wang SS, Denk W, Hausser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3:1266–1273PubMedCrossRefGoogle Scholar
  97. Wang H, Pineda VV, Chan GC, Wong ST, Muglia LJ, Storm DR (2003) Type 8 adenylyl cyclase is targeted to excitatory synapses and required for mossy fiber long-term potentiation. J Neurosci 23:9710–9718PubMedGoogle Scholar
  98. Wayman GA, Impey S, Wu Z, Kindsvogel W, Prichard L, Storm DR (1994) Synergistic activation of the type I adenylyl cyclase by Ca2+ and Gs-coupled receptors in vivo. J Biol Chem 269:25400–25405PubMedGoogle Scholar
  99. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA (1994) Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265:1878–1882PubMedCrossRefGoogle Scholar
  100. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signaling at hippocampal synapses. Nature 410:588–592PubMedCrossRefGoogle Scholar
  101. Wong ST, Athos J, Figueroa XA, Pineda VV, Schaefer ML, Chavkin CC, Muglia LJ, Storm DR (1999) Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23:787–798PubMedCrossRefGoogle Scholar
  102. Yoshida T, Fukaya M, Uchigashima M, Miura E, Kamiya H, Kano M, Watanabe M (2006) 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 26:4740–4751PubMedCrossRefGoogle Scholar
  103. Zalutsky RA, Nicoll RA (1990) Comparison of two forms of long-term potentiation in single hippocampal neurons. Science 248:1619–1624PubMedCrossRefGoogle Scholar
  104. Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci USA 96:5780–5785PubMedCrossRefGoogle Scholar
  105. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452–457PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of NeurobiologyHarvard Medical SchoolBostonUSA

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