Synaptic targets of Δ9-tetrahydrocannabinol in the central nervous system

Cold Spring Harbor Perspectives in Medicine

Volumn 3, Issue 8, 2013, Pages

  Hoffman, Alexander F ^a   Lupica, Carl R ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR AGONIST; DRONABINOL; PSYCHOTROPIC AGENT;

ANIMAL; ARTICLE; CANNABIS ADDICTION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CORPUS STRIATUM; DRUG EFFECT; EVIDENCE BASED MEDICINE; HIPPOCAMPUS; HUMAN; METABOLISM; NUCLEUS ACCUMBENS; SYNAPTIC TRANSMISSION;

ANIMALS; CANNABINOID RECEPTOR AGONISTS; CENTRAL NERVOUS SYSTEM; CEREBELLUM; CORPUS STRIATUM; DRONABINOL; EVIDENCE-BASED MEDICINE; HIPPOCAMPUS; HUMANS; MARIJUANA ABUSE; NUCLEUS ACCUMBENS; PSYCHOTROPIC DRUGS; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; RECEPTORS, CANNABINOID; SYNAPTIC TRANSMISSION;

EID: 84881052672     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a012237     Document Type: Article

References (109)

1. Abel EL. 1970. Marijuana and memory. Nature 227: 1151-1152.
2. Adams IB, Martin BR. 1996. Cannabis: Pharmacology and toxicology in animals and humans. Addiction 91: 1585-1614.
3. Alger BE. 2002. Retrograde signaling in the regulation of synaptic transmission: Focus on endocannabinoids. Prog Neurobiol 68: 247-286.
4. Alger BE, Kim J. 2011. Supply and demand for endocanna-binoids. Trends Neurosci 34: 304-315.
5. American Psychiatric Association. 2000. DSM-IV-TR diagnostic and statistical manual of mental disorders. American Psychratric Association, Arlington, VA.
6. Argilli E, Sibley DR, Malenka RC, England PM, Bonci A. 2008. Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J Neurosci 28: 9092-9100.
7. Atwood BK, Mackie K. 2010. CB2: A cannabinoid receptor with an identity crisis. Br J Pharmacol 160: 467-479.
8. Benard G, Massa F, Puente N, Lourenco J, Bellocchio L, Soria-Gomez E, Matias I, Delamarre A, Metna-Laurent M, Cannich A, et al. 2012. Mitochondrial CB1 receptors regulate neuronal energy metabolism. Nat Neu-rosci 15: 558-564.
9. Bird CM, Burgess N. 2008. The hippocampus and memory: Insights from spatial processing. Nat Rev Neurosci 9: 182-194.
10. Bolla KI, Brown K, Eldreth D, Tate K, Cadet JL. 2002. Dose-related neurocognitive effects of marijuana use. Neurology 59: 1337-1343.
11. 9-tetrahydrocan-nabinol treatment produces a time-dependent loss of cannabinoid receptors and cannabinoid receptor-activated G proteins in rat brain. J Neurochem 73: 2447-2459.
12. Brown TM, Brotchie JM, Fitzjohn SM. 2003. Cannabinoids decrease corticostriatal synaptic transmission via an effect on glutamate uptake. J Neurosci 23: 11073-11077.
13. Burgess N, Maguire EA, O'Keefe J. 2002. The human hippocampus and spatial and episodic memory. Neuron 35: 625-641.
14. Carlson G, Wang Y, Alger BE. 2002. Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat Neurosci 5: 723-724.
15. Centonze D, Gubellini P, Picconi B, Calabresi P, Giacomini P, Bernardi G. 1999. Unilateral dopamine denervation blocks corticostriatal LTP. J Neurophysiol 82: 3575-3579.
16. Chen BT, Hopf FW, Bonci A. 2010. Synaptic plasticity in the mesolimbic system: Therapeutic implications for infstance abuse. Ann NYAcad Sci 1187: 129-139.
17. Chevaleyre V, Castillo PE. 2003. Heterosynaptic LTD of hip-pocampal GABAergic synapses. A novel role of endocan-nabinoids in regulating excitability. Neuron 38: 461-472.
18. Chevaleyre V, Takahashi KA, Castillo PE. 2006. Endocanna-binoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 29: 37-76.
19. 9-tetrahydrocannabinol on GABAA receptor-mediated responses in a grease-gap recording preparation of the rat hippocampal slice. Neuropharmacology 36: 1387-1392.
20. Crean RD, Crane NA, Mason BJ. 2011. An evidence based review of acute and long-term effects of cannabis use on executive cognitive functions. J Addict Med 5: 1-8.
21. De Petrocellis L, Di Marzo V. 2010. Non-CB1, non-CB2 receptors for endocannabinoids, plant cannabinoids, and synthetic cannabimimetics: Focus on G-protein-coupled receptors and transient receptor potential channels. J Neuroimmune Pharmacol 5: 103-121.
22. Devane WA, Dysarz FA, Johnson MR, Melvin LS, How-lett AC. 1988. Determination and characterization of a cannabinoid receptor in rat brain. Mol Pharmacol 34: 605-613.
23. Drew WG, Miller LL. 1974. Cannabis: Neural mechanisms and behavior-A theoretical review. Pharmacology 11: 12-32.
24. Edwards CR, Skosnik PD. 2007. Cerebellar-dependent learning as a neurobehavioral index of the cannabinoid system. Crit Rev Neurobiol 19: 29-57.
25. Everitt BJ, Belin D, Economidou D, Pelloux Y, Dalley JW, Robbins TW. 2008. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans R Soc B: Biol Sci 363: 3125-3135.
26. 9-THC exposure-impaired hip-pocampal synaptic plasticity. J Neurochem 112: 691-702.
27. 9-THC and 17-b-estradiol in hippocampus. Brain Res Bull 8: 341-345.
28. Gaoni Y, Mechoulam R. 1964. Isolation, structure, and partial synthesis of an active constituent of hashish. J Am Chem Soc 86: 1646-1647.
29. Gerdeman G, Lovinger DM. 2001. CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorso-lateral striatum. J Neurophysiol 85: 468-471.
30. Gerdeman GL, Ronesi J, Lovinger DM. 2002. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5: 446-451.
31. Gerdeman GL, Partridge JG, Lupica CR, Lovinger DM. 2003. It could be habit forming: Drugs of abuse and striatal synaptic plasticity. Trends Neurosci 26: 184-192.
32. Good CH, Lupica CR. 2010. Afferent-specific AMPA receptor infunit composition and regulation of synaptic plasticity in midbrain dopamine neurons by abused drugs. J Neurosci 30: 7900-7909.
33. Hajos N, Katona I, Naiem SS, Mackie K, Ledent C, Mody I, Freund TF. 2000. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12: 3239-3249.
34. Hall W, Degenhardt L. 2009. Adverse health effects of non-medical cannabis use. Lancet 374: 1383-1391.
35. Hazekamp A, Verpoorte R. 2006. Structure elucidation of the tetrahydrocannabinol complex with randomly methylated b-cyclodextrin. Euro J Pharm Sci 29: 340-347.
36. 9-Tetrahydrocannabinol and endogenous cannabinoid anandamide directly potentiate the function of glycine receptors. Mol Pharmacol 69: 991-997.
37. Hilario MR, Clouse E, Yin HH, Costa RM. 2007. Endocan-nabinoid signaling is critical for habit formation. Front Integr Neurosci 1: 6.
38. Hoffman AF, Lupica CR. 2000. Mechanisms of cannabinoid inhibition of GABAA synaptic transmission in the hippocampus. J Neurosci 20: 2470-2479.
39. Hoffman AF, Lupica CR. 2001. Direct actions of cannabi-noids on synaptic transmission in the nucleus accum-bens: A comparison with opioids. J Neurophysiol 85: 72-83.
40. Hoffman AF, Oz M, Caulder T, Lupica CR. 2003. Functional tolerance and blockade of long-term depression at synapses in the nucleus accumbens after chronic cannabi-noid exposure. J Neurosci 23: 4815-4820.
41. 9-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation. Learn Mem 14: 63-74.
42. Hoffman AF, Laaris N, Kawamura M, Masino SA, Lupica CR. 2010. Control of cannabinoid CB1 receptor function on glutamate axon terminals by endogenous adenosine acting at A1 receptors. J Neurosci 30: 545-555.
43. Howlett AC, Bidaut-Russell M, Devane WA, Melvin LS, Johnson MR, Herkenham M. 1990. The cannabinoid receptor: Biochemical, anatomical and behavioral characterization. Trends Neurosc 13: 420-423.
44. Hoyer D, Boddeke HW. 1993. Partial agonists, full agonists, antagonists: Dilemmas of definition. Trends Pharmacol Sci 14: 270-275.
45. Huestis MA, Gorelick DA, Heishman SJ, Preston KL, Nelson RA, Moolchan ET, Frank RA. 2001. Blockade of effects of smoked marijuana by the CB1-selective canna-binoid receptor antagonist SR141716. Arch Gen Psychiatry 58: 322-328.
46. 9-tetrahydrocannabinol. Br J Pharmacol 125: 1567-1577.
47. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchiga-shima M, Watanabe M. 2009. Endocannabinoid-mediat-ed control of synaptic transmission. Physiol Rev 89: 309-380.
48. Kauer JA, Malenka RC. 2007. Synaptic plasticity and addiction. Nat Rev Neurosci 8: 844-858.
49. Kawamura Y, Fukaya M, Maejima T, Yoshida T, Miura E, Watanabe M, Ohno-Shosaku T, Kano M. 2006. The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 26: 2991-3001.
50. Kortleven C, Fasano C, Thibault D, Lacaille JC, Trudeau LE. 2011. The endocannabinoid 2-arachidonoylglycerol inhibits long-term potentiation of glutamatergic synapses onto ventral tegmental area dopamine neurons in mice. Eur J Neurosci 33: 1751-1760.
51. Kreitzer AC. 2009. Physiology and pharmacology of striatal neurons. Annu Rev Neurosci 32: 127-147.
52. Kreitzer AC, Carter AG, Regehr WG. 2002. Inhibition of interneuron firing extends the spread of endocannabi-noid signaling in the cerebellum. Neuron 34: 787-796.
53. 9-Tetrahydrocan-nabinol is a full agonist at CB1 receptors on GABA neuron axon terminals in the hippocampus. Neuropharma-cology 59: 121-127.
54. Levenes C, Daniel H, Soubrie P, Crepel F. 1998. Cannabi-noids decrease excitatory synaptic transmission and impair long- term depression in rat cerebellar Purkinje cells. J Physiol (Lond) 510: 867-879.
55. Leweke FM, Koethe D. 2008. Cannabis and psychiatric disorders: It is not only addiction. Addict Biol 13: 264-275.
56. Louise Faber ES. 2009. Functions and modulation of neu-ronal SK channels. Cell Biochem Biophys 55: 127-139.
57. Lupica CR, Riegel AC, Hoffman AF. 2004. Marijuana and cannabinoid regulation of brain reward circuits. Br J Pharmacol 143: 227-234.
58. Luscher C, Malenka RC. 2011. Drug-evoked synaptic plasticity in addiction: From molecular changes to circuit remodeling. Neuron 69: 650-663.
59. Mackie K, Hille B. 1992. Cannabinoids inhibit N-type calcium channels in neuroblastoma-glioma cells. Proc Natl Acad Sci 89: 3825-3829.
60. 9-tetrahydro-cannabinol reduces g-aminobutyric acid uptake in the globus pallidus. Eur J Pharmacol 308: 161-164.
61. Manzoni OJ, Bockaert J. 2001. Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus ac-cumbens. Eur J Pharmacol 412: R3-R5.
62. Marsicano G, Lutz B. 1999. Expression of the cannabinoid receptor CB1 in distinct neuronal infpopulations in the adult mouse forebrain. Eur J Neurosci 11: 4213-4225.
63. 9THC blocks endocannabinoid-mediated synaptic plasticity. Nat Neurosci 7: 585-586.
64. Mechoulam R. 1970. Marihuana chemistry. Science 168: 1159-1166.
65. Mechoulam R, Gaoni Y. 1965. Hashish. IV. The isolation and structure of cannabinolic cannabidiolic and cannabiger-olic acids. Tetrahedron 21: 1223-1229.
66. Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G, Gessa GL. 2004. Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 24: 53-62.
67. Mikasova L, Groc L, Choquet D, Manzoni OJ. 2008. Altered surface trafficking of presynaptic cannabinoid type 1 receptor in and out synaptic terminals parallels receptor desensitization. Proc Natl Assoc Soc 105: 18596-18601.
68. Mu J, Zhuang SY, Kirby MT, Hampson RE, Deadwyler SA. 1999. Cannabinoid receptors differentially modulate potassium A and D currents in hippocampal neurons in culture. J Pharmacol Exp Ther 291: 893-902.
69. Nazzaro C, Greco B, Cerovic M, Baxter P, Rubino T, Trusel M, Parolaro D, Tkatch T, Benfenati F, Pedarzani P, et al. 2012. SK channel modulation rescues striatal plasticity and control over habit in cannabinoid tolerance. Nat Neurosci 15: 284-293.
70. Niehaus JL, Murali M, Kauer JA. 2010. Drugs of abuse and stress impair LTP at inhibitory synapses in the ventral tegmental area. Eur J Neurosci 32: 108-117.
71. 9-tetrahydrocannabinol in the rat hippocampus, in vitro. Brain Res Bull 19: 663-672.
72. Pan B, Hillard CJ, Liu QS. 2008. D2 dopamine receptor activation facilitates endocannabinoid-mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein Kinase A signaling. J Neurosci 28: 14018-14030.
73. Patel S, Hillard CJ. 2001. Cannabinoid CB1 receptor agonists produce cerebellar dysfunction in mice. J Pharmacol Exp Ther 297: 629-637.
74. Pertwee RG. 1997. Pharmacology of cannabinoid CB1 and CB2 receptors. Pharmacol Thera 74: 129-180.
75. Piomelli D. 2003. The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4: 873-884.
76. Pope HG Jr, Gruber AJ, Hudson JI, Huestis MA, Yurgelun-Todd D. 2002. Cognitive measures in long-term cannabis users. J Clin Pharmacol 42: 41S-47S.
77. Puighermanal E, Marsicano G, Busquets-Garcia A, Lutz B, Maldonado R, Ozaita A. 2009. Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat Neurosci 12: 1152-1158.
78. Riegel AC, Lupica CR. 2004. Independent presynaptic and postsynaptic mechanisms regulate endocannabinoid signaling atmultiple synapsesinthe ventral tegmental area. J Neurosci 24: 11070-11078.
79. Robbe D, Alonso G, Duchamp F, Bockaert J, Manzoni OJ. 2001. Localization and mechanisms of action of canna- binoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J Neurosci 21: 109-116.
80. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ. 2002. Endogenous cannabinoids mediate long-term syn- aptic depression in the nucleus accumbens. Proc Natl Assoc Sci 99: 8384.
81. Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsaki G. 2006. Cannabinoids reveal importanceof spike timing coordinationinhippocampal function. Nat Neurosci 9: 1526-1533.
82. 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: 1673-1679.
83. 9-tetrahydro-cannabinol treatment increases cAMP levels and cAMP-dependent protein kinase activity in some rat brain regions. Neuropharmacology 39: 1331-1336.
84. 9-tetrahydrocannabinol treatment. Mol Cell Neurosci 25: 355-362.
85. Rubino T, Forlani G, Viganò D, Zippel R, Parolaro D. 2005. Ras/ERK signalling in cannabinoid tolerance: From behaviour to cellular aspects. J Neurochem 93: 984-991.
86. Russo SJ, Dietz DM, Dumitriu D, Morrison JH, Ma-lenka RC, Nestler EJ. 2010. The addicted synapse: Mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci 33: 267-276.
87. Saal D, Dong Y, Bonci A, Malenka RC. 2003. Drugs of abuse and stress trigger a common synaptic adaptation in dop-amine neurons. Neuron 37: 577-582.
88. Safo PK, Regehr WG. 2005. Endocannabinoids control the induction of cerebellar LTD. Neuron 48: 647-659.
89. {thorn} M-cur-rent in hippocampal CA1 neurons. J Neurosci 20: 51-58.
90. 9-Tetrahydrocannabinol actsasa partial agonist to modulate glutamatergic synaptic transmission between rat hippocampal neurons in culture. Mol Pharmacol 55: 8-13.
91. Squire LR. 1992. Memory and the hippocampus: Asynthesis from findings with rats, monkeys, and humans. Psychol Rev 99: 195-231.
92. Straiker A, Mackie K. 2005. Depolarization-induced suppression of excitation in murine autaptic hippocampal neurones. J Physiol (Lond) 569: 501-517.
93. Infstance Abuse and Mental Health Services Administration. 2002. Results from the 2001 National Household Survey on Drug Abuse: Volume II. Technical appendices and selected data tables, pp. 1-107. Office of Applied Studies, DHHS, Rockville, MD.
94. Sullivan JM. 1999. Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. J Neurophysiol 82: 1286-1294.
95. Takahashi KA, Castillo PE. 2006. The CB1 cannabinoid receptor mediates glutamatergic synaptic suppression in the hippocampus. Neuroscience 139: 795-802.
96. 9-tetrahydrocannabinol exposure. J Neurosci 26: 5810-5818.
97. Tzavara ET, Valjent E, Firmo C, Mas M, Beslot F, Defer N, Roques BP, Hanoune J, Maldonado R. 2000. Cannabi-noid withdrawal is dependent upon PKA activation in the cerebellum. Eur J Neurosci 12: 1038-1046.
98. Ungless MA, Whistler JL, Malenka RC, Bonci A. 2001. Single cocaine exposure in vivo induces long-term potenti-ation in dopamine neurons. Nature 411: 583-587.
99. Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K, Stella N, Makriyannis A, Piomelli D, Davison JS, et al. 2005. Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310: 329-332.
100. 9-tetrahydro-cannabinol and marijuana in humans. Psychopharmacol-ogy (Berl) 161: 331-339.
101. Wagner JJ, Alger BE. 1996. Homosynaptic LTD and depo-tentiation: Do they differ in name only? Hippocampus 6: 24-29.
102. Whitlock JR, Heynen AJ, Shuler MG, Bear MF. 2006. Learning induces long-term potentiation in the hippocampus. Science 313: 1093-1097.
103. Wilson RI, Nicoll RA. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410: 588-592.
104. Wilson RI, Kunos G, Nicoll RA. 2001. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31: 453-462.
105. Xi ZX, Peng XQ, Li X, Song R, Zhang HY, Liu QR, Yang HJ, Bi GH, Li J, Gardner EL. 2011. Brain cannabinoid CB2 receptors modulate cocaine's actions in mice. Nat Neuro-sci 14: 1160-1166.
106. Xiong W, Cheng K, Cui T, Godlewski G, Rice KC, Xu Y, Zhang L. 2011. Cannabinoid potentiation of glycine receptors contributes to cannabis-induced analgesia. Nat Chem Biol 7: 296-303.
107. Yin HH, Knowlton BJ, Balleine BW. 2006. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav Brain Res 166: 189-196.
108. Yin HH, Ostlund SB, Balleine BW. 2008. Reward-guided learning beyond dopamine in the nucleus accumbens: The integrative functions of cortico-basal ganglia networks. Eur J Neurosci 28: 1437-1448.
109. Yin HH, Mulcare SP, Hilario MRF, Clouse E, Holloway T, Davis MI, Hansson AC, Lovinger DM, Costa RM. 2009. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat Neurosci 12: 333-341.