Advertisement

Role of the endocannabinoid system in learning and memory

  • Stephen A. Varvel
  • Aron H. Lichtman
Part of the Milestones in Drug Therapy MDT book series (MDT)

Keywords

Fatty Acid Amide Hydrolase Conditioned Freezing Conditioned Place Preference Learning 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Devane WA, Hanuš 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: 1946–1949PubMedGoogle Scholar
  2. 2.
    Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K (1995) 2-Arachidonoyglycerol: A possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215: 89–97CrossRefPubMedGoogle Scholar
  3. 3.
    Hanuš 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: 3662–3665CrossRefPubMedGoogle Scholar
  4. 4.
    Porter AC, Sauer JM, Knierman MD, Becker GW, Berna MJ, Bao J, Nomikos GG, Carter P, Bymaster FP, Leese AB, Felder CC (2002) Characterization of a novel endocannabinoid, virodhamine, with antagonist activity at the CB1 receptor. JPharmacol Exp Ther 301: 1020–1024CrossRefGoogle Scholar
  5. 5.
    Calignano A, La Rana G, Giuffrida A, Piomelli D (1998) Control of pain initiation by endogenous cannabinoids. Nature 394: 277–281CrossRefPubMedGoogle Scholar
  6. 6.
    Walker JM, Huang SM, Strangman NM, Tsou K, Sanudo-Pena MC (1999) Pain modulation by release of the endogenous cannabinoid anandamide. Proc Natl Acad Sci USA 96: 12198–12203CrossRefPubMedGoogle Scholar
  7. 7.
    Richardson JD, Aanonsen L, Hargreaves KM (1998) Hypoactivity of the spinal cannabinoid system results in NMDA-dependent hyperalgesia. J Neurosci 18: 451–457PubMedGoogle Scholar
  8. 8.
    Di Marzo V, Goparaju SK, Wang L, Liu J, Batkai S, Jarai Z, Fezza F, Miura GI, Palmiter RD, Sugiura T, Kunos G (2001) Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410: 822–825CrossRefPubMedGoogle Scholar
  9. 9.
    Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, Bohme GA, Imperato A, Pedrazzini T, Roques BP et al. (1999) Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283: 401–404CrossRefPubMedGoogle Scholar
  10. 10.
    Gonzalez S, Cascio MG, Fernandez-Ruiz J, Fezza F, Di Marzo V, Ramos JA (2002) Changes in endocannabinoid contents in the brain of rats chronically exposed to nicotine, ethanol or cocaine. Brain Res 954: 73–81CrossRefPubMedGoogle Scholar
  11. 11.
    Lichtman AH, Sheikh SM, Loh HH, Martin BR (2001) Opioid and cannabinoid modulation of precipitated withdrawal in delta(9)-tetrahydrocannabinol and morphine-dependent mice. J Pharmacol Exp Ther 298: 1007–1014PubMedGoogle Scholar
  12. 12.
    Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutierrez SO, van der Stelt M et al. (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302: 84–88CrossRefPubMedGoogle Scholar
  13. 13.
    Terranova JP, Storme JJ, Lafon N, Perio A, Rinaldi-Carmona M, Le Fur G, Soubrie P (1996) Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR 141716. Psychopharmacology 126: 165–172PubMedGoogle Scholar
  14. 14.
    Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W et al. (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418: 530–534CrossRefPubMedGoogle Scholar
  15. 15.
    Johnston LD, O’Malley PM, Bachman JG (2002) Monitoring the future. National results on adolescent drug use: Overview of Key Findings 2001. NIH Publication no. 02-5105. National Institute on Drug Abuse, Bethdesda, MD, 61Google Scholar
  16. 16.
    Miller LL, Branconnier RJ (1983) Cannabis: Effects on memory and the cholinergic limbic system. Psychol Bull 93: 441–456CrossRefPubMedGoogle Scholar
  17. 17.
    Chait LD, Pierri J (1992) Effects of smoked marijuana on human performance: A critical review. In: L Murphy, A Bartke (eds): Marijuana/Cannabinoids: Neurobiology and Neurophysiology. CRC Press, Boca Raton, FL, 387–423Google Scholar
  18. 18.
    Heyser CJ, Hampson RE, Deadwyler SA (1993) Effects of Δ9-tetrahydrocannabinol on delayed match to sample performance in rats: Alterations in short-term memory associated with changes in task specific firing of hippocampal cells. J Pharmacol Exp Ther 264: 294–307PubMedGoogle Scholar
  19. 19.
    Hampson RE, Deadwyler SA (1999) Cannabinoids, hippocampal function and memory. Life Sci 65: 715–723CrossRefPubMedGoogle Scholar
  20. 20.
    Hampson RE, Deadwyler SA (2000) Cannabinoids reveal the necessity of hippocampal neural encoding for short-term memory in rats. J Neurosci 20: 8932–8942PubMedGoogle Scholar
  21. 21.
    Deadwyler SA, Heyser C, Hampson RE (1995) Complete adaptation to the memory disruptive effects of delta-9-the following 35 days of exposure. Neurosci Res Commun 17: 9–18Google Scholar
  22. 22.
    Mallet PE, Beninger RJ (1996) The endogenous cannabinoid receptor agonist anandamide impairs memory in rats. Behav Pharmacol 7: 276–284Google Scholar
  23. 23.
    Mallet PE, Beninger RJ (1998) The cannabinoid CB1 receptor antagonist SR141716A attenuates the memory impairment produced by delta-9-tetrahydrocannabinol or anandamide. Psychopharmacology 140: 11–19CrossRefPubMedGoogle Scholar
  24. 24.
    Brodkin J, Moerschbaecher JM (1997) SR141716A antagonizes the disruptive effects of cannabinoid ligands on learning in rats. J Pharmacol Exp Ther 282: 1526–1532PubMedGoogle Scholar
  25. 25.
    Delatte MS, Winsauer PJ, Moerschbaecher JM (2002) Tolerance to the disruptive effects of Delta(9)-THC on learning in rats. Pharmacol Biochem Behav 74: 129–140CrossRefPubMedGoogle Scholar
  26. 26.
    Daniel JM, Winsauer PJ, Brauner IN, Moerschbaecher JM (2002) Estrogen improves response accuracy and attenuates the disruptive effects of delta9-THC in ovariectomized rats responding under a multiple schedule of repeated acquisition and performance. Behav Neurosci 116: 989–998CrossRefPubMedGoogle Scholar
  27. 27.
    Schulze GE, McMillan DE, Bailey JR, Scallet AC, Ali SF, Slikker W Jr, Paule MG (1989) Acute effects of marijuana smoke on complex operant behavior in rhesus monkeys. Life Sci 45: 465–475CrossRefPubMedGoogle Scholar
  28. 28.
    Schulze GE, McMillan DE, Bailey JR, Scallet A, Ali SF, Slikker W Jr, Paule MG (1988) Acute effects of delta-9-tetrahydrocannabinol in rhesus monkeys as measured by performance in a battery of complex operant tests. J Pharmacol Exp Ther 245: 178–186PubMedGoogle Scholar
  29. 29.
    Winsauer PJ, Lambert P, Moerschbaecher JM (1999) Cannabinoid ligands and their effects on learning and performance in rhesus monkeys. Behav Pharmacol 10: 497–511PubMedGoogle Scholar
  30. 30.
    Nakamura-Palacios EM, Winsauer PJ, Moerschbaecher JM (2000) Effects of the cannabinoid ligand SR 141716A alone or in combination with delta9-tetrahydrocannabinol or scopolamine on learning in squirrel monkeys. Behav Pharmacol 11: 377–386PubMedGoogle Scholar
  31. 31.
    Aigner TG (1988) Delta-9-tetrahydrocannabinol impairs visual recognition memory but not discrimination learning in rhesus monkeys. Psychopharmacology 95: 507–511CrossRefPubMedGoogle Scholar
  32. 32.
    Nakamura EM, da Silva EA, Concilio GV, Wilkinson DA, Masur J (1991) Reversible effects of acute and long-term administration of Δ9-tetrahydrocannabinol (THC) on memory in the rat. Drug Alc Depend 28: 167–175CrossRefGoogle Scholar
  33. 33.
    Lichtman AH, Dimen KR, Martin BR (1995) Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology 119: 282–290PubMedGoogle Scholar
  34. 34.
    Lichtman AH, Cook SA, Martin BR (1996) Investigation of brain sites mediating cannabinoid-induced antinociception in rats: evidence supporting periaqueductal gray involvement. J Pharmacol Exp Ther 276: 585–593PubMedGoogle Scholar
  35. 35.
    Mishima K, Egashira N, Matsumoto Y, Iwasaki K, Fujiwara M (2002) Involvement of reduced acetylcholine release in Delta9-tetrahydrocannabinol-induced impairment of spatial memory in the 8-arm radial maze. Life Sci 72: 397–407CrossRefPubMedGoogle Scholar
  36. 36.
    Braida D, Sala M (2000) Cannabinoid-induced working memory impairment is reversed by a second generation cholinesterase inhibitor in rats. Neuroreport 11: 2025–2029PubMedGoogle Scholar
  37. 37.
    Molina-Holgado F, Gonzalez MI, Leret ML (1995) Effect of delta 9-tetrahydrocannabinol on short-term memory in the rat. Physiol Behav 57: 177–179CrossRefPubMedGoogle Scholar
  38. 38.
    Ferrari F, Ottani A, Vivoli R, Giuliani D (1999) Learning impairment produced in rats by the cannabinoid agonist HU 210 in a water-maze task. Pharmacol Biochem Behav 64: 555–561CrossRefPubMedGoogle Scholar
  39. 39.
    Varvel SA, Hamm RJ, Martin BR, Lichtman AH (2001) Differential effects of delta9-THC on spatial reference and working memory in mice. Psychopharmacology (Berl) 157: 142–150CrossRefGoogle Scholar
  40. 40.
    Varvel SA, Lichtman AH (2002) Evaluation of CB1 receptor knockout mice in the Morris water maze. J Pharmacol Exp Ther 301: 915–924CrossRefPubMedGoogle Scholar
  41. 41.
    Jentsch J, Andrusiak E, Tran A, Bowers M, Roth R (1997) Δ9-Tetrahydrocannabinol increases prefrontal cortical catecholaminergic utilization and impairs spatial working memory in the rat: blockade of dopaminergic effects with HA966. Neuropsychopharmacology 16: 426–432CrossRefPubMedGoogle Scholar
  42. 42.
    Varvel SA, Anum E, Niyuhire F, Wise LE, Lichtman AH (2005) Delta(9)-THC-induced cognitive deficits in mice are reversed by the GABA(A) antagonist bicuculline. Psychopharmacology (Berl) 178: 317–327CrossRefGoogle Scholar
  43. 43.
    Nava F, Carta G, Colombo G, Gessa GL (2001) Effects of chronic Delta(9)-tetrahydrocannabinol treatment on hippocampal extracellular acetylcholine concentration and alternation performance in the T-maze. Neuropharmacology 41: 392–399CrossRefPubMedGoogle Scholar
  44. 44.
    Castellano C, Cabib S, Palmisano A, Di Marzo V, Puglisi-Allegra S (1997) The effects of anandamide on memory consolidation in mice involve both D1 and D2 dopamine receptors. Behav Pharmacol 8: 707–712PubMedGoogle Scholar
  45. 45.
    Murillo-Rodriguez E, Sanchez-Alavez M, Navarro L, Martinez-Gonzalez D, Drucker-Colin R, Prospero-Garcia O (1998) Anandamide modulates sleep and memory in rats. Brain Res 812: 270–274CrossRefPubMedGoogle Scholar
  46. 46.
    Costanzi M, Battaglia M, Populin R, Cestari V, Castellano C (2003) Anandamide and memory in CD1 mice: effects of immobilization stress and of prior experience. Neurobiol Learn Memory 79: 204–211CrossRefGoogle Scholar
  47. 47.
    Costanzi M, Battaglia M, Rossi-Arnaud C, Cestari V, Castellano C (2004) Effects of anandamide and morphine combinations on memory consolidation in cdl mice: involvement of dopaminergic mechanisms. Neurobiol Learn Memory 81: 144–149CrossRefGoogle Scholar
  48. 48.
    Castellano C, Cabib S, Puglisi-Allegra S, Gasbarri A, Sulli A, Pacitti C, Introini-Collison IB, McGaugh JL (1999) Strain-dependent involvement of D1 and D2 dopamine receptors in muscarinic cholinergic influences on memory storage. Behav Brain Res 98: 17–26CrossRefPubMedGoogle Scholar
  49. 49.
    Reibaud M, Obinu MC, Ledent C, Parmentier M, Bohme GA, Imperato A (1999) Enhancement of memory in cannabinoid CB 1 receptor knock-out mice. Eur J Pharmacol 379: R1–R2CrossRefPubMedGoogle Scholar
  50. 50.
    Bohme GA, Laville M, Ledent C, Parmentier M, Imperato A (2000) Enhanced long-term potentiation in mice lacking cannabinoid CB1 receptors. Neuroscience 95: 5–7CrossRefPubMedGoogle Scholar
  51. 51.
    Lichtman AH (2000) SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats. Eur J Pharmacol 404: 175–179CrossRefPubMedGoogle Scholar
  52. 52.
    Wolff MC, Leander JD (2003) SR141716A, a cannabinoid CB1 receptor antagonist, improves memory in a delayed radial maze task. Eur J Pharmacol 477: 213–217CrossRefPubMedGoogle Scholar
  53. 53.
    Mansbach RS, Rovetti CC, Winston EN, Lowe III JA (1996) Effects of the cannabinoid CB1 receptor antagonist SR141716A on the behavior of pigeons and rats. Psychopharmacology 124: 315–322PubMedGoogle Scholar
  54. 54.
    Baskfield CY, Martin BR, Wiley JL (2004) Differential effects of delta9-tetrahydrocannabinol and methanandamide in CB1 knockout and wild-type mice. J Pharmacol Exp Ther 309: 86–91CrossRefPubMedGoogle Scholar
  55. 55.
    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: 5780–5785CrossRefPubMedGoogle Scholar
  56. 56.
    Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O (2002) Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology (Berl) 159: 379–387CrossRefGoogle Scholar
  57. 57.
    Westlake TM, Howlett AC, Bonner TI, Matsuda LA, Herkenham M (1994) Cannabinoid receptor binding and messenger RNA expression in human brain: an in vitro receptor autoradiography and in situ hybridization histochemistry study of normal aged and Alzheimer’s brains. Neuroscience 63: 637–652CrossRefPubMedGoogle Scholar
  58. 58.
    Richfield EK, Herkenham M (1994) Selective vulnerability in Huntington’s disease: preferential loss of cannabinoid receptors in lateral globus pallidus. Ann Neurol 36: 577–584CrossRefPubMedGoogle Scholar
  59. 59.
    Benito C, Nunez E, Tolon RM, Carrier EJ, Rabano A, Hillard CJ, Romero J (2003) Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer’s disease brains. J Neurosci 23: 11136–11141PubMedGoogle Scholar
  60. 60.
    Mazzola C, Micale V, Drago F (2003) Amnesia induced by beta-amyloid fragments is counteracted by cannabinoid CB1 receptor blockade. Eur J Pharmacol 477: 219–225CrossRefPubMedGoogle Scholar
  61. 61.
    Lichtman AH, Martin BR (1996) Δ9-Tetrahydrocannabinol impairs spatial memory through a cannabinoid receptor mechanism. Psychopharmacology 126: 125–131PubMedGoogle Scholar
  62. 62.
    Cannich A, Wotjak CT, Kamprath K, Hermann H, Lutz B, Marsicano G (2004) CB1 cannabinoid receptors modulate kinase and phosphatase activity during extinction of conditioned fear in mice. Learn Memory 11: 625–632CrossRefGoogle Scholar
  63. 63.
    Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24: 4787–4795CrossRefPubMedGoogle Scholar
  64. 64.
    Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106: 274–285CrossRefPubMedGoogle Scholar
  65. 65.
    Varvel SA, Anum E, Lichtman AH (2005) Disruption of CBI receptor signaling impairs extinction of spatial memory in mice. Psychopharmacology; in pressGoogle Scholar
  66. 66.
    Parker LA, Burton P, Sorge RE, Yakiwchuk C, Mechoulam R (2004) Effect of low doses of Delta(9)-tetrahydrocannabinol and cannabidiol on the extinction of cocaine-induced and amphetamine-induced conditioned place preference learning in rats. Psychopharmacology (Berl) 175: 360–366CrossRefGoogle Scholar
  67. 67.
    Landsman RS, Burkey TH, Consroe P, Roeske WR, Yamamura HI (1997) SR141716A is an inverse agonist at the human cannabinoid CB 1 receptor. Eur J Pharmacol 334: R1–R2CrossRefPubMedGoogle Scholar
  68. 68.
    Pan X, Ikeda SR, Lewis DL (1998) SR 141716A acts as an inverse agonist to increase neuronal voltage-dependent Ca2+ currents by reversal of tonic CB 1 cannabinoid receptor activity. American Society for Pharmacology and Experimental Therapeutics 54: 1064–1072Google Scholar
  69. 69.
    Sim LJ, Selley DE, Xiao R, Childers SR (1996) Differences in G-protein activation by μ-and Δ-opioid, and cannabinoid, receptors in rat striatum. Eur J Pharmacol 307: 97–105CrossRefPubMedGoogle Scholar
  70. 70.
    Burkey TH, Quock RM, Consroe P, Roeske WR, Yamamura HI (1997) Δ9-Tetrahydrocannabinol is a partial agonist of cannabinoid receptors in mouse brain. Eur J Pharmacol 323: R3–R4CrossRefPubMedGoogle Scholar
  71. 71.
    Burkey TH, Quock RM, Consroe P, Ehlert FJ, Hosohata Y, Roeske WR, Yamamura HI (1997) Relative efficacies of cannabinoid CB1 receptor agonists in the mouse brain. Eur J Pharmacol 336: 295–298CrossRefPubMedGoogle Scholar
  72. 72.
    Sim-Selley LJ, Brunk LK, Selley DE (2001) Inhibitory effects of SR141716A on G-protein activation in rat brain. Eur J Pharmacol 414: 135–143CrossRefPubMedGoogle Scholar
  73. 73.
    Rinaldi-Carmona M, Barth F, Héaulme M, Shire D, Calandra B, Congy C, Martinez S, Maruani J, Nl1iat G, Caput D et al. (1994) SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. FEBS Lett 350: 240–244CrossRefPubMedGoogle Scholar
  74. 74.
    Compton D, Aceto M, Lowe J, Martin B (1996) In vivo characterization of a specific cannabinoid receptor antagonist (SR141716A): Inhibition of Δ9-tetrahdrocannabinol-induced responses and apparent agonist activity. J Pharmacol Exp Ther 277: 586–594PubMedGoogle Scholar
  75. 75.
    Hajos N, Ledent C, Freund TF (2001) Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106: 1–4CrossRefGoogle Scholar
  76. 76.
    Hajos N, Freund T (2002) Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibers. Neuropharmacology 43: 503CrossRefPubMedGoogle Scholar
  77. 77.
    Mogil JS, Grisel JE (1998) Transgenic studies of pain. Pain 77: 107–128CrossRefPubMedGoogle Scholar
  78. 78.
    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
  79. 79.
    Rinaldi-Carmona M, Pialot F, Congy C, Redon E, Barth F, Bachy A, Brelière JC, Soubrié P, Le Fur G (1996) Characterization and distribution of binding sites for [3H]-SR 141716A a selective brain (CB1) cannabinoid receptor antagonist in rodent brain. Life Sci 58: 1239–1247CrossRefPubMedGoogle Scholar
  80. 80.
    Matsuda LA, Bonner TI, Lolait SJ (1993) Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327: 535–550CrossRefPubMedGoogle Scholar
  81. 81.
    Twitchell W, Brown S, Mackie K (1997) Cannabinoids inhibit N-and P/Q-type calcium channels in cultured rat hippocampal neurons. Amer Physiol Soc 78: 43–50Google Scholar
  82. 82.
    Egertova M, Elphick MR (2000) Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB(1). J Comp Neurol 422: 159–171CrossRefPubMedGoogle Scholar
  83. 83.
    Felder CC, Nielsen A, Briley EM, Palkovits M, Priller J, Axelrod J, Nguyen DN, Richardson JM, Riggin RM, Koppel GA et al. (1996) Isolation and measurement of the endogenous cannabinoid receptor agonist, anandamide, in brain and peripheral tissues of human and rat. FEBS Lett 393: 231–235CrossRefPubMedGoogle Scholar
  84. 84.
    Bisogno T, Berrendero F, Ambrosino G, Cebeira M, Ramos JA, Fernandez-Ruiz JJ, Di Marzo V (1999) Brain regional distribution of endocannabinoids: implications for their biosynthesis and biological function. Biochem Biophys Res Commun 256: 377–380CrossRefPubMedGoogle Scholar
  85. 85.
    Egertova M, Giang DK, Cravatt BF, Elphick MR (1998) A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc R Soc Lond B Biol Sci 265: 2081–2085CrossRefGoogle Scholar
  86. 86.
    Tsou K, Nogueron MI, Muthian S, Sanudo-Pena MC, Hillard CJ, Deutsch DG, Walker JM (1998) Fatty acid amide hydrolase is located preferentially in large neurons in the rat central nervous system as revealed by immunohistochemistry. Neurosci Lett 254: 137–140CrossRefPubMedGoogle Scholar
  87. 87.
    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: 10819–10824CrossRefPubMedGoogle Scholar
  88. 88.
    Dinh TP, Freund TF, Piomelli D (2002) A role for monoglyceride lipase in 2-arachidonoylglycerol inactivation. Chem Phys Lipids 121: 149–158CrossRefPubMedGoogle Scholar
  89. 89.
    Di Marzo V, Breivogel CS, Tao Q, Bridgen DT, Razdan RK, Zimmer AM, Zimmer A, Martin BR (2000) Levels, metabolism, and pharmacological activity of anandamide in CB(1) cannabinoid receptor knockout mice: evidence for non-CB(1), non-CB(2) receptor-mediated actions of anandamide in mouse brain. J Neurochem 75: 2434–2444CrossRefPubMedGoogle Scholar
  90. 90.
    Egashira N, Mishima K, Iwasaki K, Fujiwara M (2002) Intracerebral microinjections of delta 9-tetrahydrocannabinol: search for the impairment of spatial memory in the eight-arm radial maze in rats. Brain Res 952: 239–245CrossRefPubMedGoogle Scholar
  91. 91.
    Pistis M, Ferraro L, Pira L, Flore G, Tanganelli S, Gessa GL, Devoto P (2002) Delta(9)-tetrahydrocannabinol decreases extracellular GABA and increases extracellular glutamate and dopamine levels in the rat prefrontal cortex: an in vivo microdialysis study. Brain Res 948: 155–158CrossRefPubMedGoogle Scholar
  92. 92.
    Verrico CD, Jentsch JD, Dazzi L, Roth RH (2003) Systemic, but not local, administration of cannabinoid CB1 receptor agonists modulate prefrontal cortical acetylcholine efflux in the rat. Synapse 48: 178–183CrossRefPubMedGoogle Scholar
  93. 93.
    Gerdeman GL, Partridge JG, Lupica CR, Lovinger DM (2003) It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci 26: 184–192CrossRefPubMedGoogle Scholar
  94. 94.
    Maingret F, Patel AJ, Lazdunski M, Honore E (2001) The endocannabinoid anandamide is a direct and selective blocker of the background K(+) channel TASK-1. EMBO J 20: 47–54CrossRefPubMedGoogle Scholar
  95. 95.
    Venance L, Piomelli D, Glowinski J, Giaume C (1995) Inhibition by anandamide of gap junctions and intercellular clacium signalling in striatal astrocytes. Nature 376: 590–594CrossRefPubMedGoogle Scholar
  96. 96.
    Zygmunt PM, Peterson J, Andersson DA, Chuang HH, Sorgard M, DiMarzo V, Julius D (1999) Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400: 452–457CrossRefPubMedGoogle Scholar
  97. 97.
    Tognetto M, Amadesi S, Harrison S, Creminon C, Trevisani M, Carreras M, Matera M, Geppetti P, Bianchi A (2001) Anandamide excites central terminals of dorsal root ganglion neurons via vanilloid receptor-1 activation. J Neurosci 21: 1104–1109PubMedGoogle Scholar
  98. 98.
    Bidaut-Russell M, Devane WA, Howlett AC (1990) Cannabinoid receptors and modulation of cyclic AMP accumulation in the rat brain. J Neurochem 55: 21–26PubMedGoogle Scholar
  99. 99.
    Howlett AC, Qualy JM, Khachatrian LL (1986) Involvement of Gi in the inhibition of adenylate cyclase by cannabimimetic drugs. Mol Pharmacol 29: 307–313PubMedGoogle Scholar
  100. 100.
    Pacheco M, Childers SR, Arnold R, Casiano F, Ward SJ (1991) Aminoalkylindoles: Actions on specific G-protein-linked receptors. J Pharmacol Exp Ther 257: 170–183PubMedGoogle Scholar
  101. 101.
    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. J Biochem 312: 637–641Google Scholar
  102. 102.
    Wartmann M, Campbell D, Subramanian A, Burstein SH, Davis RJ (1995) The MAP kinase signal transduction pathway is activated by the endogenous cannabinoid anandamine. FEBS Lett 359: 133–136CrossRefPubMedGoogle Scholar
  103. 103.
    Caulfield MP, Brown DA (1992) Cannabinoid receptor agonists inhibit Ca current in NG108-15 neuroblastoma cells via a pertussis toxin-sensitive mechanism. Br J Pharmacol 106: 231–232PubMedGoogle Scholar
  104. 104.
    Mackie K, Hille B (1992) Cannabinoids inhibit N-type calcium channels in neurobalstoma-glioma cells. Proc Natl Acad Sci USA 89: 3825–3829PubMedGoogle Scholar
  105. 105.
    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
  106. 106.
    Henry D, Chavkin C (1995) Activation of inwardly rectifying potassium channels (GIRK1) by co-expressed rat brain cannabinoid receptors in xenopus oocytes. Neurosci Lett 186: 91–94CrossRefPubMedGoogle Scholar
  107. 107.
    Deadwyler SA, Hampson RE, Bennett BA, Edwards TA, Mu J, Pacheco MA, Ward SJ, Childers SR (1993) Cannabinoids modulate potassium current in cultured hippocampal neurons. Receptors and Channels, ed. Publishers HA: Harwood Academic Publishers. 121–134Google Scholar
  108. 108.
    Sullivan JM (1999) Mechanisms of cannabinoid-receptor-mediated inhibition of synaptic transmission in cultured hippocampal pyramidal neurons. Amer Physiol Society 82: 1286–1294Google Scholar
  109. 109.
    Shen M, Thayer SA (1999) Delta9-tetrahydrocannabinol acts as a partial agonist to modulate glutamatergic synaptic transmission between rat hippocampal neurons in culture. Mol Pharmacol 55: 8–13PubMedGoogle Scholar
  110. 110.
    Shen M, Piser TM, Seybold VS, Thayer SA (1996) Cannabinoid receptor agonists inhibit glutamatergic synaptic transmission in rat hippocampal cultures. J Neurosci 16: 4322–4334PubMedGoogle Scholar
  111. 111.
    Handelmann GE, Contreras PC, O’Donohue TL (1987) Selective memory impairment by phencyclidine in rats. Eur J Pharmacol 140: 69–73CrossRefPubMedGoogle Scholar
  112. 112.
    Butelman ER (1989) A novel NMDA antagonist, MK-801, impairs performance in a hippocampal-dependent spatial learning task. Pharmacol Biochem Behav 34: 13–16CrossRefPubMedGoogle Scholar
  113. 113.
    Ungerer A, Mathis C, Melan C (1998) Are glutamate receptors specifically implicated in some forms of memory processes? Exp Brain Res 123: 45–51CrossRefPubMedGoogle Scholar
  114. 114.
    Kesner RP, Dakis M, Bolland BL (1993) Phencyclidine disrupts long-but not short-term memory within a spatial learning task. Psychopharmacology 111: 85–90PubMedGoogle Scholar
  115. 115.
    Kesner RP, Dakis M (1995) Phencyclidine injections into the dorsal hippocampus disrupt long-but not short-term memory within a spatial learning task. Psychopharmacology (Berl) 120: 203–208Google Scholar
  116. 116.
    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: 4544–4558PubMedGoogle Scholar
  117. 117.
    Marsicano G, Lutz B (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11: 4213–4225CrossRefPubMedGoogle Scholar
  118. 118.
    Tsou K, Mackie K, Sanudo-Pena MC, Walker JM (1999) Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience 93: 969–975CrossRefPubMedGoogle Scholar
  119. 119.
    Katona I, Sperlagh B, Magloczky Z, Santha E, Kofalvi A, Czirjak S, Mackie K, Vizi ES, Freund TF (2000) GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus. Neuroscience 100: 797–804CrossRefPubMedGoogle Scholar
  120. 120.
    Hoffman AF, Lupica CR (2000) Mechanisms of cannabinoid inhibition of GABA(A) synaptic transmission in the hippocampus. J Neurosci 20: 2470–2479PubMedGoogle Scholar
  121. 121.
    Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410: 588–592CrossRefPubMedGoogle Scholar
  122. 122.
    Banerjee SP, Snyder SH, Mechoulam R (1975) Cannabinoids: influence on neurotransmitter uptake in rat brain synaptosomes. J Pharmacol Exp Ther 194: 74–81PubMedGoogle Scholar
  123. 123.
    Hershkowitz M, Goldman R, Raz A (1977) Effect of cannabinoids on neurotransmitter uptake, atpase activity and morphology of mouse brain synaptosomes. Biochem Pharmacol 26: 1327–1331CrossRefGoogle Scholar
  124. 124.
    Romero J, de Miguel R, Ramos JA, Femandez-Ruiz JJ (1998) The activation of cannabinoid receptors in striatonigral GABAergic neurons inhibited GABA uptake. Life Sci 62: 351–363CrossRefPubMedGoogle Scholar
  125. 125.
    Revuelta AV, Cheney DL, Wood PL, Costa E (1979) GABAergic mediation in the inhibition of hippocampal acetylcholine turnover rate elicited by Δ9-tetrahydrocannabinol. Neuropharm 18: 525–530CrossRefGoogle Scholar
  126. 126.
    Kirby MT, Hampson RE, Deadwyler SA (2000) Cannabinoid receptor activation in CA1 pyramidal cells in adult rat hippocampus. Brain Res 863: 120–131CrossRefPubMedGoogle Scholar
  127. 127.
    Ohno-Shosaku T, Maejima T, Kano M (2001) Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29: 729–738CrossRefPubMedGoogle Scholar
  128. 128.
    Lindamood C, Colasanti BK (1980) Effects of Δ9-tetrahydrocannabinol and cannabidiol on sodium-dependent high affinity choline uptake in the rat hippocampus. J Pharmacol Exp Ther 213: 216–221PubMedGoogle Scholar
  129. 129.
    Lindamood C, Colasanti BK (1981) Interaction between impulse-flow and Δ9-tetrahydrocannabinol within the septal-hippocampal cholinergic pathway of rat brain. J Pharmacol Exp Ther 219: 580–584PubMedGoogle Scholar
  130. 130.
    Gifford AN, Ashby CRJ (1996) Electrically evoked acetylcholine release from hippocampal slices in inhibited by the cannabinoid receptor agonist, WIN 55212-2, and is potentiated by the cannabinoid antagonist, SR 141716A. JPET 277: 1431–1436Google Scholar
  131. 131.
    Gifford AN, Samiian L, Gatley S, Ashby C (1997) Examination of the effect of the cannabinoid receptor agonist, CP 55,940, on electrically evoked transmitter release from rat brain slices. Eur J Pharmacol 324: 187–192CrossRefPubMedGoogle Scholar
  132. 132.
    Kathmann M, Weber B, Schlicker E (2001) Cannabinoid CB1 receptor-mediated inhibition of acetylcholine release in the brain of NMRI, CD-1 and C57BL/6J mice. Naunyn Schmiedebergs Arch Pharmacol 363: 50–56CrossRefPubMedGoogle Scholar
  133. 133.
    Gifford AN, Bruneus M, Gatley SJ, Volkow ND (2000) Cannabinoid receptor-mediated inhibition of acetylcholine release from hippocampal and cortical synaptosomes. Br J Pharmacol 131: 645–650CrossRefPubMedGoogle Scholar
  134. 134.
    Carta G, Nava F, Gessa GL (1998) Inhibition of hippocampal acetylcholine release after acute and repeated Delta9-tetrahydrocannabinol in rats. Brain Res 809: 1–4CrossRefPubMedGoogle Scholar
  135. 135.
    Gessa GL, Mascia MS, Casu MA, Carta G (1997) Inhibition of hippocampal acetylcholine release by cannabinoids: reversal by SR141716A. Eur J Pharmacol 327: R1–R2CrossRefPubMedGoogle Scholar
  136. 136.
    Gessa GL, Casu MA, Carta G, Mascia MS (1998) Cannabinoids decrease acetylcholine release in the medial-prefontal cortex and hippocampus, reversal by SR 141716 A. Eur J Pharmacol 355: 119–124CrossRefPubMedGoogle Scholar
  137. 137.
    Kathmann M, Weber B, Zimmer A, Schlicker E (2001) Enhanced acetylcholine release in the hippocampus of cannabinoid CB(1) receptor-deficient mice. Br J Pharmacol 132: 1169–1173CrossRefPubMedGoogle Scholar
  138. 138.
    Pitler TA, Alger BE (1992) Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J Neurosci 12: 4122–4132PubMedGoogle Scholar
  139. 139.
    Pitler TA, Alger BE (1994) Depolarization-induced suppression of GABAergic inhibition in rat hippocampal pyramidal cells: G protein involvement in a presynaptic mechanism. Neuron 13: 1447–1455CrossRefPubMedGoogle Scholar
  140. 140.
    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: 565–574CrossRefPubMedGoogle Scholar
  141. 141.
    Vincent P, Armstrong CM, Marty A (1992) Inhibitory synaptic currents in rat cerebellar Purkinje cells: modulation by postsynaptic depolarization. J Physiol 456: 453–471PubMedGoogle Scholar
  142. 142.
    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: 53–62CrossRefPubMedGoogle Scholar
  143. 143.
    Glitsch M, Llano I, Marty A (1996) Glutamate as a candidate retrograde messenger at interneurone-Purkinje cell synapses of rat cerebellum. J Physiol 497: 531–537PubMedGoogle Scholar
  144. 144.
    Morishita W, Kirov SA, Alger BE (1998) Evidence for metabotropic glutamate receptor activation in the induction of depolarization-induced suppression of inhibition in hippocampal CA1. J Neurosci 18: 4870–4882PubMedGoogle Scholar
  145. 145.
    Wilson RI, Kunos G, Nicoll RA (2001) Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31: 453–462CrossRefPubMedGoogle Scholar
  146. 146.
    Kreitzer AC, Regehr WG (2001) Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21: RC174PubMedGoogle Scholar
  147. 147.
    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: 200–208PubMedGoogle Scholar
  148. 148.
    Yoshida T, Hashimoto K, Zimmer A, Maejima T, Araishi K, Kano M (2002) The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22: 1690–1697PubMedGoogle Scholar
  149. 149.
    Hampson RE, Zhuang SY, Weiner JL, Deadwyler SA (2003) Functional significance of cannabinoid-mediated, depolarization-induced suppression of inhibition (DSI) in the hippocampus. J Neurophysiol 90: 55–64PubMedGoogle Scholar
  150. 150.
    Bliss TV, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232: 357–374PubMedGoogle Scholar
  151. 151.
    Nowicky AV, Teyloer TJ, Vardaris RM (1987) The modulation of long-term potentiation by Δ9-tetrahydrocannabinol in the rat hippocampus, in vitro. Brain Res Bull 19: 663–672CrossRefPubMedGoogle Scholar
  152. 152.
    Collins DR, Pertwee RG, Davies SN (1994) The action of synthetic cannabinoids on the induction of long-term potentiation in the rat hippocampal slice. Eur J Pharmacol 259: R7–R8CrossRefPubMedGoogle Scholar
  153. 153.
    Collins DR, Pertwee RG, Davies SN (1995) Prevention by the cannabinoid antagonist, SR141716A, of cannabinoid-mediated blockade of long-term potentiation in the rat hippocampal slice. Br J Pharmacol 115: 869–870PubMedGoogle Scholar
  154. 154.
    Terranova J-P, Michaud J-C, Le Fur G, Soubrie P (1995) Inhibition of long-term potentiation in rat hippocampal slices by anandamide and WIN55212-2: Reversal by SR141716A, a selective antagonist of CB1 cannabinoid receptors. Nauyn-Schmiedeberg’s Arch Pharmacol 352: 576–579Google Scholar
  155. 155.
    Stella N, Schweitzer P, Piomelli D (1997) A second endogenous cannabinoid that modulates long-term potentiation. Nature 388: 773–778CrossRefPubMedGoogle Scholar
  156. 156.
    Lees G, Dougalis A (2004) Differential effects of the sleep-inducing lipid oleamide and cannabinoids on the induction of long-term potentiation in the CA1 neurons of the rat hippocampus in vitro. Brain Res 997: 1–14CrossRefPubMedGoogle Scholar
  157. 157.
    Sullivan JM (2000) Cellular and molecular mechanisms underlying learning and memory impairments produced by cannabinoids. Learn Memory 7: 132–139CrossRefGoogle Scholar
  158. 158.
    Carlson G, Wang Y, Alger BE (2002) Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat Neurosci 5: 723–724PubMedGoogle Scholar
  159. 159.
    Derkinderen P, Valjent E, Toutant M, Corvol JC, Enslen H, Ledent C, Trzaskos J, Caboche J, Girault JA (2003) Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J Neurosci 23: 2371–2382PubMedGoogle Scholar
  160. 160.
    Kemp N, Bashir ZI (2001) Long-term depression: a cascade of induction and expression mechanisms. Prog Neurobiol 65: 339–365CrossRefPubMedGoogle Scholar
  161. 161.
    Gaiarsa JL, Caillard O, Ben-Ari Y (2002) Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci 25: 564–570CrossRefPubMedGoogle Scholar
  162. 162.
    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
  163. 163.
    Huang YC, Wang SJ, Chiou LC, Gean PW (2003) Mediation of amphetamine-induced long-term depression of synaptic transmission by CB1 cannabinoid receptors in the rat amygdala. J Neurosci 23: 10311–10320PubMedGoogle Scholar
  164. 164.
    Sjostrom PJ, Turrigiano GG, Nelson SB (2003) Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39: 641–654CrossRefPubMedGoogle Scholar
  165. 165.
    Robbe D, Alonso G, Manzoni OJ (2003) Exogenous and endogenous cannabinoids control synaptic transmission in mice nucleus accumbens. Ann N YAcad Sci 1003: 212–225CrossRefGoogle Scholar
  166. 166.
    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 cannabinoid exposure. J Neurosci 23: 4815–4820PubMedGoogle Scholar
  167. 167.
    Auclair N, Otani S, Soubrie P, Crepel F (2000) Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefriontal cortex pyramidal neurons. J Neurophysiol 83: 3287–3293PubMedGoogle Scholar
  168. 168.
    Collin C, Devane WA, Dahl D, Lee CJ, Axelrod J, Alkon DL (1995) Long-term synaptic transformation of hippocampal CA1 gamma-aminobutyric acid synapses and the effect of anandamide. Brain Res 697: 83–90CrossRefPubMedGoogle Scholar
  169. 169.
    Kim D, Thayer SA (2001) Cannabinoids inhibit the formation of new synapses between hippocampal neurons in culture. J Neurosci 21: RC146PubMedGoogle Scholar
  170. 170.
    Hampson RE, Simeral JD, Kelly EJ, Deadwyler SA (2003) Tolerance to the memory disruptive effects of cannabinoids involves adaptation by hippocampal neurons. Hippocampus 13: 543–556CrossRefPubMedGoogle Scholar
  171. 171.
    Hernandez-Tristan R, Arevalo C, Canals S, Leret ML (2000) The effects of acute treatment with delta9-THC on exploratory behaviour and memory in the rat. J Physiol Biochem 56: 17–24PubMedGoogle Scholar
  172. 172.
    Mishima K, Egashira N, Hirosawa N, Fujii M, Matsumoto Y, Iwasaki K, Fujiwara M (2001) Characteristics of learning and memory impairment induced by delta9-tetrahydrocannabinol in rats. Jpn J Pharmacol 87: 297–308CrossRefPubMedGoogle Scholar
  173. 173.
    Diana G, Malloni M, Pieri M (2003) Effects of the synthetic cannabinoid nabilone on spatial learning and hippocampal neurotransmission. Pharmacol Biochem Behav 75: 585–591CrossRefPubMedGoogle Scholar
  174. 174.
    Robinson L, Hinder L, Pertwee RG, Riedel G (2003) Effects of delta9-THC and WIN-55,212-2 on place preference in the water maze in rats. Psychopharmacology (Berl) 166: 40–50Google Scholar
  175. 175.
    Nava F, Carta G, Battasi AM, Gessa GL (2000) D(2) dopamine receptors enable delta(9)-tetrahydrocannabinol induced memory impairment and reduction of hippocampal extracellular acetylcholine concentration. Br J Pharmacol 130: 1201–1210CrossRefPubMedGoogle Scholar
  176. 176.
    Ciccocioppo R, Antonelli L, Biondini M, Perfumi M, Pompei P, Massi M (2002) Memory impairment following combined exposure to delta(9)-tetrahydrocannabinol and ethanol in rats. Eur J Pharmacol 449: 245–252CrossRefPubMedGoogle Scholar
  177. 177.
    Kosiorek P, Hryniewicz A, Bialuk I, Zawadzka A, Winnicka MM (2003) Cannabinoids alter recognition memory in rats. Pol J Pharmacol 55: 903–910PubMedGoogle Scholar
  178. 178.
    Da S, Takahashi RN (2002) SR 141716A prevents delta 9-tetrahydrocannabinol-induced spatial learning deficit in a Morris-type water maze in mice. Prog Neuropsychopharmacol Biol Psychiat 26:321–325Google Scholar

Copyright information

© Birkhäuser Verlag/Switzerland 2005

Authors and Affiliations

  • Stephen A. Varvel
    • 1
  • Aron H. Lichtman
    • 1
  1. 1.Department of Pharmacology and ToxicologyVirginia Commonwealth UniversityRichmondUSA

Personalised recommendations