The endocannabinoid system and extinction learning

Molecular Neurobiology

Volumn 36, Issue 1, 2007, Pages 92-101

  Lutz, Beat ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Anxiety; Cannabinoid receptor; Endocannabinoids; Extinction; Fear conditioning; Habituation; Phobia; Posttraumatic stress disorder; Rodent; THC

Indexed keywords

CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; 1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 5 (4 BROMOPHENYL) 1 (2,4 DICHLOROPHENYL) 4 ETHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABIDIOL; FATTY ACID AMIDASE INHIBITOR; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; OL 135; OLEAMIDE; RIMONABANT; TETRAHYDROCANNABINOL; UNCLASSIFIED DRUG;

ANIMAL; FEAR; HUMAN; MEMORY; METABOLISM; NERVE CELL PLASTICITY; REINFORCEMENT; REVIEW; AVERSIVE BEHAVIOR; CONFERENCE PAPER; DRUG EFFECT; LEARNING; LOW DRUG DOSE; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; TASK PERFORMANCE; WORKING MEMORY;

ANIMALS; ENDOCANNABINOIDS; EXTINCTION, PSYCHOLOGICAL; FEAR; HUMANS; MEMORY; NEURONAL PLASTICITY; RECEPTOR, CANNABINOID, CB1;

EID: 38449115285     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-007-8004-x     Document Type: Review

References (107)

1. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873-884
2. Di Marzo V, De Petrocellis L, Bisogno T (2005) The biosynthesis, fate and pharmacological properties of endocannabinoids. Handb Exp Pharmacol 168:147-185
3. Pertwee RG (2005) Pharmacological actions of cannabinoids. Handb Exp Pharmacol 168:1-51
4. Valverde O, Karsak M, Zimmer A (2005) Analysis of the endocannabinoid system by using CB1 cannabinoid receptor knockout mice. Handb Exp Pharmacol 168:117-145
5. Pagotto U, Marsicano G, Cota D, Lutz B, Pasquali R (2006) The emerging role of the endocannabinoid system in endocrine regulation and energy balance. Endocr Rev 27:73-100 (Pubitemid 43228239)
6. Mackie K (2006) Cannabinoid receptors as therapeutic targets. Annu Rev Pharmacol Toxicol 46:101-122
7. Matias I, Di Marzo V (2007) Endocannabinoids and the control of energy balance. Trends Endocrinol Metab 18:27-37 (Pubitemid 44960014)
8. Harkany T, Guzman M, Galve-Roperh I, Berghuis P, Devi LA, Mackie K (2007) The emerging functions of endocannabinoid signaling during CNS development. Trends Pharmacol Sci 28:83-92 (Pubitemid 46161836)
9. Wotjak CT (2005) Role of endogenous cannabinoids in cognition and emotionality. Mini Rev Med Chem 5:659-670
10. Sullivan JM (2000) Cellular and molecular mechanisms underlying learning and memory impairments produced by cannabinoids. Learn Mem 7:132-139
11. Riedel G, Davies SN (2005) Cannabinoid function in learning, memory and plasticity. Handb Exp Pharmacol 168:445-477
12. Ranganathan M, D'Souza DC (2006) The acute effects of cannabinoids on memory in humans: a review. Psychopharmacology (Berl) 188:425-444 (Pubitemid 44498214)
13. Lichtman AH, Varvel SA, Martin BR (2002) Endocannabinoids in cognition and dependence. Prostaglandins Leukot. Essent Fatty Acids 66:269-285 (Pubitemid 34743601)
14. Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsaki G (2006) Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci 9:1526-1533 (Pubitemid 44862661)
15. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066 (Pubitemid 36828930)
16. Mackie K (2005) Distribution of cannabinoid receptors in the central and peripheral nervous system. Handb Exp Pharmacol 168:299-325
17. Marsicano G, Lutz B (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11:4213-4225 (Pubitemid 30009252)
18. Lutz B (2002) Molecular biology of cannabinoid receptors. Prostaglandins Leukot Essent Fatty Acids 66:123-142
19. 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 96:5780-5785 (Pubitemid 29234695)
20. Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, Bohme GA, Imperato A, Pedrazzini T, Roques BP, Vassart G, Fratta W, Parmentier M (1999) Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283:401-404
21. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534 (Pubitemid 34851398)
22. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutierrez SO, van der Stelt M, Lopez-Rodriguez ML, Casanova E, Schütz G, Zieglgänsberger W, Di Marzo V, Behl C, Lutz B (2003) CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84-88 (Pubitemid 37210691)
23. Monory K, Massa F, Egertova M, Eder M, Blaudzun H, Westenbroek R, Kelsch W, Jacob W, Marsch R, Ekker M, Long J, Rubenstein JL, Goebbels S, Nave KA, During M, Klugmann M, Wolfel B, Dodt HU, Zieglgänsberger W, Wotjak CT, Mackie K, Elphick MR, Marsicano G, Lutz B (2006) The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455-466 (Pubitemid 44209321)
24. Chevaleyre V, Takahashi KA, Castillo PE (2006) Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 29:37-76 (Pubitemid 44476839)
25. Marsicano G, Lutz B (2006) Neuromodulatory functions of the endocannabinoid system. J Endocrinol Invest 29:27-46
26. Klein TW (2005) Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat Rev Immunol 5:400-411
27. 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 98:9371-9376 (Pubitemid 32743923)
28. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313 (Pubitemid 30226186)
29. Rinaldi-Carmona M, Barth F, Heaulme M, Shire D, Calandra B, Congy C, Martinez S, Maruani J, Neliat G, Caput D, Ferrara P, Soubrié P, Brelière JC, Le Fur G (1994) SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. FEBS Lett 350:240-244 (Pubitemid 24268029)
30. Gatley SJ, Gifford AN, Volkow ND, Lan R, Makriyannis A (1996) 123I-labeled AM251: a radioiodinated ligand which binds in vivo to mouse brain cannabinoid CB1 receptors. Eur J Pharmacol 307:331-338 (Pubitemid 26233375)
31. Rinaldi-Carmona M, Barth F, Congy C, Martinez S, Oustric D, Perio A, Poncelet M, Maruani J, Arnone M, Finance O, Soubrie P, Le Fur G (2004) SR147778 [5-(4-bromophenyl)-1-(2,4-dichlorophenyl)-4-ethyl-N-(1-piperidinyl)-1H-pyr azole-3-carboxamide], a new potent and selective antagonist of the CB1cannabinoid receptor: biochemical and pharmacological characterization. J Pharmacol Exp Ther 310:905-914 (Pubitemid 39108910)
32. Kathuria S, Gaetani S, Fegley D, Valino F, Duranti A, Tontini A, Mor M, Tarzia G, Rana GL, Calignano A, Giustino A, Tattoli M, Palmery M, Cuomo V, Piomelli D (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9:76-81 (Pubitemid 36098263)
33. Beltramo M, Stella N, Calignano A, Lin SY, Makriyannis A, Piomelli D (1997) Functional role of high-affinity anandamide transport, as revealed by selective inhibition. Science 277:1094-1097 (Pubitemid 27371630)
34. De Petrocellis L, Bisogno T, Davis JB, Pertwee RG, Di Marzo V (2000) Overlap between the ligand recognition properties of the anandamide transporter and the VR1 vanilloid receptor: inhibitors of anandamide uptake with negligible capsaicin-like activity. FEBS Lett 483:52-56
35. Lopez-Rodriguez ML, Viso A, Ortega-Gutierrez S, Lastres-Becker I, Gonzalez S, Fernandez-Ruiz J, Ramos JA (2001) Design, synthesis and biological evaluation of novel arachidonic acid derivatives as highly potent and selective endocannabinoid transporter inhibitors. J Med Chem 44:4505-4508
36. de Sousa N, Almeida OF, Wotjak CT (2006) A hitchhiker's guide to behavioral analysis in laboratory rodents. Genes Brain Behav 5(Suppl 2):5-24
37. Reibaud M, Obinu MC, Ledent C, Parmentier M, Bohme GA, Imperato A (1999) Enhancement of memory in cannabinoid CB1 receptor knock-out mice. Eur J Pharmacol 379:R1-R2 (Pubitemid 29492956)
38. Maccarrone M, Valverde O, Barbaccia ML, Castane A, Maldonado R, Ledent C, Parmentier M, Finazzi-Agro A (2002) Age-related changes of anandamide metabolism in CB1 cannabinoid receptor knockout mice: correlation with behaviour. Eur J Neurosci 15:1178-1186 (Pubitemid 35463618)
39. Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O (2002) Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology (Berl) 159:379-387 (Pubitemid 34143362)
40. Bilkei-Gorzo A, Racz I, Valverde O, Otto M, Michel K, Sastre M, Zimmer A (2005) Early age-related cognitive impairment in mice lacking cannabinoid CB1 receptors. Proc Natl Acad Sci USA 102:15670-15675 (Pubitemid 41528114)
41. Lutz B (2004) On-demand activation of the endocannabinoid system in the control of neuronal excitability and epileptiform seizures. Biochem Pharmacol 68:1691-1698
42. van der Stelt M, Di Marzo V (2005) Cannabinoid receptors and their role in neuroprotection. Neuromolecular Med 7:37-50
43. Terranova JP, Storme JJ, Lafon N, Perio A, Rinaldi-Carmona M, LeFur G, Soubrie P (1996) Improvement of memory in rodents by the selective CB1 cannabinoid receptor antagonist, SR141716. Psychopharmacology 126:165-172 (Pubitemid 26246767)
44. Lichtman AH (2000) SR 141716A enhances spatial memory as assessed in a radial-arm maze task in rats. Eur J Pharmacol 404:175-179
45. Wolff MC, Leander JD (2003) SR141716A, a cannabinoid CB1 receptor antagonist, improves memory in a delayed radial maze task. Eur J Pharmacol 477:213-217 (Pubitemid 38366393)
46. Mallet PE, Beninger RJ (1998) The cannabinoid CB1 receptor antagonist SR141716A attenuates the memory impairment produced by delta9- tetrahydrocannabinol or anandamide. Psychopharmacology (Berl) 140:11-19 (Pubitemid 28524302)
47. Hampson RE, Deadwyler SA (2000) Cannabinoids reveal the necessity of hippocampal neural encoding for short-term memory in rats. J Neurosci 20:8932-8942
48. Mansbach RS, Rovetti CC, Winston EN, Lowe JA III (1996) Effects of the cannabinoid CB1 receptor antagonist SR141716A on the behavior of pigeons and rats. Psychopharmacology (Berl) 124:315-322 (Pubitemid 26149916)
49. Kishimoto Y, Kano M (2006) Endogenous cannabinoid signaling through the CB1 receptor is essential for cerebellum-dependent discrete motor learning. J Neurosci 26:8829-8837 (Pubitemid 44319418)
50. Varvel SA, Wise LE, Niyuhire F, Cravatt BF, Lichtman AH (2007) Inhibition of fatty-acid amide hydrolase accelerates acquisition and extinction rates in a spatial memory task. Neuropsychopharmacology 32:1032-1041 (Pubitemid 46631982)
51. Mikics E, Dombi T, Barsvari B, Varga B, Ledent C, Freund TF, Haller J (2006) The effects of cannabinoids on contextual conditioned fear in CB1 knockout and CD1 mice. Behav Pharmacol 17:223-230
52. Marsch R, Foeller E, Rammes G, Bunck M, Kossl M, Holsboer F, Zieglgänsberger W, Landgraf R, Lutz B, Wotjak CT (2007) Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J Neurosci 27:832-839 (Pubitemid 46174502)
53. Brewin CR (2001) A cognitive neuroscience account of posttraumatic stress disorder and its treatment. Behav Res Ther 39:373-393
54. Nemeroff CB, Bremner JD, Foa EB, Mayberg HS, North CS, Stein MB (2006) Posttraumatic stress disorder: a state-of-thescience review. J Psychiatr Res 40:1-21 (Pubitemid 43117523)
55. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184
56. Kim JJ, Jung MW (2006) Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 30:188-202 (Pubitemid 41821808)
57. Rodrigues SM, Schafe GE, LeDoux JE (2004) Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44:75-91 (Pubitemid 39348831)
58. Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev Neurosci 5:844-852 (Pubitemid 39482153)
59. Wotjak CT (2005) Learning and memory. Handb Exp Pharmacol 169:1-34
60. Myers KM, Davis M (2002) Behavioral and neural analysis of extinction. Neuron 36:567-584 (Pubitemid 35346753)
61. Myers KM, Davis M (2007) Mechanisms of fear extinction. Mol Psychiatry 12:120-150 (Pubitemid 46160979)
62. Barad M, Gean PW, Lutz B (2006) The role of the amygdala in the extinction of conditioned fear. Biol Psychiatry 60:322-328 (Pubitemid 44215854)
63. Quirk GJ, Garcia R, Gonzalez-Lima F (2006) Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 60:337-343 (Pubitemid 44215848)
64. Sotres-Bayon F, Cain CK, LeDoux JE (2006) Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol Psychiatry 60:329-336 (Pubitemid 44215846)
65. Milad MR, Rauch SL, Pitman RK, Quirk GJ (2006) Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 73:61-71
66. Berghuis P, Rajnicek AM, Morozov YM, Ross RA, Mulder J, Urban GM, Monory K, Marsicano G, Matteoli M, Canty A, Irving AJ, Katona I, Yanagawa Y, Rakic P, Lutz B, Mackie K, Harkany T (2007) Hardwiring the brain: endocannabinoids shape neuronal connectivity. Science 316:1212-1216 (Pubitemid 46880959)
67. Kamprath K, Marsicano G, Tang J, Monory K, Bisogno T, Di Marzo V, Lutz B, Wotjak CT (2006) Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci 26:6677-6686 (Pubitemid 44315229)
68. Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301:846-850 (Pubitemid 36962628)
69. Burgos-Robles A, Vidal-Gonzalez I, Santini E, Quirk GJ (2007) Consolidation of fear extinction requires NMDA receptordependent bursting in the ventromedial prefrontal cortex. Neuron 53:871-880 (Pubitemid 46367556)
70. Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ (2006) Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13:728-733 (Pubitemid 44871673)
71. Varvel SA, Lichtman AH (2002) Evaluation of CB1 receptor knockout mice in the Morris water maze. J Pharmacol Exp Ther 301:915-924 (Pubitemid 34595080)
72. Varvel SA, Anum EA, Lichtman AH (2005) Disruption of CB1 receptor signaling impairs extinction of spatial memory in mice. Psychopharmacology (Berl) 179:863-872 (Pubitemid 40767906)
73. Chhatwal JP, Davis M, Maguschak KA, Ressler KJ (2005) Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 30:516-524 (Pubitemid 40271154)
74. 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 24:4787-4795 (Pubitemid 38668203)
75. Finn DP, Beckett SR, Richardson D, Kendall DA, Marsden CA, Chapman V (2004) Evidence for differential modulation of conditioned aversion and fear-conditioned analgesia by CB1 receptors. Eur J Neurosci 20:848-852 (Pubitemid 39036946)
76. 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 Mem 11:625-632 (Pubitemid 39299714)
77. Chhatwal JP, Stanek-Rattiner L, Davis M, Ressler KJ (2006) Amygdala BDNF signaling is required for consolidation but not encoding of extinction. Nat Neurosci 9:870-872 (Pubitemid 43980497)
78. Lin HC, Mao SC, Gean PW (2006) Effects of intra-amygdala infusion of CB1 receptor agonists on the reconsolidation of fearpotentiated startle. Learn Mem 13:316-321
79. Pamplona FA, Prediger RD, Pandolfo P, Takahashi RN (2006) The cannabinoid receptor agonist WIN 55,212-2 facilitates the extinction of contextual fear memory and spatial memory in rats. Psychopharmacology (Berl) 188:641-649 (Pubitemid 46758971)
80. Niyuhire F, Varvel SA, Thorpe AJ, Stokes RJ, Wiley JL, Lichtman AH (2007) The disruptive effects of the CB(1) receptor antagonist rimonabant on extinction learning in mice are task-specific. Psychopharmacology (Berl) 191:223-231 (Pubitemid 46354610)
81. Shiflett MW, Rankin AZ, Tomaszycki ML, DeVoogd TJ (2004) Cannabinoid inhibition improves memory in food-storing birds, but with a cost. Proc R Soc Lond B Biol Sci 271:2043-2048
82. Hölter SM, Kallnik M, Wurst W, Marsicano G, Lutz B, Wotjak CT (2005) Cannabinoid CB1 receptor is dispensable for memory extinction in an appetitively-motivated learning task. Eur J Pharmacol 510:69-74 (Pubitemid 40312391)
83. Sanchis-Segura C, Cline BH, Marsicano G, Lutz B, Spanagel R (2004) Reduced sensitivity to reward in CB1 knockout mice. Psychopharmacology (Berl) 176:223-232 (Pubitemid 39517952)
84. Thornton-Jones ZD, Kennett GA, Vickers SP, Clifton PG (2007) A comparison of the effects of the CB(1) receptor antagonist SR141716A, pre-feeding and changed palatability on the microstructure of ingestive behaviour. Psychopharmacology (Berl) 193:1-9 (Pubitemid 46906621)
85. Thornton-Jones ZD, Vickers SP, Clifton PG (2005) The cannabinoid CB1 receptor antagonist SR141716A reduces appetitive and consummatory responses for food. Psychopharmacology (Berl) 179:452-460 (Pubitemid 40569048)
86. Lin CH, Yeh SH, Leu TH, Chang WC, Wang ST, Gean PW (2003) Identification of calcineurin as a key signal in the extinction of fear memory. J Neurosci 23:1574-1579 (Pubitemid 36314710)
87. Lu KT, Walker DL, Davis M (2001) Mitogen-activated protein kinase cascade in the basolateral nucleus of amygdala is involved in extinction of fear-potentiated startle. J Neurosci 21:RC162
88. Kamprath K, Wotjak CT (2004) Nonassociative learning processes determine expression and extinction of conditioned fear in mice. Learn Mem 11:770-786 (Pubitemid 39602518)
89. McSweeney FK, Swindell S (2002) Common processes may contribute to extinction and habituation. J Gen Psychol 129:364-400
90. Viveros MP, Marco EM, File SE (2005) Endocannabinoid system and stress and anxiety responses. Pharmacol Biochem Behav 81:331-342 (Pubitemid 40807131)
91. Hill MN, Gorzalka BB (2005) Is there a role for the endocannabinoid system in the etiology and treatment of melancholic depression? Behav Pharmacol 16:333-352 (Pubitemid 41404805)
92. Witkin JM, Tzavara ET, Davis RJ, Li X, Nomikos GG (2005) A therapeutic role for cannabinoid CB1 receptor antagonists in major depressive disorders. Trends Pharmacol Sci 26:609-617 (Pubitemid 41636305)
93. Cota D, Marsicano G, Tschöp M, Grübler Y, Flachskamm C, Schubert M, Auer D, Yassouridis A, Thone-Reineke C, Ortmann S, Tomassoni F, Cervino C, Nisoli E, Linthorst AC, Pasquali R, Lutz B, Stalla GK, Pagotto U (2003) The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Invest 112:423-431 (Pubitemid 38063771)
94. Cota D, Steiner MA, Marsicano G, Cervino C, Herman JP, Grubler Y, Stalla J, Pasquali R, Lutz B, Stalla GK, Pagotto U (2007) Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamic-pituitary-adrenal axis function. Endocrinology 148:1574-1581 (Pubitemid 46457104)
95. Patel S, Roelke CT, Rademacher DJ, Hillard CJ (2005) Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Eur J Neurosci 21:1057-1069 (Pubitemid 40461057)
96. Nader K, Schafe GE, Le Doux JE (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722-726
97. Kobilo T, Hazvi S, Dudai Y (2007) Role of cortical cannabinoid CB1 receptor in conditioned taste aversion memory. Eur J Neurosci 25:3417-3421 (Pubitemid 46872762)
98. Murillo-Rodriguez E, Giordano M, Cabeza R, Henriksen SJ, Mendez DM, Navarro L, Prospero-Garcia O (2001) Oleamide modulates memory in rats. Neurosci Lett 313:61-64 (Pubitemid 32973895)
99. Parker LA, Burton P, Sorge RE, Yakiwchuk C, Mechoulam R (2004) Effect of low doses of delta9-tetrahydrocannabinol and cannabidiol on the extinction of cocaine-induced and amphetamine-induced conditioned place preference learning in rats. Psychopharmacology (Berl) 175:360-366 (Pubitemid 39361924)
100. Azad SC, Monory K, Marsicano G, Cravatt BF, Lutz B, Zieglgansberger W, Rammes G (2004) Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling. J Neurosci 24:9953-9961 (Pubitemid 39463576)
101. Chevaleyre V, Heifets BD, Kaeser PS, Sudhof TC, Purpura DP, Castillo PE (2007) Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1alpha. Neuron 54:801-812 (Pubitemid 46843526)
102. Chevaleyre V, Castillo PE (2004) Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron 43:871-881 (Pubitemid 39215017)
103. Wilson RI, Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592 (Pubitemid 32267203)
104. Alger E (2002) Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247-286
105. Lafourcade M, Elezgarai I, Mato S, Bakiri Y, Grandes P, Manzoni OJ (2007) Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. PLoS ONE 2:e709
106. Bruchey AK, Shumake J, Gonzalez-Lima F (2007) Network model of fear extinction and renewal functional pathways. Neuroscience 145:423-437 (Pubitemid 46350816)
107. Siegmund A, Wotjak CT (2007) A mouse model of posttraumatic stress disorder that distinguishes between conditioned and sensitised fear. J Psychiatr Res 41:848-860 (Pubitemid 46693894)