Cannabidiol enhances consolidation of explicit fear extinction in humans

Psychopharmacology

Volumn 226, Issue 4, 2013, Pages 781-792

  Das, Ravi K ^a   Kamboj, Sunjeev K ^a   Ramadas, Mayurun ^b   Yogan, Kishoj ^b   Gupta, Vivek ^b   Redman, Emily ^a   Curran, H Valerie ^a   Morgan, Celia J A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

Anxiety; Cannabidiol; Cannabinoids; Conditioning; Consolidation; Extinction; Pavlovian

Indexed keywords

CANNABIDIOL; PLACEBO;

ADULT; ARTICLE; CONDITIONING; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFECT; ELECTRIC SHOCK; EXPECTANCY; FEAR; FEAR EXTINCTION; HUMAN; HUMAN EXPERIMENT; LEARNING; MEMORY CONSOLIDATION; NORMAL HUMAN; PRIORITY JOURNAL; REINFORCEMENT; SKIN CONDUCTANCE;

CANNABIDIOL; CONDITIONING, CLASSICAL; DOUBLE-BLIND METHOD; ELECTROSHOCK; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; HUMANS; MALE; TIME FACTORS;

EID: 84876462372     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-012-2955-y     Document Type: Article

References (48)

1. Akirav I (2011) The role of cannabinoids in modulating emotional and non-emotional memory processes in the hippocampus. Front Behav Neurosci 5:34
2. Atsak P, Roozendaal B, Campolongo P (2011) Role of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences. Neuroscience 204:104-116
3. Baddeley A, Emslie H, Nimmo-Smith I (1993) The spot-the word test: a robust estimate of verbal intelligence based on lexical decision. Br J Clin Psychol 32:55-65
4. Bechara A, Tranel D, Damasio H, Adophs R, Rockland C, Damasio AR (1995) Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269:1115-1118
5. Beck AT, Steer RA, Brown GK (1996) Manual for the Beck Depression Inventory-II. Psychological Corporation, San Antonio
6. 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
7. Bergamaschi MM, Quieroz RHC, Crippa JAS, Zuardi AW (2011) Safety and side effects of cannabidiol, a Cannabis sativa constituent. Current Drug Safety 6(4):237-49
8. Bitencourt RM, Pamplona FA, Takahashi RN (2008) Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. Eur Neuropsychopharmacol 18:849-859
9. Boddez Y, Baeyens F, Luyten L, Vanteenwegen D, Hermans D, Beckers T (2012) Rating data are underrated: validity of US expectancy in human fear conditioning. J Behav Ther Exp Psychiatry 44:201-206
10. Bond A, Lader M (1974) The use of analogue scales in rating subjective feelings. Br J Med Psychol 47:211-218
11. Campolongo P, Roozendaal B, Trezza V, Hauer D, Schelling G, McGaugh JL, Cuomo V (2009) Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. PNAS 106:4888-4893
12. Campolongo P, Ratano P, Manduca A, Scattoni ML, Palmery M, Trezza V, Cuomo V (2012) The endocannabinoid transport inhibitor AM404 differentially modulates recognition memory in rats depending on environmental aversiveness. Front Behav Neurosci 6:11
13. Chhatwal JP, Davis M, Maguschak KA, Ressler KJ (2005) Role of endogenous cannabinoids in cognition and emotionality. Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 30(3):516-524
14. de Bitencourt RM, Pamplona FA, Takahashi RN (2013) A current overview of cannabinoids and glucocorticoids in facilitating extinction of aversive memories: potential extinction enhancers. Neuropharmacology 64:389-395
15. DeHouwer J (2009) The propositional approach to associative learning as an alternative for association formation models. Learn Behav 37:1-20
16. Dudai Y (2004) The neurobiology of consolidation, or, how stable is the engram? Annu Rev Psychol 55:51-86
17. Fowler CJ, Tiger G, Ligresti A, López-Rodriguez ML, Di Marzo V (2004) Selective inhibition of anandamide cellular uptake versus enzymatic hydrolysis - a difficult issue to handle. European Journal of Pharmacology 492:1-11
18. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signalling. Physiol Rev 83:1017-1066
19. Grillon C (2009) D-Cycloserine facilitation of fear extinction and exposure-based therapy might rely on lower-level, automatic mechanisms. Biol Psychiatry 66:636-641
20. Hill MN, McEwen BS (2009) Endocannabinoids: the silent partner of glucocorticoids in the synapse. PNAS 106:4579-4580
21. Hill MN, Froese LM, Morrish AC, Sun JC, Floresco SB (2006) Alterations in behavioral flexibility by cannabinoid CB1 receptor agonists and antagonists. Psychopharmacology 187:245-259
22. Kaplan GB, Moore KA (2011) The use of cognitive enhancers in animal models of fear extinction. Pharmacol Biochem Behav 99(2):217-228
23. Leweke FM, Piomelli D, Pahlisch F, Muhl D, Gerth CW, Hoyer C, Klosterkötter J, Hellmich M, Koethe D (2012) Cannabidiol enhances anandamide signaling and alleviates psychotic symptoms of schizophrenia. Transl Psychiatry 2:e94
24. Lovibond PF, Shanks DR (2002) The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implications. J Exp Psychol 28:3-26
25. Lutz B (2007) The endocannabinoid system and extinction learning. Mol Neurobiol 36:92-101
26. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534
27. Mineka S (1979) The role of fear in theories of avoidance learning, flooding and extinction. Psychol Bull 86:985-1010
28. Mineka S, Zinbarg R (1996) Conditioning and ethological models of anxiety disorders: stress-in-dynamic-context anxiety models. In: Hope DA (ed) Nebraska symposium on motivation, vol 43. Perspectives on anxiety, panic, and fear. University of Nebraska Press, Lincoln
29. Morgan CJA, Schafer G, Freeman TP, Curran HV (2010) Impact of cannabidiol on the acute memory and psychotomimetic effects of smoked cannabis: naturalistic study. Br J Psychiatry 197:285-290
30. Müller GE, Pilzecker A (1900) Experimentelle Beiträge zur Lehre vom Gedächtnis. Z Psychol Ergänzungsband 1:1-300
31. 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 191:223-231
32. Nurmikko TJ, Serpell MG, Hoggart B, Toomey PJ, Morlion BJ, Haines D (2007) Sativex successfully treats neuropathic pain characterised by allodynia: a randomised, double-blind, placebo controlled clinical trial. Pain 133:210-220
33. Ohman A, Minkea S (2001) Fears, phobias and preparedness: toward an evolved module of fear and fear learning. Psychol Rev 108:483-522
34. Osan R, Tort ABL, Amaral OB (2011) A mismatch-based model for memory reconsolidation and extinction in attractor networks. PLoS One 6(8):e23113
35. 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 188:641-649
36. Pamplona FA, Bitencourt RM, Takahashi RN (2008) Short- and long-term effects of cannabinoids on the extinction of contextual fear memory in rats. Neurobiol Learn Mem 90:290-293
37. Pavlov IP (1927) Conditioned reflexes. Oxford, London
38. Pertwee RG (2008) The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: Δ9-tetrahydrocannabinol, cannabidiol and Δ9-tetrahydrocannabivarin. Br J Pharmacol 153(2):199-215
39. Petitet F, Jeantaud B, Reibaud M, Imperato A, Dubroeucq MC (1998) Complex pharmacology of natural cannabinoids: evidence for partial agonist activity of delta9-tetrahydrocannabinol and antagonist activity of cannabidiol on rat brain cannabinoid receptors. Life Sci 63:PL1-PL6
40. Rachman S, Radomsky AS, Shafran R (2008) Safety behaviour: a reconsideration. Behav Res Ther 46:163-173
41. Reiss S (1991) Expectancy model of fear, anxiety and panic. Clin Psychol Rev 11(92):141-153
42. Sevenster D, Beckers T, Kindt M (2012) Retrieval per se is not sufficient to trigger reconsolidation of human fear memory. Neurobiol Learn Mem 97:338-345
43. Spielberger CD, Gorssuch RL, Lushene PR, Vagg PR, Jacobs GA (1983) Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press, Inc., Palo Alto
44. Stern CAJ, Gazarini L, Takahashi RN, Guimaraes FS, Bertogliuo LJ (2012) On disruption of fear memory by reconsolidation blockade: evidence from cannabidiol treatment. Neuropsychopharmacology 37:2132-2142
45. Suzuki A, Josselyn SA, Frankland PW, Massuhige S, Silva AJ, Kida S (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24:4787-4795
46. Thomas A, Baillie GL, Phillips AM, Razdan RK, Ross RA, Pertwee RG (2007) Cannabidiol displays unexpectedly high potency as an antagonist of CB1 and CB2 receptor agonists in vitro. Br J Pharmacol 150(5):613-623
47. Varvel SA, Lichtman AH (2002) Evaluation of CB1 receptor knockout mice in the Morris water maze. J Pharmacol Exp Ther 301:915-924
48. Watson JB, Rayner R (1920) Conditioned emotional reactions. J Exp Psychol 3:1-14