δ9-Tetrahydrocannabinol alone and combined with cannabidiol mitigate fear memory through reconsolidation disruption

European Neuropsychopharmacology

Volumn 25, Issue 6, 2015, Pages 958-965

  Stern, Cristina A J ^a   Gazarini, Lucas ^a   Vanvossen, Ana C ^a   Zuardi, Antonio W ^b   Galve Roperh, Ismael ^c,d   Guimaraes, Francisco S ^b   Takahashi, Reinaldo N ^a   Bertoglio, Leandro J ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Cannabidiol; CB1 receptor; Fear memory; Medial prefrontal cortex; Reconsolidation; 9 Tetrahydrocannabinol

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABIDIOL; CANNABINOID 1 RECEPTOR; DRONABINOL; DRUG COMBINATION;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CONDITIONING; CONTROLLED STUDY; DOSE RESPONSE; DRUG BRAIN LEVEL; ELEVATED PLUS MAZE TEST; EXPLORATORY BEHAVIOR; FEAR; LIGHT DARK CYCLE; LOCOMOTION; MALE; MEDIAL PREFRONTAL CORTEX; MEMORY CONSOLIDATION; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRELIMBIC CORTEX; PRIORITY JOURNAL; RAT; RECALL; STEREOTAXIC SURGERY; ANALYSIS OF VARIANCE; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG COMBINATION; DRUG EFFECTS; MAZE TEST; MEMORY; MEMORY DISORDER; TIME FACTOR; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; CANNABIDIOL; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRONABINOL; DRUG COMBINATIONS; FEAR; MALE; MAZE LEARNING; MEMORY; MEMORY DISORDERS; RATS; RATS, WISTAR; TIME FACTORS;

EID: 84930276369     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2015.02.001     Document Type: Article

References (46)

1. Agurell S., Halldin M., Lindgren J.E., et al. Pharmacokinetics and metabolism of delta 1-tetrahydrocannabinol and other cannabinoids with emphasis on man. Pharmacol. Rev. 1986, 38:21-43.
2. Alberini C.M. The role of reconsolidation and the dynamic process of long-term memory formation and storage. Front. Behav. Neurosci. 2011, 5:12.
3. Bhattacharyya S., Fusar-Poli P., Borgwardt S., et al. Modulation of mediotemporal and ventrostriatal function in humans by Delta9-tetrahydrocannabinol: a neural basis for the effects of Cannabis sativa on learning and psychosis. Arch. Gen. Psychiatry 2009, 66:442-451.
4. Bisogno T., Hanus L., De Petrocellis L., et al. Molecular targets for cannabidiol and its synthetic analogues: effect on vanilloid VR1 receptors and on the cellular uptake and enzymatic hydrolysis of anandamide. Br. J. Pharmacol. 2001, 134:845-852.
5. Cain C.K., Maynard G.D., Kehne J.H. Targeting memory processes with drugs to prevent or cure PTSD. Expert Opin. Investig. Drugs 2012, 21:1323-1350.
6. Carobrez A.P., Bertoglio L.J. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci. Biobehav. Rev. 2005, 29:1193-1205.
7. Cornelius J.R., Kirisci L., Reynolds M., et al. PTSD contributes to teen and young adult cannabis use disorders. Addict. Behav. 2010, 35:91-94.
8. Da Silva G.E., Takahashi R.N. SR 141716A prevents delta 9-tetrahydrocannabinol-induced spatial learning deficit in a Morris-type water maze in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 2002, 26:321-325.
9. Debiec J. Memory reconsolidation processes and posttraumatic stress disorder: promises and challenges of translational research. Biol. Psychiatry 2012, 71:284-285.
10. de Oliveira Alvares L., Pasqualini Genro B., Diehl F., et al. Opposite action of hippocampal CB1 receptors in memory reconsolidation and extinction. Neuroscience 2008, 154:1648-1655.
11. Duvarci S., Nader K. Characterization of fear memory reconsolidation. J. Neurosci. 2004, 24:9269-9275.
12. Gatley S.J., Gifford A.N., Volkow N.D., et al. 123I-labeled AM251: a radioiodinated ligand which binds in vivo to mouse brain cannabinoid CB1 receptors. Eur. J. Pharmacol. 1996, 307:331-338.
13. Gazarini L., Stern C.A., Piornedo R.R., et al. PTSD-like memory generated through enhanced noradrenergic activity is mitigated by a dual step pharmacological intervention targeting its reconsolidation. Int. J. Neuropsychopharmacol. 2015, 18(1). http://dx.doi.org/10.1093/ijnp/pyu026.
14. Guimarães F.S., de Aguiar J.C., Mechoulam R., et al. Anxiolytic effect of cannabidiol derivatives in the elevated plus-maze. Gen. Pharmacol. 1994, 25:161-164.
15. Hauer D., Schelling G., Gola H., et al. Plasma concentrations of endocannabinoids and related primary fatty acid amides in patients with post-traumatic stress disorder. PLoS One 2013, 8:e62741.
16. Hoffman A.F., Oz M., Yang R., et al. Opposing actions of chronic Delta9-tetrahydrocannabinol and cannabinoid antagonists on hippocampal long-term potentiation. Learn. Mem. 2007, 3:63-74.
17. Izzo A.A., Borrelli F., Capasso R., et al. Non-psychotropic plant cannabinoids: new therapeutic opportunities from an ancient herb. Trends Pharmacol. Sci. 2009, 30:515-527.
18. Kessler R.C., Sonnega A., Bromet E., et al. Posttraumatic stress disorder in the National Comorbidity Survey. Arch. Gen. Psychiatry 1995, 52:1048-1060.
19. Klein C., Karanges E., Spiro A., et al. Cannabidiol potentiates δ9-tetrahydrocannabinol (THC) behavioural effects and alters THC pharmacokinetics during acute and chronic treatment in adolescent rats. Psychopharmacology 2011, 218:443-457.
20. Lin H.C., Mao S.C., Gean P.W. Effects of intra-amygdala infusion of CB1 receptor agonists on the reconsolidation of fear-potentiated startle. Learn. Mem. 2006, 13:316-321.
21. Malone D.T., Jongejan D., Taylor D.A. Cannabidiol reverses the reduction in social interaction produced by low dose Delta(9)-tetrahydrocannabinol in rats. Pharmacol. Biochem. Behav. 2009, 93:91-96.
22. Mechoulam R., Lichtman A.H. Stout guards of the central nervous system. Science 2003, 302:65-67.
23. Mishima K., Egashira N., Hirosawa N., et al. Characteristics of learning and memory impairment induced by delta9-tetrahydrocannabinol in rats. Jpn. J. Pharmacol. 2001, 87:297-308.
24. Morgan C.J., Gardener C., Schafer G., et al. Sub-chronic impact of cannabinoids in street cannabis on cognition, psychotic-like symptoms and psychologicalwell-being. Psychol. Med. 2012, 42:391-400.
25. Niesink R.J., van Laar M.W. Does cannabidiol protect against adverse psychological effects of THC?. Front. Psychiatry 2013, 4:130.
26. Niyuhire F., Varvel S.A., Thorpe A.J., et al. The disruptive effects of the CB1 receptor antagonist rimonabant on extinction learning in mice are task-specific. Psychopharmacology 2007, 191:223-231.
27. Neumeister A., Normandin M.D., Pietrzak R.H., et al. Elevated brain cannabinoid CB1 receptor availability in post-traumatic stress disorder: a positron emission tomography study. Mol. Psychiatry 2013, 18:1034-1040.
28. Parsons R.G., Ressler K.J. Implications of memory modulation for post-traumatic stress and fear disorders. Nat. Neurosci. 2013, 16:146-153.
29. Passie T., Emrich H.M., Karst M., et al. Mitigation of post-traumatic stress symptoms by Cannabis resin: a review of the clinical and neurobiological evidence. Drug Test. Anal. 2012, 4:649-659.
30. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2009, Academic Press, San Diego. Compact 6th ed.
31. Pertwee R.G. The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol, cannabidiol and delta9-tetrahydrocannabivarin. Br. J. Pharmacol. 2008, 153:199-215.
32. Pertwee R.G. Targeting the endocannabinoid system with cannabinoid receptor agonists: pharmacological strategies and therapeutic possibilities. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2012, 5:3353-3363.
33. Pitman R.K., Rasmusson A.M., Koenen K.C., et al. Biological studies of post-traumatic stress disorder. Nat. Rev. Neurosci. 2012, 13:769-787.
34. Puighermanal E., Busquets-Garcia A., Gomis-González M., et al. Dissociation of the pharmacological effects of THC by mTOR blockade. Neuropsychopharmacology 2013, 38:1334-1343.
35. Puighermanal E., Marsicano G., Busquets-Garcia A., et al. Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling. Nat. Neurosci. 2009, 12:1152-1158.
36. Reid M.J., Bornheim L.M. Cannabinoid-induced alterations in brain disposition of drugs of abuse. Biochem. Pharmacol. 2001, 61:1357-1367.
37. Roitman P., Mechoulam R., Cooper-Kazaz R., et al. Preliminary, open-label, pilot study of add-on oral δ9-tetrahydrocannabinol in chronic post-traumatic stress disorder. Clin. Drug Investig. 2014, 34:587-591.
38. Stern C.A., Do Monte F.H., Gazarini L., et al. Activity in prelimbic cortex is required for adjusting the anxiety response level during the elevated plus-maze retest. Neuroscience 2010, 170:214-222.
39. Stern C.A., Gazarini L., Takahashi R.N., et al. On disruption of fear memory by reconsolidation blockade: evidence from cannabidiol treatment. Neuropsychopharmacology 2012, 37:2132-2142.
40. Stern C.A., Gazarini L., Vanvossen A.C., et al. Activity in prelimbic cortex subserves fear memory reconsolidation over time. Learn. Mem. 2014, 21:14-20.
41. Trezza V., Campolongo P. The endocannabinoid system as a possible target to treat both the cognitive and emotional features of post-traumatic stress disorder (PTSD). Front. Behav. Neurosci. 2013, 7:100.
42. Vann R.E., Gamage T.F., Warner J.A., et al. Divergent effects of cannabidiol on the discriminative stimulus and place conditioning effects of Delta(9)-tetrahydrocannabinol. Drug Alcohol Depend. 2008, 94:191-198.
43. Varvel S.A., Wiley J.L., Yang R., et al. Interactions between THC and cannabidiol in mouse models of cannabinoid activity. Psychopharmacology 2006, 186:226-234.
44. Volkow N.D., Baler R.D., Compton W.M., et al. Adverse health effects of marijuana use. N. Engl. J. Med. 2014, 370:2219-2227.
45. Wise L.E., Thorpe A.J., Lichtman A.H. Hippocampal CB(1) receptors mediate the memory impairing effects of Delta(9)-tetrahydrocannabinol. Neuropsychopharmacology 2009, 34:2072-2080.
46. Zamengo L., Frison G., Bettin C., et al. Variability of cannabis potency in the Venice area (Italy): a survey over the period 2010-2012. Drug Test. Anal. 2014, 6:46-51.