The CB1 Receptor Antagonist AM251 Impairs Reconsolidation of Pavlovian Fear Memory in the Rat Basolateral Amygdala

Neuropsychopharmacology

Volumn 39, Issue 11, 2014, Pages 2529-2537

  Ratano, Patrizia ^a,b   Everitt, Barry J ^a   Milton, Amy L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; AMIDASE; BENZAMIDE DERIVATIVE; BICUCULLINE; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CARBAMIC ACID DERIVATIVE; CYCLOHEXYL CARBAMIC ACID 3'-CARBAMOYLBIPHENYL-3-YL ESTER; ENZYME INHIBITOR; FATTY-ACID AMIDE HYDROLASE; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE;

ANIMAL; ANTAGONISTS AND INHIBITORS; BASOLATERAL AMYGDALA; CONDITIONED REFLEX; DRUG EFFECTS; ELECTRIC SHOCK; FEAR; HEARING; MALE; MEMORY; METABOLISM; PHYSIOLOGY; RAT;

AMIDOHYDROLASES; ANIMALS; AUDITORY PERCEPTION; BASOLATERAL NUCLEAR COMPLEX; BENZAMIDES; BICUCULLINE; CANNABINOID RECEPTOR ANTAGONISTS; CARBAMATES; CONDITIONING, CLASSICAL; ELECTROSHOCK; ENZYME INHIBITORS; FEAR; GABA-A RECEPTOR ANTAGONISTS; MALE; MEMORY; PIPERIDINES; PYRAZOLES; RATS; RECEPTOR, CANNABINOID, CB1; RECEPTORS, GABA-A;

EID: 84939894948     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.103     Document Type: Article

References (56)

1. Arenos JD, Musty RE, Bucci DJ (2006). Blockade of cannabinoid CB1 receptors alters contextual learning and memory. Eur J Pharmacol 539: 177-183.
2. Azad SC, Eder M, Marsicano G, Lutz B, Zieglgä nsberger W, Rammes G (2003). Activation of the cannabinoid receptor type 1 decreases glutamatergic and GABAergic synaptic transmission in the lateral amygdala of the mouse. Learn Memory 10: 116-128.
3. Azad SC, Monory K, Marsicano G, Cravatt BF, Lutz B, Zieglgansberger W et al (2004). Circuitry for associative plasticity in the amygdala involves endocannabinoid s ignalling. J Neurosci 24: 9953-9961.
4. Barad M, Gean P-W, Lutz B (2006). The role of the amygdala in the extinction of conditioned fear. Biol Psychiatry 60: 322-328.
5. Ben Mamou C, Gamache K, Nader K (2006). NMDA receptors are critical for unleashing consolidated auditory fear memories. Nat Neurosci 9: 1237-1239.
6. Berlau DJ, McGaugh JL (2006). Enhancement of extinction memory consolidation: The role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol Learn Mem 86: 123-132.
7. Bouton ME (1991). Context and retrieval in extinction and in other examples of interference in simple associative learning. In: Dachowski LFlaherty CF (eds) Current Topics in Animal Learning: Brain, Emotion and Cognition. Lawrence Erlbaum Associates: Hillsdale, NJ. pp. 25-53.
8. Brewin CR, Dalgleish T, Joseph S (1996). A dual representation theory of post traumatic stress disorder. Psychol Rev 103: 670-686.
9. Brunet A, Orr SP, Tremblay J, Robertson K, Nader K, Pitman RK (20 08). Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. J Psychiatr Res 42: 503-506.
10. Bucherelli C, Baldi E, Mariottini C, Passani MB, Blandina P (2006). Aversive memory reactivation engages in the amygdala only some neurotransmitters involved in consolidation. Learn Mem 13: 426-430.
11. Bustos SG, Maldonado H, Molina VA (2006). Midazolam disrupts fear memory reconsolidation. Neuroscience 139: 831-842.
12. Campolongo P (2010). The role of endocannabinoids in the amygdala in the regulation of emotional memory. Eur Neuropsychopharmacol 20(Suppl 3): S169.
13. Campolongo P, Roozendaal B, Trezza V, Hauer D, Schelling G, McGaugh JL et al (2009). Endocannabinoids in the rat basolateral amygdala enhance memory consolidation a nd enable glucocorticoid modulation of memory. Proc Natl Acad Sci USA 106: 4888-4893.
14. Cardinal RN, Aitken MRF (2006). ANOVA for the Behavioural Sciences Researcher. Lawrence Erlbaum Associates, Inc.: London.
15. Chhatwal JP, Davis M, Maguschak KA, Ressler KJ (2005). Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 30: 516-524.
16. Daskalakis NP, Yehuda R, Diamond DM (2013). Animal models in translational studies of PTSD. Psychoneuroendocrinology 38: 1895-1911.
17. De Oliveira Alvares L, Genro BP, Diehl F, Quillfeldt JA (2008). Differential role of the hippocampal endocannabinoid system in the memory consolidation and retrieval mechanisms. Neurobiol Learn Mem 90: 1-9.
18. D?ebiec J, LeDoux JE (2004). Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129: 267-272.
19. D?ebiec J, LeDoux JE (2006). Noradrenergic signaling in the amygdala contributes to the reconsolidation of fear memory: Treatment implications for PTSD. Ann N Y Acad Sci 1071: 521-524.
20. D?ebiec J, LeDo ux JE, Nader K (2002). Cellular and systems reconsolidation in the hippocampus. Neuron 36: 527-538.
21. Dickinson-Anson H, McGaugh JL (1997). Bicuculline administered into the amygdala after training blocks benzodiazepine-induced amnesia. Brain Res 752: 197-202.
22. Fattore L, Cossu G, Martellotta CM, Fratta W (2001). Intravenous self-administration of the cannabinoid CB1 receptor agonist WIN 55,212-2 in rat s. Psychopharmacology 156: 410-416.
23. Finnie PSB, Nader K (2012). The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation. Neuroscie Biobehav Rev 36: 1667-1707.
24. Gale GD, Anagnostaras SG, Godsil BP, Mitchell S, Nozawa T, Sage JR et al (2004). Role of the basolateral amygdala in the storage of fear memories across the adult lifetime of rats. J Neurosci 24: 3810-3815.
25. Hasanein P Mohsen P Keshavarz M Javanmardi K 2007 CB1 receptor activation in the basolateral amygdala produces antinociception in animal models of acute and tonic nociception. Clin Exp Pharm acol Physiol 34 439-449.
26. Hauer D, Ratano P, Morena M, Scaccianoce S, Briegel I, Palmery M et al (2011). Propofol enhances memory formation via an interaction with the endocannabinoid system. An esthesiology 114: 1380-1388.
27. Hohmann AG, Suplita RL, Bolton NM, Neely MH, Fegley D, Mangieri R et al (2005). An endocannabinoid mechanism for stress-induced analgesia. Nature 435: 1108-1112.
28. Johansen JP, Cain CK, Ostroff LE, LeDoux JE (2011). Molecular mechanisms of fear learning and memory. Cell 147: 509-524.
29. Katona I, Rancz EA, Acsá dy L, Ledent C, Mackie K, Há jos N et al (2001). Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21: 9506-9518.
30. Kobilo T , Hazvi S, Dudai Y (2007). Role of cortical cannabinoid CB1 receptor in conditioned taste aversion memory. Eur J Neurosci 25: 3417-3421.
31. Lan R, Liu Q, Fan P, Lin S, Fernando SR, McCallio n D et al (1999). Structure-activity relationships of pyrazole derivatives as cannabinoid receptor antagonists. J Med Chem 42: 769-776.
32. Lee JLC (2008). Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci 11: 1264-1266.
33. Lee JLC, Di Ciano P, Thomas KL, Everitt BJ (2005). Disrupting reconsolidation of drug memories reduces cocaine seeking behavior. Neuron 47: 795-801.
34. Lee JLC, Milton AL, Everitt BJ (2006). Reconsolidation and extinction of conditioned fear: Inhibition and potentiation. J Neurosci 26: 10051-10056.
35. Lewis DJ (1979). Psychobiology of active and inactive memory. Psychol Bull 86: 1054-1083.
36. 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.
37. Mać kowiak M, Chocyk A, Dudys D, Wedzony K (2009). Activation of CB1 cannabinoid receptors impairs memory consolidation and hippocampal polysialylated neura l cell adhesion molecule expression in contextual fear conditioning. Neuroscience 158: 1708-1716.
38. Mahan AL, Ressler KJ (2012). Fear conditioning, synaptic plasticity and the amygdala: Implications for posttraumatic stress disorder. Trends Neurosci 35: 24-35.
39. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Casclo MG et al (2002). The endogenous cannabinoid system controls extinction of aversive m emories. Nature 418: 530-534.
40. Metna-Laurent M, Soria-Gó mez E, Verrier D, Conforzi M, Jégo P, Lafenêtre P et al (2012). Bimodal control of fear-coping strategies by CB1 cannabinoid receptors. J Neurosci 32: 7109-7118.
41. Milekic MH, Alberini CM (2002). Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36: 521-525.
42. Milton AL, Lee JLC, Butler VJ, Gardner RJ, Everitt BJ (2008). Intraamygdala and systemic antagonism of NMDA receptors prevents the reconsolidation of drug-associated memory and impairs subsequently both novel and previousl y acquired drug-seeking behaviors. J Neurosci 28: 8230-8237.
43. Milton AL, Merlo E, Ratano P, Gregory BL, Dumbreck JK, Everitt BJ (2013). Double dissociation of the requirement for GluN2Band GluN2A-con taining NMDA receptors in the destabilization and restabilization of a reconsolidating memory. J Neurosci 33: 1109-1115.
44. Mor M, Rivara S, Lodola A, Plazzi PV, Tarzia G, Duranti A et al (2004). Cyclohexylcarbamic acid 3'-or 4'-substituted biphenyl-3-yl esters as Fatty Acid Amide Hydrolase inhibitors: Synthesis, quantitative structure-activity relationships, and molecular modeling studies. J Med Chem 47: 4998-5008.
45. Nader K (2003). Memory traces unbound. Trends Neurosci 26: 65-72.
46. Nader K Schafe GE LeDoux JE 2000 Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406 722-726.
47. Parsons RG, Ressler KJ (2013). Implications of memory modulation for post-traumatic stress and fear disorders. Nat Neurosci 16: 146-153.
48. Paxinos G, Watson C (2004). The Rat Brain in Stereotaxic Coordinates, 5th ed. Academic Press: New York.
49. Piomelli D, Tarzia G, Duranti A, Tontini A, Mor M, Compton TR et al (2006). Pharmacological pr ofile of the selective FAAH inhibitor KDS-4103 (URB597). CNS Drug Rev 12: 21-38.
50. Ratano P, Trezza V, Morena M, Manduca A, Miele J, Campolongo P et al (2011). Effects of central administration of the indirect cannabinoid agonist URB597 in the modulation of emotional memory in rats. Eur Neuropsychopharmacol 21(Supplement 3): S342-S343.
51. Schiller D, Monfils MH, Raio CM, Johnson DC, LeDoux JE, Phelps EA (2010 ). Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463: 49-54.
52. Schiller D, Phelps EA (2011). Does reconsolidation occur in humans? Front Behav Neurosci 5: 24.
53. 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.
54. Suzuki A, Mukawa T, Tsukagoshi A, Frankland PW, Kida S (2008). Activation of LVGCCs and CB1 receptors required for destabilization of reactivated contextual fear memories. Learn Mem 15: 426-433.
55. Tan H, Lauzon NM, Bishop SF, Chi N, Bechard M, Laviolette SR (2011). Cannabinoid transmission in the basolateral amygdala modulates fear memory formation via functional inputs to the prelimbic cortex. J Neurosci 31: 5300-5312.
56. Zhang S, Cranney J (2008). The role of GABA and anxiety in the reconsolidation of conditioned fear. Behav Neurosci 122: 1295-1305.