A current overview of cannabinoids and glucocorticoids in facilitating extinction of aversive memories: Potential extinction enhancers

Neuropharmacology

Volumn 64, Issue , 2013, Pages 389-395

  De Bitencourt, Rafael Mariano ^a   Pamplona, Fabrício Alano ^b   Takahashi, Reinaldo Naoto ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b D OR INSTITUTE FOR RESEARCH AND EDUCATION IDOR   (Brazil)

Author keywords

Cannabinoids; Extinction; Extinction enhancers; Fear conditioning; Glucocorticoid

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 11BETA,17BETA DIHYDROXY 6 METHYL 17ALPHA (1 PROPYNYL)ANDROSTA 1,4,6 TRIEN 3 ONE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ANANDAMIDE; ANXIOLYTIC AGENT; CANNABIDIOL; CANNABINOID; CORTICOSTERONE; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; DEXAMETHASONE; GLUCOCORTICOID; HYDROCORTISONE; METYRAPONE; MIFEPRISTONE; N (4 HYDROXYPHENYL)ARACHIDONAMIDE; RIMONABANT; SPIRONOLACTONE;

AMYGDALOID NUCLEUS; ANXIETY DISORDER; AVERSION; AVERSIVE MEMORY; AVOIDANCE BEHAVIOR; CONDITIONING; DRUG MECHANISM; FACILITATION; FEAR; FEEDBACK SYSTEM; HIPPOCAMPUS; HORMONE ACTION; HUMAN; MEMORY; MEMORY CONSOLIDATION; MEMORY EXTINCTION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PSYCHOTHERAPY; PSYCHOTRAUMA; REINFORCEMENT; REVIEW; SIGNAL TRANSDUCTION; STARTLE REFLEX; TREATMENT RESPONSE;

ANIMALS; CANNABINOIDS; CENTRAL NERVOUS SYSTEM AGENTS; COMBINED MODALITY THERAPY; ENDOCANNABINOIDS; EXTINCTION, PSYCHOLOGICAL; FEAR; GLUCOCORTICOIDS; HUMANS; LIFE CHANGE EVENTS; MEMORY, EPISODIC; MENTAL RECALL; PSYCHOTHERAPY; STRESS, PSYCHOLOGICAL;

EID: 84866418810     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.05.039     Document Type: Review

References (91)

1. H. Abush, and I. Akirav Cannabinoids modulate hippocampal memory and plasticity Hippocampus 20 2009 1126 1138
2. A. Aerni, R. Traber, C. Hock, B. Roozendaal, G. Schelling, A. Papassotiropoulos, R.M. Nitsch, U. Schnyder, and D.J. de Quervain Low-dose cortisol for symptoms of posttraumatic stress disorder Am. J. Psychiatry 161 2004 1488 1490
3. D. Anglada-Figueroa, and G.J. Quirk Lesions of the basal amygdala block expression of conditioned fear but not extinction J. Neurosci. 25 2005 9680 9685
4. P. Atsak, D. Hauer, P. Campolongo, G. Schelling, J.L. McGaugh, and B. Roozendaal Glucocorticoids interact with the hippocampal endocannabinoid system in impairing retrieval of contextual fear memory Proc. Natl. Acad. Sci. U S A 109 2012 3504 3509
5. I. Barna, D. Zelena, A.C. Arszovszki, and C. Ledent The role of endogenous cannabinoids in the hypothalamo-pituitary-adrenal axis regulation: in vivo and in vitro studies in CB1 receptor knockout mice Life Sci. 75 2004 2959 2970
6. D. Barrett, and F. Gonzalez-Lima Behavioral effects of metyrapone on Pavlovian extinction Neurosci. Lett. 371 2004 91 96
7. D. Bentz, T. Michael, de Quervain D.J.; and F.H. Wilhelm Enhancing exposure therapy for anxiety disorders with glucocorticoids: from basic mechanisms of emotional learning to clinical applications J. Anxiety Disord. 24 2009 223 230
8. R.M. Bitencourt, F.A. Pamplona, and R.N. Takahashi Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats Eur. Neuropsychopharmacol. 2008
9. R.J. Blanchard, and D.C. Blanchard Crouching as an index of fear J. Comp. Physiol. Psychol. 67 1969 370 375
10. S. Blum, A.E. Hebert, and P.K. Dash A role for the prefrontal cortex in recall of recent and remote memories Neuroreport 17 2006 341 344
11. J. Blundell, C.A. Blaiss, D.C. Lagace, A.J. Eisch, and C.M. Powell Block of glucocorticoid synthesis during re-activation inhibits extinction of an established fear memory Neurobiol. Learn. Mem. 95 2011 453 460
12. B. Bohus, R.E. De Kloet, and H.D. Veldhuis Adrenal Steroids and Behavioral Adaptation: Relationship to Brain Corticoid Receptors. Adrenal Actions on Brain 1982 Springer-Verlag Berlin pp. 107-148
13. M.E. Bouton, and D. Swartzentruber Slow reacquisition following extinction - context, encoding, and retrieval mechanisms J. Exp. Psychology-Animal Behav. Process. 15 1989 43 53
14. D.C. Brooks, and M.E. Bouton A retrieval cue for extinction attenuates spontaneous-recovery J. Exp. Psychology-Animal Behav. Process. 19 1993 77 89
15. A.K. Bruchey, J. Shumake, and F. Gonzalez-Lima Network model of fear extinction and renewal functional pathways Neuroscience 145 2007 423 437
16. R.A. Bryant Acute stress disorder as a predictor of posttraumatic stress disorder: a systematic review J. Clin. Psychiatry 72 2011 233 239
17. M. Cammarota, L.R. Bevilaqua, D. Kerr, J.H. Medina, and I. Izquierdo Inhibition of mRNA and protein synthesis in the CA1 region of the dorsal hippocampus blocks reinstallment of an extinguished conditioned fear response J. Neurosci. 23 2003 737 741
18. P. Campolongo, B. Roozendaal, V. Trezza, D. Hauer, G. Schelling, J.L. McGaugh, and V. Cuomo Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory Proc. Natl. Acad. Sci. U S A 106 2009 4888 4893
19. A. Cannich, C.T. Wotjak, K. Kamprath, H. Hermann, B. Lutz, and G. Marsicano CB1 cannabinoid receptors modulate kinase and phosphatase activity during extinction of conditioned fear in mice Learn. Mem. 11 2004 625 632
20. J.P. Chhatwal, M. Davis, K.A. Maguschak, and K.J. Ressler Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear Neuropsychopharmacology 30 2005 516 524
21. S.R. Childers, and C.S. Breivogel Cannabis and endogenous cannabinoid systems Drug Alcohol Depend. 51 1998 173 187
22. R. Clay, M. Hebert, G. Gill, L.A. Stapleton, A. Pridham, M. Coady, J. Bishop, R.E. Adamec, and J.J. Blundell Glucocorticoids are required for extinction of predator stress-induced hyperarousal Neurobiol. Learn. Mem. 96 2011 367 377
23. K.A. Corcoran, and G.J. Quirk Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears J. Neurosci. 27 2007 840 844
24. M. Davis, K.M. Myers, J. Chhatwal, and K.J. Ressler Pharmacological treatments that facilitate extinction of fear: relevance to psychotherapy NeuroRx 3 2006 82 96
25. S. Di, R. Malcher-Lopes, K.C. Halmos, and J.G. Tasker Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism J. Neurosci. 23 2003 4850 4857
26. S. Dubreucq, M. Koehl, D.N. Abrous, G. Marsicano, and F. Chaouloff CB1 receptor deficiency decreases wheel-running activity: consequences on emotional behaviours and hippocampal neurogenesis Exp. Neurol. 224 2010 106 113
27. van Eekelen J.A.; J.Z. Kiss, H.M. Westphal, and E.R. de Kloet Immunocytochemical study on the intracellular localization of the type 2 glucocorticoid receptor in the rat brain Brain Res. 436 1987 120 128
28. K. Fuxe, A.C. Wikstrom, S. Okret, L.F. Agnati, A. Harfstrand, Z.Y. Yu, L. Granholm, M. Zoli, W. Vale, and J.A. Gustafsson Mapping of glucocorticoid receptor immunoreactive neurons in the rat tel- and diencephalon using a monoclonal antibody against rat liver glucocorticoid receptor Endocrinology 117 1985 1803 1812
29. E. Ganon-Elazar, and I. Akirav Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance J. Neurosci. 29 2009 11078 11088
30. E. Ganon-Elazar, and I. Akirav Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress Neuropsychopharmacology 37 2012 456 466
31. M.R. Gilmartin, and M.D. McEchron Single neurons in the medial prefrontal cortex of the rat exhibit tonic and phasic coding during trace fear conditioning Behav. Neurosci. 119 2005 1496 1510
32. J.H. Gordon, B.L. Bromley, R.A. Gorski, and E. Zimmermann Delta9-tetrahydrocannabinol enhancement of lordosis behavior in estrogen treated female rats Pharmacol. Biochem. Behav. 8 1978 603 608
33. U. Heresco-Levy, I. Kremer, D.C. Javitt, R. Goichman, A. Reshef, M. Blanaru, and T. Cohen Pilot-controlled trial of D-cycloserine for the treatment of post-traumatic stress disorder Int. J. Neuropsychopharmacol. 5 2002 301 307
34. U. Heresco-Levy, A. Vass, B. Bloch, H. Wolosker, E. Dumin, L. Balan, L. Deutsch, and I. Kremer Pilot controlled trial of D-serine for the treatment of post-traumatic stress disorder Int. J. Neuropsychopharmacol. 12 2009 1275 1282
35. C. Herry, F. Ferraguti, N. Singewald, J.J. Letzkus, I. Ehrlich, and A. Luthi Neuronal circuits of fear extinction Eur. J. Neurosci. 31 2010 599 612
36. M.N. Hill, W.S. Ho, S.E. Meier, B.B. Gorzalka, and C.J. Hillard Chronic corticosterone treatment increases the endocannabinoid 2-arachidonylglycerol in the rat amygdala Eur. J. Pharmacol. 528 2005 99 102
37. M.N. Hill, S. Patel, P. Campolongo, J.G. Tasker, C.T. Wotjak, and J.S. Bains Functional interactions between stress and the endocannabinoid system: from synaptic signaling to behavioral output J. Neurosci. 30 2010 14980 14986
38. M.N. Hill, R.J. McLaughlin, B. Pan, M.L. Fitzgerald, C.J. Roberts, T.T. Lee, I.N. Karatsoreos, K. Mackie, V. Viau, V.M. Pickel, B.S. McEwen, Q.S. Liu, B.B. Gorzalka, and C.J. Hillard Recruitment of prefrontal cortical endocannabinoid signaling by glucocorticoids contributes to termination of the stress response J. Neurosci. 31 2011 10506 10515
39. A.L. Jackson, and L.L. Murphy Role of the hypothalamic-pituitary-adrenal axis in the suppression of luteinizing hormone release by delta-9- tetrahydrocannabinol Neuroendocrinology 65 1997 446 452
40. K. Kamprath, and C.T. Wotjak Nonassociative learning processes determine expression and extinction of conditioned fear in mice Learn. Mem. 11 2004 770 786
41. K. Kamprath, G. Marsicano, J. Tang, K. Monory, T. Bisogno, V. Di Marzo, B. Lutz, and C.T. Wotjak Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes J. Neurosci. 26 2006 6677 6686
42. G.B. Kaplan, and K.A. Moore The use of cognitive enhancers in animal models of fear extinction Pharmacol. Biochem. Behav. 2011
43. J.J. Kim, and M.W. Jung Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review Neurosci. Biobehav. Rev. 30 2006 188 202
44. S.M. Korte Corticosteroids in relation to fear, anxiety and psychopathology Neurosci. Biobehav. Rev. 25 2001 117 142
45. P. Lafenetre, F. Chaouloff, and G. Marsicano The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction Pharmacol. Res. 56 2007 367 381
46. S.R. Laviolette, W.J. Lipski, and A.A. Grace A subpopulation of neurons in the medial prefrontal cortex encodes emotional learning with burst and frequency codes through a dopamine D4 receptor-dependent basolateral amygdala input J. Neurosci. 25 2005 6066 6075
47. K. Lebron, M.R. Milad, and G.J. Quirk Delayed recall of fear extinction in rats with lesions of ventral medial prefrontal cortex Learn. Mem. 11 2004 544 548
48. H.C. Lin, S.C. Mao, C.L. Su, and P.W. Gean The role of prefrontal cortex CB1 receptors in the modulation of fear memory Cereb. Cortex 19 2009 165 175
49. P. Mailleux, and J.J. Vanderhaeghen Glucocorticoid regulation of cannabinoid receptor messenger RNA levels in the rat caudate-putamen. An in situ hybridization study Neurosci. Lett. 156 1993 51 53
50. S. Maren Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats Eur. J. Neurosci. 28 2008 1661 1666
51. A. Marowsky, Y. Yanagawa, K. Obata, and K.E. Vogt A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function Neuron 48 2005 1025 1037
52. G. Marsicano, C.T. Wotjak, S.C. Azad, T. Bisogno, G. Rammes, M.G. Cascio, H. Hermann, J. Tang, C. Hofmann, W. Zieglgansberger, V. Di Marzo, and B. Lutz The endogenous cannabinoid system controls extinction of aversive memories Nature 418 2002 530 534
53. A.J. McDonald, F. Mascagni, and L. Guo Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat Neuroscience 71 1996 55 75
54. M.R. Milad, and G.J. Quirk Neurons in medial prefrontal cortex signal memory for fear extinction Nature 420 2002 70 74
55. M.R. Milad, I. Vidal-Gonzalez, and G.J. Quirk Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner Behav. Neurosci. 118 2004 389 394
56. F.A. Moreira, and C.T. Wotjak Cannabinoids and anxiety Curr. Top. Behav. Neurosci. 2 2010 429 450
57. M.A. Morgan, L.M. Romanski, and J.E. LeDoux Extinction of emotional learning: contribution of medial prefrontal cortex Neurosci. Lett. 163 1993 109 113
58. D. Mueller, J.T. Porter, and G.J. Quirk Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction J. Neurosci. 28 2008 369 375
59. K.M. Myers, and M. Davis Mechanisms of fear extinction Mol. Psychiatry 12 2007 120 150
60. R.M. Napier, M. Macrae, and E.J. Kehoe Rapid reacquisition in conditioning of the rabbits nictitating-membrane response J. Exp. Psychology-Animal Behav. Process. 18 1992 182 192
61. E.M. Ninomiya, B.J. Martynhak, J.M. Zanoveli, D. Correia, C. da Cunha, and R. Andreatini Spironolactone and low-dose dexamethasone enhance extinction of contextual fear conditioning Prog. Neuropsychopharmacol. Biol. Psychiatry 34 2010 1229 1235
62. F. Niyuhire, S.A. Varvel, A.J. Thorpe, R.J. Stokes, J.L. Wiley, and A.H. Lichtman The disruptive effects of the CB1 receptor antagonist rimonabant on extinction learning in mice are task-specific Psychopharmacology (Berl) 191 2007 223 231
63. L. de Oliveira Alvares, B. Pasqualini Genro, F. Diehl, V.A. Molina, and J.A. Quillfeldt Opposite action of hippocampal CB1 receptors in memory reconsolidation and extinction Neuroscience 154 2008 1648 1655
64. L. de Oliveira Alvares, D.S. Engelke, F. Diehl, R. Scheffer-Teixeira, J. Haubrich, L. de Freitas Cassini, V.A. Molina, and J.A. Quillfeldt Stress response recruits the hippocampal endocannabinoid system for the modulation of fear memory Learn. Mem. 17 2010 202 209
65. F.A. Pamplona, R.D. Prediger, P. Pandolfo, and R.N. Takahashi The cannabinoid receptor agonist WIN 55,212-2 facilitates the extinction of contextual fear memory and spatial memory in rats Psychopharmacology (Berl) 188 2006 641 649
66. F.A. Pamplona, R.M. Bitencourt, and R.N. Takahashi Short- and long-term effects of cannabinoids on the extinction of contextual fear memory in rats Neurobiol. Learn. Mem. 90 2008 290 293
67. H.C. Pape, and D. Pare Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear Physiol. Rev. 90 2010 419 463
68. D. Pare, and Y. Smith The intercalated cell masses project to the central and medial nuclei of the amygdala in cats Neuroscience 57 1993 1077 1090
69. D. Pare, and Y. Smith Intrinsic circuitry of the amygdaloid complex: common principles of organization in rats and cats Trends Neurosci. 21 1998 240 241
70. D. Pare, G.J. Quirk, and J.E. Ledoux New vistas on amygdala networks in conditioned fear J. Neurophysiol. 92 2004 1 9
71. S. Patel, C.T. Roelke, D.J. Rademacher, and C.J. Hillard Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling Eur. J. Neurosci. 21 2005 1057 1069
72. W. Plendl, and C.T. Wotjak Dissociation of within- and between-session extinction of conditioned fear J. Neurosci. 30 2010 4990 4998
73. G. Pryce, G. Giovannoni, and D. Baker Mifepristone or inhibition of 11beta-hydroxylase activity potentiates the sedating effects of the cannabinoid receptor-1 agonist Delta(9)-tetrahydrocannabinol in mice Neurosci. Lett. 341 2003 164 166
74. C.B. Pull Combined pharmacotherapy and cognitive-behavioural therapy for anxiety disorders Curr. Opin. Psychiatry 20 2007 30 35
75. de Quervain D.J.; A. Aerni, G. Schelling, and B. Roozendaal Glucocorticoids and the regulation of memory in health and disease Front. Neuroendocrinol. 30 2009 358 370
76. de Quervain D.J.; D. Bentz, T. Michael, O.C. Bolt, B.K. Wiederhold, J. Margraf, and F.H. Wilhelm Glucocorticoids enhance extinction-based psychotherapy Proc. Natl. Acad. Sci. U S A 108 2011 6621 6625
77. G.J. Quirk, and D. Mueller Neural mechanisms of extinction learning and retrieval Neuropsychopharmacology 33 2008 56 72
78. G.J. Quirk, D. Pare, R. Richardson, C. Herry, M.H. Monfils, D. Schiller, and A. Vicentic Erasing fear memories with extinction training J. Neurosci. 30 2010 14993 14997
79. C.J. Riebe, F. Pamplona, K. Kamprath, and C.T. Wotjak Fear relief-toward a new conceptual frame work and what endocannabinoids gotta do with it Neuroscience 204 2012 159 185
80. J.I. Rossato, L.R. Bevilaqua, R.H. Lima, J.H. Medina, I. Izquierdo, and M. Cammarota On the participation of hippocampal p38 mitogen-activated protein kinase in extinction and reacquisition of inhibitory avoidance memory Neuroscience 143 2006 15 23
81. S. Royer, M. Martina, and D. Pare An inhibitory interface gates impulse traffic between the input and output stations of the amygdala J. Neurosci. 19 1999 10575 10583
82. G. Schelling, E. Kilger, B. Roozendaal, de Quervain D.J.; J. Briegel, A. Dagge, H.B. Rothenhausler, T. Krauseneck, G. Nollert, and H.P. Kapfhammer Stress doses of hydrocortisone, traumatic memories, and symptoms of posttraumatic stress disorder in patients after cardiac surgery: a randomized study Biol. Psychiatry 55 2004 627 633
83. L.M. Shin, and I. Liberzon The neurocircuitry of fear, stress, and anxiety disorders Neuropsychopharmacology 35 2009 169 191
84. L.M. Soravia, M. Heinrichs, A. Aerni, C. Maroni, G. Schelling, U. Ehlert, B. Roozendaal, and D.J. de Quervain Glucocorticoids reduce phobic fear in humans Proc. Natl. Acad. Sci. U S A 103 2006 5585 5590
85. A. Suzuki, S.A. Josselyn, P.W. Frankland, S. Masushige, A.J. Silva, and S. Kida Memory reconsolidation and extinction have distinct temporal and biochemical signatures J. Neurosci. 24 2004 4787 4795
86. I. Vidal-Gonzalez, B. Vidal-Gonzalez, S.L. Rauch, and G.J. Quirk Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear Learn. Mem. 13 2006 728 733
87. D.L. Walker, and M. Davis The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction Pharmacol. Biochem. Behav. 71 2002 379 392
88. J. Weidenfeld, S. Feldman, and R. Mechoulam Effect of the brain constituent anandamide, a cannabinoid receptor agonist, on the hypothalamo-pituitary-adrenal axis in the rat Neuroendocrinology 59 1994 110 112
89. Y.L. Yang, P.K. Chao, and K.T. Lu Systemic and intra-amygdala administration of glucocorticoid agonist and antagonist modulate extinction of conditioned fear Neuropsychopharmacology 31 2006 912 924
90. Y.L. Yang, P.K. Chao, L.S. Ro, Y.Y. Wo, and K.T. Lu Glutamate NMDA receptors within the amygdala participate in the modulatory effect of glucocorticoids on extinction of conditioned fear in rats Neuropsychopharmacology 32 2007 1042 1051
91. R. Yehuda, J.A. Golier, S.L. Halligan, M. Meaney, and L.M. Bierer The ACTH response to dexamethasone in PTSD Am. J. Psychiatry 161 2004 1397 1403