Cannabinoid receptors activation and glucocorticoid receptors deactivation in the amygdala prevent the stress-induced enhancement of a negative learning experience

Neurobiology of Learning and Memory

Volumn 97, Issue 4, 2012, Pages 393-401

  Ramot, Assaf ^a   Akirav, Irit ^a  

^a UNIVERSITY OF HAIFA   (Israel)

Author keywords

Alley maze; Basolateral amygdala; Cannabinoids; Glucocorticoids; Stress; WIN55,212 2

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID RECEPTOR; CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; MIFEPRISTONE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CONTROLLED STUDY; FEAR; LATENT PERIOD; LEARNING; MALE; MEMORY CONSOLIDATION; NEGATIVE LEARNING EXPERIENCE; NONHUMAN; RAT; REINFORCEMENT; REWARD; STRESS;

AMYGDALA; ANIMALS; BENZOXAZINES; HORMONE ANTAGONISTS; LEARNING; MALE; MEMORY; MIFEPRISTONE; MORPHOLINES; NAPHTHALENES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CANNABINOID; RECEPTORS, GLUCOCORTICOID; REWARD; STRESS, PSYCHOLOGICAL;

EID: 84861185269     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2012.03.003     Document Type: Article

References (61)

1. Abush H., Akirav I. Cannabinoids modulate hippocampal memory and plasticity. Hippocampus 2010, 20:1126-1138.
2. Akirav I., Kozenicky M., Tal D., Sandi C., Venero C., Richter-Levin G. A facilitative role for corticosterone in the acquisition of a spatial task under moderate stress. Learning and Memory 2004, 11:188.
3. Akirav I., Sandi C., Richter-Levin G. Differential activation of hippocampus and amygdala following spatial learning under stress. European Journal of Neuroscience 2001, 14:719-725.
4. Amsel A. The role of frustrative nonreward in noncontinuous reward situations. Psychological Bulletin 1958, 55:102-119.
5. Amsel A. Frustrative nonreward in partial reinforcement and discrimination learning: Some recent history and a theoretical extension. Psychological Review 1962, 69:306-328.
6. Atsak P., Roozendaal B., Campolongo P. Role of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences. Neuroscience 2011.
7. Brown G., Bifulco A., Harris T. Life events, vulnerability and onset of depression: Some refinements. British Journal of Psychiatry 1987, 150:30.
8. Cahill L., McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory. Trends in Neurosciences 1998, 21:294-299.
9. Campolongo P., Roozendaal B., Trezza V., Hauer D., Schelling G., McGaugh J.L., et al. Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:4888.
10. Conrad C.D., MacMillan I., Donald D., Tsekhanov S., Wright R.L., Baran S.E., et al. Influence of chronic corticosterone and glucocorticoid receptor antagonism in the amygdala on fear conditioning. Neurobiology of Learning and Memory 2004, 81:185-199.
11. Cordero M.I., Merino J.J., Sandi C. Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. Behavioral Neuroscience 1998, 112:885-890.
12. Crespi L.P. Quantitative variation of incentive and performance in the white rat. American Journal of Psychology 1942, 55:467-517.
13. Davis M., Myers K.M., Chhatwal J., Ressler K.J. Pharmacological treatments that facilitate extinction of fear: relevance to psychotherapy. NeuroRx 2006, 3:82-96.
14. de Kloet E.R., Oitzl M.S., Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends in Neurosciences 1999, 22:422-426.
15. Di Marzo V., Matias I. Endocannabinoid control of food intake and energy balance. Nature Neuroscience 2005, 8:585-589.
16. Diamond D.M., Campbell A.M., Park C.R., Woodson J.C., Conrad C.D., Bachstetter A.D., et al. Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 2006, 16:571-576.
17. Donley M.P., Schulkin J., Rosen J.B. Glucocorticoid receptor antagonism in the basolateral amygdala and ventral hippocampus interferes with long-term memory of contextual fear. Behavioural Brain Research 2005, 164:197-205.
18. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1. Behavioral data. Behavioural Brain Research 1988, 1:47-59.
19. Flaherty C.F., Becker H.C., Pohorecky L. Correlation of corticosterone elevation and negative contrast varies as a function of postshift day. Animal Learning and Behavior 1985, 13:309-314.
20. Fraser G.A. The use of a synthetic cannabinoid in the management of treatment-resistant nightmares in posttraumatic stress disorder (PTSD) CNS. Neuroscience and Therapeutics 2009, 15:84-88.
21. Gallagher M., Chiba A.A. The amygdala and emotion. Current Opinion in Neurobiology 1996, 6:221-227.
22. Ganon-Elazar E., Akirav I. Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. Journal of Neuroscience 2009, 29:11078.
23. Ganon-Elazar E., Akirav I. Cannabinoids prevent the development of behavioral and endocrine alterations in a rat model of intense stress. Neuropsychopharmacology 2012, 37:456-466.
24. Ginsberg A.B., Pecoraro N.C., Warne J.P., Horneman H.F., Dallman M.F. Rapid alteration of stress-induced hypothalamic-pituitary-adrenal hormone secretion in the rat: A comparison of glucocorticoids and cannabinoids. Stress 2010, 13:248-257.
25. Goldman L., Coover G.D., Levine S. Bidirectional effects of reinforcement shifts on pituitary adrenal activity. Physiology and Behavior 1973, 10:209-214.
26. Gomez R., Navarro M., Ferrer B., Trigo J.M., Bilbao A., Del Arco I., et al. A peripheral mechanism for CB1 cannabinoid receptor-dependent modulation of feeding. Journal of Neuroscience 2002, 22:9612.
27. Gorzalka B.B., Hill M.N., Hillard C.J. Regulation of endocannabinoid signaling by stress: implications for stress-related affective disorders. Neuroscience and Biobehavioral Reviews 2008, 32:1152-1160.
28. Hamann S.B., Ely T.D., Grafton S.T., Kilts C.D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience 1999, 2:289-293.
29. Hennessy M.B., Heybach J.P., Vernikos J., Levine S. Plasma corticosterone concentrations sensitively reflect levels of stimulus intensity in the rat. Physiology and Behavior 1979, 22:821-825.
30. Hill M.N., Hillard C.J., Bambico F.R., Patel S., Gorzalka B.B., Gobbi G. The therapeutic potential of the endocannabinoid system for the development of a novel class of antidepressants. Trends in Pharmacological Sciences 2009, 30:484-493.
31. Hill M.N., McLaughlin R.J., Morrish A.C., Viau V., Floresco S.B., Hillard C.J., et al. Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the Hypothalamic-Pituitary-Adrenal axis. Neuropsychopharmacology 2009, 34:2733-2745.
32. Hopwood S., Bryant R.A. Intrusive experiences and hyperarousal in acute stress disorder. British Journal of Clinical Psychology 2006, 45:137-142.
33. Katona I., Rancz E.A., Acsady L., Ledent C., Mackie K., Hajos N., et al. Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. Journal of Neuroscience 2001, 21:9506-9518.
34. Kerfoot E.C., Chattillion E.A., Williams C.L. Functional interactions between the nucleus tractus solitarius (NTS) and nucleus accumbens shell in modulating memory for arousing experiences. Neurobiology of Learning and Memory 2008, 89:47-60.
35. Kirkham T. Endocannabinoids in the regulation of appetite and body weight. Behavioural Pharmacology 2005, 16:297.
36. Laviolette S.R., Grace A.A. Cannabinoids potentiate emotional learning plasticity in neurons of the medial prefrontal cortex through basolateral amygdala inputs. Journal of Neuroscience 2006, 26:6458.
37. Maroun M., Akirav I. Arousal and stress effects on consolidation and reconsolidation of recognition memory. Neuropsychopharmacology 2008, 339:394-405.
38. Marsicano G., Wotjak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., et al. Nature 2002, 418:530-534.
39. McGaugh J. Memory - a century of consolidation. Science 2000, 287:248-251.
40. McGhee N.K., Jefferson L.S., Kimball S.R. Elevated corticosterone associated with food deprivation upregulates expression in rat skeletal muscle of the mTORC1 repressor, REDD1. Journal of Nutrition 2009, 139:828.
41. Oitzl M.S., Fluttert M., Sutanto W., de Kloet E.R. Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. European Journal of Neuroscience 1998, 10:3759-3766.
42. Okuda S., Roozendaal B., McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proceedings of the National Academy of Sciences of the United States of America 2004, 20:853-858.
43. Patel S., Cravatt B.F., Hillard C.J. Synergistic interactions between cannabinoids and environmental stress in the activation of the central amygdala. Neuropsychopharmacology 2005, 30:497-507.
44. Patel S., Roelke C.T., Rademacher D.J., Cullinan W.E., Hillard C.J. Endocannabinoid signaling negatively modulates stress-induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology 2004, 145:5431.
45. Phan K.L., Angstadt M., Golden J., Onyewuenyi I., Popovska A., de Wit H. Cannabinoid modulation of amygdala reactivity to social signals of threat in humans. Journal of Neuroscience 2008, 28:2313-2319.
46. Pistis M., Perra S., Pillolla G., Melis M., Gessa G.L., Muntoni A.L. Cannabinoids modulate neuronal firing in the rat basolateral amygdala: evidence for CB1- and non-CB1-mediated actions. Neuropharmacology 2004, 46:115-125.
47. Pugh C.R., Tremblay D., Fleshner M., Rudy J.W. A selective role for corticosterone in contextual-fear conditioning. Behavioral Neuroscience 1997, 111:503-511.
48. Quirarte G.L., Roozendaal B., McGaugh J.L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:14048.
49. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory 2002, 78:578-595.
50. Roozendaal B., McGaugh J.L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiology of Learning and Memory 1997, 67:176-179.
51. Roozendaal B., Nguyen B.T., Power A.E., McGaugh J.L. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:11642.
52. Salinas J.A., Gold P.E. Glucose regulation of memory for reward reduction in young and aged rats. Neurobiology of Aging 2005, 26:45-52.
53. Salinas J., McGaugh J. Muscimol induces retrograde amnesia for changes in reward magnitude. Neurobiology of Learning and Memory 1995, 63:277-285.
54. Sandi C., Loscertales M., Guaza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. European Journal of Neuroscience 1997, 9:637-642.
55. Sandi C., Rose S.P.R. Corticosteroid receptor antagonists are amnestic for passive avoidance learning in day-old chicks. European Journal of Neuroscience 1994, 6:1292-1297.
56. Sapolsky R.M. Stress and plasticity in the limbic system. Neurochemical Research 2003, 28:1735-1742.
57. Segev A., Ramot A., Akirav I. Stress hormones receptors in the amygdala mediate the effects of stress on the consolidation, but not the retrieval, of a non aversive spatial task. PLoS ONE 2012, 7:e29988.
58. Shors T.J. Learning during stressful times. Learning and Memory 2004, 11:137.
59. Sinha R. How does stress increase risk of drug abuse and relapse?. Psychopharmacology (Berlin) 2001, 158:343-359.
60. Spence K.W. Behavior theory and conditioning 1956, Yale university Press, New Haven.
61. Viveros M.P., Marco E.M., File S.E. Endocannabinoid system and stress and anxiety responses. Pharmacology, Biochemistry and Behavior 2005, 81:331-342.