Role of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences

Neuroscience

Volumn 204, Issue , 2012, Pages 104-116

  Atsak, P ^a   Roozendaal, B ^a   Campolongo, P ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Anandamide; Glucocorticoid; Memory; Nongenomic; Norepinephrine

Indexed keywords

CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; GLUCOCORTICOID; NORADRENALIN; STRESS HORMONE;

BASOLATERAL AMYGDALA; BRAIN REGION; EMOTIONALITY; EXECUTIVE FUNCTION; HUMAN; MEMORY CONSOLIDATION; MOLECULAR INTERACTION; NONHUMAN; NORADRENALIN RELEASE; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; WORKING MEMORY;

AMYGDALA; EMOTIONS; ENDOCANNABINOIDS; GLUCOCORTICOIDS; HUMANS; MEMORY;

EID: 84857126806     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.08.047     Document Type: Review

References (144)

1. Abercrombie H.C., Speck N.S., Monticelli R.M. Endogenous cortisol elevations are related to memory facilitation only in individuals who are emotionally aroused. Psychoneuroendocrinology 2006, 31:187-196.
2. Adolphs R., Cahill L., Schul R., Babinsky R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn Mem 1997, 4:291-300.
3. Arbel I., Kadar T., Silbermann M., Levy A. The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats. Brain Res 1994, 657:227-235.
4. Arnsten A.F. Catecholamine modulation of prefrontal cortical cognitive function. Trends Cogn Sci 1998, 2:436-447.
5. Baddeley A. Working memory. Science 1992, 255:556-559.
6. Barros D.M., Carlis V., Maidana M., Silva E.S., Baisch A.L., Ramirez M.R., Izquierdo I. Interactions between anandamide-induced anterograde amnesia and post-training memory modulatory systems. Brain Res 2004, 1016:66-71.
7. Barsegyan A., Mackenzie S.M., Kurose B.D., McGaugh J.L., Roozendaal B. Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism. Proc Natl Acad Sci U S A 2010, 107:16655-16660.
8. Beckwith B.E., Petros T.V., Scaglione C., Nelson J. Dose-dependent effects of hydrocortisone on memory in human males. Physiol Behav 1986, 36:283-286.
9. Bohus B., Lissák K. Adrenocortical hormones and avoidance behaviour of rats. Int J Neuropharmacol 1968, 7:301-306.
10. Brito G.N., Thomas G.J., Davis B.J., Gingold S.I. Prelimbic cortex, mediodorsal thalamus, septum, and delayed alternation in rats. Exp Brain Res 1982, 46:52-58.
11. Bucherelli C., Baldi E., Mariottini C., Passani M.B., Blandina P. Aversive memory reactivation engages in the amygdala only some neurotransmitters involved in consolidation. Learn Mem 2006, 13:426-430.
12. Buss C., Wolf O.T., Witt J., Hellhammer D.H. Autobiographic memory impairment following acute cortisol administration. Psychoneuroendocrinology 2004, 29:1093-1096.
13. Cahill L., Babinsky R., Markowitsch H.J., McGaugh J.L. The amygdala and emotional memory. Nature 1995, 377:295-296.
14. Cahill L., Haier R.J., Fallon J., Alkire M.T., Tang C., Keator D., Wu J., McGaugh J.L. Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc Natl Acad Sci U S A 1996, 93:8016-8021.
15. Campolongo P., Roozendaal B., Trezza V., Cuomo V., Astarita G., Fu J., McGaugh J.L., Piomelli D. Fat-induced satiety factor oleoylethanolamide enhances memory consolidation. Proc Natl Acad Sci U S A 2009, 106:8027-8031.
16. Campolongo P., Roozendaal B., Trezza V., Hauer D., Schelling G., McGaugh J.L., Cuomo V. Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc Natl Acad Sci U S A 2009, 106:4888-4893.
17. Canli T., Zhao Z., Brewer J., Gabrieli J.D., Cahill L. Event-related activation in the human amygdala associates with later memory for individual emotional experience. J Neurosci 2000, 20:RC99.
18. Chhatwal J.P., Davis M., Maguschak K.A., Ressler K.J. Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 2005, 30:516-524.
19. Chiyo T., Yamazaki T., Aoshika K., Kominami S., Ohta Y. Corticosterone enhances adrenocorticotropin-induced calcium signals in bovine adrenocortical cells. Endocrinology 2003, 144:3376-3381.
20. Coluccia D., Wolf O.T., Kollias S., Roozendaal B., Forster A., de Quervain D.J. Glucocorticoid therapy-induced memory deficits: acute versus chronic effects. J Neurosci 2008, 28:3474-3478.
21. Cordero M.I., Kruyt N.D., Merino J.J., Sandi C. Glucocorticoid involvement in memory formation in a rat model for traumatic memory. Stress 2002, 5:73-79.
22. Dallman M. Fast glucocorticoid actions on brain: back to the future. Front Neuroendocrinol 2005, 26:103-108.
23. de Boer S.F., Koopmans S.J., Slangen J.L., Van der Gugten J. Plasma catecholamine, corticosterone and glucose responses to repeated stress in rats: effect of interstressor interval length. Physiol Behav 1990, 47:1117-1124.
24. de Kloet E.R. Stress in the brain. Eur J Pharmacol 2000, 405:187-198.
25. de Kloet E.R., Karst H., Joëls M. Corticosteroid hormones in the central stress response: quick-and-slow. Front Neuroendocrinol 2008, 29:268-272.
26. de Oliveira Alvares L., de Oliveira L.F., Camboim C., Diehl F., Genro B.P., Lanziotti V.B., Quillfeldt J.A. Amnestic effect of intrahippocampal AM251, a CB1-selective blocker, in the inhibitory avoidance, but not in the open field habituation task, in rats. Neurobiol Learn Mem 2005, 83:119-124.
27. de Oliveira Alvares L., Engelke D.S., Diehl F., Scheffer-Teixeira R., Haubrich J., de Freitas Cassini L., Molina V.A., Quillfeldt J.A. Stress response recruits the hippocampal endocannabinoid system for the modulation of fear memory. Learn Mem 2010, 17:202-209.
28. de Oliveira Alvares L., Genro B.P., Vaz Breda R., Pedroso M.F., Da Costa J.C., Quillfeldt J.A. AM251, a selective antagonist of the CB1 receptor, inhibits the induction of long-term potentiation and induces retrograde amnesia in rats. Brain Res 2006, 1075:60-67.
29. de Quervain D.J., Aerni A., Roozendaal B. Preventive effect of beta-adrenoceptor blockade on glucocorticoid-induced memory retrieval deficits. Am J Psychiatry 2007, 164:967-969.
30. de Quervain D.J., Aerni A., Schelling G., Roozendaal B. Glucocorticoids and the regulation of memory in health and disease. Front Neuroendocrinol 2009, 30:358-370.
31. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
32. de Quervain D.J., Roozendaal B., Nitsch R.M., McGaugh J.L., Hock C. Acute cortisone administration impairs retrieval of long-term declarative memory in humans. Nat Neurosci 2000, 3:313-314.
33. Di S., Boudaba C., Popescu I.R., Weng F.J., Harris C., Marcheselli V.L., Bazan N.G., Tasker J.G. Activity-dependent release and actions of endocannabinoids in the rat hypothalamic supraoptic nucleus. J Physiol 2005, 569:751-760.
34. Di S., Malcher-Lopes R., Halmos K.C., Tasker J.G. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci 2003, 23:4850-4857.
35. Di S., Malcher-Lopes R., Marcheselli V.L., Bazan N.G., Tasker J.G. Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and gamma-aminobutyric acid inputs to hypothalamic magnocellular neurons. Endocrinology 2005, 146:4292-4301.
36. Di S., Maxson M., Franco A., Tasker J. Glucocorticoids regulate glutamate and GABA synapse-specific retrograde transmission via divergent nongenomic signaling pathways. J Neurosci 2009, 29:393-401.
37. Duvarci S., Paré D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 2007, 27:4482-4491.
38. Egerton A., Allison C., Brett R.R., Pratt J.A. Cannabinoids and prefrontal cortical function: insights from preclinical studies. Neurosci Biobehav Rev 2006, 30:680-695.
39. Evanson N.K., Tasker J.G., Hill M.N., Hillard C.J., Herman J.P. Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology 2010, 151:4811-4819.
40. Falkenstein E., Tillmann H.C., Christ M., Feuring M., Wehling M. Multiple actions of steroid hormones-a focus on rapid, nongenomic effects. Pharmacol Rev 2000, 52:513-556.
41. Ferry B., McGaugh J.L. Clenbuterol administration into the basolateral amygdala post-training enhances retention in an inhibitory avoidance task. Neurobiol Learn Mem 1999, 72:8-12.
42. Flood J.F., Vidal D., Bennett E.L., Orme A.E., Vasquez S., Jarvik M.E. Memory facilitating and anti-amnesic effects of corticosteroids. Pharmacol Biochem Behav 1978, 8:81-87.
43. Freund T.F., Katona I., Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 2003, 83:1017-1066.
44. Fuster J.M. The prefrontal cortex and its relation to behavior. Prog Brain Res 1991, 87:201-211.
45. 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. J Neurosci 2009, 29:11078-11088.
46. Gerard C.M., Mollereau C., Vassart G., Parmentier M. Molecular cloning of a human cannabinoid receptor which is also expressed in testis. Biochem J 1991, 279(Pt 1):129-134.
47. Groc L., Choquet D., Chaouloff F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci 2008, 11:868-870.
48. Haller J., Mikics É., Makara G. The effects of non-genomic glucocorticoid mechanisms on bodily functions and the central neural system: a critical evaluation of findings. Front Neuroendocrinol 2008, 29:273-291.
49. Hamann S.B., Ely T.D., Grafton S.T., Kilts C.D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat Neurosci 1999, 2:289-293.
50. Hashimotodani Y., Ohno-Shosaku T., Kano M. Endocannabinoids and synaptic function in the CNS. Neuroscientist 2007, 13:127-137.
51. Hatfield T., Spanis C., McGaugh J.L. Response of amygdalar norepinephrine to footshock and GABAergic drugs using in vivo microdialysis and HPLC. Brain Res 1999, 835:340-345.
52. Het S., Ramlow G., Wolf O.T. A meta-analytic review of the effects of acute cortisol administration on human memory. Psychoneuroendocrinology 2005, 30:771-784.
53. Hill M., Karatsoreos I., Hillard C., McEwen B. Rapid elevations in limbic endocannabinoid content by glucocorticoid hormones in vivo. Psychoneuroendocrinology 2010, 35:1333-1338.
54. Hill M., Mclaughlin R., Bingham B., Shrestha L., Lee T., Gray J., Hillard C., Gorzalka B., Viau V. Endogenous cannabinoid signaling is essential for stress adaptation. Proc Natl Acad Sci U S A 2010, 107:9406-9411.
55. Hill M., Patel S., Campolongo P., Tasker J.G., Wotjak C.T., Bains J.S. Functional interactions between stress and the endocannabinoid system: from synaptic signaling to behavioral output. J Neurosci 2010, 30:14980-14986.
56. Hill M., McEwen B. Endocannabinoids: the silent partner of glucocorticoids in the synapse. Proc Natl Acad Sci U S A 2009, 106:4579-4580.
57. Hill M.N., Patel S., Campolongo P., Tasker J.G., Wotjak C.T., Bains J.S. Functional interactions between stress and the endocannabinoid system: from synaptic signaling to behavioral output. J Neurosci 2010, 30:14980-14986.
58. Hoffman A.F., Lupica C.R. Mechanisms of cannabinoid inhibition of GABA(A) synaptic transmission in the hippocampus. J Neurosci 2000, 20:2470-2479.
59. Introini-Collison I.B., Miyazaki B., McGaugh J.L. Involvement of the amygdala in the memory-enhancing effects of clenbuterol. Psychopharmacology (Berl) 1991, 104:541-544.
60. Joëls M., Fernandez G., Roozendaal B. Stress and emotional memory: a matter of timing. Trends Cogn Sci 2011, 15:280-288.
61. Johnson L., Farb C., Morrison J., McEwen B., Ledoux J. Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience 2005, 136:289-299.
62. Kano M., Ohno-Shosaku T., Hashimotodani Y., Uchigashima M., Watanabe M. Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 2009, 89:309-380.
63. Karst H., Berger S., Turiault M., Tronche F., Schütz G., Joëls M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci U S A 2005, 102:19204-19207.
64. Katona I., Rancz E.A., Acsady L., Ledent C., Mackie K., Hajos N., Freund T.F. Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 2001, 21:9506-9518.
65. Katona I., Sperlágh B., Sík A., Käfalvi A., Vizi E.S., Mackie K., Freund T.F. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 1999, 19:4544-4558.
66. Killgore W.D., Yurgelun-Todd D.A. Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces. Neuroimage 2004, 21:1215-1223.
67. Kuhlmann S., Kirschbaum C., Wolf O.T. Effects of oral cortisol treatment in healthy young women on memory retrieval of negative and neutral words. Neurobiol Learn Mem 2005, 83:158-162.
68. Kuhlmann S., Piel M., Wolf O.T. Impaired memory retrieval after psychosocial stress in healthy young men. J Neurosci 2005, 25:2977-2982.
69. Lee E., Son G., Chung S., Lee S., Kim J., Choi S., Kim K. Impairment of fear memory consolidation in maternally stressed male mouse offspring: evidence for nongenomic glucocorticoid action on the amygdala. J Neurosci 2011, 31:7131-7140.
70. Liang K.C., Chen L.L., Huang T.E. The role of amygdala norepinephrine in memory formation: involvement in the memory enhancing effect of peripheral epinephrine. Chin J Physiol 1995, 38:81-91.
71. Liebmann L., Karst H., Joëls M. Effects of corticosterone and the beta-agonist isoproterenol on glutamate receptor-mediated synaptic currents in the rat basolateral amygdala. Eur J Neurosci 2009, 30:800-807.
72. Liposits Z., Bohn M.C. Association of glucocorticoid receptor immunoreactivity with cell membrane and transport vesicles in hippocampal and hypothalamic neurons of the rat. J Neurosci Res 1993, 35:14-19.
73. Liu L., Tsuji M., Takeda H., Takada K., Matsumiya T. Adrenocortical suppression blocks the enhancement of memory storage produced by exposure to psychological stress in rats. Brain Res 1999, 821:134-140.
74. Losel R.M., Falkenstein E., Feuring M., Schultz A., Tillmann H.C., Rossol-Haseroth K., Wehling M. Nongenomic steroid action: controversies, questions, and answers. Physiol Rev 2003, 83:965-1016.
75. Luine V.N., Spencer R.L., McEwen B.S. Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function. Brain Res 1993, 616:65-70.
76. Lupien S.J., Gillin C.J., Hauger R.L. Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a dose-response study in humans. Behav Neurosci 1999, 113:420-430.
77. Maheu F.S., Joober R., Beaulieu S., Lupien S.J. Differential effects of adrenergic and corticosteroid hormonal systems on human short- and long-term declarative memory for emotionally arousing material. Behav Neurosci 2004, 118:420-428.
78. Malcher-Lopes R., Di S., Marcheselli V.S., Weng F.J., Stuart C.T., Bazan N.G., Tasker J.G. Opposing crosstalk between leptin and glucocorticoids rapidly modulates synaptic excitation via endocannabinoid release. J Neurosci 2006, 26:6643-6650.
79. Marsicano G., Lafenetre P. Roles of the endocannabinoid system in learning and memory. Curr Top Behav Neurosci 2009, 1:201-230.
80. Marsicano G., Wotjak C.T., Azad S.C., Bisogno T., Rammes G., Cascio M.G., Hermann H., Tang J., Hofmann C., Zieglgänsberger W., Di Marzo V., Lutz B. The endogenous cannabinoid system controls extinction of aversive memories. Nature 2002, 418:530-534.
81. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346:561-564.
82. McEwen B.S. Stress, adaptation, and disease: allostasis and allostatic load. Ann N Y Acad Sci 1998, 840:33-44.
83. McEwen B.S. Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann N Y Acad Sci 2001, 933:265-277.
84. McEwen B.S., Weiss J.M., Schwartz L.S. Selective retention of corticosterone by limbic structures in rat brain. Nature 1968, 220:911-912.
85. McGaugh J.L. Memory-a century of consolidation. Science 2000, 287:248-251.
86. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 2004, 27:1-28.
87. McGaugh J.L., Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 2002, 12:205-210.
88. McIntyre C., Hatfield T., McGaugh J.L. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. Eur J Neurosci 2002, 16:1223-1226.
89. McReynolds J.R., Donowho K., Abdi A., McGaugh J.L., Roozendaal B., McIntyre C.K. Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiol Learn Mem 2010, 93:312-321.
90. Miranda M.I., Quirarte G.L., Rodriguez-Garcia G., McGaugh J.L., Roozendaal B. Glucocorticoids enhance taste aversion memory via actions in the insular cortex and basolateral amygdala. Learn Mem 2008, 15:468-476.
91. Mizoguchi K., Ishige A., Takeda S., Aburada M., Tabira T. Endogenous glucocorticoids are essential for maintaining prefrontal cortical cognitive function. J Neurosci 2004, 24:5492-5499.
92. Morgan N.H., Stanford I.M., Woodhall G.L. Functional CB2 type cannabinoid receptors at CNS synapses. Neuropharmacology 2009, 57:356-368.
93. Ohno-Shosaku T., Maejima T., Kano M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 2001, 29:729-738.
94. Oitzl M.S., de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci 1992, 106:62-71.
95. Okuda S., Roozendaal B., McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proc Natl Acad Sci U S A 2004, 101:853-858.
96. Orchinik M., Murray T.F., Moore F.L. A corticosteroid receptor in neuronal membranes. Science 1991, 252:1848-1851.
97. Oropeza V.C., Page M.E., Van Bockstaele E.J. Systemic administration of WIN 55,212-2 increases norepinephrine release in the rat frontal cortex. Brain Res 2005, 1046:45-54.
98. Pacher P., Mechoulam R. Is lipid signaling through cannabinoid 2 receptors part of a protective system?. Prog Lipid Res 2011, 50:193-211.
99. Page M.E., Oropeza V.C., Sparks S.E., Qian Y., Menko A.S., Van Bockstaele E.J. Repeated cannabinoid administration increases indices of noradrenergic activity in rats. Pharmacol Biochem Behav 2007, 86:162-168.
100. Pamplona F.A., Takahashi R.N. WIN 55212-2 impairs contextual fear conditioning through the activation of CB1 cannabinoid receptors. Neurosci Lett 2006, 397:88-92.
101. Patel S., Hillard C. Adaptations in endocannabinoid signaling in response to repeated homotypic stress: a novel mechanism for stress habituation. Eur J Neurosci 2008, 27:2821-2829.
102. Patel S., Roelke C.T., Rademacher D.J., Hillard C.J. Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Eur J Neurosci 2005, 21:1057-1069.
103. Pattij T., Wiskerke J., Schoffelmeer A.N. Cannabinoid modulation of executive functions. Eur J Pharmacol 2008, 585:458-463.
104. Pelletier J.G., Likhtik E., Filali M., Paré D. Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories. Learn Mem 2005, 12:96-102.
105. 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.
106. Pugh C.R., Tremblay D., Fleshner M., Rudy J.W. A selective role for corticosterone in contextual-fear conditioning. Behav Neurosci 1997, 111:503-511.
107. Quirarte G.L., de la Teja I.S., Casillas M., Serafín N., Prado-Alcalá R.A., Roozendaal B. Corticosterone infused into the dorsal striatum selectively enhances memory consolidation of cued water-maze training. Learn Mem 2009, 16:586-589.
108. Quirarte G.L., Roozendaal B., McGaugh J.L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 1997, 94:14048-14053.
109. Rashidy-Pour A., Sadeghi H., Taherain A.A., Vafaei A.A., Fathollahi Y. The effects of acute restraint stress and dexamethasone on retrieval of long-term memory in rats: an interaction with opiate system. Behav Brain Res 2004, 154:193-198.
110. Reul J.M., van den Bosch F.R., de Kloet E.R. Differential response of type I and type II corticosteroid receptors to changes in plasma steroid level and circadian rhythmicity. Neuroendocrinology 1987, 45:407-412.
111. Riedemann T., Patchev A., Cho K., Almeida O. Corticosteroids: way upstream. Mol Brain 2010, 3:2.
112. Robinson L., McKillop-Smith S., Ross N.L., Pertwee R.G., Hampson R.E., Platt B., Riedel G. Hippocampal endocannabinoids inhibit spatial learning and limit spatial memory in rats. Psychopharmacology (Berl) 2008, 198:551-563.
113. Roozendaal B. 1999 Curt P. Richter award. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 2000, 25:213-238.
114. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol Learn Mem 2002, 78:578-595.
115. Roozendaal B., Bohus B., McGaugh J.L. Dose-dependent suppression of adrenocortical activity with metyrapone: effects on emotion and memory. Psychoneuroendocrinology 1996, 21:681-693.
116. Roozendaal B., Carmi O., McGaugh J.L. Adrenocortical suppression blocks the memory-enhancing effects of amphetamine and epinephrine. Proc Natl Acad Sci U S A 1996, 93:1429-1433.
117. Roozendaal B., de Quervain D.J., Schelling G., McGaugh J.L. A systemically administered beta-adrenoceptor antagonist blocks corticosterone-induced impairment of contextual memory retrieval in rats. Neurobiol Learn Mem 2004, 81:150-154.
118. Roozendaal B., Griffith Q.K., Buranday J., de Quervain D.J., McGaugh J.L. The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proc Natl Acad Sci U S A 2003, 100:1328-1333.
119. Roozendaal B., Hahn E.L., Nathan S.V., de Quervain D.J., McGaugh J.L. Glucocorticoid effects on memory retrieval require concurrent noradrenergic activity in the hippocampus and basolateral amygdala. J Neurosci 2004, 24:8161-8169.
120. Roozendaal B., Hernandez A., Cabrera S.M., Hagewoud R., Malvaez M., Stefanko D.P., Haettig J., Wood M.A. Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J Neurosci 2010, 30:5037-5046.
121. Roozendaal B., McEwen B., Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci 2009, 10:423-433.
122. Roozendaal B., McGaugh J.L. Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiol Learn Mem 1997, 67:176-179.
123. Roozendaal B., McReynolds J.R., McGaugh J.L. The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci 2004, 24:1385-1392.
124. Roozendaal B., Okuda S., de Quervain D.J., McGaugh J.L. Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 2006, 138:901-910.
125. Roozendaal B., Okuda S., Van der Zee E.A., McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 2006, 103:6741-6746.
126. Roozendaal B., Quirarte G.L., McGaugh J.L. Glucocorticoids interact with the basolateral amygdala beta-adrenoceptor-cAMP/PKA system in influencing memory consolidation. Eur J Neurosci 2002, 15:553-560.
127. Rose J.D., Moore F.L., Orchinik M. Rapid neurophysiological effects of corticosterone on medullary neurons: relationship to stress-induced suppression of courtship clasping in an amphibian. Neuroendocrinology 1993, 57:815-824.
128. Rubino T., Realini N., Castiglioni C., Guidali C., Viganó D., Marras E., Petrosino S., Perletti G., Maccarrone M., Di Marzo V., Parolaro D. Role in anxiety behavior of the endocannabinoid system in the prefrontal cortex. Cereb Cortex 2008, 18:1292-1301.
129. Sajadi A.A., Samaei S.A., Rashidy-Pour A. Intra-hippocampal microinjections of anisomycin did not block glucocorticoid-induced impairment of memory retrieval in rats: an evidence for non-genomic effects of glucocorticoids. Behav Brain Res 2006, 173:158-162.
130. Sajadi A.A., Samaei S.A., Rashidy-Pour A. Blocking effects of intra-hippocampal naltrexone microinjections on glucocorticoid-induced impairment of spatial memory retrieval in rats. Neuropharmacology 2007, 52:347-354.
131. Sandi C., Pinelo-Nava M. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007, 2007:1-20.
132. Sandi C., Rose S.P. Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm. Brain Res 1994, 647:106-112.
133. Schoofs D., Preuss D., Wolf O.T. Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology 2008, 33:643-653.
134. Smeets T., Otgaar H., Candel I., Wolf O.T. True or false?. Memory is differentially affected by stress-induced cortisol elevations and sympathetic activity at consolidation and retrieval. Psychoneuroendocrinology 2008, 33:1378-1386.
135. Solowij N., Michie P.T. Cannabis and cognitive dysfunction: parallels with endophenotypes of schizophrenia?. J Psychiatry Neurosci 2007, 32:30-52.
136. Sutanto W., de Kloet E.R. Species-specificity of corticosteroid receptors in hamster and rat brains. Endocrinology 1987, 121:1405-1411.
137. Suzuki A., Josselyn S.A., Frankland P.W., Masushige S., Silva A.J., Kida S. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 2004, 24:4787-4795.
138. Tan H., Lauzon N.M., Bishop S.F., Chi N., Bechard M., Laviolette S.R. Cannabinoid transmission in the basolateral amygdala modulates fear memory formation via functional inputs to the prelimbic cortex. J Neurosci 2011, 31:5300-5312.
139. Tasker J.G., Di S., Malcher-Lopes R. Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 2006, 147:5549-5556.
140. Vouimba R.M., Yaniv D., Richter-Levin G. Glucocorticoid receptors and beta-adrenoceptors in basolateral amygdala modulate synaptic plasticity in hippocampal dentate gyrus, but not in area CA1. Neuropharmacology 2007, 52:244-252.
141. Wilson R.I., Kunos G., Nicoll R.A. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 2001, 31:453-462.
142. Wolf O.T. The influence of stress hormones on emotional memory: relevance for psychopathology. Acta Psychol 2008, 127:513-531.
143. Wolf O.T., Schommer N.C., Hellhammer D.H., McEwen B.S., Kirschbaum C. The relationship between stress induced cortisol levels and memory differs between men and women. Psychoneuroendocrinology 2001, 26:711-720.
144. Young A.H., Sahakian B.J., Robbins T.W., Cowen P.J. The effects of chronic administration of hydrocortisone on cognitive function in normal male volunteers. Psychopharmacology (Berl) 1999, 145:260-266.