Glucocorticoid effects on memory consolidation depend on functional interactions between the medial prefrontal cortex and basolateral amygdala

Journal of Neuroscience

Volumn 29, Issue 45, 2009, Pages 14299-14308

  Roozendaal, Benno ^a   McReynolds, Jayme R ^b   Van Der Zee, Eddy A ^c   Lee, Sangkwan ^d   McGaugh, James L ^d   McIntyre, Christa K ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF TEXAS AT DALLAS   (United States)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA,17BETA DIHYDROXY 6 METHYL 17ALPHA (1 PROPYNYL)ANDROSTA 1,4,6 TRIEN 3 ONE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; GLUCOCORTICOID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN REGION; COGNITION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FOOTSHOCK; MALE; MEMORY CONSOLIDATION; NEUROMODULATION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM;

AMYGDALA; ANDROSTANOLS; ANIMALS; AVOIDANCE LEARNING; CENTRAL NERVOUS SYSTEM AGENTS; ENZYME INHIBITORS; FLAVONOIDS; FUNCTIONAL LATERALITY; GLUCOCORTICOIDS; MALE; MEMORY; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PREFRONTAL CORTEX; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION;

EID: 70449657822     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3626-09.2009     Document Type: Article

References (70)

1. Akirav I, Maroun M (2006) Ventromedial prefrontal cortex is obligatory for consolidation and reconsolidation of object recognition memory. Cereb Cortex 16:1759-1765. (Pubitemid 44729914)
2. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365-371. (Pubitemid 40300194)
3. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609. (Pubitemid 128406370)
4. Bechara A, Damasio H, Damasio AR, Lee GP (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decisionmaking. J Neurosci 19:5473-5481. (Pubitemid 29300212)
5. Bremner JD, Staib LH, Kaloupek D, Southwick SM, Soufer R, Charney DS (1999) Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biol Psychiatry 45:806-816. (Pubitemid 29185471)
6. Burgos-Robles A, Vidal-Gonzalez I, Santini E, Quirk GJ (2007) Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex. Neuron 53:871-880. (Pubitemid 46367556)
7. Campolongo P, Roozendaal B, Trezza V, Hauer D, Schelling G, McGaugh JL, Cuomo V (2009) Endocannabinoids in the rat basolateral amygdala enhance memory consolidaton and enable glucocortiocid modulation of memory. Proc Natl Acad Sci U S A 106:4888-4893.
8. Cassell MD, Wright DJ (1986) Topography of projections from the medial prefrontal cortex to the amygdala in the rat. Brain Res Bull 17:321-333. (Pubitemid 16032983)
9. Dallman MF (2005) Fast glucocorticoid actions on brain: back to the future. Front Neuroendocrinol 26:103-108.
10. Davidson RJ (2002) Anxiety and affective style: role of prefrontal cortex and amygdala. Biol Psychiatry 51:68-80.
11. de Kloet ER, Oitzl MS, Joëls M (1999) Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 22:422-426.
12. Dolcos F, LaBar KS, Cabeza R (2004) Interaction between the amygala and the medial temporal lobe system predicts better memory for emotional events. Neuron 42:855-863. (Pubitemid 38748797)
13. Duvarci S, Nader K, LeDoux JE (2005) Activation of extracellular signal-regulated kinase-mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning. Eur J Neurosci 21:283-289. (Pubitemid 40193898)
14. Garcia R, Vouimba RM, Baudry M, Thompson RF (1999) The amygdala modulates prefrontal cortex activity relative to conditioned fear. Nature 402:294-296. (Pubitemid 129516265)
15. Huff NC, Frank M, Wright-Hardesty K, Sprunger D, Matus-Amat P, Higgins E, Rudy JW (2006) Amygdala regulation of immediate-early gene expression in the hippocampus induced by contextual fear conditioning. J Neurosci 26:1616-1623. (Pubitemid 43237032)
16. Izquierdo LA, Barros DM, da Costa JC, Furini C, Zinn C, Cammarota M, Bevilaqua LR, Izquierdo I (2007) A link between role of two prefrontal areas in immediate memory and in long-term memory consolidation. Neurobiol Learn Mem 88:160-166. (Pubitemid 47225218)
17. Johnson LR, Farb C, Morrison JH, McEwen BS, LeDoux JE (2005) Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience 136:289-299. (Pubitemid 41487104)
18. Johnstone T, van Reekum CM, Urry HL, Kalin NH, Davidson RJ (2007) Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci 7:8877-8884. (Pubitemid 47292771)
19. Krettek JE, Price JL (1977) Projections from the amygdaloid complex in the cerebral cortex and thalamus in the rat and cat. J Comp Neurol 172:687-722. (Pubitemid 8059157)
20. Laviolette SR, Grace AA (2006) Cannabinoids potentiate emotional learning plasticity in neurons of the medial prefrontal cortex through basolateral amygdala inputs. J Neurosci 26:6458-6468.
21. Laviolette SR, Lipski WJ, Grace AA (2005) 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 25:6066-6075.
22. Likhtik E, Pelletier JG, Paz R, Paré D (2005) Prefrontal control of the amygdala. J Neurosci 25:7429-7437.
23. Lyons DM, Lopez JM, Yang C, Schatzberg AF (2000) Stress-level cortisol treatment impairs inhibitory control of behavior in monkeys. J Neurosci 20:7816-7821. (Pubitemid 30776606)
24. Malin EL, McGaugh JL (2006) Differential involvement of the hippocampus, anterior cingulate cortex, and basolateral amygdala in memory for context and footshock. Proc Natl Acad Sci U S A 103:1959-1963.
25. Malin EL, Ibrahim DY, Tu JW, McGaugh JL (2007) Involvement of the rostral anterior cingulate cortex in consolidation of inhibitory avoidance memory: interaction with the basolateral amygdala. Neurobiol Learn Mem 87:295-302.
26. Maroun M, Richter-Levin G (2003) Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J Neurosci 23:4406-4409. (Pubitemid 36706170)
27. McDonald RJ, King AL, Foong N, Rizos Z, Hong NS (2008) Neurotoxic lesions of the medial prefrontal cortex or medial striatum impair multiple-location place learning in the water maze: evidence for neural structures with complementary roles in behavioural flexibility. Exp Brain Res 187:419-427.
28. McGaugh JL (1966) Time-dependent processes in memory storage. Science 153:1351-1358.
29. McGaugh JL (2002) Memory consolidation and the amygdala: a systems perspective. Trends Neurosci 25:456-461. (Pubitemid 35222999)
30. McGaugh JL, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205-210.
31. McGaugh JL, Introini-Collison IB, Nagahara AH (1988) Memory-enhancing effects of posttraining naloxone: involvement of beta-noradrenergic influences in the amygdaloid complex. Brain Res 446:37-49.
32. McIntyre CK, Miyashita T, Setlow B, Marjon KD, Steward O, Guzowski JF, McGaugh JL (2005) Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. Proc Natl Acad Sci U S A 102:10718-10723. (Pubitemid 41061620)
33. Medina AC, Charles JR, Espinoza-González V, Sánchez- Resendis O, Prado-Alcalá RA, Roozendaal B, Quirarte GL (2007) Glucocorticoid administratium into the dorsal striatum facilitates memory consolidation of inhibitory avoidance training but not of the context or footshock components. Learn Mem 14:673-677. (Pubitemid 350036779)
34. Merino SM, Maren S (2006) Hitting Ras where it counts: Ras antagonism in the basolateral amygdala inhibits long-term fear memory. Eur J Neurosci 23:196-204.
35. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70-74. (Pubitemid 35291441)
36. Miranda MI, McGaugh JL (2004) Enhancement of inhibitory avoidance and conditioned taste aversion memory with insular cortex infusions of 8-Br-cAMP: involvement of the basolateral amygdala. Learn Mem 11:312-317.
37. Mueller D, Porter JT, Quirk GJ (2008) Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J Neurosci 28:369-375.
38. Patterson SL, Pittenger C, Morozov A, Martin KC, Scanlin H, Drake C, Kandel ER (2001) Some forms of cAMP-mediated long-lasting potentiation are associated with release of BDNF and nuclear translocation of phospho-MAP kinase. Neuron 32:123-140. (Pubitemid 32995895)
39. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, Ed 4. San Diego: Academic.
40. Pérez-Jaranay JM, Vives F (1991) Electrophysiological study of the response of medial prefrontal cortex neurons to stimulation of the basolateral nucleus of the amygdala in the rat. Brain Res 564:97-101.
41. Pu Z, Krugers HJ, Joëls M (2007) Corticosterone time-dependently modulates beta-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus. Learn Mem 14:359-367.
42. Quirarte GL, Roozendaal B, McGaugh JL (1997) Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 94:14048-14053. (Pubitemid 28009707)
43. Quirk GJ, Gehlert DR (2003) Inhibition of the amygdala: key to pathological states? Ann N Y Acad Sci 985:263-272.
44. Revest JM, Di Blasi F, Kitchener P, Rougé-Pont F, Desmedt A, Turiault M, Tronche F, Piazza PV (2005) The MAPK pathway and Egr-1 mediate stress-related behavioral effects of glucocorticoids. Nat Neurosci 8:664-672. (Pubitemid 40594209)
45. Roesler R, Roozendaal B, McGaugh JL (2002) Basolateral amygdala lesions block the memory-enhancing effect of 8-Br-cAMP infused into the entorhinal cortex of rats after training. Eur J Neurosci 15:905-910. (Pubitemid 35463654)
46. Roozendaal B (2000) Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinology 25:213-238.
47. Roozendaal B (2002) Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol Learn Mem 78:578-595.
48. Roozendaal B, McGaugh JL (1996) Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol Learn Mem 65:1-8. (Pubitemid 26112649)
49. Roozendaal B, McGaugh JL (1997a) Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur J Neurosci 9:76-83. (Pubitemid 27083477)
50. Roozendaal B, McGaugh JL (1997b) Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiol Learn Mem 67:176-179. (Pubitemid 27424473)
51. Roozendaal B, Portillo-Marquez G, McGaugh JL (1996) Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav Neurosci 110:1074-1083. (Pubitemid 26365806)
52. Roozendaal B, Quirarte GL, McGaugh JL (2002) Glucocorticoids interact with the basolateral amygdala β-adrenoceptor-cAMP/PKA system in influencing memory consolidation. Eur J Neurosci 15:553-560. (Pubitemid 35463674)
53. Roozendaal B, McReynolds JR, McGaugh JL (2004) The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci 24:1385-1392. (Pubitemid 38222989)
54. Roozendaal B, Okuda S, Van der Zee EA, McGaugh JL (2006) Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 103:6741-6746.
55. Roozendaal B, Lengvilas R, McGaugh JL, Civelli O, Reinscheid RK (2007) Orphanin FQ/nociceptin interacts with the basolateral amygdala noradrenergic system in memory consolidation. Learn Mem 14:29-35. (Pubitemid 46203564)
56. Roozendaal B, Barsegyan A, Lee S (2008) Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. Prog Brain Res 167:79-97. (Pubitemid 350123226)
57. Rosenkranz JA, Grace AA (2002) Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J Neurosci 22:324-337.
58. Runyan JD, Dash PK (2004) Intra-medial prefrontal administration of SCH-23390 attenuates ERK phosphorylation and long-term memory for trace fear conditioning in rats. Neurobiol Learn Mem 82:65-70.
59. Russchen FT (1982) Amygdalopetal projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques. J Comp Neurol 206:159-179.
60. Sandi C, Pinelo-Nava MT (2007) Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007:78970. (Pubitemid 46655445)
61. Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, LeDoux JE (2000) Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J Neurosci 20:8177-8187.
62. Schoenbaum G, Chiba AA, Gallagher M (1998) Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nat Neurosci 1:155-159. (Pubitemid 128652664)
63. Sharma SK, Carew TJ (2002) Inclusion of phosphatase inhibitors during Western blotting enhances signal detection with phospho-specific antibodies. Anal Biochem 307:187-189.
64. Sharma SK, Sherff CM, Shobe J, Bagnall MW, Sutton MA, Carew TJ (2003) Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. J Neurosci 23:3899-3907. (Pubitemid 36958495)
65. Teutsch G, Costerousse G, Deraedt R, Benzoni J, Fortin M, Philibert D (1981) 17alpha-alkynyl-11beta,17-dihydroxyandrostane derivates: a new class of potent glucocorticoids. Steroids 38:651-665.
66. Timms RJ (1977) Cortical inhibition and facilitation of the defense reaction. J Physiol 266:98P-99P.
67. Touzani K, Puthanveettil SV, Kandel ER (2007) Consolidation of learning strategies during spatial working memory task requires protein synthesis in the prefrontal cortex. Proc Natl Acad Sci U S A 104:5632-5637. (Pubitemid 47175732)
68. Tronel S, Sara SJ (2003) Blockade of NMDA receptors in prelimbic cortex induces an enduring amnesia for odor-reward associative learning. J Neurosci 2:5472-5476. (Pubitemid 36807821)
69. Tsoory MM, Vouimba RM, Akirav I, Kavushansky A, Avital A, Richter-Levin G (2008) Amygdala modulation of memory-related processes in the hippocampus: potential relevance to PTSD. Prog Brain Res 167:35-51. (Pubitemid 350123223)
70. Xiang JZ, Brown MW (2004) Neuronal responses related to long-term recognition memory processes in prefrontal cortex. Neuron 42:817-829.