Corticotropin-releasing factor in the basolateral amygdala enhances memory consolidation via an interaction with the β-adrenoceptor-cAMP pathway: Dependence on glucocorticoid receptor activation

Journal of Neuroscience

Volumn 28, Issue 26, 2008, Pages 6642-6651

  Roozendaal, Benno ^a   Schelling, Gustav ^b   McGaugh, James L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

helical CRF9 41; Atenolol; Corticosterone; CRF; CRF binding protein; CRF6 33; Emotional arousal; Inhibitory avoidance; Norepinephrine

Indexed keywords

8 BROMO CYCLIC AMP; ATENOLOL; BETA ADRENERGIC RECEPTOR; BINDING PROTEIN; CIRAZOLINE; CLENBUTEROL; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR [6-33]; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR[9-41]; CYCLIC AMP; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYPOTHALAMUS RELEASING FACTOR; UNCLASSIFIED DRUG; 8 ((4 CHLOROPHENYL)THIO)CYCLIC 3',5' AMP; 8-((4-CHLOROPHENYL)THIO)CYCLIC-3',5'-AMP; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CORTICOTROPIN RELEASING HORMONE (9 41); CORTICOTROPIN RELEASING HORMONE (9-41); DRUG DERIVATIVE; NORADRENALIN; NUCLEOTIDE; PEPTIDE FRAGMENT;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOSE RESPONSE; DRUG INFUSION; LATENT PERIOD; MALE; MEMORY CONSOLIDATION; MODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; TRAINING; ANIMAL; DRUG EFFECT; HISTOLOGY; MEMORY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADRENERGIC BETA-ANTAGONISTS; AMYGDALA; ANIMALS; CORTICOTROPIN-RELEASING HORMONE; CYCLIC AMP; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MEMORY; NOREPINEPHRINE; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION; THIONUCLEOTIDES;

EID: 48549094903     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1336-08.2008     Document Type: Article

References (90)

1. Abercrombie HC, Speck NS, Monticelli RM (2006) Endogenous cortisol elevations are related to memory facilitation only in individuals who are emotionally aroused. Psychoneuroendocrinology 31:187-196.
2. Aldenhoff JB, Gruol DL, Rivier J, Vale W, Siggins GR (1983) Corticotropin releasing factor decreases postburst hyperpolarizations and excites hippocampal neurons. Science 221:875-877.
3. Asbach S, Schulz C, Lehnert H (2001) Effects of corticotropin-releasing hormone on locus coeruleus neurons in vivo: a microdialysis study using a novel bilateral approach. Eur J Endocrinol 145:359-363.
4. Bale TL, Vale WW (2004) CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44:525-557.
5. Behan DP, Heinrichs SC, Troncoso JC, Liu XJ, Kawas CH, Ling N, De Souza EB (1995) Displacement of corticotropin releasing factor from its binding protein as a possible treatment for Alzheimer's disease. Nature 378:284-287.
6. Blank T, Nijholt I, Eckart K, Spiess J (2002) Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J Neurosci 22:3788-3794.
7. Bricca G, Dontenwill M, Molines A, Feldman J, Tibirica E, Belcourt A, Bousquet P (1989) Rilmenidine selectivity for imidazoline receptors in human brain. Eur J Pharmacol 163:373-377.
8. Buchanan TW, Lovallo WR (2001) Enhanced memory for emotional material following stress-level cortisol treatment in humans. Psychoneuroendocrinology 26:307-317.
9. Chen MF, Chiu TH, Lee EHY (1992) Noradrenergic mediation of the memory-enhancing effect of corticotropin-releasing factor in the locus coeruleus of rats. Psychoneuroendocrinology 17:113-124.
10. Cole BJ, Koob GF (1988) Propranolol antagonizes the enhanced conditioned fear produced by corticotropin releasing factor. J Pharmacol Exp Ther 247:902-910.
11. Conrad CD, Lupien SJ, McEwen BS (1999) Support for a bimodal role for type II adrenal steroid receptors in spatial memory. Neurobiol Learn Mem 72:39-46.
12. Dias RD, Carrasco MA, Souza DO, Izquierdo I (1979) Effect of naloxone, haloperidol and propranolol on cyclic 3′,5′-adenosine monophosphate content of rat amygdala. Eur J Pharmacol 60:345-347.
13. 2-adrenoceptors. Eur J Pharmacol 361:1-15.
14. Duman RS, Strada SJ, Enna SJ (1989) Glucocorticoid administration increases receptor-mediated and forskolin-stimulated cyclic AMP accumulation in rat brain cerebral cortical slices. Brain Res 477:166-171.
15. 1-adrenoceptors in the basolateral amygdala in modulation of memory storage. Eur J Pharmacol 372:9-16.
16. 1-adrenoceptors. J Neurosci 19:5119-5123.
17. Finlay JM, Jedema HP, Rabinovic AD, Mana MJ, Zigmund MJ, Sved AF (1997) Impact of corticotropin-releasing hormone on extracellular norepinephrine in prefrontal cortex after chronic cold stress. J Neurochem 69:144-150.
18. Hatfield T, Spanis C, McGaugh JL (1999) Response of amygdalar norepinephrine to footshock and GABAergic drugs using in vivo microdialysis and HPLC. Brain Res 835:340-345.
19. Heinrichs SC, Vale EA, Lapsansky J, Behan DP, McClure LV, Ling N, De Sousa EB, Schulteis G (1997) Enhancement of performance in multiple learning tasks by corticotropin-releasing factor-binding protein ligand inhibitors. Peptides 18:711-716.
20. Helmreich DL, Itoi K, Lopez-Figueroa MO, Akil H, Watson SJ (2001) Norepinephrine-induced CRH and AVP gene transcription within the hypothalamus: differential regulation by corticosterone. Mol Brain Res 88:62-73.
21. Herringa RJ, Nanda SA, Hsu DT, Roseboom PH, Kalin NH (2004) The effects of acute stress on the regulation of central and basolateral amygdala CRF-binding protein gene expression. Mol Brain Res 131:17-25.
22. Hollrigel GS, Chen K, Baram TZ, Soltesz I (1998) The pro-convulsant actions of corticotropin-releasing hormone in the hippocampus of infant rats. Neuroscience 84:71-79.
23. Hubbard DT, Nakashima BR, Lee I, Takahashi LK (2007) Activation of basolateral amygdala corticotropin-releasing factor 1 receptors modulates the consolidation of contextual fear. Neuroscience 150:818-828.
24. Introini-Collison IB, Nagahara AH, McGaugh JL (1989) Memory enhancement with intra-amygdala post-training naloxone is blocked by concurrent administration of propranolol. Brain Res 476:94-101.
25. Isogawa K, Akiyoshi J, Hikichi T, Yamamoto Y, Tsutsumi T, Nagayama H (2000) Effect of corticotropin releasing factor receptor 1 antagonist on extracellular norepinephrine, dopamine and serotonin in hippocampus and prefrontal cortex of rats in vivo. Neuropeptides 34:234-239.
26. Jedema HP, Grace AA (2004) Corticotropin-releasing hormone directly activates noradrenergic neurons of the locus ceruleus recorded in vitro. J Neurosci 24:9703-9713.
27. 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.
28. Koob GF (1999) Corticotropin-releasing factor, norepinephrine, and stress. Biol Psychiatry 46:1167-1180.
29. Kuhlmann S, Wolf OT (2006) Arousal and cortisol interact in modulating memory consolidation in healthy young men. Behav Neurosci 120:217-223.
30. LaLumiere RT, Nguyen LT, McGaugh JL (2004) Post-training intrabasolateral amygdala infusions of dopamine modulate consolidation of inhibitory avoidance memory: involvement of noradrenergic and cholinergic systems. Eur J Neurosci 20:2804-2810.
31. Lavicky J, Dunn AJ (1993) Corticotropin-releasing factor stimulates catecholamine release in hypothalamus and prefrontal cortex in freely moving rats as assessed by microdialysis. J Neurochem 60:602-612.
32. Lee EH, Sung YJ (1989) Differential influences of corticotropin-releasing factor on memory retention of aversive learning and appetitive learning in rats. Behav Neural Biol 52:285-294.
33. Liang KC, Lee EHY (1988) Intra-amygdala injections of corticotropin releasing factor facilitate inhibitory avoidance learning and reduce exploratory behavior in rats. Psychopharmacology 96:232-236.
34. Liang KC, Juler RG, McGaugh JL (1986) Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain Res 368:125-133.
35. Liang KC, Melia KR, Campeau S, Falls WA, Miserendino MJ, Davis M (1992) Lesions of the central nucleus of the amygdala, but not the paraventricular nucleus of the hypothalamus, block the excitatory effects of corticotropin-releasing factor on the acoustic startle reflex. J Neurosci 12:2313-2320.
36. Liang KC, Chen HC, Chen DY (2001) Posttraining infusion of norepinephrine and corticotropin releasing factor into the bed nucleus of the stria terminalis enhanced retention in an inhibitory avoidance task. Chin J Physiol 44:33-43.
37. Liebsch G, Landgraf R, Gerstberger R, Probst JC, Wotjak CT, Engelmann M, Holsboer F, Montkowski A (1995) Chronic infusion of a CRH1 receptor antisense oligodeoxynucleotide into the central nucleus of the amygdala reduced anxiety-related behavior in socially defeated rats. Regul Pept 59:229-239.
38. Ma S, Roozendaal B, Burazin TCD, Tregear GW, McGaugh JL, Gundlach AL (2005) Relaxin receptor activation in the basolateral amygdala impairs memory consolidation. Eur J Neurosci 22:2117-2122.
39. Ma XM, Aguilera G (1999) Differential regulation of corticotropin- releasing hormone and vasopressin transcription by glucocorticoids. Endocrinology 140:5642-5650.
40. McGaugh JL (1966) Time-dependent processes in memory storage. Science 153:1351-1358.
41. McGaugh JL (2000) Memory: a century of consolidation. Science 287:248-251.
42. McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1-28
43. McGaugh JL, Introini-Collison IB, Nagahara AH (1988) Memory-enhancing effects of post-training naloxone: involvement of β-noradrenergic influences in the amygdaloid complex. Brain Res 446:37-49.
44. McGaugh JL, Cahill L, Roozendaal B (1996) Involvement of the amygdala in memory storage: interaction with other brain systems. Proc Natl Acad Sci USA 93:13508-13514. .
45. Merali Z, Michaud D, McIntosh J, Kent P, Anisman H (2003) Differential involvement of amygdaloid CRH system(s) in the salience and valence of the stimuli. Prog Neuropsychopharmacol Biol Psychiatry 27:1201-1212.
46. Merali Z, Khan S, Michaud DS, Shippy SA, Anisman H (2004) Does amygdaloid corticotropin-releasing hormone (CRH) mediate anxiety-like behaviors? Dissociation of anxiogenic effects and CRH release. Eur J Neurosci 20:229-239.
47. Oitzl MS, de Kloet ER (1992) Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav Neurosci 106:62-71.
48. Okuda S, Roozendaal B, McGaugh JL (2004) Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proc Natl Acad Sci USA 101:853-858.
49. Owens MJ, Bartolome J, Schanberg SM, Nemeroff CB (1990) Corticotropin-releasing factor concentrations exhibit an apparent diurnal rhythm in hypothalamic and extrahypothalamic brain regions: differential sensitivity to corticosterone. Neuroendocrinology 52:626-631.
50. Parent MB, McGaugh JL (1994) Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training. Brain Res 661:97-103.
51. Pavcovich LA, Valentino RJ (1997) Regulation of a putative neurotransmitter effect of corticotropin-releasing factor: effects of adrenalectomy. J Neurosci 17:401-408.
52. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, Ed 5. San Diego: Academic.
53. Perkins JP, Moore MM (1973) Characterization of the adrenergic receptors mediating a rise in cyclic 3′,5′-adenosine monophosphate in rat cerebral cortex. J Pharmacol Exp Ther 185:371-378.
54. Perrin MH, Donaldson CJ, Chen R, Lewis KA, Vale WW (1993) Cloning and functional expression of a rat brain corticotropin releasing factor (CRF) receptor. Endocrinology 133:3058-3061.
55. Philibert D, Costerousse G, Gaillard-Moguilewsky M, Nedelec L, Nique F, Tournemine C, Teutsch G (1991) From RU 38486 towards dissociated antiglucocorticoid and antiprogresterone. In: Antihormones in health and disease. Frontiers in hormonal research (Agarwal MK, ed), pp 1-17. Basel: Karger.
56. Pigini M, Quaglia W, Gentili F, Marucci G, Cantalamessa F, Franchini S, Sorbi C, Brasili L (2000) Structure-activity relationship at α-adrenergic receptors within a series of imidazoline analogues of cirazoline. Bioorg Med Chem 8:883-888.
57. Pineda J, Ugedo L, Garcia-Sevilla JA (1993) Stimulatory effects of clonidine, cirazoline and rilmenidine on locus coeruleus noradrenergic neurones: possible involvement of imidazoline-preferring receptors. Naunyn Schmiedebergs Arch Pharmacol 348:134-140.
58. Quirarte GL, Roozendaal B, McGaugh JL (1997) Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci USA 94:14048-14053.
59. Radulovic J, Rühmann A, Liepold T, Spiess J (1999) Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J Neurosci 19:5016-5025.
60. Radulovic J, Fischer A, Katerkamp U, Spiess J (2000) Role of regional neurotransmitter receptors in corticotropin-releasing factor (CRF)-mediated modulation of fear conditioning. Neuropharmacology 39:707-710.
61. Rainnie DG, Fernhout BJ, Shinnick-Gallagher P (1992) Differential actions of corticotropin-releasing factor on basolateral and central amygdala neurones, in vitro. J Pharmacol Exp Ther 263:846-858.
62. Roozendaal B (2007) Norepinephrine and long-term memory function. In: Brain norepinephrine: neurobiology and therapeutics (Ordway GA, Schwartz MA, Frazer A, eds), pp 236-274. Cambridge, UK: Cambridge UP.
63. 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.
64. Roozendaal B, McGaugh JL (1997) Glucocorticoid receptor agonist and antagonist administration into the basolateral but not central amygdala modulates memory storage. Neurobiol Learn Mem 67:176-179.
65. 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.
66. Roozendaal B, Quirarte GL, McGaugh JL (2002a) Glucocorticoids interact with the basolateral amygdala β-adrenoceptor-cAMP/PKA system in influencing memory consolidation. Eur J Neurosci 15:553-560.
67. Roozendaal B, Brunson KL, Holloway BL, McGaugh JL, Baram TZ (2002b) Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc Natl Acad Sci USA 99:13908-13913.
68. Roozendaal B, Okuda S, de Quervain DJ-F, McGaugh JL (2006a) Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 138:901-910.
69. Roozendaal B, Okuda S, Van der Zee EA, McGaugh JL (2006b) Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci USA 103:6741-6746.
70. 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.
71. Roseboom PH, Nanda SA, Bakshi VP, Trentani A, Newman SM, Kalin NH (2007) Predator threat induces behavioral inhibition, pituitary-adrenal activation and changes in amygdala CRF-binding protein gene expression. Psychoneuroendocrinology 32:44-55.
72. Sahgal A, Wright C, Edwardson JA, Keith AB (1983) Corticotrophin releasing factor is more potent than some corticotrophin-related peptides in affecting passive avoidance behaviour in rats. Neurosci Lett 36:81-86.
73. Sajdyk TJ, Schober DA, Gehlert DR, Shekhar A (1999) Role of corticotropin-releasing factor and urocortin within the basolateral amygdala of rats in anxiety and panic responses. Behav Brain Res 100:207-215.
74. Sauvage M, Steckler T (2001) Detection of corticotropin-releasing hormone receptor 1 immunoreactivity in cholinergic, dopaminergic and noradrenergic neurons of the murine basal forebrain and brainstem nuclei: potential implication for arousal and attention. Neuroscience 104:643-652.
75. Sawchenko PE (1987) Evidence for a local site of action for glucocorticoids in inhibiting CRF and vasopressin expression in the paraventricular nucleus. Brain Res 403:213-223.
76. Schultz J, Daly JW (1973) Accumulation of cyclic adenosine 3′,5′-monophosphate in cerebral cortical slices from rat and mouse: stimulatory effect of α- and β-adrenergic agents and adenosine. J Neurochem 21:1319-1326.
77. Shepard JD, Liu Y, Sassone-Corsi P, Aguilera G (2005) Role of glucocorticoids and cAMP-mediated repression in limiting corticotropin-releasing hormone transcription during stress. J Neurosci 25:4073-4081.
78. Smagin GN, Swiergel AH, Dunn AJ (1995) Corticotropin-releasing factor administered into the locus coeruleus, but not the parabrachial nucleus, stimulates norepinephrine release in the prefrontal cortex. Brain Res Bull 36:71-76.
79. Spiess J, Rivier J, River C, Vale W (1981) Primary structure of corticotropin-releasing factor from ovine hypothalamus. Proc Natl Acad Sci USA 78:6517-6521.
80. Stone EA, McEwen BS, Herrera AS, Carr KD (1987) Regulation of α and β components of noradrenergic cyclic AMP response in cortical slices. Eur J Pharmacol 141:347-356.
81. Strange BA, Dolan RJ (2004) β-Adrenergic modulation of emotional-evoked human amygdala and hippocampal responses. Proc Natl Acad Sci USA 101:11454-11458.
82. Sutton SW, Behan DP, Lahrichi SL, Kaiser R, Corrigan A, Lowry P, Potter E, Perrin MH, Rivier J, Vale WW (1995) Ligand requirements of the human corticotropin-releasing factor-binding protein. Endocrinology 136:1097-1102.
83. Swiergiel AH, Takahashi LK, Kalin NH (1993) Attenuation of stress-induced behavior by antagonism of corticotropin-releasing factor receptors in the central amygdala in the rat. Brain Res 623:229-234.
84. Teutsch G, Costerousse G, Deraedt R, Benzoni J, Fortin M, Philibert D (1981) 17alpha-alkynyl-11beta, 17-dihydroxyandrostane derivatives: a new class of potent glucocorticoids. Steroids 38:651-665.
85. Thompson BL, Erickson K, Schulkin J, Rosen JB (2004) Corticosterone facilitates retention of contextually conditioned fear and increases CRH mRNA expression in the amygdala. Behav Brain Res 149:209-215.
86. Vale W, Spiess J, Rivier C, Rivier J (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and β-endorphin. Science 213:1394-1397.
87. Valentino RJ, Foote SL, Aston-Jones G (1983) Corticotropin-releasing factor activates noradrenergic neurons of the locus coeruleus. Brain Res 270:363-367.
88. Van Bockstaele EJ, Peoples J, Valentino RJ (1999) Anatomic basis for differential regulation of the rostrolateral peri-locus coeruleus region by limbic afferents. Biol Psychiatry 46:1352-1363.
89. Van Stegeren AH, Goekoop R, Everaerd W, Scheltens P, Barkhof F, Kuijer JPA, Rombouts SARB (2005) Noradrenaline mediates amygdala activation in men and women during encoding of emotional material. Neuro-Image 24:898-909.
90. Van Stegeren AH, Wolf OT, Everaerd W, Scheltens P, Barkhof F, Rombouts SARB (2007) Endogenous cortisol level interacts with noradrenergic activation in the human amygdala. Neurobiol Learn Mem 87:57-66.