Noradrenergic modulation of extinction learning and exposure therapy

Behavioural Brain Research

Volumn 208, Issue 1, 2010, Pages 1-11

  Mueller, Devin ^a   Cahill, Shawn P ^a  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Addiction; Amygdala; Anxiety disorders; Beta adrenoceptor; Fear conditioning; Infralimbic medial prefrontal cortex; Intrinsic excitability; Noradrenaline; Norepinephrine; Posttraumatic stress disorder

Indexed keywords

ALPRAZOLAM; ATENOLOL; BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CLENBUTEROL; GABAPENTIN; GLUCOCORTICOID; HYDROCORTISONE; NORADRENALIN; PLACEBO; PROPRANOLOL; YOHIMBINE; ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT;

ANXIETY DISORDER; APPETITE; ATTENTION; CONDITIONING; DRUG EFFICACY; DRUG MECHANISM; EXCITABILITY; EXTINCTION LEARNING; HUMAN; LEARNING; MEMORY; MOTIVATION; NERVE CELL PLASTICITY; NONHUMAN; NORADRENALIN RELEASE; NORADRENERGIC SYSTEM; PHOBIA; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SOCIAL PHOBIA; SPIDER PHOBIA; STIMULUS RESPONSE; ANIMAL; ANIMAL BEHAVIOR; BEHAVIOR THERAPY; DRUG EFFECT; FEAR; MEMORY DISORDER; METABOLISM; METHODOLOGY; PHYSIOLOGY; REINFORCEMENT;

ADRENERGIC ALPHA-AGONISTS; ANIMALS; BEHAVIOR THERAPY; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); EXTINCTION, PSYCHOLOGICAL; FEAR; HUMANS; MEMORY DISORDERS; NOREPINEPHRINE; RECEPTORS, ADRENERGIC, BETA; SIGNAL TRANSDUCTION;

EID: 77951888211     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.11.025     Document Type: Review

References (155)

1. Aerni A., Traber R., Hock C., Roozendaal B., Schelling G., Papassotiropoulos A., et al. Low-dose cortisol for symptoms of posttraumatic stress disorder. Am J Psychiatry 2004, 161:1488-1490.
2. Archer T., Cotic T., Jarbe T.U. Attenuation of the context effect and lack of unconditioned stimulus-preexposure effect in taste-aversion learning following treatment with DSP4, the selective noradrenaline neurotoxin. Behav Neural Biol 1982, 35:159-173.
3. Aston-Jones G., Rajkowski J., Kubiak P. Conditioned responses of monkey locus coeruleus neurons anticipate acquisition of discriminative behavior in a vigilance task. Neuroscience 1997, 80:697-715.
4. Barlow D.H. Anxiety and its disorders: the nature and treatment of anxiety and panic 2002, Guilford Press, New York. 2nd ed.
5. 2+ responses of basal dendrites in layer 5 pyramidal neurons of the prefrontal cortex. Neurochem Int 2007, 51:323-327.
6. Berlau D.J., McGaugh J.L. Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol Learn Mem 2006, 86:123-132.
7. Berman D.E., Dudai Y. Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 2001, 291:2417-2419.
8. Bongiovanni M., See R.E. A comparison of the effects of different operant training experiences and dietary restriction on the reinstatement of cocaine-seeking in rats. Pharmacol Biochem Behav 2008, 89:227-233.
9. Bouret S., Sara S.J. Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning. Eur J Neurosci 2004, 20:791-802.
10. Bouton M.E., Westbrook R.F., Corcoran K.A., Maren S. Contextual and temporal modulation of extinction: behavioral and biological mechanisms. Biol Psychiatry 2006, 60:352-360.
11. Brunet A., Orr S.P., Tremblay J., Robertson K., Nader K., Pitman R.K. Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. J Psychiatr Res 2008, 42:503-506.
12. Burgos-Robles A., Vidal-Gonzalez I., Santini E., Quirk G.J. Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex. Neuron 2007, 53:871-880.
13. Cahill L., Prins B., Weber M., McGaugh J.L. Beta-adrenergic activation and memory for emotional events. Nature 1994, 371:702-704.
14. Cahill S.P., Foa E.B. Anxiety disorders: cognitive behavior therapy 2005, Lippincott, Williams, & Wilkins, Philadelphia. 8th ed. B.J. Sadock, V.A. Sadock (Eds.).
15. Cain C.K., Blouin A.M., Barad M. Adrenergic transmission facilitates extinction of conditional fear in mice. Learn Mem 2004, 11:179-187.
16. Cassens G., Roffman M., Kuruc A., Orsulak P.J., Schildkraut J.J. Alterations in brain norepinephrine metabolism induced by environmental stimuli previously paired with inescapable shock. Science 1980, 209:1138-1140.
17. Charney D.S., Woods S.W., Heninger G.R. Noradrenergic function in generalized anxiety disorder: effects of yohimbine in healthy subjects and patients with generalized anxiety disorder. Psychiatry Res 1989, 27:173-182.
18. Charney D.S., Woods S.W., Krystal J.H., Nagy L.M., Heninger G.R. Noradrenergic neuronal dysregulation in panic disorder: the effects of intravenous yohimbine and clonidine in panic disorder patients. Acta Psychiatr Scand 1992, 86:273-282.
19. Conklin C.A., Tiffany S.T. Applying extinction research and theory to cue-exposure addiction treatments. Addiction 2002, 97:155-167.
20. Corcoran K.A., Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J Neurosci 2001, 21:1720-1726.
21. Corcoran K.A., Maren S. Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction. Learn Mem 2004, 11:598-603.
22. Crombag H.S., Shaham Y. Renewal of drug seeking by contextual cues after prolonged extinction in rats. Behav Neurosci 2002, 116:169-173.
23. Crow T.J., Deakin J.F., File S.E., Longden A., Wendlandt S. The locus coeruleus noradrenergic system-evidence against a role in attention, habituation, anxiety and motor activity. Brain Res 1978, 155:249-261.
24. Dahlstrom A., Fuxe K. Localization of monoamines in the lower brain stem. Experientia 1964, 20:398-399.
25. Davis A.R., Shields A.D., Brigman J.L., Norcross M., McElligott Z.A., Holmes A., et al. Yohimbine impairs extinction of cocaine-conditioned place preference in an alpha2-adrenergic receptor independent process. Learn Mem 2008, 15:667-676.
26. de Kloet E.R., Oitzl M.S., Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci 1999, 22:422-426.
27. Debiec J., LeDoux J.E. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 2004, 129:267-272.
28. Dragunow M., Laverty R. Failure of dorsal bundle lesions in rats to increase distractibility to a low intensity tone. Pharmacol Biochem Behav 1983, 18:673-675.
29. Dudai Y. Molecular bases of long-term memories: a question of persistence. Curr Opin Neurobiol 2002, 12:211-216.
30. Duvarci S., Mamou C.B., Nader K. Extinction is not a sufficient condition to prevent fear memories from undergoing reconsolidation in the basolateral amygdala. Eur J Neurosci 2006, 24:249-260.
31. Eisenberg M., Kobilo T., Berman D.E., Dudai Y. Stability of retrieved memory: inverse correlation with trace dominance. Science 2003, 301:1102-1104.
32. Famularo R., Kinscherff R., Fenton T. Propranolol treatment for childhood posttraumatic stress disorder, acute type. A pilot study. Am J Dis Child 1988, 142:1244-1247.
33. Feenstra M.G., Vogel M., Botterblom M.H., Joosten R.N., de Bruin J.P. Dopamine and noradrenaline efflux in the rat prefrontal cortex after classical aversive conditioning to an auditory cue. Eur J Neurosci 2001, 13:1051-1054.
34. Fricks-Gleason A.N., Marshall J.F. Post-retrieval beta-adrenergic receptor blockade: effects on extinction and reconsolidation of cocaine-cue memories. Learn Mem 2008, 15:643-648.
35. Gallagher M., Kapp B.S., Musty R.E., Driscoll P.A. Memory formation: evidence for a specific neurochemical system in the amygdala. Science 1977, 198:423-425.
36. Gelinas J.N., Nguyen P.V. Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J Neurosci 2005, 25:3294-3303.
37. Gelinas J.N., Tenorio G., Lemon N., Abel T., Nguyen P.V. Beta-adrenergic receptor activation during distinct patterns of stimulation critically modulates the PKA-dependence of LTP in the mouse hippocampus. Learn Mem 2008, 15:281-289.
38. Grillon C., Cordova J., Morgan C.A., Charney D.S., Davis M. Effects of the beta-blocker propranolol on cued and contextual fear conditioning in humans. Psychopharmacology (Berl) 2004, 175:342-352.
39. Gurguis G.N., Vitton B.J., Uhde T.W. Behavioral, sympathetic and adrenocortical responses to yohimbine in panic disorder patients and normal controls. Psychiatry Res 1997, 71:27-39.
40. Haile C.N., GrandPre T., Kosten T.A. Chronic unpredictable stress, but not chronic predictable stress, enhances the sensitivity to the behavioral effects of cocaine in rats. Psychopharmacology (Berl) 2001, 154:213-220.
41. Hayes P.E., Schultz S.C. The use of beta-adrenergic blocking agents in anxiety disorders and schizophrenia. Pharmacotherapy 1983, 32:101-117.
42. Hayes P.E., Schultz S.C. Beta-blockers in anxiety disorders. J Affect Disord 1987, 13:119-130.
43. Hefner K., Whittle N., Juhasz J., Norcross M., Karlsson R.M., Saksida L.M., et al. Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J Neurosci 2008, 28:8074-8085.
44. Henry M., Fishman J.R., Youngner S.J. Propranolol and the prevention of post-traumatic stress disorder: is it wrong to erase the " sting" of bad memories?. Am J Bioeth 2007, 7:12-20.
45. Hobin J.A., Ji J., Maren S. Ventral hippocampal muscimol disrupts context-specific fear memory retrieval after extinction in rats. Hippocampus 2006, 16:174-182.
46. Hu H., Real E., Takamiya K., Kang M.G., Ledoux J., Huganir R.L., et al. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 2007, 131:160-173.
47. Hugues S., Deschaux O., Garcia R. Postextinction infusion of a mitogen-activated protein kinase inhibitor into the medial prefrontal cortex impairs memory of the extinction of conditioned fear. Learn Mem 2004, 11:540-543.
48. Hugues S., Garcia R., Lena I. Time course of extracellular catecholamine and glutamate levels in the rat medial prefrontal cortex during and after extinction of conditioned fear. Synapse 2007, 61:933-937.
49. Jefferson J.W. Social phobia: everyone's disorder?. J Clin Psychiatry 1996, 57(Suppl. 6):28-32.
50. Ji J.Z., Wang X.M., Li B.M. Deficit in long-term contextual fear memory induced by blockade of beta-adrenoceptors in hippocampal CA1 region. Eur J Neurosci 2003, 17:1947-1952.
51. Jones B.E., Halaris A.E., McIlhany M., Moore R.Y. Ascending projections of the locus coeruleus in the rat. I. Axonal transport in central noradrenaline neurons. Brain Res 1977, 127:1-21.
52. Kampman K.M., Volpicelli J.R., Mulvaney F., Alterman A.I., Cornish J., Gariti P., et al. Effectiveness of propranolol for cocaine dependence treatment may depend on cocaine withdrawal symptom severity. Drug Alcohol Depend 2001, 63:69-78.
53. Katsuki H., Izumi Y., Zorumski C.F. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J Neurophysiol 1997, 77:3013-3020.
54. Kim J., Lee S., Park H., Song B., Hong I., Geum D., et al. Blockade of amygdala metabotropic glutamate receptor subtype 1 impairs fear extinction. Biochem Biophys Res Commun 2007, 355:188-193.
55. Koob G.F., Kelley A.E., Mason S.T. Locus coeruleus lesions: learning and extinction. Physiol Behav 1978, 20:709-716.
56. Kupferschmidt D.A., Tribe E., Erb S. Effects of repeated yohimbine on the extinction and reinstatement of cocaine seeking. Pharmacol Biochem Behav 2009, 91:473-480.
57. Lalumiere RT, Niehoff KE, Kalivas PW. The infralimbic cortex regulates the consolidation of extinction after cocaine self-administration. Learn Mem; in press.
58. Laverdure B., Boulenger J.P. Beta-blocking drugs and anxiety. A proven therapeutic value. Encephale 1991, 17:481-492.
59. Lee J.L., Everitt B.J. Reactivation-dependent amnesia in Pavlovian approach and instrumental transfer. Learn Mem 2008, 15:597-602.
60. Liang K.C., Juler R.G., McGaugh J.L. Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain Res 1986, 368:125-133.
61. Liang K.C., McGaugh J.L., Yao H.Y. Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res 1990, 508:225-233.
62. Lin C.H., Yeh S.H., Lu H.Y., Gean P.W. The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. J Neurosci 2003, 23:8310-8317.
63. Loughlin S.E., Foote S.L., Bloom F.E. Efferent projections of nucleus locus coeruleus: topographic organization of cells of origin demonstrated by three-dimensional reconstruction. Neuroscience 1986, 18:291-306.
64. Maguire M.E., Ross E.M., Gilman A.G. Beta-adrenergic receptor: ligand binding properties and the interaction with adenylyl cyclase. Adv Cyclic Nucleotide Res 1977, 8:1-83.
65. Mason S.T. Dorsal bundle extinction effect: motivation or attention?. Physiol Behav 1979, 23:43-51.
66. Mason S.T. The neurochemistry and pharmacology of extinction behavior. Neurosci Biobehav Rev 1983, 7:325-347.
67. Mason S.T., Fibiger H. Noradrenaline, fear and extinction. Brain Res 1979, 165:47-56.
68. Mason S.T., Fibiger H.C. Evidence for a role of brain noradrenaline in attention and stimulus sampling. Brain Res 1978, 159:421-426.
69. Mason S.T., Iversen S.D. Learning in the absence of forebrain noradrenaline. Nature 1975, 258:422-424.
70. Mason S.T., Iversen S.D. The dorsal noradrenergic bundle, extinction and non-reward. Physiol Behav 1978, 21:1043-1045.
71. Mayr B., Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2001, 2:599-609.
72. McCormick D.A., Thompson R.F. Locus coeruleus lesions and resistance to extinction of a classically conditioned response: involvement of the neocortex and hippocampus. Brain Res 1982, 245:239-249.
73. McGaugh J.L. Memory consolidation and the amygdala: a systems perspective. Trends Neurosci 2002, 25:456-461.
74. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 2004, 27:1-28.
75. McGaugh J.L., McIntyre C.K., Power A.E. Amygdala modulation of memory consolidation: interaction with other brain systems. Neurobiol Learn Mem 2002, 78:539-552.
76. McGaugh J.L., Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 2002, 12:205-210.
77. McGaugh J.L., Roozendaal B. Drug enhancement of memory consolidation: historical perspective and neurobiological implications. Psychopharmacology (Berl) 2009, 202:3-14.
78. McIntyre C.K., Hatfield T., McGaugh J.L. Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. Eur J Neurosci 2002, 16:1223-1226.
79. Merlo A.B., Izquierdo I. The effect of catecholamines on learning in rats. Med Pharmacol Exp Int J Exp Med 1967, 16:343-349.
80. Mingote S., de Bruin J.P., Feenstra M.G. Noradrenaline and dopamine efflux in the prefrontal cortex in relation to appetitive classical conditioning. J Neurosci 2004, 24:2475-2480.
81. Miranda M.I., Lalumiere R.T., Buen T.V., Bermudez-Rattoni F., McGaugh J.L. Blockade of noradrenergic receptors in the basolateral amygdala impairs taste memory. Eur J Neurosci 2003, 18:2605-2610.
82. Monfils M.H., Cowansage K.K., Klann E., LeDoux J.E. Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 2009, 324:951-955.
83. Morissette S.B., Spiegel D.A., Barlow D.H. Combining exposure and pharmacotherapy in the treatment of social anxiety disorder: a preliminary study of state-dependent learning. J Psychopathol Behav Assess 2008, 30:211-219.
84. Morris R.W., Bouton M.E. The effect of yohimbine on the extinction of conditioned fear: a role for context. Behav Neurosci 2007, 121:501-514.
85. Mueller D., Olivera-Figueroa L.A., Pine D.S., Quirk G.J. The effects of yohimbine and amphetamine on fear expression and extinction in rats. Psychopharmacology (Berl) 2009, 204:599-606.
86. Mueller D., Porter J.T., Quirk G.J. Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J Neurosci 2008, 28:369-375.
87. Murchison C.F., Zhang X.Y., Zhang W.P., Ouyang M., Lee A., Thomas S.A. A distinct role for norepinephrine in memory retrieval. Cell 2004, 117:131-143.
88. Myers K.M., Davis M. Mechanisms of fear extinction. Mol Psychiatry 2007, 12:120-150.
89. Nader K., Schafe G.E., Le Doux J.E. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 2000, 406:722-726.
90. Nguyen P.V., Woo N.H. Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 2003, 71:401-437.
91. O'Brien C.P., Childress A.R., McLellan T., Ehrman R. Integrating systemic cue exposure with standard treatment in recovering drug dependent patients. Addict Behav 1990, 15:355-365.
92. Ouyang M., Thomas S.A. A requirement for memory retrieval during and after long-term extinction learning. Proc Natl Acad Sci USA 2005, 102:9347-9352.
93. Pavlov I.P. Conditioned reflexes 1927, Oxford University Press, London.
94. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 1993, 11:1023-1035.
95. Pedreira M.E., Maldonado H. Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 2003, 38:863-869.
96. Pelletier J.G., Likhtik E., Filali M., Pare D. Lasting increases in basolateral amygdala activity after emotional arousal: implications for facilitated consolidation of emotional memories. Learn Mem 2005, 12:96-102.
97. Peters J., Kalivas P.W., Quirk G.J. Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 2009, 16:279-288.
98. Peters J., Lalumiere R.T., Kalivas P.W. Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. J Neurosci 2008, 28:6046-6053.
99. Peters J., Vallone J., Laurendi K., Kalivas P.W. Opposing roles for the ventral prefrontal cortex and the basolateral amygdala on the spontaneous recovery of cocaine-seeking in rats. Psychopharmacology (Berl) 2008, 197:319-326.
100. Pitman R.K. Post-traumatic stress disorder, hormones, and memory. Biol Psychiatry 1989, 26:221-223.
101. Pitman R.K., Sanders K.M., Zusman R.M., Healy A.R., Cheema F., Lasko N.B., et al. Pilot study of secondary prevention of posttraumatic stress disorder with propranolol. Biol Psychiatry 2002, 51:189-192.
102. Powers M.B., Smits J.A., Otto M.W., Sanders C., Emmelkamp P.M. Facilitation of fear extinction in phobic participants with a novel cognitive enhancer: a randomized placebo controlled trial of yohimbine augmentation. J Anxiety Disord 2009, 23:350-356.
103. President's Council on Bioethics Beyond therapy: biotechnology and the pursuit of happiness 2003, Government Printing Office, Washington, DC.
104. Price M.T., Murray G.N., Fibiger H.C. Schedule dependent changes in operant responding after lesions of the dorsal tegmental noradrenergic projection. Pharmacol Biochem Behav 1977, 6:11-15.
105. Przybyslawski J., Roullet P., Sara S.J. Attenuation of emotional and nonemotional memories after their reactivation: role of beta adrenergic receptors. J Neurosci 1999, 19:6623-6628.
106. Quirarte G.L., Roozendaal B., McGaugh J.L. Glucocorticoid enhancement of memory storage involves noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci USA 1997, 94:14048-14053.
107. Quirk G.J., Garcia R., Gonzalez-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol Psychiatry 2006, 60:337-343.
108. Quirk G.J., Likhtik E., Pelletier J.G., Pare D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 2003, 23:8800-8807.
109. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
110. Raskind M.A., Peskind E.R., Kanter E.D., Petrie E.C., Radant A., Thompson C.E., et al. Reduction of nightmares and other PTSD symptoms in combat veterans by prazosin: a placebo-controlled study. Am J Psychiatry 2003, 160:371-373.
111. Rescorla R.A. Retraining of extinguished Pavlovian stimuli. J Exp Psychol Anim Behav Process 2001, 27:115-124.
112. Rescorla R.A. Spontaneous recovery. Learn Mem 2004, 11:501-509.
113. Rescorla R.A., Heth C.D. Reinstatement of fear to an extinguished conditioned stimulus. J Exp Psychol Anim Behav Process 1975, 1:88-96.
114. Richards J.K., Simms J.A., Bartlett S.E. Conditioned cues and yohimbine induce reinstatement of beer and near-beer seeking in Long-Evans rats. Addict Biol 2009, 14:144-151.
115. Roberts D.C., Price M.T., Fibiger H.C. The dorsal tegmental noradrenergic projection: an analysis of its role in maze learning. J Comp Physiol Psychol 1976, 90:363-372.
116. Rodriguez-Romaguera J., Sotres-Bayon F., Mueller D., Quirk G.J. Systemic propranolol acts centrally to reduce conditioned fear in rats without impairing extinction. Biol Psychiatry 2009, 65:887-892.
117. Roozendaal B., Castello N.A., Vedana G., Barsegyan A., McGaugh J.L. Noradrenergic activation of the basolateral amygdala modulates consolidation of object recognition memory. Neurobiol Learn Mem 2008, 90:576-579.
118. Roozendaal B., McGaugh J.L. The memory-modulatory effects of glucocorticoids depend on an intact stria terminalis. Brain Res 1996, 709:243-250.
119. 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 USA 2006, 103:6741-6746.
120. Roozendaal B., Quirarte G.L., McGaugh J.L. Glucocorticoids interact with the basolateral amygdala beta-adrenoceptor-cAMP/cAMP/PKA system in influencing memory consolidation. Eur J Neurosci 2002, 15:553-560.
121. Roozendaal B., Williams C.L., McGaugh J.L. Glucocorticoid receptor activation in the rat nucleus of the solitary tract facilitates memory consolidation: involvement of the basolateral amygdala. Eur J Neurosci 1999, 11:1317-1323.
122. Roullet P., Sara S. Consolidation of memory after its reactivation: involvement of beta noradrenergic receptors in the late phase. Neural Plast 1998, 6:63-68.
123. Sangha S., Scheibenstock A., Morrow R., Lukowiak K. Extinction requires new RNA and protein synthesis and the soma of the cell right pedal dorsal 1 in Lymnaea stagnalis. J Neurosci 2003, 23:9842-9851.
124. Santini E., Ge H., Ren K., Pena dO., Quirk G.J. Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J Neurosci 2004, 24:5704-5710.
125. Santini E., Quirk G.J., Porter J.T. Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J Neurosci 2008, 28:4028-4036.
126. Sara S.J. The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 2009, 10:211-223.
127. Sara S.J., Segal M. Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. Prog Brain Res 1991, 88:571-585.
128. Schelling G., Briegel J., Roozendaal B., Stoll C., Rothenhausler H.B., Kapfhammer H.P. The effect of stress doses of hydrocortisone during septic shock on posttraumatic stress disorder in survivors. Biol Psychiatry 2001, 50:978-985.
129. Schelling G., Kilger E., Roozendaal B., de Quervain D.J., Briegel J., Dagge A., et al. Stress doses of hydrocortisone, traumatic memories, and symptoms of posttraumatic stress disorder in patients after cardiac surgery: a randomized study. Biol Psychiatry 2004, 55:627-633.
130. Schimanski L.A., Ali D.W., Baker G.B., Nguyen P.V. Impaired hippocampal LTP in inbred mouse strains can be rescued by beta-adrenergic receptor activation. Eur J Neurosci 2007, 25:1589-1598.
131. Schultz W., Dickinson A. Neuronal coding of prediction errors. Annu Rev Neurosci 2000, 23:473-500.
132. Seeds N.W., Gilman A.G. Norepinephrine stimulated increase of cyclic AMP levels in developing mouse brain cell cultures. Science 1971, 174:292.
133. Setlow B., Roozendaal B., McGaugh J.L. Involvement of a basolateral amygdala complex-nucleus accumbens pathway in glucocorticoid-induced modulation of memory consolidation. Eur J Neurosci 2000, 12:367-375.
134. Shepard J.D., Bossert J.M., Liu S.Y., Shaham Y. The anxiogenic drug yohimbine reinstates methamphetamine seeking in a rat model of drug relapse. Biol Psychiatry 2004, 55:1082-1089.
135. 2+-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning. Neuron 2007, 53:79-89.
136. Skeberdis V.A., Chevaleyre V., Lau C.G., Goldberg J.H., Pettit D.L., Suadicani S.O., et al. Protein kinase A regulates calcium permeability of NMDA receptors. Nat Neurosci 2006, 9:501-510.
137. Snyder E.M., Colledge M., Crozier R.A., Chen W.S., Scott J.D., Bear M.F. Role for A kinase-anchoring proteins (AKAPS) in glutamate receptor trafficking and long term synaptic depression. J Biol Chem 2005, 280:16962-16968.
138. Soravia L.M., Heinrichs M., Aerni A., Maroni C., Schelling G., Ehlert U., et al. Glucocorticoids reduce phobic fear in humans. Proc Natl Acad Sci USA 2006, 103:5585-5590.
139. Sotres-Bayon F., Bush D.E., LeDoux J.E. Acquisition of fear extinction requires activation of NR2B-containing NMDA receptors in the lateral amygdala. Neuropsychopharmacology 2007, 32:1929-1940.
140. Sotres-Bayon F., Cain C.K., LeDoux J.E. Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol Psychiatry 2006, 60:329-336.
141. Southwick S.M., Krystal J.H., Bremner J.D., Morgan C.A., Nicolaou A.L., Nagy L.M., et al. Noradrenergic and serotonergic function in posttraumatic stress disorder. Arch Gen Psychiatry 1997, 54:749-758.
142. Southwick S.M., Krystal J.H., Morgan C.A., Johnson D., Nagy L.M., Nicolaou A., et al. Abnormal noradrenergic function in posttraumatic stress disorder. Arch Gen Psychiatry 1993, 50:266-274.
143. Stein M.B., Kerridge C., Dimsdale J.E., Hoyt D.B. Pharmacotherapy to prevent PTSD: results from a randomized controlled proof-of-concept trial in physically injured patients. J Trauma Stress 2007, 20:923-932.
144. Sterpenich V., D'Argembeau A., Desseilles M., Balteau E., Albouy G., Vandewalle G., et al. The locus ceruleus is involved in the successful retrieval of emotional memories in humans. J Neurosci 2006, 26:7416-7423.
145. 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.
146. Taylor F., Raskind M.A. The alpha1-adrenergic antagonist prazosin improves sleep and nightmares in civilian trauma posttraumatic stress disorder. J Clin Psychopharmacol 2002, 22:82-85.
147. Thomas M.J., Moody T.D., Makhinson M., O'Dell T.J. Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 1996, 17:475-482.
148. Torda C. Effects of catecholamines on behavior. J Neurosci Res 1976, 2:193-202.
149. Tronson N.C., Taylor J.R. Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 2007, 8:262-275.
150. Tully K., Li Y., Tsvetkov E., Bolshakov V.Y. Norepinephrine enables the induction of associative long-term potentiation at thalamo-amygdala synapses. Proc Natl Acad Sci USA 2007, 104:14146-14150.
151. Vaiva G., Ducrocq F., Jezequel K., Averland B., Lestavel P., Brunet A., et al. Immediate treatment with propranolol decreases posttraumatic stress disorder two months after trauma. Biol Psychiatry 2003, 54:947-949.
152. Ventura R., Latagliata E.C., Morrone C., La M., Puglisi-Allegra I.S. Prefrontal norepinephrine determines attribution of " high" motivational salience. PLoS ONE 2008, 3:e3044.
153. Ventura R., Morrone C., Puglisi-Allegra S. Prefrontal/accumbal catecholamine system determines motivational salience attribution to both reward- and aversion-related stimuli. Proc Natl Acad Sci USA 2007, 104:5181-5186.
154. Vidal-Gonzalez I., Vidal-Gonzalez B., Rauch S.L., Quirk G.J. Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 2006, 13:728-733.
155. Zarrindast M.R., Bahreini T., Adl M. Effect of imipramine on the expression and acquisition of morphine-induced conditioned place preference in mice. Pharmacol Biochem Behav 2002, 73:941-949.