Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats - A possible mechanism for the persistence of traumatic memories in PTSD

Depression and Anxiety

Volumn 28, Issue 3, 2011, Pages 186-193

  Dȩbiec, Jacek ^a,b   Bush, David E A ^a   LeDoux, Joseph E ^a,c  

^a NEW YORK UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY CHILD STUDY CENTER   (United States)

^c NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

Author keywords

adrenergic receptor; Amygdala; Anxiety; Exposure therapy; Extinction; Fear; Fear conditioning; Isoproterenol; Late onset ptsd; Norepinephrine; Posttraumatic stress disorder; Propranolol; PTSD; Reconsolidation

Indexed keywords

ISOPRENALINE; PROPRANOLOL;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY CORTEX; CONDITIONING; CONTROLLED STUDY; FEAR; MALE; MEMORY; MEMORY CONSOLIDATION; NONHUMAN; NORADRENERGIC NERVE; NORADRENERGIC SYSTEM; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RAT;

ACOUSTIC STIMULATION; ADRENERGIC BETA-AGONISTS; ADRENERGIC BETA-ANTAGONISTS; AMYGDALA; ANIMALS; CONDITIONING, CLASSICAL; CUES; EXTINCTION, PSYCHOLOGICAL; FEAR; HUMANS; IMPLOSIVE THERAPY; ISOPROTERENOL; MALE; NOREPINEPHRINE; PROPRANOLOL; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA; RETENTION (PSYCHOLOGY); SIGNAL TRANSDUCTION; STRESS DISORDERS, POST-TRAUMATIC;

EID: 79952577258     PISSN: 10914269     EISSN: 15206394     Source Type: Journal    
DOI: 10.1002/da.20803     Document Type: Article

References (65)

1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. Text Revision. 4th ed. Washington, DC: American Psychiatric Association; 2000.
2. Foa EB. Psychosocial therapy for posttraumatic stress disorder. J Clin Psychiatry 2006;67:40-45. (Pubitemid 43268188)
3. Cukor J, Olden M, Lee F, Difede J. Evidence-based treatments for PTSD, new directions, and special challenges. Ann N Y Acad Sci 2010;1208:82-89.
4. Keane TM, Marshall AD, Taft CT. Posttraumatic stress disorder: etiology, epidemiology, and treatment outcome. Annu Rev Clin Psychol 2006;2:161-197. (Pubitemid 43799803)
5. Berger W, Mendlowicz MV, Marques-Portella C, et al. Pharmacologic alternatives to antidepressants in posttraumatic stress disorder: a systematic review. Prog Neuropsychopharmacol Biol Psychiatry 2009;33:169-180.
6. Hetrick SE, Purcell R, Garner B, Parslow R. Combined pharmacotherapy and psychological therapies for post traumatic stress disorder (PTSD). Cochrane Database Syst Rev 2010;CD007316.
7. Morgan III CA, Krystal JH, Southwick SM. Toward early pharmacological posttraumatic stress intervention. Biol Psychiatry 2003;53:834-843. (Pubitemid 36513760)
8. Ressler KJ, Mayberg HS. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nat Neurosci 2007;10:1116-1124. (Pubitemid 47339944)
9. Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB. Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 1995;52:1048-1060.
10. Aston-Jones G, Rajkowski J, Cohen J. Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 1999;46:1309-1320. (Pubitemid 30114448)
11. Bandura A. Principles of Behavior Modification. New York: Holt; 1969.
12. Bremner JD, Krystal JH, Southwick SM, Charney DS. Noradrenergic mechanisms in stress and anxiety: I. Preclinical studies. Synapse 1996;23:28-38.
13. Bremner JD, Krystal JH, Southwick SM, Charney DS. Noradrenergic mechanisms in stress and anxiety: II. Clinical studies. Synapse 1996;23:39-51.
14. Krystal JH, Neumeister A. Noradrenergic and serotonergic mechanisms in the neurobiology of posttraumatic stress disorder and resilience. Brain Res 2009;1293:13-23.
15. McGaugh JL. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 2004;27:1-28. (Pubitemid 39050395)
16. Southwick SM, Bremner JD, Rasmusson A, Morgan III CA, Arnsten A, Charney DS. Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder. Biol Psychiatry 1999;46:1192-1204. (Pubitemid 30114437)
17. Southwick SM, Davis M, Horner B, et al. Relationship of enhanced norepinephrine activity during memory consolidation to enhanced long-term memory in humans. Am J Psychiatry 2002;159:1420-1422. (Pubitemid 34832726)
18. Southwick SM, Krystal JH, Bremner JD, et al. Noradrenergic and serotonergic function in posttraumatic stress disorder. Arch Gen Psychiatry 1997;54:749-758. (Pubitemid 27344103)
19. Cahill L. The neurobiology of emotionally influenced memory. Implications for understanding traumatic memory. Ann N Y Acad Sci 1997;821:238-246.
20. Grillon C, Cordova J, Morgan CA, Charney DS, Davis M. Effects of the beta-blocker propranolol on cued and contextual fear conditioning in humans. Psychopharmacology (Berlin) 2004;175:342-352. (Pubitemid 39361922)
21. Grillon C, Southwick SM, Charney DS. The psychobiological basis of posttraumatic stress disorder. Mol Psychiatry 1996;1:278-297. (Pubitemid 126441313)
22. McGaugh JL. Memory - a century of consolidation. Science 2000;287:248-251.
23. Roozendaal B, McEwen BS, Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci 2009;10:423-433.
24. Prager EM, Johnson LR. Stress at the synapse: signal transduction mechanisms of adrenal steroids at neuronal membranes. Sci Signal 2009;2:re5.
25. Rodrigues SM, LeDoux JE, Sapolsky RM. The influence of stress hormones on fear circuitry. Annu Rev Neurosci 2009;32:289-313.
26. O'Donnell T, Hegadoren KM, Coupland NC. Noradrenergic mechanisms in the pathophysiology of post-traumatic stress disorder. Neuropsychobiology 2004;50:273-283. (Pubitemid 39482664)
27. Pitman RK. Post-traumatic stress disorder, hormones, and memory. Biol Psychiatry 1989;26:221-223. (Pubitemid 19173044)
28. Pitman RK, Sanders KM, Zusman RM, et al. Pilot study of secondary prevention of posttraumatic stress disorder with propranolol. Biol Psychiatry 2002;51:189-192. (Pubitemid 34127909)
29. Vaiva G, Ducrocq F, Jezequel K, et al. Immediate treatment with propranolol decreases posttraumatic stress disorder two months after trauma. Biol Psychiatry 2003;54:947-949. (Pubitemid 37311359)
30. Geracioti Jr TD, Baker DG, Ekhator NN, et al. CSF norepinephrine concentrations in posttraumatic stress disorder. Am J Psychiatry 2001;158:1227-1230. (Pubitemid 32717695)
31. Nemeroff CB, Bremner JD, Foa EB, Mayberg HS, North CS, Stein MB. Posttraumatic stress disorder: a state-of-the-science review. J Psychiatr Res 2006;40:1-21. (Pubitemid 43117523)
32. Strawn JR, Geracioti Jr TD. Noradrenergic dysfunction and the psychopharmacology of posttraumatic stress disorder. Depress Anxiety 2008;25:260-271. (Pubitemid 351499905)
33. Dollard JC, Miller NE. Personality and Psychopathology. New York: McGraw-Hill; 1950.
34. Eysenck HJ. The conditioning model of neuroses. Behav Brain Sci 1979;34:155-199.
35. Milad MR, Rauch SL, Pitman RK, Quirk GJ. Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 2006;73:61-71.
36. Rasmusson AM, Charney DS. Animal models of relevance to PTSD. Ann N Y Acad Sci 1997;821:332-351. (Pubitemid 27343032)
37. Rosen JB, Schulkin J. From normal fear to pathological anxiety. Psychol Rev 1998;105:325-350. (Pubitemid 128457850)
38. Lang PJ, Davis M, Ohman A. Fear and anxiety: animal models and human cognitive psychophysiology. J Affect Disord 2000;61:137-159. (Pubitemid 32119263)
39. LeDoux J. The amygdala. Curr Biol 2007;17:R868-R874. (Pubitemid 47576655)
40. Maren S. Synaptic mechanisms of associative memory in the amygdala. Neuron 2005;47:783-786. (Pubitemid 41266945)
41. Bush DEA, Caparosa EM, Gekker A, LeDoux JE. Beta-adrenergic receptos in the lateral nucleus of the amygdala contribute to the acquisition but not the consolidation of auditory fear conditioning. Front Behav Neurosci 2010;4:1-7.
42. Dȩbiec J, Ledoux JE. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 2004;129:267-272. (Pubitemid 39388847)
43. Lazzaro SC, Hou M, Cunha C, LeDoux JE, Cain CK. Antagonism of lateral amygdala alpha1-adrenergic receptors facilitates fear conditioning and long-term potentiation. Learn Mem 2010;17:489-493.
44. Dȩbiec J, Diaz-Mataix L, Bush DE, Doyère V, Ledoux JE. The amygdala encodes specific sensory features of an aversive reinforcer. Nat Neurosci 2010;13:536-537.
45. Dȩbiec J, Doyère V, Nader K, Ledoux JE. Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala. Proc Natl Acad Sci USA 2006;103:3428-3433. (Pubitemid 43346485)
46. Dȩbiec J, LeDoux JE, Nader K. Cellular and systems reconsolidation in the hippocampus. Neuron 2002;36:527-538. (Pubitemid 35291098)
47. Doyère V, Dȩbiec J, Monfils MH, Schafe GE, LeDoux JE. Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala. Nat Neurosci 2007;10:414-416. (Pubitemid 46494591)
48. Nader K, Schafe GE, Le Doux JE. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 2000;406:722-726.
49. Sara SJ. Retrieval and reconsolidation: toward a neurobiology of remembering. Learn Mem 2000;7:73-84. (Pubitemid 30213021)
50. Tronson NC, Taylor JR. Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 2007;8:262-275. (Pubitemid 46452320)
51. Alberini CM, Milekic MH, Tronel S. Mechanisms of memory stabilization and de-stabilization. Cell Mol Life Sci 2006;63:999-1008. (Pubitemid 43800769)
52. Dudai Y. Reconsolidation: the advantage of being refocused. Curr Opin Neurobiol 2006;16:174-178.
53. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press; 1986.
54. Dȩbiec J, LeDoux JE. Noradrenergic signaling in the amygdala contributes to the reconsolidation of fear memory: treatment implications for PTSD. Ann N Y Acad Sci 2006;1071:521-524. (Pubitemid 44126769)
55. Rodriguez-Ortiz CJ, De la Cruz V, Gutierrez R, Bermudez-Rattoni F. Protein synthesis underlies post-retrieval memory consolidation to a restricted degree only when updated information is obtained. Learn Mem 2005;12:533-537. (Pubitemid 41397214)
56. Tronson NC, Wiseman SL, Olausson P, Taylor JR. Bidirectional behavioral plasticity of memory reconsolidation depends on amygdalar protein kinase A. Nat Neurosci 2006;9:167-169. (Pubitemid 43164537)
57. Brunet A, Orr SP, Tremblay J, Robertson K, Nader K, Pitman RK. 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. (Pubitemid 351240920)
58. Przybyslawski J, Roullet P, Sara SJ. Attenuation of emotional and nonemotional memories after their reactivation: role of beta adrenergic receptors. J Neurosci 1999;19:6623-6628. (Pubitemid 29347461)
59. Kindt M, Soeter M, Vervliet B. Beyond extinction: erasing human fear responses and preventing the return of fear. Nat Neurosci 2009;12:256-258.
60. Soeter M, Kindt M. Dissociating response systems: erasing fear from memory. Neurobiol Learn Mem 2010;94:30-41.
61. Foa EB, Zoellner LA, Feeny NC, Hembree EA, Alvarez-Conrad J. Does imaginal exposure exacerbate PTSD symptoms? J Consult Clin Psychol 2002;70:1022-1028.
62. Andrews B, Brewin CR, Philpott R, Stewart L. Delayed-onset posttraumatic stress disorder: a systematic review of the evidence. Am J Psychiatry 2007;164:1319-1326. (Pubitemid 47461130)
63. Smid GE, Mooren TT, van der Mast RC, Gersons BP, Kleber RJ. Delayed posttraumatic stress disorder: systematic review, meta-analysis, and meta-regression analysis of prospective studies. J Clin Psychiatry 2009;70:1572-1582.
64. Monfils MH, Cowansage KK, Klann E, LeDoux JE. Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 2009;324:951-955.
65. Schiller D, Monfils MH, Raio CM, Johnson DC, Ledoux JE, Phelps EA. Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 2010;463:49-53.