Preclinical Assessment for Selectively Disrupting a Traumatic Memory via Postretrieval Inhibition of Glucocorticoid Receptors

Biological Psychiatry

Volumn 65, Issue 3, 2009, Pages 249-257

  Taubenfeld, Stephen M ^a   Riceberg, Justin S ^a   New, Antonia S ^a   Alberini, Cristina M ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Fear conditioning; glucocorticoid receptor; inhibitory avoidance; memory; PTSD; reconsolidation; RU38486

Indexed keywords

GLUCOCORTICOID RECEPTOR ANTAGONIST; MIFEPRISTONE;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CONDITIONING; DOSE RESPONSE; FEAR; LONG EVANS RAT; MALE; MEMORY; MEMORY CONSOLIDATION; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RAT; SYSTEMIC THERAPY;

AGING; ANIMALS; AVOIDANCE LEARNING; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROSHOCK; HORMONE ANTAGONISTS; MALE; MEMORY; MENTAL RECALL; MIFEPRISTONE; MOTOR ACTIVITY; RATS; RATS, LONG-EVANS; RECEPTORS, GLUCOCORTICOID; STRESS DISORDERS, POST-TRAUMATIC; STRESS DISORDERS, TRAUMATIC, ACUTE; WOUNDS AND INJURIES;

EID: 58149313654     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2008.07.005     Document Type: Article

References (76)

1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. text revision (2000), American Psychiatric Association Press, Washington, DC
2. Kessler R.C., Sonnega A., Bromet E., Hughes M., and Nelson C.B. Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 52 (1995) 1048-1060
3. Brady K., Pearlstein T., Asnis G.M., Baker D., Rothbaum B., Sikes C.R., et al. Efficacy and safety of sertraline treatment of posttraumatic stress disorder: a randomized controlled trial. JAMA 283 (2000) 1837-1844
4. Tucker P., Zaninelli R., Yehuda R., Ruggiero L., Dillingham K., and Pitts C.D. Paroxetine in the treatment of chronic posttraumatic stress disorder: Results of a placebo-controlled, flexible-dosage trial. J Clin Psychiatry 62 (2001) 860-868
5. Fairbank J.A., and Nicholson R.A. Theoretical and empirical issues in the treatment of post-traumatic stress disorder in Vietnam veterans. J Clin Psychol 43 (1987) 44-55
6. Keane T.M., Scott W.O., Chavoya G.A., Lamparski D.M., and Fairbank J.A. Social support in Vietnam veterans with posttraumatic stress disorder: A comparative analysis. J Consult Clin Psychol 53 (1985) 95-102
7. Bouton M.E., Mineka S., and Barlow D.H. A modern learning theory perspective on the etiology of panic disorder. Psychol Rev 108 (2001) 4-32
8. Grillon C., Morgan C.A., Southwick S.M., Davis M., and Charney D.S. Baseline startle amplitude and prepulse inhibition in Vietnam veterans with posttraumatic stress disorder. Psychiatry Res 64 (1996) 169-178
9. Rau V., DeCola J.P., and Fanselow M.S. Stress-induced enhancement of fear learning: An animal model of posttraumatic stress disorder. Neurosci Biobehav Rev 29 (2005) 1207-1223
10. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 23 (2000) 155-184
11. Miller M.M., and McEwen B.S. Establishing an agenda for translational research on PTSD. Ann N Y Acad Sci 1071 (2006) 294-312
12. Siegmund A., and Wotjak C.T. Toward an animal model of posttraumatic stress disorder. Ann N Y Acad Sci 1071 (2006) 324-334
13. Alberini C.M. Mechanisms of memory stabilization: Are consolidation and reconsolidation similar or distinct processes?. Trends Neurosci 28 (2005) 51-56
14. Dudai Y. Reconsolidation: The advantage of being refocused. Curr Opin Neurobiol 16 (2006) 174-178
15. Nader K. Memory traces unbound. Trends Neurosci 26 (2003) 65-72
16. Yehuda R., Flory J.D., Southwick S., and Charney D.S. Developing an agenda for translational studies of resilience and vulnerability following trauma exposure. Ann N Y Acad Sci 1071 (2006) 379-396
17. Dudai Y., and Eisenberg M. Rites of passage of the engram: Reconsolidation and the lingering consolidation hypothesis. Neuron 44 (2004) 93-100
18. Nader K., Schafe G.E., and Le Doux J.E. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406 (2000) 722-726
19. Sara S.J. Retrieval and reconsolidation: Toward a neurobiology of remembering. Learn Mem 7 (2000) 73-84
20. Davis S., and Laroche S. Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: A review. Genes Brain Behav 5 Suppl 2 (2006) 61-72
21. Blundell J., Kouser M., and Powell C.M. Systemic inhibition of mammalian target of rapamycin inhibits fear memory reconsolidation. Neurobiol Learn Mem 90 (2008) 28-35
22. Ben Mamou C., Gamache K., and Nader K. NMDA receptors are critical for unleashing consolidated auditory fear memories. Nat Neurosci 9 (2006) 1237-1239
23. Debiec J., and Ledoux J.E. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129 (2004) 267-272
24. Przybyslawski J., Roullet P., and Sara S.J. Attenuation of emotional and nonemotional memories after their reactivation: Role of beta adrenergic receptors. J Neurosci 19 (1999) 6623-6628
25. Jin X.C., Lu Y.F., Yang X.F., Ma L., and Li B.M. Glucocorticoid receptors in the basolateral nucleus of amygdala are required for postreactivation reconsolidation of auditory fear memory. Eur J Neurosci 25 (2007) 3702-3712
26. Tronel S., and Alberini C.M. Persistent disruption of a traumatic memory by postretrieval inactivation of glucocorticoid receptors in the amygdala. Biol Psychiatry 62 (2007) 33-39
27. Pugh C.R., Fleshner M., and Rudy J.W. Type II glucocorticoid receptor antagonists impair contextual but not auditory-cue fear conditioning in juvenile rats. Neurobiol Learn Mem 67 (1997) 75-79
28. Flint Jr. R.W., and Marino C.L. Cycloheximide impairs reconsolidation of a contextually reactivated memory in a conditioned taste aversion paradigm. Behav Neurosci 121 (2007) 433-438
29. Milekic M.H., Brown S.D., Castellini C., and Alberini C.M. Persistent disruption of an established morphine conditioned place preference. J Neurosci 26 (2006) 3010-3020
30. Milekic M.H., and Alberini C.M. Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36 (2002) 521-525
31. Taubenfeld S.M., Milekic M.H., Monti B., and Alberini C.M. The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat Neurosci 4 (2001) 813-818
32. Weaver I.C., Meaney M.J., and Szyf M. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci U S A 103 (2006) 3480-3485
33. Duvarci S., and Nader K. Characterization of fear memory reconsolidation. J Neurosci 24 (2004) 9269-9275
34. Lattal K.M., and Abel T. Behavioral impairments caused by injections of the protein synthesis inhibitor anisomycin after contextual retrieval reverse with time. Proc Natl Acad Sci U S A 101 (2004) 4667-4672
35. Anokhin K.V., Tiunova A.A., and Rose S.P. Reminder effects-reconsolidation or retrieval deficit?. Pharmacological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks. Eur J Neurosci 15 (2002) 1759-1765
36. Milekic M.H., Pollonini G., and Alberini C.M. Temporal requirement of C/EBPbeta in the amygdala following reactivation but not acquisition of inhibitory avoidance. Learn Mem 14 (2007) 504-511
37. Nader K., Schafe G.E., and LeDoux J.E. The labile nature of consolidation theory. Nat Rev Neurosci 1 (2000) 216-219
38. Bisson J.I., Jenkins P.L., Alexander J., and Bannister C. Randomised controlled trial of psychological debriefing for victims of acute burn trauma. Br J Psychiatry 171 (1997) 78-81
39. Gray M.J., and Litz B.T. Behavioral interventions for recent trauma: Empirically informed practice guidelines. Behav Modif 29 (2005) 189-215
40. McNally R.J., Bryant R.A., and Ehlers A. Does early psychological intervention promote recovery from posttraumatic stress?. Psychol Sci Publ Inter 4 (2003) 45-79
41. Rothbaum B.O., and Davis M. Applying learning principles to the treatment of post-trauma reactions. Ann N Y Acad Sci 1008 (2003) 112-121
42. Belanoff J.K., Flores B.H., Kalezhan M., Sund B., and Schatzberg A.F. Rapid reversal of psychotic depression using mifepristone. J Clin Psychopharmacol 21 (2001) 516-521
43. Belanoff J.K., Rothschild A.J., Cassidy F., DeBattista C., Baulieu E.E., Schold C., et al. An open label trial of C-1073 (mifepristone) for psychotic major depression. Biol Psychiatry 52 (2002) 386-392
44. DeBattista C., and Belanoff J. The use of mifepristone in the treatment of neuropsychiatric disorders. Trends Endocrinol Metab 17 (2006) 117-121
45. Flores B.H., Kenna H., Keller J., Solvason H.B., and Schatzberg A.F. Clinical and biological effects of mifepristone treatment for psychotic depression. Neuropsychopharmacology 31 (2006) 628-636
46. Simpson G.M., El Sheshai A., Loza N., Kingsbury S.J., Fayek M., Rady A., et al. An 8-week open-label trial of a 6-day course of mifepristone for the treatment of psychotic depression. J Clin Psychiatry 66 (2005) 598-602
47. Belanoff J.K., Jurik J., Schatzberg L.D., DeBattista C., and Schatzberg A.F. Slowing the progression of cognitive decline in Alzheimer's disease using mifepristone. J Mol Neurosci 19 (2002) 201-206
48. DeBattista C., and Belanoff J. C-1073 (mifepristone) in the adjunctive treatment of Alzheimer's disease. Curr Alzheimer Res 2 (2005) 125-129
49. Pomara N., Doraiswamy P.M., Tun H., and Ferris S. Mifepristone (RU 486) for Alzheimer's disease. Neurology 58 (2002) 1436
50. Gallagher P., Watson S., Smith M.S., Ferrier I.N., and Young A.H. Effects of adjunctive mifepristone (RU-486) administration on neurocognitive function and symptoms in schizophrenia. Biol Psychiatry 57 (2005) 155-161
51. Young A.H., Gallagher P., Watson S., Del-Estal D., Owen B.M., and Ferrier I.N. Improvements in neurocognitive function and mood following adjunctive treatment with mifepristone (RU-486) in bipolar disorder. Neuropsychopharmacology 29 (2004) 1538-1545
52. Quirk G.J., and Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33 (2008) 56-72
53. Bouton M.E., Westbrook R.F., Corcoran K.A., and Maren S. Contextual and temporal modulation of extinction: Behavioral and biological mechanisms. Biol Psychiatry 60 (2006) 352-360
54. Abrari K., Rashidy-Pour A., Semnanian S., and Fathollahi Y. Administration of corticosterone after memory reactivation disrupts subsequent retrieval of a contextual conditioned fear memory: Dependence upon training intensity. Neurobiol Learn Mem 89 (2008) 178-184
55. Cai W.H., Blundell J., Han J., Greene R.W., and Powell C.M. Postreactivation glucocorticoids impair recall of established fear memory. J Neurosci 26 (2006) 9560-9566
56. Yang Y.L., Chao P.K., and Lu K.T. Systemic and intra-amygdala administration of glucocorticoid agonist and antagonist modulate extinction of conditioned fear. Neuropsychopharmacology 31 (2006) 912-924
57. Barrett D., and Gonzalez-Lima F. Behavioral effects of metyrapone on Pavlovian extinction. Neurosci Lett 371 (2004) 91-96
58. Donley M.P., Schulkin J., and Rosen J.B. Glucocorticoid receptor antagonism in the basolateral amygdala and ventral hippocampus interferes with long-term memory of contextual fear. Behav Brain Res 164 (2005) 197-205
59. Roozendaal B., Okuda S., de Quervain D.J., and McGaugh J.L. Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 138 (2006) 901-910
60. Yang Y.L., Chao P.K., Ro L.S., Wo Y.Y., and Lu K.T. Glutamate NMDA receptors within the amygdala participate in the modulatory effect of glucocorticoids on extinction of conditioned fear in rats. Neuropsychopharmacology 32 (2007) 1042-1051
61. de Quervain D.J., and Margraf J. Glucocorticoids for the treatment of post-traumatic stress disorder and phobias: A novel therapeutic approach. Eur J Pharmacol 583 (2008) 365-371
62. Debiec J., Doyere V., Nader K., and Ledoux J.E. Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala. Proc Natl Acad Sci U S A 103 (2006) 3428-3433
63. Campfield K.M., and Hills A.M. Effect of timing of critical incident stress debriefing (CISD) on posttraumatic symptoms. J Trauma Stress 14 (2001) 327-340
64. Everly Jr. G.S., and Mitchell J.T. The debriefing "controversy" and crisis intervention: A review of lexical and substantive issues. Int J Emerg Ment Health 2 (2000) 211-225
65. Maren S., and Chang C.H. Recent fear is resistant to extinction. Proc Natl Acad Sci U S A 103 (2006) 18020-18025
66. Roozendaal B. Stress and memory: Opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol Learn Mem 78 (2002) 578-595
67. Sandi C., and Rose S.P. Corticosteroid receptor antagonists are amnestic for passive avoidance learning in day-old chicks. Eur J Neurosci 6 (1994) 1292-1297
68. Cordero M.I., Merino J.J., and Sandi C. Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. Behav Neurosci 112 (1998) 885-891
69. Roozendaal B., and McGaugh J.L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol Learn Mem 65 (1996) 1-8
70. Sandi C., Loscertales M., and Guaza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur J Neurosci 9 (1997) 637-642
71. Suzuki A., Josselyn S.A., Frankland P.W., Masushige S., Silva A.J., and Kida S. Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24 (2004) 4787-4795
72. Boccia M.M., Blake M.G., Acosta G.B., and Baratti C.M. Post-retrieval effects of icv infusions of hemicholinium in mice are dependent on the age of the original memory. Learn Mem 13 (2006) 376-381
73. Eisenberg M., and Dudai Y. Reconsolidation of fresh, remote, and extinguished fear memory in Medaka: Old fears don't die. Eur J Neurosci 20 (2004) 3397-3403
74. Frankland P.W., Ding H.K., Takahashi E., Suzuki A., Kida S., and Silva A.J. Stability of recent and remote contextual fear memory. Learn Mem 13 (2006) 451-457
75. Kemenes G., Kemenes I., Michel M., Papp A., and Muller U. Phase-dependent molecular requirements for memory reconsolidation: Differential roles for protein synthesis and protein kinase A activity. J Neurosci 26 (2006) 6298-6302
76. Litvin O.O., and Anokhin K.V. Mechanisms of memory reorganization during retrieval of acquired behavioral experience in chicks: The effects of protein synthesis inhibition in the brain. Neurosci Behav Physiol 30 (2000) 671-678