Disrupting reconsolidation of fear memory in humans by a noradrenergic β-blocker

Journal of Visualized Experiments

Volumn , Issue 94, 2014, Pages

  Kindt, Merel ^a   Soeter, Marieke ^a   Sevenster, Dieuwke ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Behavior; Fear memory; Human fear conditioning; Issue 94; Noradrenergic blocker; Reconsolidation; Startle potentiation; Translational research

Indexed keywords

EID: 84921683803     PISSN: 1940087X     EISSN: None     Source Type: Journal    
DOI: 10.3791/52151     Document Type: Article

References (65)

1. LeDoux, J. E. The Emotional Brain. Simon & Schuster New York (1996).
2. Rescorla, R. A., Holland, P. C. Behavioral studies of associative learning in animals. Ann. Rev. Psychol.33, 265-308 (1982).
3. LeDoux, J. E. Coming to terms with fear. PNAS. 111, (8), 2871-2878 (2014).
4. Kandel, E. R. The biology of memory: a forty-year perspective. J. Neurosci. 29, (41), 12748-12756 (2009).
5. Mineka, S., Zinbarg, R. A contemporary learning theory perspective on the etiology of anxiety disorders: It's not what you thought it was. Am. Psychol. 6, (1), 10-26 (2006).
6. Rachman, S. The conditioning theory of fear acquisition: a critical examination. Beh. Res. Ther. 15, (5), 375-387 (1977).
7. Bouton, M. E., Bolles, C. R. Contextual control of the extinction of conditioned fear. Learn. Mot. 10, (4), 455-466 (1979).
8. Rescorla, R. A. Experimental Extinction. Lawrence Erlbaum Associates Publishers Mahwah, NJ (2001).
9. Rescorla, R. A., Heth, C. D. Reinstatement of fear to an extinguished conditioned context. J. Exp. Psychol.1, (1), 88-98 (1975).
10. Baum, M. Spontaneous recovery from the effects of flooding in animals. Beh. Res. Ther. 26, (2), 185-186 (1988).
11. Bouton, M. E. Context, time, and memory retrieval in the interference paradigm of Pavlovian learning.Psychol. Bull. 114, (1), 80-99 (1993).
12. LeDoux, J. E. Emotion: Clues from the brain. Ann. Rev. Psychol. 46, 209-235 (1995).
13. Bouton, M. E. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol. Psych. 52, (10), 976-986 (2002).
14. Nader, K., Schafe, G. E., LeDoux, J. E. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature. 406, (6797), 722-726 (2000).
15. Sara, S. J. Retrieval and reconsolidation: toward a neurobiology of remembering. Learn. Mem. 7, (2), 73-84 (2000).
16. Dudai, Y. The neurobiology of consolidation, Or, How stable is the engram?. Ann. Rev. Psychol. 55, 51-86 (2004).
17. Tronson, N. C., Taylor, J. R. Molecular mechanisms of memory reconsolidation. Nat. Rev. 8, (4), 262-275 (2007).
18. Lee, J. L. C. Reconsolidation: maintaining memory relevance. Trends. Neurosci. 32, (8), 413-420 (2009).
19. Debiec, J., Doyere, V., Nader, K., LeDoux, J. E. Directly reactivated, but not indirectly reactivated, memories undergo reconsolidation in the amygdala. PNAS. 130, (9), 3428-3433 (2006).
20. Doyere, V., Debiec, J., Monfils, M. -H., Schafe, G. E., LeDoux, J. E. Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala. Nat. Neurosci. 10, (4), 414-416 (2007).
21. Canal, C. E., Chang, Q., Gold, P. E. Amnesia produced by altered release of neurotransmitters after intra-amygdala injections of a protein synthesis inhibitor. PNAS. 104, (30), 12500-12505 (2007).
22. Qi, Z., Gold, P. E. Intrahippocampal infusions of anisomycin produce amnesia: Contribution of increased release of norepinephrine, dopamine. 16, (5), 308-314 (2009).
23. Jockers, R., et al. Desensitization of the beta-adrenergic response in human brown adipocytes.Endocrinology. 139, (6), 2676-2684 (1998).
24. Chaundhry, A., Granneman, J. G. Differential regulation of function responses by beta-adrenergic receptor subtypes in brown adipocytes. Am. J. Physiol. 227, (1 Pt 2), 137-153 (1999).
25. Thonberg, H., Frederiksson, J. M., Nedergaard, J., Cannon, B. A novel pathway for adrenergic stimulation of camp-response-element-binding protein (CREB) phosphorylation: mediation via alpha-adrenoceptors and protein kinase C activation. Biochem. J. 264, (1), 73-79 (2002).
26. Debiec, J., LeDoux, J. E. Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience. 129, (2), 267-272 (2004).
27. Kindt, M., Soeter, M., Vervliet, B. Beyond extinction: erasing human fear responding and preventing the return of fear. Nat. Neurosci. 12, (3), 256-258 (2009).
28. Soeter, M., Kindt, M. Dissociating response systems: erasing fear from memory. Neurobiol. Learn. Mem.94, (1), 30-41 (2010).
29. Soeter, M., Kindt, M. Disrupting reconsolidation: pharmacological and behavioral manipulations. Learn. Mem. 18, (6), 357-366 (2011).
30. Soeter, M., Kindt, M. Stimulation of the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation. Neuropsychopharmacology. 37, (5), 1204-1215 (2012).
31. Sevenster, D., Beckers, T., Kindt, M. Retrieval per se is not sufficient to trigger reconsolidation of human fear memory. Neurobiol. Learn. Mem. 97, (3), 338-345 (2012).
32. Sevenster, D., Beckers, T., Kindt, M. Prediction error governs pharmacologically induced amnesia for learned fear. Science. 339, (6121), 830-833 (2013).
33. Gilman, A. G., Goodman, L. S. Goodman and Gilman's the pharmacological basis of therapeutics. McGraw-Hill New York (1996).
34. Hamm, A. O., Weike, A. I. The neuropsychology of fear learning and fear regulation. Int. J. Psychophysiol.57, (1), 5-14 (2005).
35. Davis, M. Neural systems involved in fear and anxiety measured with fear potentiated startle. Am. Psychol.61, (8), 741-756 (2006).
36. Landis, C., Hunt, W. A. The startle pattern. Ferrar New York (1939).
37. Soeter, M., Kindt, M. Erasing fear for an imagined threat event. Psychoneuroendocrinology. 37, (11), 1769-1779 (2012).
38. Soeter, M., Kindt, M. Reconsolidation of associative fear memory is not restricted to exact replica of the original learning experience. In Press, Forthcoming.
39. Sevenster, D., Beckers, T., Kindt, M. Prediction error uncovers the transition from retrieval to reconsolidation, to new learning. In Press, Forthcoming.
40. Bos, M. G. N., Beckers, T., Kindt, M. The effects of noradrenergic blockade on extinction in humans. Biol. Psychol. 89, (3), 598-605 (2012).
41. Eisenberg, M., Kobilo, T., Berman, D. E., Dudai, Y. Stability of retrieved memory: inverse correlation with trace dominance. Science. 301, (5636), 1102-1104 (2003).
42. Pedreira, M. E., Perez-Cuesta, K. M., Maldonado, H. Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction. Learn. Mem. 11, (5), 579-585 (2004).
43. Forcato, C., Argibay, P. F., Pedreira, M. E., Maldonado, H. Human reconsolidation does not always occur when a memory is retrieved: the relevance of the reminder structure. Neurobiol. Learn. Mem. 91, (1), 50-57 (2009).
44. Spielberger, C. D., Gorsuch, R. L., Luthene, R. E. Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press Palo Alto (1970).
45. Peterson, R. A., Reiss, S. Anxiety Sensitivity Index Manual. International Diagnostic System. Worthington. (1992).
46. Klorman, R., Weerts, T. C., Hastings, J. E., Melamed, G. B. G., Lang, P. J. Psychometric description of some specific fear quistionnaires. Behav. Ther. 5, (3), 401-409 (1974).
47. Soeter, M., Kindt, M. High trait anxiety: a challenge for disrupting fear memory reconsolidation. PloSONE.8, (11), e75239(2013).
48. Well, S. M., Visser, R. M., Scholte, H. S., Kindt, M. Neural substrates of individual differences in human fear learning: evidence from concurrent fMRI, fear-potentiated startle and US-expectancy data. Cog. Affec. Beh. Neurosci. 12, (3), 499-512 (2012).
49. Lipp, O. V., Sheridan, J., Siddle, D. A. T. Human blink startle during aversive and nonaversive Pavlovian conditioning. J. Exp. Psychol. 20, (4), 380-389 (1994).
50. Hamm, A. O., Vaitl, D. Affective learning: awareness and aversion. Psychophysiology. 33, (6), 698-710 (1996).
51. Schiller, D., et al. Preventing the return of fear in humans using reconsolidation update mechanisms.Nature. 463, (7277), 49-53 (2012).
52. Kindt, M., Soeter, M. Reconsolidation in a human fear conditioning study: a test of extinction as updating mechanism. Biol. Psychol. 92, (1), 43-50 (2013).
53. Golkar, A., et al. Are fear memories erasable? - Reconsolidation of learned fear with fear-relevant and fear-irrelevant stimuli. Front. Behav. Neurosci. 6, 1-11 (2012).
54. Chan, W. Y. M., Leung, H. T., Westbrook, F., McNally, G. P. Effects of recent exposure to a conditionied stimulus on extinction of Pavlovian fear conditioning. Learn. Mem. 17, (10), 512-521 (2010).
55. Agren, T., Furmakr, T., Eriksson, E., Redrikson, M. Human fear reconsolidation and ellelic differences in serotonergic and dopaminergic genes. Trans. Psych. 2, e76(2012).
56. Oyarzun, J. P., et al. Updating Fearful Memories with Extinction Training during Reconsolidation: A Human Study using Auditory Aversive Stimuli. PloSONE. 7, (6), e38849(2012).
57. Minnen, A., Hagenaars, M. Fear activation and habituation patterns as early process predictors of response to prolonged exposure treatment in PTSD. J. Traum. Stress. 15, (5), 359-367 (2002).
58. Balderas, I., Rodriguez-Ortiz, C. J., Bermudez-Rattoni, F. Retrieval and reconsolidation of object recognition memory are independent processes in the periphinal cortex. Neurosci. 253, 398-405 (2013).
59. Ben Mamou, C., Gamache, K., Nader, K. NMDA receptors are critical for unleashing consolidated auditory fear memories. Nat. Neurosci. 9, (10), 1237-1239 (2006).
60. Caffaro, P. A., Suarez, L. D., Blake, M. G., Delorenzi, A. Dissociation between memory reactivation and its behavioral expression: scopolamine interferes with memory expression without disrupting long-term storage. Neurobiol. Learn. Mem. 98, (3), 235-245 (2012).
61. Coccoz, V., Maldonado, H., Delorenzi, A. The enhancement of reconsolidation with a naturalistic mild stressor improves the expression of declarative memory in humans. Neurosci. 185, 61-72 (2011).
62. Rodriguez-Ortiz, C. J., Balderas, I., Garcia-DeLaTorre, P., Bermudez-Rattoni, F. Taste aversion memory reconsolidation is independent of its retrieval. Neurobiol. Learn. Mem. 98, (3), 215-219 (2012).
63. Barreiro, K. A., Suarez, L. D., Lynch, V. M., Molina, V. A., Delorenzi, A. Memory expression is independent of memory labilization-reconsolidation. Neurobiol. Learn. Mem. 106, 283-291 (2013).
64. Milton, A. L., Merlo, E., Ratano, P., Gregory, B. L., Dumbreck, J. K., Everitt, B. J. Double dissociation of the requirement for GluN2B and GluN2A-containing NMDA receptors in the destabilization and restabilization of a reconsolidation memory. J. Neurosci. 33, (3), 1109-1115 (2013).
65. Merlo, E., Milton, A. L., Goozee, Z. Y., Theobald, D. E., Everitt, B. J. Reconsolidation and extinction are dissociable and mutually exclusive processes: behavioral and molecular evidence. J. Neurosci. 34, (7), 2422-2431 (2014).