Effects of postretrieval-extinction learning on return of contextually controlled cued fear

Behavioral Neuroscience

Volumn 128, Issue 4, 2014, Pages 474-481

  Drexler, Shira Meir ^a   Merz, Christian J ^a   Hamacher Dang, Tanja C ^a   Marquardt, Veronica ^a   Fritsch, Nathalie ^a   Otto, Tobias ^a   Wolf, Oliver T ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Extinction; Fear learning; Fear relevant; Reconsolidation; Skin conductance response (SCR)

Indexed keywords

ADULT; ARTICLE; ASSOCIATION; AVERSION; CONDITIONING; ELECTRIC SHOCK; ELECTRODERMAL RESPONSE; FEAR; FEMALE; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MEMORY CONSOLIDATION; NEUROMODULATION; NORMAL HUMAN; POSTRETRIEVAL EXTINCTION LEARNING; RECALL; REINFORCEMENT; STIMULUS RESPONSE; CONDITIONED REFLEX; ELECTROSTIMULATION; MEMORY; YOUNG ADULT;

ADULT; CONDITIONING, CLASSICAL; CUES; ELECTRIC STIMULATION; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; GALVANIC SKIN RESPONSE; HUMANS; MALE; MEMORY; YOUNG ADULT;

EID: 84904727694     PISSN: 07357044     EISSN: 19390084     Source Type: Journal    
DOI: 10.1037/a0036688     Document Type: Article

References (61)

1. Agren, T., Engman, J., Frick, A., Björkstrand, J., Larsson, E., Furmark, M., & Fredrikson, M. (2012). Disruption of reconsolidation erases a fear memory trace in the human amygdala. Science, 337, 1550-1552. doi: 10.1126/science.1223006
2. Alberini, C. M. (2005). Mechanisms of memory stabilization: Are consolidation and reconsolidation similar or distinct processes? Trends in Neurosciences, 28, 51-56. doi:10.1016/j.tins.2004.11.001
3. Alberini, C. M. (2008). The role of protein synthesis during the labile phases of memory: Revisiting the skepticism. Neurobiology of Learning and Memory, 89, 234-246. doi:10.1016/j.nlm.2007.08.007
4. Auber, A., Tedesco, V., Jones, C., Monfils, M., & Chiamulera, C. (2013). Post-retrieval extinction as reconsolidation interference? Methodological issues or boundary conditions? Psychopharmacology, 226, 631-647. doi:10.1007/s00213-013-3004-1
5. Baas, J. M. (2013). Individual differences in predicting aversive events and modulating contextual anxiety in a context and cue conditioning paradigm. Biological Psychology, 92, 17-25. doi:10.1016/j.biopsycho.2012 .02.001
6. Bouton, M. E. (2002). Context, ambiguity, and unlearning: Sources of relapse after behavioral extinction. Biological Psychiatry, 52, 976-986. doi:10.1016/S0006-3223(02)01546-9
7. Bouton, M. E., & King, D. (1983). Contextual control of the extinction of conditioned fear: Tests for the associative value of the context. Journal of Experimental Psychology: Animal Behavior Processes, 9, 248-265. doi:10.1037/0097-7403.9.3.248
8. Brunet, A., Orr, S. P., Tremblay, J., Robertson, K., Nader, K., & Pitman, R. K. (2008). Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in posttraumatic stress disorder. Journal of Psychiatric Research, 42, 503-506. doi:10.1016/j.jpsychires.2007.05.006
9. Cahill, L., Gorski, L., & Le, K. (2003). Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding. Learning & Memory, 10, 270-274. doi:10.1101/lm.62403
10. Cahill, L., Prins, B., Webe, M., & McGaugh, J. (1994). Beta-adrenergic activation and memory for emotional events. Nature, 371, 702-704. doi:10.1038/371702a0
11. Cai, W. H., Blundell, J., Han, J., Greene, R., & Powell, C. (2006). Postreactivation glucocorticoids impair recall of established fear memory. The Journal of Neuroscience, 26, 9560 -9566. doi:10.1523/ JNEUROSCI.2397-06.2006
12. Chan, W. Y., Leung, H., Westbrook, R., & McNally, G. (2010). Effects of recent exposure to a conditioned stimulus on extinction of Pavlovian fear conditioning. Learning & Memory, 17, 512-521. doi:10.1101/lm .1912510
13. Clem, R. L., & Huganir, R. L. (2010). Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science, 330, 1108-1112. doi: 10.1126/science.1195298
14. Craske, M. (1999). Anxiety disorders: Psychological approaches to theory and treatment. Boulder, CO: Westview Press.
15. Delgado, M. R., Olsson, A., & Phelps, E. (2006). Extending animal models of fear conditioning to humans. Biological Psychology, 73, 39-48. doi:10.1016/j.biopsycho.2006.01.006
16. Dudai, Y. (2004). The neurobiology of consolidations, or, how stable is the engram? Annual Review of Psychology, 55, 51-86. doi:10.1146/annurev .psych.55.090902.142050
17. Duvarci, S., & Nader, K. (2004). Characterization of fear memory reconsolidation. The Journal of Neuroscience, 24, 9269-9275. doi:10.1523/ JNEUROSCI.2971-04.2004
18. Forcato, C., Burgos, V., Argibay, P., Molina, V., Pedreira, M., & Maldonado, H. (2007). Reconsolidation of declerative memory in humans. Learning & Memory, 14, 295-303. doi:10.1101/lm.486107
19. Golkar, A., Bellander, M., Olsson, A., & Öhman, A. (2012). Are fear memories erasable? Reconsolidation of learned fear with fear-relevant and fear-irrelevant stimuli. Frontiers in Behavioral Neuroscience, 6, 80-89. doi:10.3389/fnbeh.2012.00080
20. Graham, B. M., & Milad, M. R. (2013). Blockade of estrogen by hormonal contraceptives impairs fear extinction in female rats and women. Biological Psychiatry, 73, 371-378. doi:10.1016/j.biopsych.2012.09.018
21. Grillon, C. (2002). Startle reactivity and anxiety disorders: Aversive conditioning, context and neurobiology. Biological Psychiatry, 52, 958- 975. doi:10.1016/S0006-3223(02)01665-7
22. Hamacher-Dang, T., Ungör, M., & Wolf, O. T. (2013). Stress impairs retrieval of extinguished and unextinguished associations in a predictive learning task. Neurobiology of Learning and Memory, 104, 1-8. doi: 10.1016/j.nlm.2013.04.007
23. Hamm, A., Vaitl, D., & Lang, P. (1989). Fear conditioning, meaning and belongingness: A selective association analysis. Journal of Abnormal Psychology, 98, 395-406. doi:10.1037/0021-843X.98.4.395
24. Hupbach, A., Gomez, L., Hardt, O., & Nadel, R. (2007). Reconsolidation of episodic memories: A subtle reminder triggers integration of new information. Learning & Memory, 14, 47-53. doi:10.1101/lm.365707
25. Kessler, R., Berglund, P., Demler, O., Jin, R., Merikangas, K., & Walters, E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry, 62, 593-602. doi:10.1001/archpsyc.62 .6.593
26. Kindt, M., & Soeter, M. (2013). Reconsolidation in a human fear conditioning study: A test of extinction as updating mechanism. Biological Psychology, 92, 43-50. doi:10.1016/j.biopsycho.2011.09.016
27. Kindt, M., Soeter, M., & Vervliet, B. (2009). Beyond extinction: Erasing human fear responses and preventing the return of fear. Nature Neuroscience, 12, 256-258. doi:10.1038/nn.2271
28. Knight, D. C., Nguyen, H. T., & Bandettini, P. A. (2003). Expression of conditional fear with and without awareness. Proceedings of the National Academy of Sciences of the United States of America, 100, 15280-15283. doi:10.1073/pnas.2535780100
29. Lang, P., Bradley, M., & Cuthbert, B. (2005). International affective picture system (IAPS): Affective ratings of pictures and instruction manual (Technical Report No. A-6). Gainesville, FL: University of Florida.
30. Lee, J., Everitt, B., & Thomas, K. (2004). Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science, 304, 839-843. doi:10.1126/science.1095760
31. Lewis, D. (1979). Psychobiology of active and inactive memory. Psychological Bulletin, 86, 1054-1083. doi:10.1037/0033-2909.86.5.1054
32. Merz, C., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R., & Wolf, O. T. (2012). Neuronal correlates of extinction learning are modulated by sex hormones. Social Cognitive and Affective Neuroscience, 7, 819-830. doi:10.1093/scan/nsr063
33. Milad, M., Igoe, S., Lebron-Milad, K., & Novales, J. (2009). Estrous cycle phase and gonadal hormones influence conditioned fear extinction. Neuroscience, 164, 887-895. doi:10.1016/j.neuroscience.2009.09.011
34. Milad, M. R., Orr, S. P., Pitman, R. K., & Rauch, S. L. (2005). Context modulation of memory for fear extinction in humans. Psychophysiology, 42, 456-464. doi:10.1111/j.1469-8986.2005.00302.x
35. Milad, M. R., Zeidan, M. A., Contero, A., Pitman, R. K., Klibanski, A., Rauch, S. L., & Goldstein, J. M. (2010). The influence of gonadal hormones on conditioned fear extinction in healthy humans. Neuroscience, 168, 652-658. doi:10.1016/j.neuroscience.2010.04.030
36. Monfils, M., Cowansage, K., Klann, E., & LeDoux, J. (2009). Extinctionreconsolidation boundaries: Key to persistent attenuation of fear memories. Science, 324, 951-955. doi:10.1126/science.1167975
37. Myers, K., & Davis, M. (2007). Mechanisms of fear extinction. Molecular Psychiatry, 12, pp.120 -150. doi:10.1038/sj.mp.4001939
38. Nader, K., Schafe, G., & LeDoux, J. (2000). Fear memories requires protein synthesis in the amygdala for reconsolidation after retrieval. Nature, 406, 722-726. doi:10.1038/35021052
39. Norrholm, S., Javanovic, T., Vervliet, B., Myers, K., Davis, M., Rothbaum, B., & Duncan, E. (2006). Conditioned fear extinction and reinstatement in a human fear potentiated startle paradigm. Learning & Memory, 13, 681-686. doi:10.1101/lm.393906
40. Oyarzún, J., Lopez-Barroso, D., Fuentemilla, L., Curcurell, D., Pedraza, C., Rodriguez-Fornells, A., & de Diego-Balaguer, R. (2012). Updating fearful memories with extinction training during reconsolidation: A human study using auditory aversive stimuli. PloS ONE, 7, e38849. doi:10.1371/journal.pone.0038849
41. Pedreira, M. (2004). Mismatch between what is expected and what actually occurs triggers memory reconsolidation or Extinction. Learning & Memory, 11, 579-585. doi:10.1101/lm.76904
42. Rao-Ruiz, P., Rotaru, D. C., van der Loo, R. J., Mansvelder, H. D., Stiedl, O., Smit, A. B., & Spijker, S. (2011). Retrieval-specific endocytosis ofGluA2-AMPARs underlies adaptive reconsolidation of contextual fear. Nature Neuroscience, 14, 1302-1308. doi:10.1038/nn.2907
43. Rescorla, R. (1988). Pavlovian conditioning. It's not what you think it is. American Psychologist, 43, 151-160. doi:10.1037/0003-066X.43.3.151
44. Rescorla, R. (2004). Spontaneous recovery. Learning & Memory, 11, 501-509. doi:10.1101/lm.77504
45. Rescorla, R., & Heth, C. (1975). Reinstatement of fear to an extinguished conditioned stimulus. Journal of Experimental Psychology: Animal Behavior Processes, 1, 88-96. doi:10.1037/0097-7403.1.1.88
46. Roozendaal, B. (2002). Stress and memory: Opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory, 78, 578-595. doi:10.1006/nlme.2002.4080
47. Schiller, D., Monfils, M., Raio, C., Johnson, D., Ledoux, J., & Phelps, E. (2010). Preventing the return of fear in humans using reconsolidation update mechanisms. Nature, 463, 49-53. doi:10.1038/nature08637
48. Schwabe, L., Nader, K., Wolf, O. T., Beaudry, T., & Pruessner, J. (2012). Neural signature of reconsolidation impairments by propranolol in humans. Biological Psychiatry, 71, 380-386. doi:10.1016/j.biopsych.2011 .10.028
49. Schwabe, L., & Wolf, O. T. (2009). New episodic learning interferes with the reconsolidation of autobiographical memories. PLoS ONE, 4, e7519. doi:10.1371/journal.pone.0007519
50. Sevenster, D., Beckers, T., & Kindt, M. (2012). Retrieval per se is not sufficient to trigger reconsolidation of human fear memory. Neurobiology of Learning and Memory, 97, 338-345. doi:10.1016/j.nlm.2012.01 .009
51. Soeter, M., & Kindt, M. (2010). Dissociating response systems: Erasing fear from memory. Neurobiology of Learning and Memory, 94, 30-41. doi:10.1016/j.nlm.2010.03.004
52. Soeter, M., & Kindt, M. (2011). Disrupting reconsolidation: Pharmacological and bahavioral manipulations. Learning & Memory, 18, 357-366. doi:10.1101/lm.2148511
53. Strange, B., & Dolan, R. (2004). Beta-adrenergic modulation of emotional memory-evoked human amaygdala and hippocampus responses. Proceedings of the National Academy of Sciences of the United States of America, 101, 11454-11458. doi:10.1073/pnas.0404282101
54. Strange, B., Kroes, M., Fan, J., & Dolan, R. (2010). Emotion causes targeted forgetting of established memories. Frontiers in Behavioral Neuroscience, 4, doi:10.3389/fnbeh.2010.00175
55. Tabbert, K., Merz, C. J., Klucken, T., Schweckendiek, J., Vaitl, D., Wolf, O. T., & Stark, R. (2011). Influence of contingency awareness on neural, electrodermal and evaluative responses during fear conditioning. Social Cognitive and Affective Neuroscience, 6, 495-506. doi:10.1093/scan/ nsq070
56. Taubenfeld, S. M., Milekic, M., Monti, B., & Alberini, C. (2001). The consolidation of new but not reactivated memories requires hippocampal C/EBPb. Nature Neuroscience, 4, pp. 813-818. doi:10.1038/90520
57. Ungör, M., & Lachnit, H. (2006). Contextual control in discrimination reversal learning. Journal of Experimental Psychology: Animal Behavior Processes, 32, 441-453. doi:10.1037/0097-7403.32.4.441
58. Ungör, M., & Lachnit, H. (2008). Dissociations among ABA, ABC, and AAB recovery effects. Learning and Motivation, 39, pp. 181-195. doi:10.1016/j.lmot.2007.08.001
59. Walker, M., Brakefield, T., Hobson, J., & Stickgold, R. (2003). Dissociable stages of human memory consolidation and reconsolidation. Nature, 425, 616-620. doi:10.1038/nature01930
60. Wichert, S., Wolf, O. T., & Schwabe, L. (2011). Reactivation, interference, and reconsolidation: Are recent and remote memories likewise susceptible? Behavioral Neuroscience, 125, 699-704. doi:10.1037/a0025235
61. Zeidan, M. A., Igoe, S. A., Linnman, C., Vitalo, A., Levine, J. B., Klibanski, A., Milad, M. R. (2011). Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biological Psychiatry, 70, 920-927. doi:10.1016/j .biopsych.2011.05.016