Multimodal Assessment of Long-Term Memory Recall and Reinstatement in a Combined Cue and Context Fear Conditioning and Extinction Paradigm in Humans

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Haaker, Jan ^a   Lonsdorf, Tina B ^a   Thanellou, Alexandra ^a   Kalisch, Raffael ^a,b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; AROUSAL; ARTICLE; ASSOCIATION; CONDITIONING; DEPENDENT VARIABLE; ELECTRODERMAL RESPONSE; EMOTION; FEAR; FEMALE; HUMAN; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; PSYCHOPHYSIOLOGY; QUALITATIVE ANALYSIS; RATING SCALE; RECALL; REINSTATEMENT; SKIN CONDUCTANCE;

ADULT; AROUSAL; ASSOCIATION LEARNING; CONDITIONING, CLASSICAL; CUES; EXTINCTION, PSYCHOLOGICAL; FEAR; GALVANIC SKIN RESPONSE; HUMANS; MEMORY, LONG-TERM; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; STARTLE REACTION;

EID: 84885083703     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076179     Document Type: Article

References (58)

1. Davis M, Walker DL, Miles L, Grillon C, (2010) Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 35: 105-135 doi:10.1038/npp.2009.109.
2. Grillon C, Baas JMP, Cornwell B, Johnson L, (2006) Context conditioning and behavioral avoidance in a virtual reality environment: effect of predictability. Biol Psychiatry 60: 752-759 doi:10.1016/j.biopsych.2006.03.072.
3. Rachman S, (1989) The return of fear: Review and prospect. Clinical Psychology Review 9: 147-168 doi:10.1016/0272-7358(89)90025-1.
4. Lommen MJJ, Engelhard IM, Sijbrandij M, van den Hout MA, Hermans D, (2013) Pre-trauma individual differences in extinction learning predict posttraumatic stress. Behav Res Ther 51: 63-67 doi:10.1016/j.brat.2012.11.004.
5. Bouton ME, (2004) Context and behavioral processes in extinction. LearnMem 11: 485-494.
6. Myers KM, Davis M, (2007) Mechanisms of fear extinction. Mol Psychiatry 12: 120-150 doi:10.1038/sj.mp.4001939.
7. Craske MG, Kircanski K, Zelikowsky M, Mystkowski J, Chowdhury N, et al. (2008) Optimizing inhibitory learning during exposure therapy. Behaviour Research and Therapy 46: 5-27 doi:10.1016/j.brat.2007.10.003.
8. Bouton ME, Bolles RC, (1979) Contextual control of the extinction of conditioned fear. Learning and Motivation 10: 445-466 doi:10.1016/0023-9690(79)90057-2.
9. Rescorla RA, (2004) Spontaneous recovery. Learn Mem 11: 501-509 doi:10.1101/lm.77504.
10. Bouton ME, Bolles RC, (1979) Role of conditioned contextual stimuli in reinstatement of extinguished fear. J Exp Psychol Anim Behav Process 5: 368-378.
11. Rescorla RA, Heth CD, (1975) Reinstatement of fear to an extinguished conditioned stimulus. J Exp Psychol Anim Behav Process 1: 88-96.
12. Harris JA, Jones ML, Bailey GK, Westbrook RF, (2000) Contextual control over conditioned responding in an extinction paradigm. J Exp Psychol Anim Behav Process 26: 174-185.
13. Frohardt RJ, Guarraci FA, Bouton ME, (2000) The effects of neurotoxic hippocampal lesions on two effects of context after fear extinction. Behav Neurosci 114: 227-240 doi:10.1037/0735-7044.114.2.227.
14. Morris RW, Westbrook RF, Killcross AS, (2005) Reinstatement of extinguished fear by beta-adrenergic arousal elicited by a conditioned context. Behav Neurosci 119: 1662-1671 doi:10.1037/0735-7044.119.6.1662.
15. Westbrook RF, Iordanova M, McNally G, Richardson R, Harris JA, (2002) Reinstatement of fear to an extinguished conditioned stimulus: two roles for context. J Exp Psychol Anim Behav Process 28: 97-110.
16. Laurent V, Westbrook RF, (2010) Role of the basolateral amygdala in the reinstatement and extinction of fear responses to a previously extinguished conditioned stimulus. Learn Mem 17: 86-96 doi:10.1101/lm.1655010.
17. Dirikx T, Beckers T, Muyls C, Eelen P, Vansteenwegen D, et al. (2007) Differential acquisition, extinction, and reinstatement of conditioned suppression in mice. Q J Exp Psychol (Hove) 60: 1313-1320 doi:10.1080/17470210701515785.
18. LaBar KS, Phelps EA, (2005) Reinstatement of conditioned fear in humans is context dependent and impaired in amnesia. Behav Neurosci 119: 677-686 doi:10.1037/0735-7044.119.3.677.
19. Schiller D, Cain CK, Curley NG, Schwartz JS, Stern SA, et al. (2008) Evidence for recovery of fear following immediate extinction in rats and humans. Learn Mem 15: 394-402 doi:10.1101/lm.909208.
20. Hermans D, Dirikx T, Vansteenwegen D, Vansteenwegenin D, Baeyens F, et al. (2005) Reinstatement of fear responses in human aversive conditioning. Behav Res Ther 43: 533-551 doi:10.1016/j.brat.2004.03.013.
21. Norrholm SD, Jovanovic T, Vervliet B, Myers KM, Davis M, et al. (2006) Conditioned fear extinction and reinstatement in a human fear-potentiated startle paradigm. Learn Mem 13: 681-685 doi:10.1101/lm.393906.
22. Dirikx T, Hermans D, Vansteenwegen D, Baeyens F, Eelen P, (2007) Reinstatement of conditioned responses in human differential fear conditioning. J Behav Ther Exp Psychiatry 38: 237-251 doi:10.1016/j.jbtep.2006.04.001.
23. Milad MR, Orr SP, Pitman RK, Rauch SL, (2005) Context modulation of memory for fear extinction in humans. Psychophysiology 42: 456-464 doi:10.1111/j.1469-8986.2005.00302.x.
24. Golkar A, Öhman A, (2012) Fear extinction in humans: effects of acquisition-extinction delay and masked stimulus presentations. Biol Psychol 91: 292-301 doi:10.1016/j.biopsycho.2012.07.007.
25. Dirikx T, Vansteenwegen D, Eelen P, Hermans D, (2009) Non-differential return of fear in humans after a reinstatement procedure. Acta Psychol (Amst) 130: 175-182 doi:10.1016/j.actpsy.2008.12.002.
26. Kull S, Müller BH, Blechert J, Wilhelm FH, Michael T, (2012) Reinstatement of fear in humans: autonomic and experiential responses in a differential conditioning paradigm. Acta Psychol (Amst) 140: 43-49 doi:10.1016/j.actpsy.2012.02.007.
27. Lissek S, Powers A, McClure E, Phelps E, Woldehawariat G, et al. (2005) Classical fear conditioning in the anxiety disorders: a meta-analysis. BEHAVIOUR RESEARCH AND THERAPY 43: 1391-1424 doi:10.1016/j.brat.2004.10.007.
28. Craske MG, Wolitzky-Taylor KB, Mineka S, Zinbarg R, Waters AM, et al. (2012) Elevated responding to safe conditions as a specific risk factor for anxiety versus depressive disorders: evidence from a longitudinal investigation. J Abnorm Psychol 121: 315-324 doi:10.1037/a0025738.
29. Sokol N, Lovibond PF, (2012) Cross-US reinstatement of human conditioned fear: return of old fears or emergence of new ones? Behav Res Ther 50: 313-322 doi:10.1016/j.brat.2012.02.005.
30. Dirikx T, Hermans D, Vansteenwegen D, Baeyens F, Eelen P, (2004) Reinstatement of extinguished conditioned responses and negative stimulus valence as a pathway to return of fear in humans. Learn Mem 11: 549-554 doi:10.1101/lm.78004.
31. Huff NC, Hernandez JA, Blanding NQ, LaBar KS, (2009) Delayed Extinction Attenuates Conditioned Fear Renewal and Spontaneous Recovery in Humans. Behav Neurosci 123: 834-843 doi:10.1037/a0016511.
32. Marschner A, Kalisch R, Vervliet B, Vansteenwegen D, Büchel C, (2008) Dissociable Roles for the Hippocampus and the Amygdala in Human Cued versus Context Fear Conditioning. The Journal of Neuroscience 28: 9030-9036 doi:10.1523/JNEUROSCI.1651-08.2008.
33. Schmitz A, Grillon C, (2012) Assessing fear and anxiety in humans using the threat of predictable and unpredictable aversive events (the NPU-threat test). Nat Protocols 7: 527-532 doi:10.1038/nprot.2012.001.
34. Fanselow MS, (1980) Signaled shock-free periods and preference for signaled shock. Journal of Experimental Psychology: Animal Behavior Processes 6: 65-80 doi:10.1037/0097-7403.6.1.65.
35. Grillon C, Baas JP, Lissek S, Smith K, Milstein J, (2004) Anxious responses to predictable and unpredictable aversive events. Behav Neurosci 118: 916-924 doi:10.1037/0735-7044.118.5.916.
36. Davis M, Walker DL, Miles L, Grillon C, (2010) Phasic vs Sustained Fear in Rats and Humans: Role of the Extended Amygdala in Fear vs Anxiety. Neuropsychopharmacology 35: 105-135 doi:10.1038/npp.2009.109.
37. Fonteyne R, Vervliet B, Hermans D, Baeyens F, Vansteenwegen D, (2009) Reducing chronic anxiety by making the threatening event predictable: an experimental approach. Behav Res Ther 47: 830-839 doi:10.1016/j.brat.2009.06.011.
38. Fonteyne R, Vervliet B, Hermans D, Baeyens F, Vansteenwegen D, (2010) Exposure to the context and removing the unpredictability of the US: two methods to reduce contextual anxiety compared. Biol Psychol 85: 361-369 doi:10.1016/j.biopsycho.2010.08.007.
39. Vansteenwegen D, Iberico C, Vervliet B, Marescau V, Hermans D, (2008) Contextual fear induced by unpredictability in a human fear conditioning preparation is related to the chronic expectation of a threatening US. Biol Psychol 77: 39-46 doi:10.1016/j.biopsycho.2007.08.012.
40. Spielberger CD, (1985) Assessment of state and trait anxiety: conceptual and methodological issues. Southern Psychologist 2: 6-16.
41. Laux L, Glanzmann P, Schaffner P, Spielberger CD (1981) Das State-Trait-Angstinventar [State-Trait Anxiety Inventory-Manual of the German version]. Weinheim, Germany: Beltz Publishers.
42. Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, et al. (1995) Double Dissociation of Conditioning and Declarative Knowledge Relative to the Amygdala and Hippocampus in Humans. Science 269: 1115-1118.
43. Fowles DC, Christie MJ, Edelberg R, Grings WW, Lykken DT, et al. (1981) Publication Recommendations for Electrodermal Measurements. Psychophysiology 18: 232-239 doi:-10.1111/j.1469-8986.1981.tb03024.x.
44. Venables PH, Christie MJ (1980) Electrodermal activity. Techniques in psychophysiology. Chichester, UK: Wiley.
45. Lykken DT, Venables PH, (1971) Direct Measurement of Skin Conductance: A Proposal for Standardization. Psychophysiology 8: 656-672 doi:10.1111/j.1469-8986.1971.tb00501.x.
46. Weike AI, Schupp HT, Hamm AO, (2007) Fear acquisition requires awareness in trace but not delay conditioning. Psychophysiology 44: 170-180 doi:10.1111/j.1469-8986.2006.00469.x.
47. Lonsdorf T, Weike A, Nikamo P, Schalling M, Hamm A, et al. (2009) Genetic Gating of Human Fear Learning and Extinction: Possible Implications for Gene-Environment Interaction in Anxiety Disorder. PSYCHOLOGICAL SCIENCE 20: 198-206 doi:10.1111/j.1467-9280.2009.02280.x.
48. Lebron-Milad K, Milad MR, (2012) Sex differences, gonadal hormones and the fear extinction network: implications for anxiety disorders. Biol Mood Anxiety Disord 2: 3 doi:10.1186/2045-5380-2-3.
49. Milad MR, Goldstein JM, Orr SP, Wedig MM, Klibanski A, et al. (2006) Fear conditioning and extinction: influence of sex and menstrual cycle in healthy humans. Behav Neurosci 120: 1196-1203 doi:10.1037/0735-7044.120.5.1196.
50. Merz CJ, Tabbert K, Schweckendiek J, Klucken T, Vaitl D, et al. (2010) Investigating the impact of sex and cortisol on implicit fear conditioning with fMRI. Psychoneuroendocrinology 35: 33-46 doi:10.1016/j.psyneuen.2009.07.009.
51. Corcoran KA, Maren S, (2001) Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J Neurosci 21: 1720-1726.
52. Quirk GJ, (2002) Memory for extinction of conditioned fear is long-lasting and persists following spontaneous recovery. Learn Mem 9: 402-407 doi:10.1101/lm.49602.
53. Vervliet B, Baeyens F, Van den Bergh O, Hermans D, (2013) Extinction, generalization, and return of fear: a critical review of renewal research in humans. Biol Psychol 92: 51-58 doi:10.1016/j.biopsycho.2012.01.006.
54. Norrholm SD, Vervliet B, Jovanovic T, Boshoven W, Myers KM, et al. (2008) Timing of extinction relative to acquisition: a parametric analysis of fear extinction in humans. Behav Neurosci 122: 1016-1030 doi:10.1037/a0012604.
55. Kalisch R, Korenfeld E, Stephan KE, Weiskopf N, Seymour B, et al. (2006) Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J Neurosci 26: 9503-9511 doi:10.1523/JNEUROSCI.2021-06.2006.
56. Milad MR, Wright CI, Orr SP, Pitman RK, Quirk GJ, et al. (2007) Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiatry 62: 446-454.
57. Maren S, Phan KL, Liberzon I, (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14: 417-428 doi:10.1038/nrn3492.
58. Lin H-C, Tseng Y-C, Mao S-C, Chen P-S, Gean P-W, (2011) GABAA receptor endocytosis in the basolateral amygdala is critical to the reinstatement of fear memory measured by fear-potentiated startle. J Neurosci 31: 8851-8861 doi:10.1523/JNEUROSCI.0979-11.2011.