Behavioral and central correlates of contextual fear learning and contextual modulation of cued fear in posttraumatic stress disorder

International Journal of Psychophysiology

Volumn 98, Issue 3, 2015, Pages 584-593

  Steiger, Frauke ^a   Nees, Frauke ^a   Wicking, Manon ^a   Lang, Simone ^a,b   Flor, Herta ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Context; Contingency; Cue; Extinction; Fear conditioning; FMRI; Posttraumatic stress disorder

Indexed keywords

ADULT; AROUSAL; ARTICLE; ASSOCIATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEAR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LEARNING; MALE; NEUROMODULATION; POSTTRAUMATIC STRESS DISORDER; RECALL; THREAT; ANALYSIS OF VARIANCE; BLOOD; COMPLICATION; CONDITIONED REFLEX; HIPPOCAMPUS; IMAGE PROCESSING; LEARNING DISORDERS; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGICAL RATING SCALE; PSYCHOLOGY; REINFORCEMENT; TIME FACTOR; VASCULARIZATION; YOUNG ADULT;

OXYGEN;

ADULT; ANALYSIS OF VARIANCE; AROUSAL; CONDITIONING, CLASSICAL; CUES; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LEARNING DISORDERS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; OXYGEN; PSYCHIATRIC STATUS RATING SCALES; STRESS DISORDERS, POST-TRAUMATIC; TIME FACTORS; YOUNG ADULT;

EID: 84943354345     PISSN: 01678760     EISSN: 18727697     Source Type: Journal    
DOI: 10.1016/j.ijpsycho.2015.06.009     Document Type: Article

References (83)

1. Acheson D.T., Gresack J.E., Risbrough V.B. Hippocampal dysfunction effects on context memory: possible etiology for posttraumatic stress disorder. Neuropharmacology 2012, 62:674-685.
2. Acheson D.T., Geyer M.A., Baker D.G., Nievergelt C.M., Yurgil K., Risbrough V.B., Team M.I. Conditioned fear and extinction learning performance and its association with psychiatric symptoms in active duty Marines. Psychoneuroendocrinology 2015, 51:495-505.
3. Alvarez R.P., Biggs A., Chen G., Pine D.S., Grillon C. Contextual fear conditioning in humans: cortical-hippocampal and amygdala contributions. J. Neurosci. 2008, 11:6211-6219.
4. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 2013, American Psychiatric Association, Alexandria, VA. Fifth Edition.
5. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, text rev. 2000, American Psychiatric Association, Alexandria, VA.
6. Baas J.M., Nugent M., Lissek S., Pine D.S., Grillon C. Fear conditioning in virtual reality contexts: a new tool for the study of anxiety. Biol. Psychiatry 2004, 55:1056-1060.
7. Blechert J., Michael T., Vriends N., Margraf J., Wilhelm F.H. Fear conditioning in posttraumatic stress disorder: evidence for delayed extinction of autonomic, experiential, and behavioural responses. Behav. Res. Ther. 2007, 45:2019-2033.
8. Bokde A.L., Karmann M., Born C., Teipel S.J., Omerovic M., Ewers M., Frodl T., Meisenzahl E., Reiser M., Möller H.J., Hampel H. Alzheimer disease: functional abnormalities in the dorsal visual pathway. J. Alzheimers Dis. 2010, 21:103-118.
9. Bouton M.E. Context, time and memory retrieval in the interference paradigms of Pavlovian learning. Psychol. Bull. 1993, 114:80-99.
10. Bouton M.E. Context, ambiguity, and classical conditioning. Curr. Dir. Psychol. Sci. 1994, 3:49-53.
11. Bouton M.E. Context and behavioral processes in extinction. Learning & Memory 2004, 11(5):485-494.
12. Bouton M.E., Nelson J.B. Context-specificity of target versus feature inhibition in a feature-negative discrimination. J. Exp. Psychol. Anim. Behav. Process. 1994, 20:51-65.
13. Bradley M.M., Lang P.J. Measuring emotion: the self-assessment manikin and the semantic differential. J. Behav. Ther. Exp. Psychiatry 1994, 25:49-59.
14. Bremner J.D., Randall P., Scott T.M., Bronen R.A., Seibyl J.P., Southwick S.M., Delaney R.C., McCarthy G., Charney D.S., Innis R.B. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am. J. Psychiatry 1995, 152:973-981.
15. Bremner J.D., Innis R.B., Ng C.K., Staib L., Duncan J., Bronen R., Zubal G., Rich D., Krystal J.H., Dey H., Soufer R., Charney D.S. PET measurement of cerebral metabolic correlates of yohimbine administration in posttraumatic stress disorder. Arch. Gen. Psychiatry 1997, 54:246-256.
16. Brohawn K.H., Offringa R., Pfaff D.L., Hughes K.C., Shin L.M. The neural correlates of emotional memory in posttraumatic stress disorder. Biol. Psychiatry 2010, 68:1023-1030.
17. Cacciaglia R., Pohlack S.T., Flor H., Nees F. Dissociable roles for hippocampal and amygdalar volume in human fear conditioning. Brain Struct. Funct. 2014, 1-12.
18. Corcoran K.A., Maren S. Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J. Neurosci. 2001, 21:1720-1726.
19. Etkin A., Wager T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder and specific phobia. Am. J. Psychiatry 2007, 164:1475-1488.
20. Fanselow M.S. From contextual fear to a dynamic view of memory systems. Altered brain activation during a verbal working memory task in subjects with amnestic mild cognitive impairment. Trends Cogn. Sci. 2010, 14:7-15.
21. Flor H., Nees F. Learning, memory and brain plasticity in posttraumatic stress disorder: context matters. Restor. Neurol. Neurosci. 2014, 32:95-102.
22. Flor H., Wessa M. Memory and posttraumatic stress disorder. A matter of context?. J. Psychol. 2010, 218:61-63.
23. Fonteyne R., Vervliet B., Hermans D., Baeyens F., Vansteenwegen D. Reducing chronic anxiety by making the threatening event predictable: an experimental approach. Behav. Res. Ther. 2009, 47:830-839.
24. Fydrich T., Renneberg B., Schmitz B., Wittchen H.-U. SKID-II. Strukturiertes Klinisches Interview für DSM-IV. Achse II: Persönlichkeitsstörungen. Interviewheft 1997, Hogrefe, Göttingen.
25. Garfinkel S.N., Abelson J.L., King A.P., Sripada R.K., Wang X., Gaines L.M., Liberzon I. Impaired contextual modulation of memories in PTSD: an fMRI and psychophysiological study of extinction retention and fear renewal, 2014. J. Neurosci. 2014, 34(40):13435-13443.
26. Gast U., Rodewald F., Nickel V., Emrich H.M. Prevalence of dissociative disorders among psychiatric inpatients in a German university clinic. J. Nerv. Ment. Dis. 2001, 89:249-257.
27. Gilbertson M.W., Shenton M.E., Ciszewski A., Kasai K., Lasko N.B., Orr S.P., Pitman R.K. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat. Neurosci. 2002, 5:1242-1247.
28. Gilbertson M.W., Williston S.K., Paulus L.A., Lasko N.B., Gurvits T.V., Shenton M.E., Pitman R.K., Orr S.P. Configural cue performance in identical twins discordant for posttraumatic stress disorder: theoretical implications for the role of hippocampal function. Biol. Psychiatry 2007, 62:513-520.
29. Grillon C., Davis M. Fear-potentiated startle conditioning in humans: explicit and contextual cue conditioning following paired vs. unpaired training. Psychophysiology 1997, 34:451-458.
30. Grillon C., Morgan C.A. Fear-potentiated startle conditioning to explicit and contextual cues in Gulf War veterans with posttraumatic stress disorder. J. Abnorm. Psychol. 1999, 108:134-142.
31. Grillon C., Morgan C.A., Davis M., Southwick S.M. Effects of experimental context and explicit threat cues on acoustic startle in Vietnam veterans with posttraumatic stress disorder. Biol. Psychiatry 1998, 44:1027-1036.
32. Grillon C., Baas J.M., Cornwell B., Johnson L. Context conditioning and behavioral avoidance in a virtual reality environment: effect of predictability. Biol. Psychiatry 2006, 60:752-759.
33. Guthrie R.M., Bryant R.A. Extinction learning before trauma and subsequent posttraumatic stress. Psychosomatic medicine 2006, 68(2):307-311.
34. Hasler G., Fromm S., Alvarez R.P., Luckenbaugh D.A., Drevets W.C., Grillon C. Cerebral blood flow in immediate and sustained anxiety. J. Neurosci. 2007, 27:6313-6319.
35. Hautzinger M., Bailer M. Allgemeine Depressionsskala (ADS). Die deutsche Version des CES-D [German version of the Center for Epidemiological Studies - Depression Scale] 1991, Beltz, Weinheim.
36. Holmes A., Singewald N. Individual differences in recovery from traumatic fear. Trends Neurosci. 2013, 36:23-31.
37. Hayes J.P., LaBar K.S., McCarthy G., Selgrade E., Nasser J., Dolcos F., Morey R.A. Reduced hippocampal and amygdala activity predicts memory distortions for trauma reminders in combat-related PTSD. Journal of psychiatric research 2011, 45(5):660-669.
38. Iordanova M.D., Burnett D.J., Aggleton J.P., Good M., Honey R.C. The role of the hippocampus in mnemonic integration and retrieval: complementary evidence from lesion and inactivation studies. Eur. J. Neurosci. 2009, 30:2177-2189.
39. Jovanovic T., Ressler K.J. How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am. J. Psychiatry 2010, 167:648-662.
40. Jovanovic T., Kazama A., Bachevalier J., Davis M. Impaired safety signal learning may be a biomarker of PTSD. Neuropharmacology 2012, 62:695-704.
41. Kalisch R., Korenfeld E., Stephan K.E., Weiskopf N., Seymour B., Dolan R.J. Context-dependent human extinction memory is mediated by a ventromedial prefrontal and hippocampal network. J. Neurosci. 2006, 26:9503-9511.
42. Karl A., Schaefer M., Malta L.S., Dorfel D., Rohleder N., Werner A. A meta-analysis of structural brain abnormalities in PTSD. J. Neurosci. 2006, 30:1004-1031.
43. Klucken T., Tabbert K., Schweckendiek J., Merz C.J., Kagerer S., Vaitl D., Stark R. Contingency learning in human fear conditioning involves the ventral striatum. Human brain mapping 2009, 30(11):3636-3644.
44. LaBar K.S., LeDoux J.E. Partial disruption of fear conditioning in rats with unilateral amygdala damage: correspondence with unilateral temporal lobectomy in humans. Behav. Neurosci. 1996, 991-997.
45. LaBar K.S., Gatenby J.C., Gore J.C., LeDoux J.E., Phelps E.A. Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 1998, 20:937-945.
46. Lang S., Kroll A., Lipinski S.J., Wessa M., Ridder S., Christmann C., Schad L.R., Flor H. Context conditioning and extinction in humans: differential contribution of the hippocampus, amygdala and prefrontal cortex. Eur. J. Neurosci. 2009, 29:823-832.
47. Lindauer R.J., Vlieger E.J., Jalink M., et al. Smaller hippocampal volume in Dutch police officers with posttraumatic stress disorder. Biol. Psychiatry 2004, 56:356-363.
48. Lissek S. Toward an account of clinical anxiety predicated on basic, neurally mapped mechanisms of Pavlovian fear-learning: the case for conditioned overgeneralization. Depress. Anxiety 2012, 29:257-263.
49. Lissek S., van Meurs B. Learning models of PTSD. Theoretical accounts and psychobiological evidence. Int. J. Psychophysiol. 2015, (in press).
50. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
51. Maren S., Phan K.L., Liberzon I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat. Rev. Neurosci. 2013, 14:417-428.
52. Marschner A., Kalisch R., Vervliet B., Vansteenwegen D., Büchel C. Dissociable roles for the hippocampus and the amygdala in human cued versus context fear conditioning. J. Neurosci. 2008, 28:9030-9036.
53. Milad M.R., Quinn B.T., Pitman R.K., Orr S.P., Fischl B., Rauch S.L. Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10706-10711.
54. Milad M.R., Wright C.I., Orr S.P., Pitman R.K., Quirk G.J., Rauch S.L. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol. Psychiatry 2007, 62:191-1914.
55. Milad M.R., Pitman R.K., Ellis C.B., Gold A.L., Shin L.M., Lasko N.B., Zeidan M.A., Handwerger K., Orr S.P., Rauch S.L. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol. Psychiatry 2009, 66:1075-1082.
56. Nielsen F.A., Hansen L.K. Modeling of activation data in the BrainMap database: detection of outliers. Hum. Brain Mapp. 2002, 15:146-156.
57. North C.S., Nixon S.J., Shariat S., Mallonee S., Mcmillen J.C., Spitznagel E.L., et al. Psychiatric disorders among survivors of the Oklahoma City bombing. JAMA 1999, 282:755-762.
58. North C.S., Oliver J., Pandya A. Examining a comprehensive model of disaster-related posttraumatic stress disorder in systematically studied survivors of 10 disasters. Am. J. Public Health 2012, 102:e40-e48.
59. O'Donovan A., Chao L.L., Paulson J., Samuelson K.W., Shigenaga J.K., Grunfeld C., Weiner M.W., Neylan T.C. Altered inflammatory activity associated with reduced hippocampal volume and more severe posttraumatic stress symptoms in Gulf War veterans. Psychoneuroendocrinology 2015, 51:557-566.
60. Orr S.P., Metzger L.J., Lasko N.B., Macklin M.L., Peri T., Pitman R.K. De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder. J. Abnorm. Psychol. 2000, 109:290-298.
61. Pavlisa G., Papa J., Pavic L., et al. Bilateral MR volumetry of the amygdala in chronic PTSD patients. Coll. Antropol. 2006, 30:565-568.
62. Peri T., Ben-Shakhar G., Orr S.P., Shalev A.Y. Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder. Biological psychiatry 2000, 47(6):512-519.
63. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48(2):175-187.
64. Pitman R.K., Orr S.P. Test of the conditioning model of neurosis: differential aversive conditioning of angry and neutral facial expressions in anxiety disorder patients. J. Abnorm. Psychol. 1986, 95:208-213.
65. Pohlack S.T., Nees F., Liebscher C., Cacciaglia R., Diener S.J., Ridder S., Woermann F.G., Flor H. Hippocampal but not amygdalar volume affects contextual fear conditioning in humans. Human brain mapping 2012, 33(2):478-488.
66. Rauch S.L., Shin L.M., Phelps E.A. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research: past, present, and future. Biol. Psychiatry 2006, 60:376-382.
67. Rougemont-Bucking A., Linnman C., Zeffiro T.A., Zeidan M.A., Lebron-Milad K., Rodriguez-Romaguera J., Rauch S.L., Pitman R.K., Milad M.R. Altered processing of contextual information during fear extinction in PTSD: an fMRI study. CNS Neurosci. Ther. 2011, 17:227-236.
68. Rudy J.W., Sutherland R.J. Configural association theory and the hippocampal formation: an appraisal and reconfiguration. Hippocampus 1995, 5:375-389.
69. Rudy J.W., Huff N.C., Matus-Amat P. Understanding contextual fear conditioning: insights from a two-process model. Neurosci. Biobehav. Rev. 2004, 7:675-685.
70. Schnyder U., Moergeli H. German version of clinician-administered PTSD scale. J. Trauma. Stress. 2002, 6:487-492.
71. Sehlmeyer C., Schoning S., Zwitserlood P., Pfleiderer B., Kircher T., Arolt V., et al. Human fear conditioning and extinction in neuroimaging: a systematic review. PLoS ONE 2009, 4:e5865.
72. Semple W.E., Goyer P.F., McCormick R., Donovan B., Muzic R.F., Rugle L., McCutcheon K., Lewis C., Liebling D., Kowaliw S., Vapenik K., Semple M.A., Flener C.R., Schulz S.C. Higher brain blood flow at amygdala and lower frontal cortex blood flow in PTSD patients with comorbid cocaine and alcohol abuse compared with normals. Psychiatry 2000, 63:65-74.
73. Shin L.H., McNally R.J., Kosslyn S.M., Thompson W.L., Rauch S.L., Alpert N.M., Metzger L.J., Lasko N.B., Orr S.P., Pitman R.K. Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related PTSD: a PET investigation. Am. J. Psychiatr. 1999, 156:575-584.
74. Shin R.M., Tsvetkov E., Bolshakov V.Y. Spatiotemporal asymmetry of associative synaptic plasticity in fear conditioning pathways. Neuron 2006, 52:883-896.
75. Sutherland R.J., McDonald R.J. Hippocampus, amygdala, and memory deficits in rats. Behav. Brain Res. 1990, 37:57-79.
76. Tomie A. Retardation of autoshaping: control by contextual stimuli. Science 1976, 192:1244-1246.
77. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
78. Vervliet B., Craske M.G., Hermans D. Fear extinction and relapse: state of the art. Annu. Rev. Clin. Psychol. 2013, 9:215-248.
79. Werner N.S., Meindl T., Engel R.R., Rosner R., Riedel M., Reiser M., Fast K. Hippocampal function during associative learning in patients with posttraumatic stress disorder. J. Psychiatr. Res. 2009, 43:309-318.
80. Wessa M., Flor H. Failure of extinction of fear responses in posttraumatic stress disorder: evidence from second-order conditioning. Am. J. Psychiatry 2007, 164:1684-1692.
81. Wignall E.L., Dickson J.M., Vaughan P., et al. Smaller hippocampal volume in patients with recent-onset posttraumatic stress disorder. Biol. Psychiatry 2004, 56:832-836.
82. Wittchen H.-U., Wunderlich U., Gruschwitz S., Zaudig M. Strukturiertes Klinisches Interview für DSM-IV. Achse I: Psychische Störungen 1997, Hogrefe, Göttingen.
83. Woon F.L., Sood S., Dawson W., Hedges D.W. Hippocampal volume deficits associated with exposure to psychological trauma and posttraumatic stress disorder in adults: a meta-analysis. Prog. Neuropsychopharmacol. Biol. Psychiatry 2010, 34:1181-1188.