Understanding posttraumatic stress disorder through fear conditioning, extinction and reconsolidation

Neuroscience and Biobehavioral Reviews

Volumn 71, Issue , 2016, Pages 48-57

  Careaga, Mariella Bodemeier Loayza ^a   Girardi, Carlos Eduardo Neves ^a   Suchecki, Deborah ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Extinction; Fear conditioning; Memory persistence; PTSD; Reconsolidation

Indexed keywords

AMYGDALA; ASSOCIATION; BRAIN FUNCTION; CONDITIONING; FEAR; FEAR CONDITIONING; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; NEUROANATOMY; NEUROBIOLOGY; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PREFRONTAL CORTEX; PRIORITY JOURNAL; PSYCHOTRAUMA; RECONSOLIDATION; REINFORCEMENT; REVIEW; STATE DEPENDENT LEARNING;

EXTINCTION, PSYCHOLOGICAL; FEAR; HUMANS; MEMORY; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84984832209     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2016.08.023     Document Type: Review

References (166)

1. Aggleton, J., The Amygdala: A Functional Analysis. 2nd ed., 2000, Oxford University Press.
2. Akirav, I., Segev, A., Motanis, H., Maroun, M., D-Cycloserine into the BLA reverses the impairing effects of exposure to stress on the extinction of contextual fear, but not conditioned taste aversion. Learn. Mem. 16 (2009), 682–686, 10.1101/lm.1565109.
3. Almada, R.C., Coimbra, N.C., Brandão, M.L., Medial prefrontal cortex serotonergic and GABAergic mechanisms modulate the expression of contextual fear: intratelencephalic pathways and differential involvement of cortical subregions. Neuroscience 284 (2015), 988–997, 10.1016/j.neuroscience.2014.11.001.
4. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders: DSM-5. 2013, American Psychiatric Association, 271–278.
5. Amos, T., Stein, D.J., Ipser, J.C., Pharmacological interventions for preventing post-traumatic stress disorder (PTSD). Cochrane database Syst. Rev., 2014, 10.1002/14651858.cd006239.pub2 CD006239.
6. Bisson, J., Andrew, M., Psychological treatment of post-traumatic stress disorder (PTSD). Cochrane Database Syst. Rev., 2005, 10.1002/14651858.cd003388.pub2 CD003388.
7. Bisson, J.I., Ehlers, A., Matthews, R., Pilling, S., Richards, D., Turner, S., Psychological treatments for chronic post-traumatic stress disorder: systematic review and meta-analysis. Br. J. Psychiatry 190 (2007), 97–104, 10.1192/bjp.bp.106.021402.
8. Blanchard, D.C., Blanchard, R.J., Innate and conditioned reactions to threat in rats with amygdaloid lesions. J. Comp. Physiol. Psychol. 81 (1972), 281–290, 10.1037/h0033521.
9. Blanchard, R.J., Blanchard, D.C., Agullana, R., Weiss, S.M., Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiol. Behav. 50 (1991), 967–972, 10.1016/0031-9384(91)90423-L.
10. 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. 45 (2007), 2019–2033, 10.1016/j.brat.2007.02.012.
11. Bouton, M.E., Bolles, R.C., Contextual control of the extinction of conditioned fear. Learn. Motiv., 1979, 10.1016/0023-9690(79)90057-2.
12. Bouton, M.E., Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol. Bull. 114 (1993), 80–99.
13. Bouton, M.E., Context and behavioral processes in extinction. Learn. Mem. 11 (2004), 485–494, 10.1101/lm.78804.
14. Bremner, J.D., Licinio, J., Darnell, A., Krystal, J.H., Owens, M.J., Southwick, S.M., Nemeroff, C.B., Charney, D.S., Elevated CSF corticotropin-releasing factor concentrations in posttraumatic stress disorder. Am. J. Psychiatry 154 (1997), 624–629, 10.1176/ajp.154.5.624.
15. Bremner, J.D., Narayan, M., Staib, L.H., Southwick, S.M., McGlashan, T., Charney, D.S., Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. Am. J. Psychiatry 156 (1999), 1787–1795.
16. Bremner, J.D., Staib, L.H., Kaloupek, D., Southwick, S.M., Soufer, R., Charney, D.S., Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biol. Psychiatry 45 (1999), 806–816, 10.1016/S0006-3223(98)00297-2.
17. Bremner, J.D., Vermetten, E., Schmahl, C., Vaccarino, V., Vythilingam, M., Afzal, N., Grillon, C., Charney, D.S., Positron emission tomographic imaging of neural correlates of a fear acquisition and extinction paradigm in women with childhood sexual-abuse-related post-traumatic stress disorder. Psychol. Med. 35 (2005), 791–806, 10.1017/S0033291704003290.
18. Breslau, N., Davis, G.C., Andreski, P., Peterson, E., Traumatic events and posttraumatic stress disorder in an urban population of young adults. Arch. Gen. Psychiatry 48 (1991), 216–222, 10.1001/archpsyc.1991.01810270028003.
19. Brinley-Reed, M., Mascagni, F., McDonald, A.J., Synaptology of prefrontal cortical projections to the basolateral amygdala: an electron microscopic study in the rat. Neurosci. Lett. 202 (1995), 45–48.
20. Broadbent, N.J., Squire, L.R., Clark, R.E., Reversible hippocampal lesions disrupt water maze performance during both recent and remote memory tests. Learn. Mem. 13 (2006), 187–191, 10.1101/lm.134706.
21. Brown, E.S., Jeon-Slaughter, H., Lu, H., Jamadar, R., Issac, S., Shad, M., Denniston, D., Tamminga, C., Nakamura, A., Thomas, B.P., Hippocampal volume in healthy controls given 3-day stress doses of hydrocortisone. Neuropsychopharmacology 40 (2015), 1216–1221, 10.1038/npp.2014.307.
22. Brunet, A., Orr, S.P., Tremblay, J., Robertson, K., Nader, K., Pitman, R.K., Effect of post-retrieval propranolol on psychophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. J. Psychiatr. Res. 42 (2008), 503–506, 10.1016/j.jpsychires.2007.05.006.
23. Cándido, A., González, F., de Brugada, I., Safety signals from avoidance learning but not from yoked classical conditioning training pass both summation and retardation tests for inhibition. Behav. Processes 66 (2004), 153–160, 10.1016/j.beproc.2004.01.011.
24. Cahill, L., Gorski, L., Le, K., Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learn. Mem. 10 (2003), 270–274, 10.1101/lm.62403.
25. Campeau, S., Falls, W.A., Cullinan, W.E., Helmreich, D.L., Davis, M., Watson, S.J., Elicitation and reduction of fear: behavioural and neuroendocrine indices and brain induction of the immediate-early gene c-fos. Neuroscience 78 (1997), 1087–1104, 10.1016/S0306-4522(96)00632-X.
26. Chen, Y., Bender, R.A., Brunson, K.L., Pomper, J.K., Grigoriadis, D.E., Wurst, W., Baram, T.Z., Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 15782–15787, 10.1073/pnas.0403975101.
27. Chilcoat, H.D., Breslau, N., Posttraumatic stress disorder and drug disorders: testing causal pathways. Arch. Gen. Psychiatry 55 (1998), 913–917.
28. Chung, Y.A., Kim, S.H., Chung, S.K., Chae, J.H., Yang, D.W., Sohn, H.S., Jeong, J., Alterations in cerebral perfusion in posttraumatic stress disorder patients without re-exposure to accident-related stimuli. Clin. Neurophysiol. 117 (2006), 637–642, 10.1016/j.clinph.2005.10.020.
29. Conrad, C.D., Galea, L.A., Kuroda, Y., McEwen, B.S., Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 110 (1996), 1321–1334.
30. Corcoran, K.A., Maren, S., Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction. Learn. Mem. 11 (2004), 598–603, 10.1101/lm.78704.
31. Corcoran, K.A., Quirk, G.J., Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J. Neurosci. 27 (2007), 840–844, 10.1523/jneurosci.5327-06.2007.
32. de Quervain, D.J., Roozendaal, B., McGaugh, J.L., Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 394 (1998), 787–790, 10.1038/29542.
33. de Quervain, D.J.-F., Aerni, A., Schelling, G., Roozendaal, B., Glucocorticoids and the regulation of memory in health and disease. Front. Neuroendocrinol. 30 (2009), 358–370, 10.1016/j.yfrne.2009.03.002.
34. Dębiec, J., Bush, D.E., LeDoux, J.E., Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats-a possible mechanism for the persistence of traumatic memories in PTSD. Depress. Anxiety 28 (2011), 186–193, 10.1002/da.20803.
35. Dȩbiec, J., Ledoux, J.E., Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129 (2004), 267–272, 10.1016/j.neuroscience.2004.08.018.
36. Davis, H.P., Squire, L.R., Protein synthesis and memory: a review. Psychol. Bull. 96 (1984), 518–559.
37. Davis, M., Falls, W., Gewirtz, J., Neural Systems Involved in Fear Inhibition: Extinction and Conditioned Inhibition. 2000, Springer, US, 10.1007/978-1-4757-4860-4_8.
38. Davis, M., Neurobiology of fear responses: the role of the amygdala. J. Neuropsychiatry Clin. Neurosci. 9 (1997), 382–402, 10.1176/jnp.9.3.382.
39. Debiec, J., LeDoux, J.E., Nader, K., Cellular and systems reconsolidation in the hippocampus. Neuron 36 (2002), 527–538, 10.1016/S0896-6273(02)01001-2.
40. Diamond, D.M., Rose, G.M., Stress impairs LTP and hippocampal-dependent memory. Ann. N. Y. Acad. Sci. 746 (1994), 411–414.
41. Dickie, E.W., Brunet, A., Akerib, V., Armony, J.L., An fMRI investigation of memory encoding in PTSD: Influence of symptom severity. Neuropsychologia 46 (2008), 1522–1531, 10.1016/j.neuropsychologia.2008.01.007.
42. Difede, J., Cukor, J., Wyka, K., Olden, M., Hoffman, H., Lee, F.S., Altemus, M., D-Cycloserine augmentation of exposure therapy for post-traumatic stress disorder: a pilot randomized clinical trial. Neuropsychopharmacology, 1–7, 2013, 10.1038/npp.2013.317.
43. Dunn, T.M., Schwartz, M., Hatfield, R.W., Wiegele, M., Measuring effectiveness of eye movement desensitization and reprocessing (EMDR) in non-clinical anxiety: a multi-subject, yoked-control design. J. Behav. Ther. Exp. Psychiatry 27 (1996), 231–239.
44. Eckart, C., Engler, H., Riether, C., Kolassa, S., Elbert, T., Kolassa, I.T., No PTSD-related differences in diurnal cortisol profiles of genocide survivors. Psychoneuroendocrinology 34 (2009), 523–531, 10.1016/j.psyneuen.2008.10.012.
45. Eckstein, M., Scheele, D., Patin, A., Preckel, K., Becker, B., Walter, A., Maier, W., Hurlemann, R., Oxytocin facilitates pavlovian fear learning in males. Neuropsychopharmacology, 2015, 10.1038/npp.2015.245.
46. Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., Lüthi, A., Amygdala inhibitory circuits and the control of fear memory. Neuron, 2009, 10.1016/j.neuron.2009.05.026.
47. El Khoury-Malhame, M., Reynaud, E., Soriano, A., Michael, K., Salgado-Pineda, P., Zendjidjian, X., Gellato, C., Eric, F., Lefebvre, M.-N., Rouby, F., Samuelian, J.-C., Anton, J.-L., Blin, O., Khalfa, S., Amygdala activity correlates with attentional bias in PTSD. Neuropsychologia 49 (2011), 1969–1973, 10.1016/j.neuropsychologia.2011.03.025.
48. Elofsson, U.O., von Schèele, B., Theorell, T., Söndergaard, H.P., Physiological correlates of eye movement desensitization and reprocessing. J. Anxiety Disord. 22 (2008), 622–634, 10.1016/j.janxdis.2007.05.012.
49. Elzinga, B.M., Schmahl, C.G., Vermetten, E., van Dyck, R., Bremner, J.D., Higher cortisol levels following exposure to traumatic reminders in abuse-related PTSD. Neuropsychopharmacology 28 (2003), 1656–1665, 10.1038/sj.npp.1300226.
50. Eysenck, H., The conditioning model of neurosis. Behav. Brain Res. 2 (1979), 155–166.
51. Felmingham, K., Kemp, A., Williams, L., Das, P., Hughes, G., Peduto, A., Bryant, R., Changes in anterior cingulate and amygdala after cognitive behavior therapy of posttraumatic stress disorder. Psychol. Sci., 2007, 10.1111/j.1467-92802007.01860.x.
52. Fendt, M., Fanselow, M.S., The neuroanatomical and neurochemical basis of conditioned fear. Neurosci. Biobehav. Rev. 23 (1999), 743–760, 10.1016/S0149-7634(99)00016-0.
53. Fitzgerald, P.J., Seemann, J.R., Maren, S., Can fear extinction be enhanced? A review of pharmacological and behavioral findings. Brain Res. Bull. 105 (2014), 46–60, 10.1016/j.brainresbull.2013.12.007.
54. Fuster, J., The prefrontal cortex—an update. Neuron 30 (2001), 319–333, 10.1016/S0896-6273(01)00285-9.
55. Galea, S., Trends of probable post-Traumatic stress disorder in new York city after the September 11 terrorist attacks. Am. J. Epidemiol. 158 (2003), 514–524, 10.1093/aje/kwg187.
56. Geracioti, J., Baker, D.G., Ekhator, N.N., West, S.A., Hill, K.K., Bruce, A.B., Schmidt, D., Rounds-Kugler, B., Yehuda, R., Keck, J., Kasckow, J.W., CSF norepinephrine concentrations in posttraumatic stress disorder. Am. J. Psychiatry 158 (2001), 1227–1230, 10.1176/appi.ajp.158.8.1227.
57. 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. 5 (2002), 1242–1247, 10.1038/nn958.
58. Girardi, C.E.N., Tiba, P.a., Llobet, G.B., Levin, R., Abilio, V.C., Suchecki, D., Contextual exploration previous to an aversive event predicts long-term emotional consequences of severe stress. Front. Behav. Neurosci., 7, 2013, 134, 10.3389/fnbeh.2013.00134.
59. Glickman, S.E., Perseverative neural processes and consolidation of the memory trace. Psychol. Bull. 58 (1961), 218–233, 10.1037/h0044212.
60. Goebel, M., Fleming, S.M., Million, M., Stengel, A., Taché, Y., Wang, L., Mice overexpressing corticotropin-releasing factor show brain atrophy and motor dysfunctions. Neurosci. Lett. 473 (2010), 11–15, 10.1016/j.neulet.2010.01.068.
61. Gold, P.E., Van Buskirk, R.B., Facilitation of time-dependent memory processes with posttrial epinephrine injections. Behav. Biol. 13 (1975), 145–153, 10.1016/S0091-6773(75)91784-8.
62. Goshen, I., Brodsky, M., Prakash, R., Wallace, J., Gradinaru, V., Ramakrishnan, C., Deisseroth, K., Dynamics of retrieval strategies for remote memories. Cell 147 (2011), 678–689, 10.1016/j.cell.2011.09.033.
63. Hamm, A.O., Vaitl, D., Affective learning: awareness and aversion. Psychophysiology 33 (1996), 698–710, 10.1111/j.1469-89861996. tb02366.x.
64. Hamm, A.O., Weike, A.I., The neuropsychology of fear learning and fear regulation. Int. J. Psychophysiol. 57 (2005), 5–14, 10.1016/j.ijpsycho.2005.01.006.
65. Herman, J.P., Schäfer, M.K., Young, E.A., Thompson, R., Douglass, J., Akil, H., Watson, S.J., Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis. J. Neurosci. 9 (1989), 3072–3082.
66. Hitchcock, J., Davis, M., Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behav. Neurosci. 100 (1986), 11–22, 10.1037/0735-7044.100.1.11.
67. Huether, G., The central adaptation syndrome: psychosocial stress as a trigger for adaptive modifications of brain structure and brain function. Prog. Neurobiol. 48 (1996), 569–612, 10.1016/0301-0082(96)00003-2.
68. Iwata, J., LeDoux, J.E., Reis, D.J., Destruction of intrinsic neurons in the lateral hypothalamus disrupts the classical conditioning of autonomic but not behavioral emotional responses in the rat. Brain Res. 368 (1986), 161–166, 10.1016/0006-8993(86)91055-3.
69. Jacobson, L., Sapolsky, R., The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr. Rev. 12 (1991), 118–134, 10.1210/edrv-12-2-118.
70. Jovanovic, T., Ressler, K.J., How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am. J. Psychiatry, 2010, 10.1176/appi.ajp.2009.09071074.
71. Jovanovic, T., Norrholm, S.D., Fennell, J.E., Keyes, M., Fiallos, A.M., Myers, K.M., Davis, M., Duncan, E.J., Posttraumatic stress disorder may be associated with impaired fear inhibition: relation to symptom severity. Psychiatry Res. 167 (2009), 151–160, 10.1016/j.psychres.2007.12.014.
72. Kandel, E.R., Schwartz, J.H., Molecular biology of learning: modulation of transmitter release. Science 218 (1982), 433–443.
73. Kaouane, N., Porte, Y., Vallée, M., Brayda-Bruno, L., Mons, N., Calandreau, L., Marighetto, A., Piazza, P.V., Desmedt, A., Glucocorticoids can induce PTSD-like memory impairments in mice. Science 335 (2012), 1510–1513, 10.1126/science.1207615.
74. Kapp, B.S., Frysinger, R.C., Gallagher, M., Haselton, J.R., Amygdala central nucleus lesions: effect on heart rate conditioning in the rabbit. Physiol. Behav. 23 (1979), 1109–1117, 10.1016/0031-9384(79)90304-4.
75. Kessler, R.C., Sonnega, A., Bromet, E., Hughes, M., Nelson, C.B., Posttraumatic stress disorder in the national comorbidity survey. Arch. Gen. Psychiatry 52 (1995), 1048–1060, 10.1001/archpsyc.1995.03950240066012.
76. Kim, J.J., Rison, R.A., Fanselow, M.S., Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav. Neurosci. 107 (1993), 1093–1098.
77. Kindt, M., Soeter, M., Vervliet, B., Beyond extinction: erasing human fear responses and preventing the return of fear. Nat. Neurosci. 12 (2009), 256–258, 10.1038/nn.2271.
78. Kitayama, N., Vaccarino, V., Kutner, M., Weiss, P., Bremner, J.D., Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: a meta-analysis. J. Affect. Disord. 88 (2005), 79–86, 10.1016/j.jad.2005.05.014.
79. Koch, S.B., van Zuiden, M., Nawijn, L., Frijling, J.L., Veltman, D.J., Olff, M., Intranasal oxytocin administration dampens amygdala reactivity towards emotional faces in male and female PTSD patients. Neuropsychopharmacology, 2015, 10.1038/npp.2015.299.
80. LaLumiere, R.T., Buen, T., McGaugh, J.L., Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. J. Neurosci. 23 (2003), 6754–6758.
81. Lang, P.J., Davis, M., Ohman, A., Fear and anxiety: animal models and human cognitive psychophysiology. J. Affect. Disord. 61 (2000), 137–159, 10.1016/S0165-0327(00)00343-8.
82. Lanius, R.A., Williamson, P.C., Hopper, J., Densmore, M., Boksman, K., Gupta, M.A., Neufeld, R.W., Gati, J.S., Menon, R.S., Recall of emotional states in posttraumatic stress disorder: an fMRI investigation. Biol. Psychiatry 53 (2003), 204–210 S000632230201466X [pii].
83. Lanius, R.A., Frewen, P.A., Girotti, M., Neufeld, R.W.J., Stevens, T.K., Densmore, M., Neural correlates of trauma script-imagery in posttraumatic stress disorder with and without comorbid major depression: a functional MRI investigation. Psychiatry Res. Neuroimaging 155 (2007), 45–56, 10.1016/j.pscychresns.2006.11.006.
84. LeDoux, J.E., The emotional brain: the mysterious underpinnings of emotional life. Simon Schuster, 1996.
85. Liang, K.C., Juler, R.G., McGaugh, J.L., Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain Res. 368 (1986), 125–133.
86. Liberzon, I., Taylor, S.F., Amdur, R., Jung, T.D., Chamberlain, K.R., Minoshima, S., Koeppe, R.A., Fig, L.M., Brain activation in PTSD in response to trauma-related stimuli. Biol. Psychiatry 45 (1999), 817–826.
87. Lissek, S., van Meurs, B., Learning models of PTSD: Theoretical accounts and psychobiological evidence. Int. J. Psychophysiol., 2015, 10.1016/j.ijpsycho.2014.11.006.
88. Magariños, A.M., McEwen, B.S., Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69 (1995), 89–98, 10.1016/0306-4522(95)00256-I.
89. Maren, S., Aharonov, G., Fanselow, M.S., Neurotoxic lesions of the dorsal hippocampus and Pavlovian fear conditioning in rats. Behav. Brain Res. 88 (1997), 261–274, 10.1016/S0166-4328(97)00088-0.
90. Maren, S., Ferrario, C.R., Corcoran, K.A., Desmond, T.J., Frey, K.A., Protein synthesis in the amygdala, but not the auditory thalamus, is required for consolidation of Pavlovian fear conditioning in rats. Eur. J. Neurosci. 18 (2003), 3080–3088, 10.1111/j.1460-9568.2003.03063.x.
91. Maren, S., Neurobiology of Pavlovian fear conditioning. Annu. Rev. Neurosci. 24 (2001), 897–931, 10.1146/annurev.neuro.24.1.897.
92. McEwen, B., Gould, E., Sakai, R., The vulnerability of the hippocampus to protective and destructive effects of glucocorticoids in relation to stress. Br. J. Psychiatry Suppl. 15 (1992), 18–23.
93. McGaugh, J.L., Time-dependent processes in memory storage. Science 153 (1966), 1351–1358, 10.1126/science.153.3742.1351.
94. McGaugh, J.L., Memory-a century of consolidation. Science 287 (2000), 248–251, 10.1126/science.287.5451.248.
95. Mcdonald, A.J., Mascagni, F., Guo, L., Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71 (1996), 55–75, 10.1016/0306-4522(95)00417-3.
96. Milad, M.R., Rauch, S.L., Pitman, R.K., Quirk, G.J., Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol. Psychol. 73 (2006), 61–71, 10.1016/j.biopsycho.2006.01.008.
97. Milad, M.R., Orr, S.P., Lasko, N.B., Chang, Y., Rauch, S.L., Pitman, R.K., Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study. J. Psychiatry Res. 42 (2008), 515–520, 10.1016/j.jpsychires.2008.01.017.
98. 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 66 (2009), 1075–1082, 10.1016/j.biopsych.2009.06.026.
99. Misanin, J.R., Miller, R.R., Lewis, D.J., Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 160 (1968), 554–555, 10.1126/science.160.3827.554.
100. Mitra, R., Jadhav, S., McEwen, B.S., Vyas, A., Chattarji, S., Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 9371–9376, 10.1073/pnas.0504011102.
101. Myers, K.M., Davis, M., Behavioral and neural analysis of extinction. Neuron, 2002, 10.1016/s0896-6273(02)01064-4.
102. Nader, K., Schafe, G.E., Le Doux, J.E., Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406 (2000), 722–726, 10.1038/35021052.
103. Nader, K., Hardt, O., Lanius, R., Memory as a new therapeutic target. Dialogues Clin. Neurosci. 15 (2013), 475–486.
104. Nicholaichuk, T.P., Quesnel, L.J., Tait, R.W., Eysenck's theory of incubation: an empirical test. Behav. Res. Ther. 20 (1982), 329–338, 10.1016/0005-7967(82)90092-4.
105. O'Donnell, T., Hegadoren, K.M., Coupland, N.C., Noradrenergic mechanisms in the pathophysiology of post-traumatic stress disorder. Neuropsychobiology, 2004, 10.1159/000080952.
106. 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. 109 (2000), 290–298, 10.1037/0021-843X.109.2.290.
107. Pagani, M., Di Lorenzo, G., Verardo, A.R., Nicolais, G., Monaco, L., Lauretti, G., Russo, R., Niolu, C., Ammaniti, M., Fernandez, I., Siracusano, A., Neurobiological correlates of EMDR monitoring – an EEG study. PLoS One, 7, 2012, e45753, 10.1371/journal.pone.0045753.
108. Pamplona, F.A., Henes, K., Micale, V., Mauch, C.P., Takahashi, R.N., Wotjak, C.T., Prolonged fear incubation leads to generalized avoidance behavior in mice. J. Psychiatr. Res. 45 (2011), 354–360, 10.1016/j.jpsychires.2010.06.015.
109. Peri, T., Ben-Shakhar, G., Orr, S.P., Shalev, A.Y., Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder. Biol. Psychiatry 47 (1999), 512–519, 10.1016/S0006-3223(99)00144-4.
110. Phillips, R.G., LeDoux, J.E., Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106 (1992), 274–285, 10.1037/0735-7044.106.2.274.
111. Pickens, C.L., Golden, S.A., Adams-Deutsch, T., Nair, S.G., Shaham, Y., Long-Lasting incubation of conditioned fear in rats. Biol. Psychiatry 65 (2009), 881–886, 10.1016/j.biopsych.2008.12.010.
112. Pinard, C.R., Mascagni, F., McDonald, A.J., Medial prefrontal cortical innervation of the intercalated nuclear region of the amygdala. Neuroscience 205 (2012), 112–124, 10.1016/j.neuroscience.2011.12.036.
113. Pitman, R.K., Gilbertson, M.W., Gurvits, T.V., May, F.S., Lasko, N.B., Metzger, L.J., Shenton, M.E., Yehuda, R., Orr, S.P., Harvard/VA PTSD Twin Study Investigators, Clarifying the origin of biological abnormalities in PTSD through the study of identical twins discordant for combat exposure. Ann. N. Y. Acad. Sci. 1071 (2006), 242–254, 10.1196/annals.1364.019.
114. Pitman, R.K., Post-traumatic stress disorder, hormones, and memory. Biol. Psychiatry, 1989, 10.1016/0006-3223(89)90033-4.
115. Pollak, D.D., Monje, F.J., Zuckerman, L., Denny, C.A., Drew, M.R., Kandel, E.R., An animal model of a behavioral intervention for depression. Neuron 60 (2008), 149–161 http://dx.doi.org/10.1016/j.neuron.2008.07.041.
116. Przybyslawski, J., Roullet, P., Sara, S.J., Attenuation of emotional and nonemotional memories after their reactivation: role of beta adrenergic receptors. J. Neurosci. 19 (1999), 6623–6628.
117. Quinn, W., Harris, W., Benzer, S., Conditioned behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 71 (1974), 708–712.
118. Rabinak, C.A., Angstadt, M., Welsh, R.C., Kenndy, A.E., Lyubkin, M., Martis, B., Phan, K.L., Altered amygdala resting-state functional connectivity in post-traumatic stress disorder. Front. Psychiatry, 2, 2011, 62, 10.3389/fpsyt.2011.00062.
119. Raboni, M.R., Alonso, F.F.D., Tufik, S., Suchecki, D., Improvement of mood and sleep alterations in posttraumatic stress disorder patients by eye movement desensitization and reprocessing. Front. Behav. Neurosci. 8 (2014), 1–11, 10.3389/fnbeh.2014.00209.
120. Rao, R.P., Anilkumar, S., McEwen, B.S., Chattarji, S., Glucocorticoids protect against the delayed behavioral and cellular effects of acute stress on the amygdala. Biol. Psychiatry 72 (2012), 466–475, 10.1016/j.biopsych.2012.04.008.
121. Rauch, S.L., Whalen, P.J., Shin, L.M., McInerney, S.C., MacKlin, M.L., Lasko, N.B., Orr, S.P., Pitman, R.K., Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biol. Psychiatry 47 (2000), 769–776, 10.1016/S0006-3223(00)00828-3.
122. Rescorla, R.A., Heth, C.D., Reinstatement of fear to an extinguished conditioned stimulus. J. Exp. Psychol. Anim. Behav. Process. 1 (1975), 88–96.
123. Rescorla, R.A., Conditioned inhibition of fear resulting from negative CS-US contingencies. J. Comp. Physiol. Psychol. 67 (1969), 504–509, 10.1037/h0027313.
124. Rescorla, R.A., Spontaneous recovery. Learn. Mem. 11 (2004), 501–509, 10.1101/lm.77504.
125. Resnick, H.S., Kilpatrick, D.G., Dansky, B.S., Saunders, B.E., Best, C.L., Prevalence of civilian trauma and posttraumatic stress disorder in a representative national sample of women. J. Consult. Clin. Psychol. 61 (1993), 984–991, 10.1037/0022-006x.61.6.984.
126. Reul, J.M.H.M., De Kloet, E.R., Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117 (1985), 2505–2511, 10.1210/endo-117-6-2505.
127. Rhudy, J.L., Davis, J.L., Williams, A.E., McCabe, K.M., Bartley, E.J., Byrd, P.M., Pruiksma, K.E., Cognitive-behavioral treatment for chronic nightmares in trauma-exposed persons: assessing physiological reactions to nightmare-related fear. J. Clin. Psychol. 66 (2010), 365–382, 10.1002/jclp.20656.
128. Ribeiro, W.S., Mari, J., de, J., Quintana, M.I., Dewey, M.E., Evans-Lacko, S., Vilete, L.M.P., Figueira, I., Bressan, R.A., de Mello, M.F., Prince, M., Ferri, C.P., Coutinho, E.S.F., Andreoli, S.B., The impact of epidemic violence on the prevalence of psychiatric disorders in Sao Paulo and Rio de Janeiro, Brazil. PLoS One, 8, 2013, e63545, 10.1371/journal.pone.0063545.
129. Rogan, M.T., Leon, K.S., Perez, D.L., Kandel, E.R., Distinct neural signatures for safety and danger in the amygdala and striatum of the mouse. Neuron 46 (2005), 309–320, 10.1016/j.neuron.2005.02.017.
130. Roozendaal, B., McGaugh, J.L., Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur. J. Neurosci. 9 (1997), 76–83.
131. Roozendaal, B., Griffith, Q.K., Buranday, J., De Quervain, D.J.-F., McGaugh, J.L., The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 1328–1333, 10.1073/pnas.0337480100.
132. Sack, M., Lempa, W., Lamprecht, F., Assessment of psychophysiological stress reactions during a traumatic reminder in patients treated with EMDR. J. EMDR Pract. Res. 1 (2007), 15–23, 10.1891/1933-3196.1.1.15.
133. Sah, P., Faber, E.S.L., Lopez De Armentia, M., Power, J., The amygdaloid complex: anatomy and physiology. Physiol. Rev. 83 (2003), 803–834, 10.1152/physrev.00002.2003.
134. Sandin, B., Chorot, P., The incubation theory of fear/anxiety: experimental investigation in a human laboratory model of Pavlovian conditioning. Behav. Res. Ther. 27 (1989), 9–18, 10.1016/0005-7967(89)90114-9.
135. Sandin, B., Chorot, P., Resistance to extinction of conditioned electrodermal responses: a study of the incubation fear hypothesis. Psychol. Rep. 91 (2002), 37–46, 10.2466/pr0.2002.91.1.37.
136. Sapolsky, R.M., Uno, H., Rebert, C.S., Finch, C.E., Hippocampal damage associated with prolonged glucocorticoid exposure in primates. J. Neurosci. 10 (1990), 2897–2902.
137. Schafe, G.E., LeDoux, J.E., Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J. Neurosci., 20, 2000, RC96.
138. Schelling, G., Briegel, J., Roozendaal, B., Stoll, C., Rothenhäusler, H.B., Kapfhammer, H.P., The effect of stress doses of hydrocortisone during septic shock on posttraumatic stress disorder in survivors. Biol. Psychiatry 50 (2001), 978–985, 10.1016/S0006-3223(01)01270-7.
139. Schlenger, W.E., Caddell, J.M., Ebert, L., Jordan, B.K., Rourke, K.M., Wilson, D., Thalji, L., Dennis, J.M., Fairbank, J.A., Kulka, R.A., Psychological reactions to terrorist attacks. JAMA 288 (2002), 581–588, 10.1001/jama.288.5.581.
140. Schneider, A.M., Sherman, W., Amnesia: a function of the temporal relation of footshock to electroconvulsive shock. Science 159 (1968), 219–221, 10.1126/science.159.3811.219.
141. Shalev, Y.A., Peri, T., Brandes, D., Freedman, S., Orr, S.P., Pitman, R.K., Auditory startle response in trauma survivors with posttraumatic stress disorder: a prospective study. Am. J. Psychiatry 157 (2000), 255–261, 10.1176/appi.ajp.157.2.255.
142. Shapiro, F., Eye movement desensitization and reprocessing (EMDR): evaluation of controlled PTSD research. J. Behav. Ther. Exp. Psychiatry 27 (1996), 209–218.
143. Shapiro, F., Eye Movement Desensitization and Reprocessing (EMDR) and the anxiety disorders: clinical and research implications of an integrated psychotherapy treatment. J. Anxiety Disord. 13 (1999), 35–67.
144. Shin, L.M., Liberzon, I., The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35 (2010), 169–191, 10.1038/npp.2009.83.
145. Shin, L.M., Kosslyn, S.M., McNally, R.J., Alpert, N.M., Thompson, W.L., Rauch, S.L., Macklin, M.L., Pitman, R.K., Visual imagery and perception in posttraumatic stress disorder. A positron emission tomographic investigation. Arch. Gen. Psychiatry 54 (1997), 233–241, 10.1001/archpsyc.1997.01830150057010.
146. Shin, L.M., Wright, C.I., Cannistraro, P.A., Wedig, M.M., McMullin, K., Martis, B., Macklin, M.L., Lasko, N.B., Cavanagh, S.R., Krangel, T.S., Orr, S.P., Pitman, R.K., Whalen, P.J., Rauch, S.L., A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch. Gen. Psychiatry 62 (2005), 273–281, 10.1001/archpsyc.62.3.273.
147. Siegmund, A., Wotjak, C.T., A mouse model of posttraumatic stress disorder that distinguishes between conditioned and sensitised fear. J. Psychiatry Res. 41 (2007), 848–860, 10.1016/j.jpsychires.2006.07.017.
148. Smith, M.E., Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: a meta-analysis of structural MRI studies. Hippocampus 15 (2005), 798–807, 10.1002/hipo.20102.
149. Soeter, M., Kindt, M., Dissociating response systems: erasing fear from memory. Neurobiol. Learn. Mem. 94 (2010), 30–41, 10.1016/j.nlm.2010.03.004.
150. Stoppelbein, L., Greening, L., Fite, P., The role of cortisol in PTSD among women exposed to a trauma-related stressor. J. Anxiety Disord. 26 (2012), 352–358, 10.1016/j.janxdis.2011.12.004.
151. Strawn, J.R., Geracioti, T.D., Noradrenergic dysfunction and the psychopharmacology of posttraumatic stress disorder. Depress. Anxiety, 2008, 10.1002/da.20292.
152. Strobel, C., Marek, R., Gooch, H.M., Sullivan, R.K.P., Sah, P., Prefrontal and auditory input to intercalated neurons of the Amygdala. Cell Rep. 10 (2015), 1435–1442, 10.1016/j.celrep.2015.02.008.
153. Todd, T.P., Winterbauer, N.E., Bouton, M.E., Contextual control of appetite. Renewal of inhibited food-seeking behavior in sated rats after extinction. Appetite 58 (2012), 484–489, 10.1016/j.appet.2011.12.006.
154. Van Etten, M., Taylor, S., Comparative efficacy of treatments for post-traumatic stress disorder: a meta-analysis. Clin. Psychol. Psychother. 5 (1998), 126–144.
155. VanElzakker, M.B., Kathryn Dahlgren, M., Caroline Davis, F., Dubois, S., Shin, L.M., From Pavlov to PTSD: The extinction of conditioned fear in rodents, humans, and anxiety disorders. Neurobiol. Learn. Mem. 113 (2014), 3–18, 10.1016/j.nlm.2013.11.014.
156. Vermetten, E., Zhohar, J., Krugers, H.J., Pharmacotherapy in the aftermath of trauma; opportunities in the golden hours. Curr. Psychiatry Rep., 16, 2014, 10.1007/s11920-014-0455-y.
157. Vervliet, B., Craske, M.G., Hermans, D., Fear extinction and relapse: state of the art. Annu. Rev. Clin. Psychol. 9 (2013), 215–248, 10.1146/annurev-clinpsy-050212-185542.
158. Vidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S.L., Quirk, G.J., Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn. Mem. 13 (2006), 728–733, 10.1101/lm.306106.
159. Weike, A.I., Schupp, H.T., Hamm, A.O., Fear acquisition requires awareness in trace but not delay conditioning. Psychophysiology 44 (2007), 170–180, 10.1111/j.1469-8986.2006.00469.x.
160. Weiss, S.J., Neurobiological alterations associated with traumatic stress. Perspect. Psychiatr. Care 43 (2007), 114–122, 10.1111/j.1744-6163.2007.00120.x.
161. Wood, N.E., Rosasco, M.L., Suris, A.M., Spring, J.D., Marin, M.-F., Lasko, N.B., Goetz, J.M., Fischer, A.M., Orr, S.P., Pitman, R.K., Pharmacological blockade of memory reconsolidation in posttraumatic stress disorder: three negative psychophysiological studies. Psychiatry Res. 225 (2015), 31–39, 10.1016/j.psychres.2014.09.005.
162. Yehuda, R., LeDoux, J., Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron, 2007, 10.1016/j.neuron.2007.09.006.
163. Yehuda, R., Teicher, M.H., Trestman, R.L., Levengood, R.A., Siever, L.J., Cortisol regulation in posttraumatic stress disorder and major depression: a chronobiological analysis. Biol. Psychiatry 40 (1996), 79–88, 10.1016/0006-3223(95)00451-3.
164. Yehuda, R., Golier, J.A., Kaufman, S., Circadian rhythm of salivary cortisol in Holocaust survivors with and without PTSD. Am. J. Psychiatry 162 (2005), 998–1000, 10.1176/appi.ajp.162.5.998.
165. Yehuda, R., Post-traumatic stress disorder. N. Engl. J. Med. 346 (2002), 108–114, 10.1056/NEJMra012941.
166. Zohar, J., Yahalom, H., Kozlovsky, N., Cwikel-Hamzany, S., Matar, M.A., Kaplan, Z., Yehuda, R., Cohen, H., High dose hydrocortisone immediately after trauma may alter the trajectory of PTSD: interplay between clinical and animal studies. Eur. Neuropsychopharmacol. 21 (2011), 796–809, 10.1016/j.euroneuro.2011.06.001.