The neurobiology of posttraumatic stress disorder: Dysfunction in the prefrontal-amygdala circuit?

Psychology and Neuroscience

Volumn 4, Issue 2, 2011, Pages 191-203

  Lobo, Isabela ^a   de Oliveira, Letícia ^a   David, Isabel A ^a   Pereira, Mirtes G ^a   Volchan, Eliane ^b   Rocha Rego, Vanessa ^c   Figueira, Ivan ^b   Mocaiber, Izabela ^a  

^a FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Amygdala; Prefrontal cortex; Ptsd

Indexed keywords

AMYGDALOID NUCLEUS; ANXIETY DISORDER; ARTICLE; EMOTION; FEAR; HELPLESSNESS; HUMAN; NATURAL DISASTER; NEUROIMAGING; PATHOPHYSIOLOGY; POSTTRAUMATIC STRESS DISORDER; PREFRONTAL CORTEX; SEXUAL CRIME;

EID: 83455260012     PISSN: 19843054     EISSN: 19833288     Source Type: Journal    
DOI: 10.3922/j.psns.2011.2.004     Document Type: Article

References (101)

1. Adami, P., Konig, P., Vetter, Z., Hausmann, A., & Conca, A. (2006). Post-traumatic stress disorder and amygdala-hippocampectomy. Acta Psychiatrica Scandinavica, 113, 360-363, discussion 363-364.
2. th edition. Washington, D.C.: American Psychiatric Press.
3. Armony, J.L., Corbo, V., Clement, M.H., & Brunet, A. (2005). Amygdala response in patients with acute PTSD to masked and unmasked emotional facial expressions. American Journal of Psychiatry, 162, 1961-1963.
4. Banks, S.J., Eddy, K.T., Angstadt, M., Nathan, P.J., & Phan, K.L. (2007). Amygdala-frontal connectivity during emotion regulation. Social Cognitive and Affective Neuroscience, 2, 303-312.
5. Barbas, H. (1995). Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neuroscience and Biobehavioral Reviews, 19, 499-510.
6. Beauregard, M., Lévesque, J., & Bourgouin, P. (2001). Neural correlates of conscious self-regulation of emotion. Journal of Neuroscience, 21, RC165.
7. Beauregard, M., Paquette, V., & Levesque, J. (2006). Dysfunction in the neural circuitry of emotional self-regulation in major depressive disorder. Neuroreport, 17, 843-846.
8. Birbaumer, N., Grodd, W., Diedrich, O., Klose, U., Erb, M., Lotze, M., Flor, H. (1998). FMRI reveals amygdala activation to human faces in social phobics. Neuroreport, 9, 1223-1226.
9. Bremner, J.D., Staib, L.H., Kaloupek, D., Southwick, S.M., Soufer, R., & Charney, D.S. (1999). Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biological Psychiatry, 45, 806-816.
10. Bremner, J.D., Vythilingam, M., Vermetten, E., Southwick, S.M., Mcglashan, T., Staib, L.H., Soufer, R., & Charney, D.S. (2003). Neural correlates of declarative memory for emotionally valenced words in women with posttraumatic stress disorder related to early childhood sexual abuse. Biological Psychiatry, 53, 879-889.
11. Bremner, J.D., Vermetten, E., Vythilingam, M., Afzal, N., Schmahl, C., Elzinga, B., & Charney, D.S. (2004). Neural correlates of the classic color and emotional Stroop in women with abuse-related posttraumatic stress disorder. Biological Psychiatry, 55, 612-620.
12. Bremner, J.D, Vermetten, E., Schmahl, C., Vaccarino, V., Vythilingam, M., Afzal, N., Grillon, C., & Charney, D.S. (2005). 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. Psychological Medicine, 35, 791-806.
13. Britton, J.C., Phan, K.L., Taylor, S.F., Figure, L.M., & Liberzon, I. (2005). Corticolimbic blood fow in posttraumatic stress disorder during script-driven imagery. Biological Psychiatry, 57, 832-840.
14. Bryant, R.A., Felmingham, K.L., Kemp, A.H., Barton, M., Peduto, A.S., Rennie, C., Gordon, E., & Williams, L.M. (2005). Neural networks of information processing in posttraumatic stress disorder: a functional magnetic resonance imaging study. Biological Psychiatry, 58, 111-118.
15. Bryant, R.A., Kemp, A.H., Felmingham, K.L., Liddell, B., Olivieri, G., Peduto, A., Gordon, E., & Williams, L.M. (2008). Enhanced amygdala and medial prefrontal activation during nonconscious processing of fear in posttraumatic stress disorder: an fMRI study. Human Brain Mapping, 29, 517-523.
16. Campbell-Sills, L., Barlow, D.H., Brown, T.A., & Hofmann, S.G. (2006). Effects of suppression and acceptance on emotional responses of individuals with anxiety and mood disorders. Behavior Research and Therapy, 44, 1251-1263.
17. Carmichael, S.T., & Price, J.L. (1995). Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. Journal of Comparative Neurology, 363, 615-641.
18. Charney, D.S. (2003). Neuroanatomical circuits modulating fear and anxiety behaviors. Acta Psychiatrica Scandinavica Supplementum, 417, 38-50.
19. Charney, D.S., & Deutch, A. (1996). A functional neuroanatomy of anxiety and fear: implications for the pathophysiology and treatment of anxiety disorders. Critical Reviews in Neurobiology, 10, 419-446.
20. Chung, Y.A., Kim, S.H., Chung, S.K., Chae, J.H., Yang, D.W., Sohn, H.S., & Jeong, J. (2006). Alterations in cerebral perfusion in posttraumatic stress disorder patients without re-exposure to accident-related stimuli. Clinical Neurophysiology, 117, 637-642.
21. Cui, H., Sakamoto, H., Higashi, S., & Kawata, M. (2008). Effects of single-prolonged stress on neurons and their afferent inputs in the amygdala. Neuroscience, 152, 703-712.
22. Davidson, R.J., Putnam, K.M., & Larson, C.L. (2000). Dysfunction in the neural circuitry of emotion regulation: a possible prelude to violence. Science, 289, 591-594.
23. Delgado, M.R., Nearing, K.I., Ledoux, J.E., & Phelps, E.A. (2008). Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron, 59, 829-838.
24. Drevets, W.C., Videen, T.O., Price, J.L., Preskorn, S.H., Carmichael, S.T., & Raichle, M.E. (1992). A functional anatomical study of unipolar depression. Journal of Neuroscience, 12, 3628-3641.
25. Eippert, F., Veit, R., Weiskopf, N., Erb, M., Birbaumer, N., & Anders, S. (2007). Regulation of emotional responses elicited by threat-related stimuli. Human Brain Mapping, 28, 409-423.
26. Etkin, A., & Wager, T.D. (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specifc phobia. American Journal of Psychiatry, 164, 1476-1488.
27. Ghashghaei, H.T., Hilgetag, C.C., & Barbas, H. (2007). Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage, 34, 905-923.
28. Gilboa, A., Shalev, A.Y., Laor, L., Lester, H., Louzoun, Y., Chisin, R., & Bonne, O. (2004). Functional connectivity of the prefrontal cortex and the amygdala in posttraumatic stress disorder. Biological Psychiatry, 55, 263-272.
29. Gillath, O., Bunge, S.A., Shaver, P.R., Wendelken, C., & Mikulincer, M. (2005). Attachment-style differences in the ability to suppress negative thoughts: exploring the neural correlates. Neuroimage, 28, 835-847.
30. Gross, J.J. (1998). Antecedent- and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. Journal of Personality and Social Psychology, 74, 224-237.
31. Gross, J.J. (2002). Emotion regulation: affective, cognitive, and social consequences. Psychophysiology, 39, 281-291.
32. Hariri, A.R., Bookheimer, S.Y., & Mazziotta, J.C. (2000). Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport, 11, 43-48.
33. Hariri, A.R., Mattay, V.S., Tessitore, A., Fera, F., & Weinberger, D.R. (2003). Neocortical modulation of the amygdala response to fearful stimuli. Biological Psychiatry, 53, 494-501.
34. Hartley, C.A., & Phelps, E.A. (2010). Changing fear: the neurocircuitry of emotion regulation. Neuropsychopharmacology, 35, 136-146.
35. Hendler, T., Rotshtein, P., Yeshurun, Y., Weizmann, T., Kahn, I., Ben-Bashat D, Malach, R., & Bleich, A. (2003). Sensing the invisible: differential sensitivity of visual cortex and amygdala to traumatic context. Neuroimage, 19, 587-600.
36. Jackson, D.C., Mueller, C.J., Dolski, I., Dalton, K.M., Nitschke, J.B., Urry, H.L., Davidson, R.J. (2003). Now you feel it, now you don't: frontal brain electrical asymmetry and individual differences in emotion regulation. Psychological Science, 14, 612-617.
37. Johnstone, T., van Reekum, C.M., Urry, H.L., Kalin, N.H., & Davidson, R.J. (2007). Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience, 27, 8877-8884.
38. Jovanovic T., & Ressler K.J. (2010). How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. American Journal of Psychiatry, 167, 648-662.
39. Juruena, M.F., Giampietro, V.P., Smith, S.D., Surguladze, S.A., Dalton, J.A., Benson, P.J., Cleare, A.J., & Fu, C.H.Y. (2010). Amygdala activation to masked happy facial expressions. Journal of the International Neuropsychological Society, 16, 383-387.
40. Koenigs, M., & Grafman, J. (2009). Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala. Neuroscientist, 15, 540-548.
41. Koenigs, M., Huey, E.D., Raymont, V., Cheon, B., Solomon, J., Wassermann, E.M., & Grafman, J. (2008). Focal brain damage protects against post-traumatic stress disorder in combat veterans. Nature Neuroscience, 11, 232-237.
42. Lang, P.J., Bradley, M.M., & Cuthbert, B.N. (1999). International affective picture system (IAPS): instruction manual and affective ratings. Bethesda, MD: NIMH Center for the Study of Emotion and Attention.
43. Lanius, R.A., Williamson, P.C., Densmore, M., Boksman, K., Gupta, M.A., Neufeld, R.W., Gati, J.S., Menon, R.S. (2001). Neural correlates of traumatic memories in posttraumatic stress disorder: a functional MRI investigation. American Journal of Psychiatry, 158, 1920-1922.
44. Lanius, R.A., Williamson, P.C., Hopper, J., Densmore, M., Boksman, K., Gupta, M.A., Neufeld, R.W., Gati, J.S., & Menon, R.S. (2003). Recall of emotional states in posttraumatic stress disorder: an fMRI investigation. Biological Psychiatry, 53, 204-210.
45. Lanius, R.A., Williamson, P.C., Densmore, M., Boksman, K., Neufeld, R.W., Gati, J.S., & Menon, R.S. (2004). The nature of traumatic memories: a 4-T fMRI functional connectivity analysis. American Journal of Psychiatry, 161, 36-44.
46. Lanius, R.A., Vermetten, E., Loewenstein, R.J., Brand, B., Schmal, C., Bremner, D.J., & Spiegel, D. (2010). A dissociative subtype of PTSD: clinical and neurobiological evidence for a dissociative subtype. American Journal of Psychiatry, 167, 640-647.
47. Levesque, J., Eugene, F., Joanette, Y., Paquette, V., Mensour, B., Beaudoin, G., Beauregard, M. (2003). Neural circuitry underlying voluntary suppression of sadness. Biological Psychiatry, 53, 502-510.
48. Levesque, J., Joanette, Y., Mensour, B., Beaudoin, G., Leroux, J.M., Bourgouin, P., & Beauregard, M. (2004). Neural basis of emotional self-regulation in childhood. Neuroscience, 129, 361-369.
49. Liberzon, I., Taylor, S.F., Amdur, R., Jung, T.D., Chamberlain, K.R., Minoshima, S., Koeppe, R.A, & Figure, L.M. (1999). Brain activation in PTSD in response to trauma-related stimuli. Biological Psychiatry, 45, 817-826.
50. Likhtik, E., Pelletier, J.G., Paz, R., & Paré, D. (2005). Prefrontal control of the amygdala. Journal of Neuroscience, 25, 7429-7437.
51. Lindauer, R.J., Booij, J., Habraken, J.B., Uylings, H.B., Olff, M., Carlier, I.V., Gersons, B.P.R. (2004). Cerebral blood fow changes during script-driven imagery in police offcers with posttraumatic stress disorder. Biological Psychiatry, 56, 853- 861.
52. Lopes, P.N., Salovey, P., Cote, S., & Beers, M. (2005). Emotion regulation abilities and the quality of social interaction. Emotion, 5, 113-118.
53. Mauss, I.B., Evers, C., Wilhelm, F.H., Gross, J.J. (2006). How to bite your tongue without blowing your top: implicit evaluation of emotion regulation predicts affective responding to anger provocation. Personality and Social Psychology Bulletin, 32, 589-602.
54. Mauss, I.B., Wilhelm, F.H., & Gross, J.J. (2003). Autonomic recovery and habituation in social anxiety. Psychophysiology, 40, 648-653.
55. McDonald, A.J. (1998). Cortical pathways to the mammalian amygdala. Progress in Neurobiology, 55, 257-332.
56. Milad, M.R., Rauch, S.L., Pitman, R.K., & Quirk, G.J. (2006). Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biological Psychology, 73, 61-71.
57. Milad, M.R., Pitman, R.K., Ellis, C.B., Gold, A.L., Shin, L.M., Lasko, N.B., Rauch, S.L. (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry, 66, 1075-1082.
58. Mocaiber, I., Pereira, M.G., Erthal, F.S., Figueira, I., Machado-Pinheiro, W., Cagy, M., Volchan, E., & Oliveira, L. (2009). Regulation of negative emotions in high trait anxious individuals: an ERP study. Psychology and Neuroscience, 2, 211-217.
59. Mocaiber, I., Pereira, M.G., Erthal, F.S., Machado-Pinheiro, W., David, I.A., Cagy, M., Volchan, E., & de Oliveira, L. (2010). Fact or fction? An event-related potential study of implicit emotion regulation. Neuroscience Letters, 476, 84-88.
60. Morey, R.A., Petty, C.M., Cooper, D.A., Labar, K.S., & McCarthy, G. (2008). Neural systems for executive and emotional processing are modulated by symptoms of posttraumatic stress disorder in Iraq War veterans. Psychiatry Research, 162, 59-72.
61. Morgan, M.A., Romanski, L.M., & LeDoux, J.E. (1993). Extinction of emotional learning: contribution of medial prefrontal cortex. Neuroscience Letters, 163, 109-113.
62. Morgan, M.A., & LeDoux, J.E. (1999). Contribution of ventrolateral prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Neurobiology of Learning and Memory, 72, 244-251.
63. Ochsner, K.N., Bunge, S.A., Gross, J.J., & Gabrieli, J.D. (2002). Rethinking feelings: an fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14, 1215-1229.
64. Ochsner, K.N., Ray, R.D., Cooper, J.C., Robertson, E.R., Chopra, S., Gabrieli, J.D., & Gross, J.J. (2004). For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. Neuroimage, 23, 483-499.
65. Ochsner, K.N., & Gross, J.J. (2005). The cognitive control of emotion. Trends in Cognitive Sciences, 9, 242-249.
66. Ohira, H., Nomura, M., Ichikawa, N., Isowa, T., Iidaka, T., Sato, A., Fukuyama, S., Nakajima, T., & Yamada, J. (2006). Association of neural and physiological responses during voluntary emotion suppression. Neuroimage, 29, 721-733.
67. Oliveira, L.A., Oliveira, L., Joffly, M., Pereira-Junior, P.P., Lang, P.J., Pereira, M.G., Figueira, I., & Volchan, E. (2009). Autonomic reactions to mutilation pictures: positive affect facilitates safety signal processing. Psychophysiology, 46, 870-873.
68. Orr, S.P., Metzger, L.J., Lasko, N.B., Macklin, M.L., Peri, T., & Pitman, R.K. (2000). De novo conditioning in trauma-exposed individuals with and without posttraumatic stress disorder. Journal of Abnormal Psychology, 109, 290-298.
69. Peri, T., Ben-Shakhar, G., Orr, S.P., & Shalev, A.Y. (2000). Psychophysiologic assessment of aversive conditioning in posttraumatic stress disorder. Biological Psychiatry, 47, 512-519.
70. Phan, K.L., Fitzgerald, D.A., Nathan, P.J., Moore, G.J., Uhde, T.W., & Tancer, M.E. (2005). Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biological Psychiatry, 57, 210-219.
71. Phan, K.L., Britton, J.C., Taylor, S.F., Figure, L.M., & Liberzon, I. (2006). Corticolimbic blood fow during nontraumatic emotional processing in posttraumatic stress disorder. Archives of General Psychiatry, 63, 184-192.
72. Pissiota, A., Frans, O., Fernandez, M., Vo n Knorring, L., Fischer, H., & Fredrikson, M. (2002). Neurofunctional correlates of posttraumatic stress disorder: a PET symptom provocation study. European Archives of Psychiatry and Clinical Neuroscience, 252, 68-75.
73. Pitman, R.K. (1989). Post-traumatic stress disorder, hormones, and memory. Biological Psychiatry, 26, 221-223.
74. Price, J.L. (2005). Free will versus survival: brain systems that underlie intrinsic constraints on behavior. Journal of Comparative Neurology, 493, 132-139.
75. Protopopescu, X., Pan, H., Tuescher, O., Cloitre, M., Goldstein, M., Engelien, W., Stern, E. (2005). Differential time courses and specifcity of amygdala activity in posttraumatic stress disorder subjects and normal control subjects. Biological Psychiatry, 57, 464-473.
76. Quirk, G.J., Likhtik, E., Pelletier, J.G., & Paré, D. (2003). Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. Journal of Neuroscience, 23, 8800-8807.
77. Rauch, S.L., van der Kolk, B.A., Fisler, R.E., Alpert, N.M, Orr, S.P., Savage, C.R., Pitman, R.K. (1996). A symptom provocation study of posttraumatic stress disorder using positron emission tomography and script-driven imagery. Archives of General Psychiatry, 53, 380-387.
78. Rauch, S.L., Whalen, P.J., Shin, L.M., McInerney, S., Macklin, M.L., Lasko, N.B., Orr, S.P., & Pitman, R.K. (2000). Exaggerated amygdala responses to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biological Psychiatry, 47, 769-776.
79. Rauch, S.L., Shin, L.M., & Phelps, E.A. (2006). Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research-past, present, and future. Biological Psychiatry, 60, 376-382.
80. Ray, R.D., Ochsner, K.N., Cooper, J.C., Robertson, E.R., Gabrieli, J.D., & Gross, J.J. (2005). Individual differences in trait rumination and the neural systems supporting cognitive reappraisal. Cognitive, Affective and Behavioral Neuroscience, 5, 156-168.
81. Schaefer, S.M., Jackson, D.C., Davidson, R.J., Aguirre, G.K., Kimberg, D.Y., Thompson-Schill, S.L. (2002). Modulation of amygdalar activity by the conscious regulation of negative emotion. Journal of Cognitive Neuroscience, 14, 913-921.
82. Schiller, D., Levy, I., Niv, Y., LeDoux, J.E., & Phelps, E.A. (2008). From fear to safety and back: reversal of fear in the human brain. Journal of Neuroscience, 28, 11517-11525.
83. Shin, L.M., Kosslyn, S.M., McNally, R.J., Alpert, N.M., Thompson, W.L., Rauch, S.L., Macklin, M.L., & Pitman, R.K. (1997). Visual imagery and perception in posttraumatic stress disorder: a positron emission tomographic investigation. Archives of General Psychiatry, 54, 233-241.
84. Shin, L.M., McNally, R.J., Kosslyn, S.M., Thompson, W.L., Rauch, S.L., Alpert, N.M., Pitman, R.K. (1999). Regional cerebral blood fow during script-driven imagery in childhood sexual abuse-related PTSD: a PET investigation. American Journal of Psychiatry, 156, 575-584.
85. Shin, L.M., Whalen, P.J., Pitman, R.K., Bush, G., Macklin, M.L., Lasko, N.B., Rauch, S.L. (2001). An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biological Psychiatry, 50, 932-942.
86. Shin, L.M., Orr, S.P., Carson, M.A., Rauch, S.L., Macklin, M.L., Lasko, N.B., Pitman, R.K. (2004). Regional cerebral blood fow in amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Archives of General Psychiatry, 61, 168-176.
87. Shin, L.M., Shin, P.S., Heckers, S., Krangel, T.S., Macklin, M.L., Orr, S.P., Lasko, N., Rauch, S.L. (2004). Hippocampal function in posttraumatic stress disorder. Hippocampus, 14, 292-300.
88. Shin, L.M., Wright, C.I., Cannistraro, P.A., Wedig, M.M., McMullin, K., Martis, B., Rauch, S.L. (2005). A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Archives of General Psychiatry, 62, 273-281.
89. Shin, L.M., & Handwerger, K. (2009). Is posttraumatic stress disorder a stress-induced fear circuitry disorder? Journal of Traumatic Stress, 22, 409-415.
90. Smith, S.D., Abou-Khalil, B., & Zald, D.H. (2008). Posttraumatic stress disorder in a patient with no left amygdala. Journal of Abnormal Psychology, 117, 479-484.
91. Sotres-Bayon, F., Cain, C.K., & LeDoux, J.E. (2006). Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biological Psychiatry, 60, 329-336.
92. Stefanacci, L., & Amaral, D.G. (2002). Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. Journal of Comparative Neurology, 451, 301-323.
93. Stroop, J.R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643-662.
94. Urry, H.L., van Reekum, C.M., Johnstone, T., Kalin, N.H., Thurow, M.E., Schaefer, H.S., Davidson, R.J. (2006). Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience, 26, 4415-4425.
95. Vermetten, E., Schmahl, C., Southwick, S.M., & Bremner, J.D. (2007). Positron tomographic emission study of olfactory induced emotional recall in veterans with and without combat-related posttraumatic stress disorder. Psychopharmacology Bulletin, 40, 8-30.
96. Weiss, S.J. (2007). Neurobiological alterations associated with traumatic stress. Perspectives in Psychiatric Care, 43, 114-122.
97. Wessa, M., & Flor, H. (2007). Failure of extinction of fear responses in posttraumatic stress disorder: evidence from second-order conditioning. American Journal of Psychiatry, 164, 1684-1692.
98. Williams, L.M., Kemp, A.H., Felmingham, K., Barton, M., Olivieri, G., Peduto, A., Gordon, E., & Bryant, R.A. (2006). Trauma modulates amygdala and medial prefrontal responses to consciously attended fear. Neuroimage, 29, 347-357.
99. Yang, P., Wu, M.T., Hsu, C.C., & Ker, J.H. (2004). Evidence of early neurobiological alternations in adolescents with posttraumatic stress disorder: a functional MRI study. Neuroscience Letters, 370, 13-18.
100. Yehuda, R., & Ledoux, J. (2007). Response variation following trauma: a translational neuroscience approach to understand PTSD. Neuron, 56, 19-32.
101. Zubieta, J.K., Chinitz, J.A., Lombardi, U., Figure, L.M., Cameron, O.G., & Liberzon, I. (1999). Medial frontal cortex involvement in PTSD symptoms: a SPECT study. Journal of Psychiatric Research, 33, 259-264.