Post-traumatic stress influences the brain even in the absence of symptoms: A systematic, quantitative meta-analysis of neuroimaging studies

Neuroscience and Biobehavioral Reviews

Volumn 56, Issue , 2015, Pages 207-221

  Stark, E A ^a,b   Parsons, C E ^a,b   Van Hartevelt, T J ^a,b   Charquero Ballester, M ^a,b   McManners, H ^a   Ehlers, A ^a   Stein, A ^a   Kringelbach, M L ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Activation likelihood estimation; Basal ganglia; FMRI; Meta analysis; Neuroimaging; OFC; Precuneus; PTSD; Trauma; Whole brain network activity

Indexed keywords

AMYGDALOID NUCLEUS; ANTERIOR INSULA; BASAL GANGLION; BRAIN FUNCTION; CINGULATE GYRUS; DISEASE COURSE; ELECTROENCEPHALOGRAM; EMOTIONALITY; FUNCTIONAL ANATOMY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL STATUS; HUMAN; IMAGE ANALYSIS; MENTAL DISEASE ASSESSMENT; META ANALYSIS; NERVE CELL NETWORK; NEUROIMAGING; ORBITAL CORTEX; PARAHIPPOCAMPAL GYRUS; POSTTRAUMATIC STRESS DISORDER; PRECUNEUS; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW; TASK PERFORMANCE; VENTROMEDIAL PREFRONTAL CORTEX; BRAIN; PATHOLOGY; PATHOPHYSIOLOGY;

BRAIN; HUMANS; NEUROIMAGING; STRESS DISORDERS, POST-TRAUMATIC;

EID: 84938077269     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2015.07.007     Document Type: Review

References (100)

1. Admon R., Milad M.R., Hendler T. A causal model of post-traumatic stress disorder: disentangling predisposed from acquired neural abnormalities. Trends Cogn. Sci. 2013, 17(7):337-347. 10.1016/j.tics.2013.05.005.
2. Adolphs R. Neural systems for recognizing emotion. Curr. Opin. Neurobiol. 2002, 12(2):169-177.
3. Anda R.F., Felitti V.J., Bremner J.D., Walker J.D., Whitfield C.H., Perry B.D., Dube S.R., Giles W.H. The enduring effects of abuse and related adverse experiences in childhood. Eur. Arch. Psychiatry Clin. Neurosci. 2006, 256(3):174-186.
4. American Psychiatric Association (APA) Diagnostic and Statistical Manual of Mental Disorders DSM 2003, 2000. 4th ed. (text revision).
5. American Psychiatric Association (APA) Diagnostic and Statistical Manual of Mental Disorders DSM 2013, 5th ed.
6. Astur R.S., St.Germain S.A., Tolin D., Ford J., Russell D., Stevens M. Hippocampus function predicts severity of post-traumatic stress disorder. Cyberpsychol. Behav. 2006, 9(2):234-240.
7. Aupperle R.L., Allard C.B., Grimes E.M., Simmons A.N., Flagan T., Behrooznia M., Cissell S.H., Twamley E.W., Thorp S.R., Norman S.B., Paulus M.P., Stein M.B. Dorsolateral prefrontal cortex activation during emotional anticipation and neuropsychological performance in posttraumatic stress disorder. Arch. Gen. Psychiatry 2012, 69(4):360-371.
8. Barrett L.F., Satpute A.B. Large-scale brain networks in affective and social neuroscience: towards an integrative functional architecture of the brain. Curr. Opin. Neurobiol. 2013, 23(3):361-372.
9. Bazarian J.J., Donnelly K., Peterson D.R., Warner G.C., Zhu T., Zhong J. The relation between posttraumatic stress disorder and mild traumatic brain injury acquired during operations enduring freedom and Iraqi freedom. J. Head Trauma Rehabil. 2013, 28(1):1-12.
10. Berridge K.C., Kringelbach M.L. Neuroscience of affect: brain mechanisms of pleasure and displeasure. Curr. Opin. Neurobiol. 2013, 23(3):294-303.
11. Bluhm R.L., Frewen P.A., Coupland N.C., Densmore M., Schore A.N., Lanius R.A. Neural correlates of self-reflection in post-traumatic stress disorder. Acta Psychiatr. Scand. 2012, 125(3):238-246.
12. 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(7):973-981.
13. Breslau N., Kessler R.C., Chilcoat H.D., Schultz L.R., Davis G.C., Andreski P. Trauma and posttraumatic stress disorder in the community: the 1996 Detroit area survey of trauma. Arch. Gen. Psychiatry 1998, 55(7):626-632. 10.1001/archpsyc.55.7.626.
14. 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(11):1023-1030.
15. Bruce S.E., Buchholz K.R., Brown W.J., Yan L., Durbin A., Sheline Y.I. Altered emotional interference processing in the amygdala and insula in women with post-traumatic stress disorder. NeuroImage 2013, 2(1):43-49. (Clinical).
16. Brunetti M., Sepede G., Mingoia G., Catani C., Ferretti A., Merla A., Del Gratta C., Romani G.L., Babiloni C. Elevated response of human amygdala to neutral stimuli in mild post traumatic stress disorder: neural correlates of generalized emotional response. Neuroscience 2010, 168(3):670-679.
17. Bryant R.A., Felmingham K.L., Kemp A.H., Barton M., Peduto A.S., Rennie C., Gordon E., Williams L.M. Neural networks of information processing in posttraumatic stress disorder: a functional magnetic resonance imaging study. Biol. Psychiatry 2005, 58(2):111-118. http://dx.doi.org/10.1016/j.biopsych.2005.03.021.
18. Bryant R.A., Kemp A., Felmingham K., Liddell B., Olivieri G., Peduto A., Gordon E., Williams L.M. Simulating emotional responses in posttraumatic stress disorder: an fMRI study. Psychol. Inj. Law 2010, 3(2):111-117.
19. Bryant R.A., Kemp A.H., Felmingham K.L., Liddell B., Olivieri G., Peduto A., Gordon E., Williams L.M. Enhanced amygdala and medial prefrontal activation during nonconscious processing of fear in posttraumatic stress disorder: an fMRI study. Hum. Brain Mapp. 2008, 29(5):517-523. 10.1002/hbm.20415.
20. Cabral J., Kringelbach M.L., Deco G. Exploring the network dynamics underlying brain activity during rest. Prog. Neurobiol. 2014, 114:102-131.
21. Cerqueira J.J., Mailliet F., Almeida O.F.X., Jay T.M., Sousa N. The prefrontal cortex as a key target of the maladaptive response to stress. J. Neurosci. 2007, 27(11):2781-2787.
22. Deco G., Jirsa V.K., McIntosh A.R. Resting brains never rest: computational insights into potential cognitive architectures. Trends Neurosci. 2013, 36(5):268-274.
23. Deco G., Kringelbach M.L. Great expectations: using whole-brain computational connectomics for understanding neuropsychiatric disorders. Neuron 2014, 84(5):892-905. 10.1016/j.neuron.2014.08.034.
24. Diener S.J., Wessa M., Ridder S., Lang S., Diers M., Steil R., Flor H. Enhanced stress analgesia to a cognitively demanding task in patients with posttraumatic stress disorder. J. Affect. Disord. 2012, 136(3):1247-1251.
25. Duvernoy H.M., Cabanis E.A., Bourgouin P. The Human Brain: Surface, Three-dimensional Sectional Anatomy and MRI 1991, Springer Verlag, Wien.
26. Eickhoff S.B., Laird A.R., Grefkes C., Wang L.E., Zilles K., Fox P.T. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: A random-effects approach based on empirical estimates of spatial uncertainty. Hum. Brain Mapp. 2009, 30(9):2907-2926.
27. 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 2011, 49(7):1969-1973.
28. Elman I., Lowen S., Frederick B.B., Chi W., Becerra L., Pitman R.K. Functional neuroimaging of reward circuitry responsivity to monetary gains and losses in posttraumatic stress disorder. Biol. Psychiatry 2009, 66(12):1083-1090. 10.1016/j.biopsych.2009.06.006.
29. 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(10):1476-1488.
30. Falconer E., Bryant R., Felmingham K.L., Kemp A.H., Gordon E., Peduto A., Williams L.M. The neural networks of inhibitory control in posttraumatic stress disorder. J. Psychiatry Neurosci. 2008, 33(5):413-422.
31. Felmingham K.L., Falconer E.M., Williams L., Kemp A.H., Allen A., Peduto A., Bryant R.A. Reduced amygdala and ventral striatal activity to happy faces in PTSD is associated with emotional numbing. PLoS ONE 2014, 9(9):e103653. 10.1371/journal.pone.0103653.
32. Felmingham K.L., Williams L.M., Kemp A.H., Liddell B., Falconer E., Peduto A., Bryant R. Neural Responses to masked fear faces: sex differences and trauma exposure in posttraumatic stress disorder. J. Abnormal Psychol. 2010, 119(1):241-247.
33. Felmingham K.L., Williams L.M., Kemp A.H., Rennie C., Gordon E., Bryant R.A. Anterior cingulate activity to salient stimuli is modulated by autonomic arousal in posttraumatic stress disorder. Psychiatry Res.-Neuroimag. 2009, 173(1):59-62.
34. Foa E.B., Ehlers A., Clark D.M., Tolin D.F., Orsillo S.M. The posttraumatic cognitions inventory (PTCI): development and validation. Psychol. Assess. 1999, 11(3):303.
35. Fonzo G.A., Simmons A.N., Thorp S.R., Norman S.B., Paulus M.P., Stein M.B. Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biol. Psychiatry 2010, 68(5):433-441. 10.1016/j.biopsych.2010.04.028.
36. Frewen P.A., Dozois D.J.A., Neufeld R.W.J., Densmore M., Stevens T.K., Lanius R.A. Social emotions and emotional valence during imagery in women with PTSD: affective and neural correlates. Psychol. Trauma 2010, 2(2):145-157. (Theory, Research, Practice, and Policy).
37. Frewen P.A., Dozois D.J.A., Neufeld R.W.J., Lane R.D., Densmore M., Stevens T.K., Lanius R.A. Emotional numbing in posttraumatic stress disorder: a functional magnetic resonance imaging study. J. Clin. Psychiatry 2012, 73(4):431-436. 10.4088/jcp.10m06477.
38. 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. J. Neurosci. 2014, 34(40):13435-13443. 10.1523/jneurosci.4287-13.2014.
39. Geuze E., Vermetten E., Ruf M., de Kloet C.S., Westenberg H.G.M. Neural correlates of associative learning and memory in veterans with posttraumatic stress disorder. J. Psychiatr. Res. 2008, 42(8):659-669.
40. Geuze E., Westenberg H.M., Jochims A., et al. ALtered pain processing in veterans with posttraumatic stress disorder. Arch. Gen. Psychiatry 2007, 64(1):76-85. 10.1001/archpsyc.64.1.76.
41. Hayes J., Hayes S., Mikedis A. Quantitative meta-analysis of neural activity in posttraumatic stress disorder. Biol. Mood Anxiety Disord. 2012, 2(1):9.
42. Hou C., Liu J., Wang K., Li L., Liang M., He Z., Liu Y., Zhang Y., Li W., Jiang T. Brain responses to symptom provocation and trauma-related short-term memory recall in coal mining accident survivors with acute severe PTSD. Brain Res. 2007, 1144(1):165-174.
43. Jatzko A., Schmitt A., Demirakca T., Weimer E., Braus D.F. Disturbance in the neural circuitry underlying positive emotional processing in post-traumatic stress disorder (PTSD): an fMRI study. Eur. Arch. Psychiatry Clin. Neurosci. 2006, 256(2):112-114.
44. Killgore W.D.S., Britton J.C., Schwab Z.J., Price L.M., Weiner M.R., Gold A.L., Rosso I.M., Simon N.M., Pollack M.H., Rauch S.L. Cortico-limbic responses to masked affective faces across ptsd, panic disorder, and specific phobia. Depress. Anxiety 2014, 31(2):150-159.
45. Kim M.J., Chey J., Chung A., Bae S., Khang H., Ham B., Yoon S.J., Jeong D.U., Lyoo I.K. Diminished rostral anterior cingulate activity in response to threat-related events in posttraumatic stress disorder. J. Psychiatr. Res. 2008, 42(4):268-277.
46. Landré L., Destrieux C., Andersson F., Barantin L., Quidé Y., Tapia G., Jaafari N., Clarys D., Gaillard P., Isingrini M., El-Hage W. Working memory processing of traumatic material in women with posttraumatic stress disorder. J. Psychiatry Neurosci. 2012, 37(2):87-94.
47. 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.-Neuroimag. 2007, 155(1):45-56.
48. Lanius R.A., Williamson P.C., Densmore M., Boksman K., Gupta M.A., Neufeld R.W., Gati J.S., Menon R.S. Neural correlates of traumatic memories in posttraumatic stress disorder: A functional MRI investigation. Am. J. Psychiatry 2001, 158(11):1920-1922.
49. 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 2003, 53(3):204-210.
50. Liberzon I., Sripada C.S. The functional neuroanatomy of PTSD: a critical review. Prog. Brain Res. 2007, 167:151-169.
51. Linnman C., Zeffiro T.A., Pitman R.K., Milad M.R. An fMRI study of unconditioned responses in post-traumatic stress disorder. Biol. Mood Anxiety Disord. 2011, 1(8):1-12.
52. Mazza M., Catalucci A., Mariano M., Pino M.C., Tripaldi S., Roncone R., Gallucci M. Neural correlates of automatic perceptual sensitivity to facial affect in posttraumatic stress disorder subjects who survived L'Aquila earthquake of April 6, 2009. Brain Imag. Behav. 2012, 6(3):374-386.
53. Mazza M., Tempesta D., Pino M.C., Catalucci A., Gallucci M., Ferrara M. Regional cerebral changes and functional connectivity during the observation of negative emotional stimuli in subjects with post-traumatic stress disorder. Eur. Arch. Psychiatry Clin. Neurosci. 2013, 263(7):575-583.
54. McEwen B.S. Stressed or stressed out: what is the difference?. J. Psychiatry Neurosci.: JPN 2005, 30(5):315-318.
55. McEwen B.S. Protective and damaging effects of stress mediators: central role of the brain. Dialog. Clin. Neurosci. 2006, 8(4):367-381.
56. McFarlane A.C., Papay P. Multiple diagnoses in posttraumatic stress disorder in the victims of a natural disaster. J. Nervous Mental Dis. 1992, 180(8):498-504. 10.1097/00005053-199208000-00004.
57. Menon V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn. Sci. 2011, 15(10):483-506. 10.1016/j.tics.2011.08.003.
58. Mickleborough M.J.S., Daniels J.K., Coupland N.J., Kao R., Williamson P.C., Lanius U.F., Hegadoren K., Schore A., Densmore M., Stevens T., Lanius R.A. Effects of trauma-related cues on pain processing in posttraumatic stress disorder: an fMRI investigation. J. Psychiatry Neurosci. 2011, 36(1):6-14.
59. 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(12):1075-1082.
60. Offringa R., Brohawn K.H., Staples L.K., Dubois S.J., Hughes K.C., Pfaff D.L., VanElzakker M.B., Davis F.C., Shin L.M., Haber S.N. Diminished rostral anterior cingulate cortex activation during trauma-unrelated emotional interference in PTSD. Biol. Mood Anxiety Dis. 2013, 3(1):10.
61. Papageorgiou V., Frangou-Garunovic A., Iordanidou R., Yule W., Smith P., Vostanis P. War trauma and psychopathology in Bosnian refugee children. Eur. Child Adolesc. Psychiatry 2000, 9(2):84-90.
62. Patel R., Spreng R.N., Shin L.M., Girard T.A. Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 2012, 36(9):2130-2142.
63. Payne J., Jackson E., Ryan L., Hoscheidt S., Jacobs J., Nadel L. The impact of stress on neutral and emotional aspects of episodic memory. Memory 2006, 14(1):1-16.
64. Pitman R.K. Post-traumatic stress disorder, hormones, and memory. Biol. Psychiatry 1989, 26(3):221-223. http://dx.doi.org/10.1016/0006-3223(89)90033-4.
65. Preis M.A., Schmidt-Samoa C., Dechent P., Kroener-Herwig B. The effects of prior pain experience on neural correlates of empathy for pain: an fMRI study. Pain 2013, 154(3):411-418. 10.1016/j.pain.2012.11.014.
66. Protopopescu X., Pan H., Tuescher O., Cloitre M., Goldstein M., Engelien W., Epstein J., Yang Y., Gorman J., LeDoux J., Silbersweig D., Stern E. Differential time courses and specificity of amygdala activity in posttraumatic stress disorder subjects and normal control subjects. Biol. Psychiatry 2005, 57(5):464-473.
67. Qin S., Hermans E.J., van Marle H.J.F., Fernández G. Understanding low reliability of memories for neutral information encoded under stress: alterations in memory-related activation in the hippocampus and midbrain. J. Neurosci. 2012, 32(12):4032-4041.
68. 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(4):376-382.
69. 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 2000, 47(9):769-776.
70. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat. Rev. Neurosci. 2009, 10(6):423-433.
71. Rothbaum B.O., Davis M. Applying learning principles to the treatment of post-trauma reactions. Ann. N.Y. Acad. Sci. 2003, 1008(1):112-121.
72. Rougemont-Bücking 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. Therap. 2011, 17(4):227-236.
73. Russo S.J., Murrough J.W., Han M.H., Charney D.S., Nestler E.J. Neurobiology of resilience. Nat. Neurosci. 2012, 15(11):1475-1484. 10.1038/nn.3234.
74. Rytwinski N.K., Scur M.D., Feeny N.C., Youngstrom E.A. The co-occurrence of major depressive disorder among individuals with posttraumatic stress disorder: a meta-analysis. J. Traum. Stress 2013, 26(3):299-309. 10.1002/jts.21814.
75. Sailer U., Robinson S., Fischmeister F.P.S., König D., Oppenauer C., Lueger-Schuster B., Moser E., Kryspin-Exner I., Bauer H. Altered reward processing in the nucleus accumbens and mesial prefrontal cortex of patients with posttraumatic stress disorder. Neuropsychologia 2008, 46(11):2836-2844.
76. Sakamoto H., Fukuda R., Okuaki T., Rogers M., Kasai K., Machida T., Shirouzu I., Yamasue H., Akiyama T., Kato N. Parahippocampal activation evoked by masked traumatic images in posttraumatic stress disorder: a functional MRI study. NeuroImage 2005, 26(3):813-821.
77. Sartory G., Cwik J., Knuppertz H., Schürholt B., Lebens M., Seitz R.J., Schulze R. In search of the trauma memory: a meta-analysis of functional neuroimaging studies of symptom provocation in posttraumatic stress disorder (PTSD). PLoS ONE 2013, 8(3).
78. Schechter D.S., Moser D.A., Wang Z., Marsh R., Hao X., Duan Y., Yu S., Gunter B., Murphy D., McCaw J., Kangarlu A., Willheim E., Myers M.M., Hofer M.A., Peterson B.S. An fMRI study of the brain responses of traumatized mothers to viewing their toddlers during separation and play. Soc. Cogn. Affect. Neurosci. 2012, 7(8):969-979.
79. Schwabe L., Jowabe, Roozendaal B., Wolf O.T., Oitzl M.S. Stress effects on memory: an update and integration. Neurosci. Biobehav. Rev. 2012, 36(7):1740-1749.
80. Shin L.M., Rauch S.L., Pitman R.K. Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann. N.Y. Acad. Sci. 2006, 1071(1):67-79.
81. Shin L.M., Whalen P.J., Pitman R.K., Bush G., Macklin M.L., Lasko N.B., Orr S.P., McInerney S.C., Rauch S.L. An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biol. Psychiatry 2001, 50(12):932-942.
82. 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 2005, 62(3):273-281.
83. Shonkoff J.P., Garner A.S., The Committee on Psychosocial Aspects of Child and Family Health, Committee on Early Childhood, Adoption, and Dependent Care, Section on Developmental and Behavioral Pediatrics, Siegel B.S., Dobbins M.I., Earls M.F., Garner A.S., McGuinn L., Pascoe J., Wood D.L. The lifelong effects of early childhood adversity and toxic stress. Pediatrics 2012, 129(1):e232-e246.
84. Simmons A.N., Flagan T.M., Wittmann M., Strigo I.A., Matthews S.C., Donovan H., Lohr J.B., Paulus M.P. The effects of temporal unpredictability in anticipation of negative events in combat veterans with PTSD. J. Affect. Disord. 2013, 146(3):426-432.
85. Simmons A.N., Matthews S.C. Neural circuitry of PTSD with or without mild traumatic brain injury: a meta-analysis. Neuropharmacology 2012, 62(2):598-606.
86. Simmons A.N., Paulus M.P., Thorp S.R., Matthews S.C., Norman S.B., Stein M.B. Functional activation and neural networks in women with posttraumatic stress disorder related to intimate partner violence. Biol. Psychiatry 2008, 64(8):681-690.
87. Simmons A.N., Strigo I.A., Matthews S.C., Paulus M.P., Stein M.B. Initial evidence of a failure to activate right anterior insula during affective set-shifting in PTSD. Psychosomatic Med. 2009, 71(4):373.
88. Southwick S.M., Bremner J.D., Rasmusson A., Morgan Iii C.A., Arnsten A., Charney D.S. Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder. Biol. Psychiatry 1999, 46(9):1192-1204. http://dx.doi.org/10.1016/S0006-3223(99)00219-X.
89. Sripada R.K., King A.P., Welsh R.C., Garfinkel S.N., Wang X., Sripada C.S., Liberzon I. Neural dysregulation in posttraumatic stress disorder: evidence for disrupted equilibrium between salience and default mode brain networks. Psychosomatic Med. 2012, 74(9):904-911.
90. Steuwe C., Daniels J.K., Frewen P.A., Densmore M., Pannasch S., Beblo T., Reiss J., Lanius R.A. Effect of direct eye contact in PTSD related to interpersonal trauma: an fMRI study of activation of an innate alarm system. Soc. Cognit. Affect. Neurosci. 2014, 9(1):88-97.
91. Strigo I.A., Simmons A.N., Matthews S.C., Grimes E.M., Allard C.B., Reinhardt L.E., Paulus M.P., Stein M.B. Neural correlates of altered pain response in women with posttraumatic stress disorder from intimate partner violence. Biol. Psychiatry 2010, 68(5):442-450.
92. Sutker P.B., Winstead D.K., Galina Z.H., Allain A.N. Cognitive deficits and psychopathology among former prisoners of war and combat veterans of the Korean conflict. Am. J. Psychiatry 1991, 148(1):67-72.
93. Thomaes K., Dorrepaal E., Draijer N.P.J., de Ruiter M.B., Elzinga B.M., van Balkom A.J., Smoor P.L.M., Smit J.H., Veltman D.J. Increased activation of the left hippocampus region in complex PTSD during encoding and recognition of emotional words: a pilot study. Psychiatry Res.: Neuroimag. 2009, 171(1):44-53.
94. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 2002, 15(1):273-289. 10.1006/nimg.2001.0978.
95. van Rooij S.J., Rademaker A.R., Kennis M., Vink M., Kahn R.S., Geuze E. Neural correlates of trauma-unrelated emotional processing in war veterans with PTSD. Psychol. Med. 2014, 1-13. 10.1017/S0033291714001706.
96. van Wingen G.A., Geuze E., Caan M.W.A, Kozicz T., Olabarriaga S.D., Denys D., Vermetten E., Fernández G. Persistent and reversible consequences of combat stress on the mesofrontal circuit and cognition. Proc. Natl. Acad. Sci. 2012, 109(38):15508-15513.
97. 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(3):309-318.
98. Williams L.M., Kemp A.H., Felmingham K., Barton M., Olivieri G., Peduto A., Gordon E., Bryant R.A. Trauma modulates amygdala and medial prefrontal responses to consciously attended fear. NeuroImage 2006, 29(2):347-357.
99. Zhang D., Raichle M.E. Disease and the brain's dark energy. Nat. Rev. Neurol. 2010, 6(1):15-28.
100. Zhang J.N., Xiong K.L., Qiu M.G., Zhang Y., Xie B., Wang J., Li M., Chen H., Zhang Y., Zhang J.J. Negative emotional distraction on neural circuits for working memory in patients with posttraumatic stress disorder. Brain Res. 2013, 1531:94-101.