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Neural correlates of trauma-unrelated emotional processing in war veterans with PTSD

Published online by Cambridge University Press:  18 July 2014

S. J. H. van Rooij ,
A. R. Rademaker ,
M. Kennis ,
M. Vink ,
R. S. Kahn  and
E. Geuze
S. J. H. van Rooij*
Affiliation:
Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, The Netherlands Research Centre, Military Mental Healthcare, Ministry of Defence, The Netherlands
A. R. Rademaker
Affiliation:
Research Centre, Military Mental Healthcare, Ministry of Defence, The Netherlands
M. Kennis
Affiliation:
Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, The Netherlands Research Centre, Military Mental Healthcare, Ministry of Defence, The Netherlands
M. Vink
Affiliation:
Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, The Netherlands
R. S. Kahn
Affiliation:
Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, The Netherlands
E. Geuze
Affiliation:
Brain Center Rudolf Magnus, Department of Psychiatry, University Medical Center Utrecht, The Netherlands Research Centre, Military Mental Healthcare, Ministry of Defence, The Netherlands
*
*Address for correspondence: Drs S. J. H. van Rooij, Heidelberglaan 100 (HPN A01.1.46), 3584 CX Utrecht, The Netherlands. (Email: [email protected])
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Abstract

Background

Post-traumatic stress disorder (PTSD) is thought to be characterized by general heightened amygdala activation. However, this hypothesis is mainly based on specific studies presenting fear or trauma-related stimuli, hence, a thorough investigation of trauma-unrelated emotional processing in PTSD is needed.

Methods

In this study, 31 male medication-naive veterans with PTSD, 28 male control veterans (combat controls; CC) and 25 non-military men (healthy controls; HC) were included. Participants underwent functional MRI while trauma-unrelated neutral, negative and positive emotional pictures were presented. In addition to the group analyses, PTSD patients with and without major depressive disorder (MDD) were compared.

Results

All groups showed an increased amygdala response to negative and positive contrasts, but amygdala activation did not differ between groups. However, a heightened dorsal anterior cingulate cortex (dACC) response for negative contrasts was observed in PTSD patients compared to HC. The medial superior frontal gyrus was deactivated in the negative contrast in HC, but not in veterans. PTSD+MDD patients showed decreased subgenual ACC (sgACC) activation to all pictures compared to PTSD–MDD.

Conclusion

Our findings do not support the hypothesis that increased amygdala activation in PTSD generalizes to trauma-unrelated emotional processing. Instead, the increased dACC response found in PTSD patients implicates an attentional bias that extends to trauma-unrelated negative stimuli. Only HC showed decreased medial superior frontal gyrus activation. Finally, decreased sgACC activation was related to MDD status within the PTSD group.

Keywords

Amygdalaanterior cingulate cortex (ACC)emotional processingfunctional magnetic resonance imaging (fMRI)major depressive disorder (MDD)post-traumatic stress disorder (PTSD)
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 3 , February 2015 , pp. 575 - 587
Copyright
Copyright © Cambridge University Press 2014 

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References

APA (2013). Diagnostic and Statistical Manual of Mental Disorders (DSM-5). American Psychiatric Association: Washington, DC.Google Scholar
Aupperle, RL, Allard, CB, Grimes, EM, Simmons, AN, Flagan, T, Behrooznia, M, Cissell, SH, Twamley, EW, Thorp, SR, Norman, SB, Paulus, MP, Stein, MB (2012). Dorsolateral prefrontal cortex activation during emotional anticipation and neuropsychological performance in posttraumatic stress disorder. Archives of General Psychiatry 69, 360–371.Google ScholarPubMed
Aupperle, RL, Allard, CB, Grimes, EM, Simmons, AN, Flagan, T, Thorp, SR, Norman, SB, Paulus, MP, Stein, MB (2013). Neural responses during emotional processing before and after cognitive trauma therapy for battered women. Psychiatry Research: Neuroimaging 214, 48–55.CrossRefGoogle ScholarPubMed
Beckmann, M, Johansen-Berg, H, Rushworth, MFS (2009). Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. Journal of Neuroscience 29, 1175–1190.CrossRefGoogle ScholarPubMed
Blake, D, Weathers, F, Nagy, L, Kaloupek, D, Klauminzer, G, Charney, DA (1990). Clinician rating scale for assessing current and lifetime ptsd: the caps-1. Behavioral Therapy 13, 187–188.Google Scholar
Bremner, JD, Narayan, M, Staib, LH, Southwick, SM, Mcglashan, T, Charney, DS (1999 a). Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. American Journal of Psychiatry 156, 1787–1795.CrossRefGoogle ScholarPubMed
Bremner, JD, Staib, LH, Kaloupek, D, Southwick, SM, Soufer, R, Charney, DS (1999 b). 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.CrossRefGoogle ScholarPubMed
Bremner, JD, Vythilingam, M, Vermetten, E, Southwick, SM, Mcglashan, T, Nazeer, A, Khan, S, Vaccarino, LV, Soufer, R, Garg, PK, Ng, CK, Staib, LH, Duncan, JS, Charney, DS (2003). MRI and pet study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. American Journal of Psychiatry 160, 924–932.CrossRefGoogle ScholarPubMed
Breslau, N, Kessler, RC, Chilcoat, HD, Schultz, LR, Davis, GC, Andreski, P (1998). Trauma and posttraumatic stress disorder in the community: the 1996 Detroit area survey of trauma. Archives of General Psychiatry 55, 626–632.Google Scholar
Britton, JC, Phan, KL, Taylor, SF, Fig, LM, Liberzon, I (2005). Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery. Biological Psychiatry 57, 832–840.Google Scholar
Brohawn, KH, Offringa, R, Pfaff, DL, Hughes, KC, Shin, LM (2010). The neural correlates of emotional memory in posttraumatic stress disorder. Biological Psychiatry 68, 1023–1030.CrossRefGoogle ScholarPubMed
Brunetti, M, Sepede, G, Mingoia, G, Catani, C, Ferretti, A, Merla, A, Del Gratta, C, Romani, GL, Babiloni, C (2010). Elevated response of human amygdala to neutral stimuli in mild post traumatic stress disorder: neural correlates of generalized emotional response. Neuroscience 168, 670–679.Google Scholar
Bryant, RA, Felmingham, KL, Kemp, AH, Barton, M, Peduto, AS, Rennie, C, Gordon, E, Williams, LM (2005). Neural networks of information processing in posttraumatic stress disorder: a functional magnetic resonance imaging study. Biological Psychiatry 58, 111–118.CrossRefGoogle ScholarPubMed
Bryant, RA, Kemp, AH, Felmingham, KL, Liddell, B, Olivieri, G, Peduto, A, Gordon, E, Williams, LM (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.CrossRefGoogle ScholarPubMed
Cutini, S, Scatturin, P, Menon, E, Bisiacchi, PS, Gamberini, L, Zorzi, M, Dell'acqua, R (2008). Selective activation of the superior frontal gyrus in task-switching: an event-related fNIRS study. NeuroImage 42, 945–955.CrossRefGoogle ScholarPubMed
Dickie, EW, Brunet, A, Akerib, V, Armony, JL (2013). Anterior cingulate cortical thickness is a stable predictor of recovery from post-traumatic stress disorder. Psychological Medicine 43, 645–653.Google Scholar
Dougherty, DD, Weiss, AP, Cosgrove, GR, Alpert, NM, Cassem, EH, Nierenberg, AA, Price, BH, Mayberg, HS, Fischman, AJ, Rauch, SL (2003). Cerebral metabolic correlates as potential predictors of response to anterior cingulotomy for treatment of major depression. Journal of Neurosurgery 99, 1010–1017.Google Scholar
Drevets, WC, Bogers, W, Raichle, ME (2002). Functional anatomical correlates of antidepressant drug treatment assessed using pet measures of regional glucose metabolism. European Neuropsychopharmacology 12, 527–544.Google Scholar
Drevets, WC, Price, JL, Simpson, JR Jr., Todd, RD, Reich, T, Vannier, M, Raichle, ME (1997). Subgenual prefrontal cortex abnormalities in mood disorders. Nature 386, 824–827.Google Scholar
Ehlers, A, Clark, DM (2000). A cognitive model of posttraumatic stress disorder. Behaviour Research and Therapy 38, 319–345.Google Scholar
Etkin, A, Egner, T, Kalisch, R (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences 15, 85–93.CrossRefGoogle ScholarPubMed
Etkin, A, Wager, TD (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry 164, 1476–1488.Google Scholar
Fani, N, Jovanovic, T, Ely, TD, Bradley, B, Gutman, D, Tone, EB, Ressler, KJ (2012). Neural correlates of attention bias to threat in post-traumatic stress disorder. Biological Psychology 90, 134–142.CrossRefGoogle ScholarPubMed
Felmingham, KL, Williams, LM, Kemp, AH, Rennie, C, Gordon, E, Bryant, RA (2009). Anterior cingulate activity to salient stimuli is modulated by autonomic arousal in posttraumatic stress disorder. Psychiatry Research: Neuroimaging 173, 59–62.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1997). Structured Clinical Interview for DSM-IV Axis I Disorders (SCID-I/P). American Psychiatric Press: Washington, DC.Google Scholar
Fonzo, GA, Simmons, AN, Thorp, SR, Norman, SB, Paulus, MP, Stein, MB (2010). Exaggerated and disconnected insular-amygdalar blood oxygenation level-dependent response to threat-related emotional faces in women with intimate-partner violence posttraumatic stress disorder. Biological Psychiatry 68, 433–441.Google Scholar
Friston, KJ, Buechel, C, Fink, GR, Morris, J, Rolls, E, Dolan, RJ (1997). Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6, 218–229.CrossRefGoogle ScholarPubMed
Geuze, E, Westenberg, HGM, Jochims, A, de Kloet, CS, Bohus, M, Vermetten, E, Schmahl, C (2007). Altered pain processing in veterans with posttraumatic stress disorder. Archives of General Psychiatry 64, 76–85.CrossRefGoogle ScholarPubMed
Gilbertson, MW, Shenton, ME, Ciszewski, A, Kasai, K, Lasko, NB, Orr, SP, Pitman, RK (2002). Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nature Neuroscience 5, 1242–1247.CrossRefGoogle ScholarPubMed
Gitelman, DR, Penny, WD, Ashburner, J, Friston, KJ (2003). Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. NeuroImage 19, 200–207.CrossRefGoogle ScholarPubMed
Gold, AL, Shin, LM, Orr, SP, Carson, MA, Rauch, SL, Macklin, ML, Lasko, NB, Metzger, LJ, Dougherty, DD, Alpert, NM, Fischman, AJ, Pitman, RK (2011). Decreased regional cerebral blood flow in medial prefrontal cortex during trauma-unrelated stressful imagery in Vietnam veterans with post-traumatic stress disorder. Psychological Medicine 41, 2563–2572.CrossRefGoogle ScholarPubMed
Hamann, S (2005). Sex differences in the responses of the human amygdala. The Neuroscientist 11, 288–293.CrossRefGoogle ScholarPubMed
Hariri, AR, Tessitore, A, Mattay, VS, Fera, F, Weinberger, DR (2002). The amygdala response to emotional stimuli: a comparison of faces and scenes. NeuroImage 17, 317–323.CrossRefGoogle ScholarPubMed
Herringa, R, Phillips, M, Almeida, J, Insana, S, Germain, A (2012). Post-traumatic stress symptoms correlate with smaller subgenual cingulate caudate, and insula volumes in unmedicated combat veterans. Psychiatry Research: Neuroimaging 203, 139–145.Google Scholar
Hutcherson, CA, Goldin, PR, Ochsner, KN, Gabrieli, JD, Feldman Barrett, L, Gross, JJ (2005). Attention and emotion: does rating emotion alter neural responses to amusing and sad films? NeuroImage 27, 656–668.Google Scholar
Jatzko, A, Schmitt, A, Demirakca, T, Weimer, E, Braus, DF (2006). Disturbance in the neural circuitry underlying positive emotional processing in post-traumatic stress disorder (PTSD). An fMRI study. European Archives of Psychiatry and Clinical Neuroscience 256, 112–114.Google Scholar
Karl, A, Schaefer, M, Malta, LS, Dörfel, D, Rohleder, N, Werner, A (2006). A meta-analysis of structural brain abnormalities in PTSD. Neuroscience and Biobehavioral Reviews 30, 1004–1031.CrossRefGoogle ScholarPubMed
Kemp, AH, Felmingham, K, Das, P, Hughes, G, Peduto, AS, Bryant, RA, Williams, LM (2007). Influence of comorbid depression on fear in posttraumatic stress disorder: an fMRI study. Psychiatry Research: Neuroimaging 155, 265–269.Google Scholar
Lang, PJ, Bradley, MM, Cuthbert, BN (1997). International Affective Picture System (IAPS) Technical Manual and Affective Rating. NIMH Center for the Study of Emotion and Attention . University of Florida: Gainesville, FL.Google Scholar
Lanius, RA, Frewen, PA, Girotti, M, Neufeld, RWJ, Stevens, TK, Densmore, M (2007). Neural correlates of trauma script-imagery in posttraumatic stress disorder with and without comorbid major depression: a functional MRI investigation. Psychiatry Research: Neuroimaging 155, 45–56.Google Scholar
Lanius, RA, Williamson, PC, Densmore, M, Boksman, K, Gupta, MA, Neufeld, RW, Gati, JS, Menon, RS (2001). Neural correlates of traumatic memories in posttraumatic stress disorder: a functional MRI investigation. American Journal of Psychiatry 158, 1920–1922.Google Scholar
Lanius, RA, Williamson, PC, Hopper, J, Densmore, M, Boksman, K, Gupta, MA, Neufeld, RWJ, Gati, JS, Menon, RS (2003). Recall of emotional states in posttraumatic stress disorder: an fMRI investigation. Biological Psychiatry 53, 204–210.CrossRefGoogle ScholarPubMed
Ledoux, JE (2000). Emotion circuits in the brain. Annual Review of Neuroscience 23, 155–184.Google Scholar
Lindauer, RNJL, Booij, J, Habraken, JBA, Uylings, HBM, Olff, M, Carlier, IVE, Den Heeten, GJ, Van Eck-Smit, BLF, Gersons, BPR (2004). Cerebral blood flow changes during script-driven imagery in police officers with posttraumatic stress disorder. Biological Psychiatry 56, 853–861.Google Scholar
Magruder, KM, Frueh, BC, Knapp, RG, Davis, L, Hamner, MB, Martin, REH, Gold, PB, Arana, GW (2005). Prevalence of posttraumatic stress disorder in veterans affairs primary care clinics. General Hospital Psychiatry 27, 169–179.CrossRefGoogle ScholarPubMed
Mayberg, HS, Liotti, M, Brannan, SK, Mcginnis, S, Mahurin, RK, Jerabek, PA, Silva, JA, Tekell, JL, Martin, CC, Lancaster, JL, Fox, PT (1999). Reciprocal limbic-cortical function and negative mood: converging pet findings in depression and normal sadness. American Journal of Psychiatry 156, 675–682.CrossRefGoogle ScholarPubMed
Mayberg, HS, Lozano, AM, Voon, V, Mcneely, HE, Seminowicz, D, Hamani, C, Schwalb, JM, Kennedy, SH (2005). Deep brain stimulation for treatment-resistant depression. Neuron 45, 651–660.CrossRefGoogle ScholarPubMed
Milad, MR, Pitman, RK, Ellis, CB, Gold, AL, Shin, LM, Lasko, NB, Zeidan, MA, Handwerger, K, Orr, SP, Rauch, SL (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry 66, 1075–1082.Google Scholar
Mitchell, RLC (2013). Further characterisation of the functional neuroanatomy associated with prosodic emotion decoding. Cortex 49, 1722–1173.CrossRefGoogle ScholarPubMed
Nagahama, Y, Okada, T, Katsumi, Y, Hayashi, T, Yamauchi, H, Sawamoto, N, Toma, K, Nakamura, K, Hanakawa, T, Konishi, J, Fukuyama, H, Shibasaki, H (1999). Transient neural activity in the medial superior frontal gyrus and precuneus time locked with attention shift between object features. NeuroImage 10, 193–199.CrossRefGoogle ScholarPubMed
Ochsner, KN, Bunge, SA, Gross, JJ, Gabrieli, JDE (2002). Rethinking feelings: an fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience 14, 1215–1229.Google Scholar
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97–113.Google Scholar
Patel, R, Spreng, RN, Shin, LM, Girard, TA (2012). Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies. Neuroscience & Biobehavioral Reviews 36, 2130–2142.Google Scholar
Phan, K, Britton, JC, Taylor, SF, Fig, LM, Liberzon, I (2006). Corticolimbic blood flow during nontraumatic emotional processing in posttraumatic stress disorder. Archives of General Psychiatry 63, 184–192.Google Scholar
Phan, KL, Wager, T, Taylor, SF, Liberzon, I (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in pet and fMRI. NeuroImage 16, 331–348.Google Scholar
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003 a). Neurobiology of emotion perception i: the neural basis of normal emotion perception. Biological Psychiatry 54, 504–514.Google Scholar
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003 b). Neurobiology of emotion perception ii: implications for major psychiatric disorders. Biological Psychiatry 54, 515–528.Google Scholar
Rauch, SL, Shin, LM, Phelps, EA (2006). Neurocircuitry models of posttraumatic stress disorder and extinction: Human neuroimaging research-past, present, and future. Biological Psychiatry 60, 376–382.Google Scholar
Rauch, SL, Whalen, PJ, Shin, LM, Mcinerney, SC, Macklin, ML, Lasko, NB, Orr, SP, Pitman, RK (2000). Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biological Psychiatry 47, 769–776.Google Scholar
Rougemont-Bucking, A, Linnman, C, Zeffiro, TA, Zeidan, MA, Lebron-Milad, K, Rodriguez-Romaguera, J, Rauch, SL, Pitman, RK, Milad, MR (2011). Altered processing of contextual information during fear extinction in PTSD: an fmri study. CNS Neuroscience & Therapeutics 17, 227–236.CrossRefGoogle ScholarPubMed
Sakamoto, H, Fukuda, R, Okuaki, T, Rogers, M, Kasai, K, Machida, T, Shirouzu, I, Yamasue, H, Akiyama, T, Kato, N (2005). Parahippocampal activation evoked by masked traumatic images in posttraumatic stress disorder: a functional MRI study. Neuroimage 26, 813–821.Google Scholar
Schneider, SL (2013). The international standard classification of education 2011. Comparative Social Research 30, 365–379.Google Scholar
Shin, LM, Bush, G, Milad, MR, Lasko, NB, Brohawn, KH, Hughes, KC, Macklin, ML, Gold, AL, Karpf, RD, Orr, SP, Rauch, SL, Pitman, RK (2011). Exaggerated activation of dorsal anterior cingulate cortex during cognitive interference: a monozygotic twin study of posttraumatic stress disorder. American Journal of Psychiatry 168, 979–985.Google Scholar
Shin, LM, Kosslyn, SM, Mcnally, RJ, Alpert, NM, Thompson, WL, Rauch, SL, Macklin, ML, Pitman, RK (1997). Visual imagery and perception in posttraumatic stress disorder. A positron emission tomographic investigation. Archives of General Psychiatry 54, 233–241.CrossRefGoogle ScholarPubMed
Shin, LM, Orr, SP, Carson, MA, Rauch, SL, Macklin, ML, Lasko, NB, Peters, PM, Metzger, LJ, Dougherty, DD, Cannistraro, PA, Alpert, NM, Fischman, AJ, Pitman, RK (2004). Regional cerebral blood flow in the amygdala and medial prefrontal cortex during traumatic imagery in male and female Vietnam veterans with PTSD. Archives of General Psychiatry 61, 168–176.CrossRefGoogle ScholarPubMed
Shin, LM, Rauch, SL, Pitman, RK (2006). Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Annals of the New York Academy of Sciences 1071, 67–79.Google Scholar
Shin, LM, Wright, CI, Cannistraro, PA, Wedig, MM, Mcmullin, K, Martis, B, Macklin, ML, Lasko, NB, Cavanagh, SR, Krangel, TS, Orr, SP, Pitman, RK, Whalen, PJ, Rauch, SL (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.CrossRefGoogle ScholarPubMed
Simmons, AN, Matthews, SC, Strigo, IA, Baker, DG, Donovan, HK, Motezadi, A, Stein, MB, Paulus, MP (2011). Altered amygdala activation during face processing in Iraqi and Afghanistani war veterans. Biology of Mood & Anxiety Disorders 1, 6.Google Scholar
Simmons, AN, Norman, SB, Spadoni, AD, Strigo, IA (2013). Neurosubstrates of remission following prolonged exposure therapy in veterans with posttraumatic stress disorder. Psychotherapy and Psychosomatics 82, 382–389.Google Scholar
Stevens, JS, Jovanovic, T, Fani, N, Ely, TD, Glover, EM, Bradley, B, Ressler, KJ (2013). Disrupted amygdala-prefrontal functional connectivity in civilian women with posttraumatic stress disorder. Journal of Psychiatric Research 47, 1469–1478.Google Scholar
St. Jacques, PL, Botzung, A, Miles, A, Rubin, DC (2011). Functional neuroimaging of emotionally intense autobiographical memories in post-traumatic stress disorder. Journal of Psychiatric Research 45, 630–637.Google Scholar
Stiglmayr, C, Schimke, P, Wagner, T, Braakmann, D, Schweiger, U, Sipos, V, Fydrich, T, Schmahl, C, Ebner-Priemer, U, Kleindienst, N, Bischkopf, J, Auckenthaler, A, Kienast, T (2010). Development and psychometric characteristics of the dissociation tension scale. Journal of Personality Assessment 92, 269–277.Google Scholar
Taylor, SF, Phan, KL, Decker, LR, Liberzon, I (2003). Subjective rating of emotionally salient stimuli modulates neural activity. NeuroImage 18, 650–659.Google Scholar
Thomaes, K, Dorrepaal, E, Draijer, NP, de Ruiter, MB, Elzinga, BM, Sjoerds, Z, van Balkom, AJ, Smit, JH, Veltman, DJ (2013). Increased anterior cingulate cortex and hippocampus activation in complex PTSD during encoding of negative words. Social Cognitive and Affective Neuroscience 8, 190–200.Google Scholar
Thomaes, K, Dorrepaal, E, Draijer, NP, de Ruiter, MB, Elzinga, BM, van Balkom, AJ, Smoor, PL, Smit, JH, Veltman, DJ (2009). Increased activation of the left hippocampus region in complex PTSD during encoding and recognition of emotional words: a pilot study. Psychiatry Research: Neuroimaging 171, 44–53.Google Scholar
Van Buuren, M, Vink, M, Rapcencu, AE, Kahn, RS (2011). Exaggerated brain activation during emotion processing in unaffected siblings of patients with schizophrenia. Biological Psychiatry 70, 81–87.CrossRefGoogle ScholarPubMed
Van Wingen, GA, Geuze, E, Vermetten, E, Fernandez, G (2011). Perceived threat predicts the neural sequelae of combat stress. Molecular Psychiatry 16, 664–671.Google Scholar
Werner, NS, Meindl, T, Engel, RR, Rosner, R, Riedel, M, Reiser, M, Fast, K (2009). Hippocampal function during associative learning in patients with posttraumatic stress disorder. Journal of Psychiatric Research 43, 309–318.Google Scholar
Whalley, MG, Rugg, MD, Smith, APR, Dolan, RJ, Brewin, CR (2009). Incidental retrieval of emotional contexts in post-traumatic stress disorder and depression: an fMRI study. Brain and Cognition 69, 98–107.Google Scholar
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