Brain Imaging and Behavior

, Volume 10, Issue 1, pp 226–237 | Cite as

Different neural modifications underpin PTSD after different traumatic events: an fMRI meta-analytic study

  • Maddalena Boccia
  • Simonetta D’Amico
  • Filippo Bianchini
  • Assunta Marano
  • Anna Maria Giannini
  • Laura Piccardi
Review Article

Abstract

Post-traumatic stress disorder (PTSD) is an anxiety condition that can develop after exposure to trauma such as physical or sexual assault, injury, combat-related trauma, natural disaster or death. Although an increasing number of neurobiological studies carried out over the past 20 years have allowed clarifying the neural substrate of PTSD, the neural modifications underpinning PTSD are still unclear. Here we used activation likelihood estimation meta-analysis (ALE) to determine whether PTSD has a consistent neural substrate. We also explored the possibility that different traumatic events produce different alterations in the PTSD neural network. In neuroimaging studies of PTSD, we found evidence of a consistent neural network including the bilateral insula and cingulate cortex as well as the parietal, frontal and limbic areas. We also found that specific networks of brain areas underpin PTSD after different traumatic events and that these networks may be related to specific aspects of the traumatic events. We discuss our results in light of the functional segregation of the brain areas involved in PTSD.

Keywords

PTSD fMRI ALE meta-analysis 

References

  1. American Psychiatric Association (2013). Diagnostic and statistical manual of mental disorders (5th edn) (DSM-V).Google Scholar
  2. Boccia, M., Nemmi, F., & Guariglia, C. (2014). Neuropsychology of environmental navigation in humans: review and meta-analysis of fMRI studies in healthy participants. Neuropsychology Review, 24(2), 236–51.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bohbot, V. D., & Corkin, S. (2007). Posterior parahippocampal place learning in H.M. Hippocampus, 17, 863–872.CrossRefPubMedGoogle Scholar
  4. Brandes, D., Ben-Schachar, G., Gilboa, A., Bonne, O., Freedman, S., & Shalev, A. Y. (2002). PTSD symptoms and cognitive performance in recent trauma survivors. Psychiatry Research, 110, 231–238.CrossRefPubMedGoogle Scholar
  5. 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. (1995). MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. The American Journal of Psychiatry, 152, 973–981.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. Britton, J. C., Phan, K. L., Taylor, S. F., Fig, L. M., & Liberzon, I. (2005). Corticolimbic blood flow in posttraumatic stress disorder during script-driven imagery. Biological Psychiatry, 57, 832–840.CrossRefPubMedGoogle Scholar
  8. Bustamante, V., Mellman, T. A., David, D., & Fins, A. I. (2001). Cognitive functioning and the early development of PTSD. Journal of Traumatic Stress, 14, 791–797.CrossRefPubMedGoogle Scholar
  9. Chen, S., Li, L., Xu, B., & Liu, J. (2009). Insular cortex involvement in declarative memory deficits in patients with post-traumatic stress disorder. BMC Psychiatry, 9, 39.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nature Review Neuroscience, 3, 655–666.CrossRefGoogle Scholar
  11. Critchley, H. D. (2005). Neural mechanisms of autonomic, affective, and cognitive integration. Journal of Comparative Neurology, 493, 154–166.CrossRefPubMedGoogle Scholar
  12. Damasio, A. R. (1999). The feeling of what happens: Body and emotion in the making of consciousness. New York: Harcourt Brace.Google Scholar
  13. Ditlevsen, D. N., & Elklit, A. (2012). Gender, trauma type, and PTSD prevalence: a re-analysis of 18 nordic convenience samples. Annals of General Psychiatry, 11, 26.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Eickhoff, S. B., Laird, A. R., Grefkes, C., Wang, L. E., Zilles, K., & Fox, P. T. (2009). Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Human Brain Mapping, 30, 2907–2926.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Ekman, P. (1993). Facial expression and emotion. American Psychologist, 48, 384–392.CrossRefPubMedGoogle Scholar
  16. Elzinga, B. M., & Bremner, J. D. (2002). Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? Journal of Affective Disorders, 70, 1–17.CrossRefPubMedGoogle Scholar
  17. Epstein, R. A., & Morgan, L. K. (2012). Neural responses to visual scenes reveals inconsistencies between fMRI adaptation and multivoxel pattern analysis. Neuropsychologia, 50, 530–543.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. The American Journal of Psychiatry, 164, 1476–1488.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Etkin, A., Egner, T., Peraza, D. M., Kandel, E. R., & Hirsch, J. (2006). Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron, 51, 871–882.CrossRefPubMedGoogle Scholar
  20. Falconer, E., Bryant, R., Felmingham, K. L., Kemp, A. H., Gordon, E., Peduto, A., Olivieri, G., & Williams, L. M. (2008). The neural networks of inhibitory control in posttraumatic stress disorder. Journal of Psychiatry and Neuroscience, 33, 413–422.PubMedPubMedCentralGoogle Scholar
  21. Fox, P. T., Lancaster, J. L., Laird, A. R., & Eickhoff, S. B. (2014). Meta-analysis in human neuroimaging: computational modeling of large-scale databases. Annual Review of Neuroscience, 37, 409–434.CrossRefPubMedGoogle Scholar
  22. Geuze, E., Westenberg, H. G., Jochims, A., de Kloet, C. S., Bohus, M., Vermetten, E., & Schmahl, C. (2007). Altered pain processing in veterans with posttraumatic stress disorder. Archives of General Psychiatry, 64, 76–85.CrossRefPubMedGoogle Scholar
  23. Gil, T., Calev, A., Greenberg, D., Kugelmass, S., & Lerer, B. (1990). Cognitive functioning in post-traumatic stress disorder. Journal of Traumatic Stress, 3, 29–45.CrossRefGoogle Scholar
  24. Gilbertson, M. W., Gurvits, T. V., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2001). Multivariate assessment of explicit memory function in combat veterans with posttraumatic stress disorder. Journal of Traumatic Stress, 14, 413–432.CrossRefPubMedGoogle Scholar
  25. Gurvits, T. V., Lasko, N. B., Schachter, S. C., Kuhne, A. A., Orr, S. P., & Pitman, R. K. (1993). Neurological status of Vietnam veterans with chronic posttraumatic stress disorder. Journal of Neuropsychiatry and Clinical Neurosciences, 5, 183–188.CrossRefPubMedGoogle Scholar
  26. Gurvits, T. V., Shenton, M. E., Hokama, H., Ohta, H., Lasko, N. B., Gilbertson, M. W., Orr, S. P., Kikinis, R., Jolesz, F. A., McCarley, R. W., & Pitman, R. K. (1996). Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biological Psychiatry, 40, 1091–1099.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gurvits, T. V., Lasko, N. B., Repak, A. L., Metzger, L. J., Orr, S. P., & Pitman, R. K. (2002). Performance on visuospatial copying tasks in individuals with chronic posttraumatic stress disorder. Psychiatry Research, 112, 263–268.CrossRefPubMedGoogle Scholar
  28. Harvey, A. G., Bryant, R. A., & Dang, S. T. (1998). Autobiographical memory in acute stress disorder. Journal of Consulting and Clinical Psychology, 66, 500–506.CrossRefPubMedGoogle Scholar
  29. Hassabis, D., & Maguire, E. A. (2007). Deconstructing episodic memory with construction. Trends in Cognitive Science, 11, 299–306.CrossRefGoogle Scholar
  30. Hayes, J. P., Hayes, S. M., & Mikedis, A. M. (2012). Quantitative meta-analysis of neural activity in posttraumatic stress disorder. Biology of Mood and Anxiety Disorders, 2, 9.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Herry, C., Ferraguti, F., Singewald, N., Letzkus, J. J., Ehrlich, I., & Luthi, A. (2010). Neuronal circuits of fear extinction. European Journal of Neuroscience, 31, 599–612.CrossRefPubMedGoogle Scholar
  32. Hopper, J. W., Frewen, P. A., van der Kolk, B. A., & Lanius, R. A. (2007). Neural correlates of reexperiencing, avoidance, and dissociation in PTSD: symptom dimensions and emotion dysregulation in responses to script-driven trauma imagery. Journal of Traumatic Stress, 20(5), 713–25.CrossRefPubMedGoogle Scholar
  33. Hou, C., Liu, J., Wang, K., Li, L., Liang, M., He, Z., Liu, Y., Zhang, Y., Li, W., & Jiang, T. (2007). Brain responses to symptom provocation and trauma-related short-term memory recall in coal mining accident survivors with acute severe PTSD. Brain Research, 1144, 165–174.CrossRefPubMedGoogle Scholar
  34. Husarewycz, M. N., El-Gabalawy, R., Logsetty, S., & Sareen, J. (2014). The association between number and type of traumatic life experiences and physical conditions in a nationally representative sample. General Hospital Psychiatry, 36, 26–32.CrossRefPubMedGoogle Scholar
  35. Jenkins, M. A., Langlais, P. J., Delis, D. A., & Cohen, R. A. (2000). Attentional dysfunction associated with posttraumatic stress disorder among rape survivors. Clinical Neuropsychology, 14, 7–12.CrossRefGoogle Scholar
  36. Kalisch, R., Wiech, K., Critchley, H. D., Seymour, B., O’Doherty, J. P., Oakley, D. A., Allen, P., & Dolan, R. J. (2005). Anxiety reduction through detachment: subjective, physiological, and neural effects. Journal of Cognitive Neuroscience, 17, 874–883.CrossRefPubMedGoogle Scholar
  37. Kandel, E. R., Schwarz, J. H., & Jessell, T. M. (Eds.). (1991). Principles of Neural Science. New York: Elsevier Science.Google Scholar
  38. Karl, A., Schaefer, M., Malta, L. S., Dorfel, D., Rohleder, N., & Werner, A. (2006). A meta-analysis of structural brain abnormalities in PTSD. Neuroscience and Biobehavioral Reviews, 30, 1004–1031.CrossRefPubMedGoogle Scholar
  39. Kasai, K., Yamasue, H., Gilbertson, M. W., Shenton, M. E., Rauch, S. L., & Pitman, R. K. (2008). Evidence for acquired pregenual anterior cingulate gray matter loss from a twin study of combat-related posttraumatic stress disorder. Biological Psychiatry, 63, 550–556.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kitayama, N., Vaccarino, V., Kutner, M., Weiss, P., & Bremner, J. D. (2005). Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: a meta-analysis. Journal of Affective Disorders, 88, 79–86.CrossRefPubMedGoogle Scholar
  41. Koenen, K. C., Driver, K. L., Oscar-Berman, M., Wolfe, J., Folsom, S., Huang, M. T., & Schlesinger, L. (2001). Measures of prefrontal system dysfunction in posttraumatic stress disorder. Brain and Cognition, 45, 64–78.CrossRefPubMedGoogle Scholar
  42. Lanius, R. A., Williamson, P. C., Boksman, K., Densmore, M., Gupta, M., Neufeld, R. W. J., Gati, J. S., & Menon, R. S. (2002). Brain activation during script-driven imagery induced dissociative responses in PTSD: a functional magnetic resonance imaging investigation. Biological Psychiatry, 52, 305–311.CrossRefPubMedGoogle Scholar
  43. Lanius, R. A., Williamson, P. C., Hopper, J., Densmore, M., Boksman, K., Gupta, M. A., Neufeld, R. W. J., Gati, J. S., & Menon, R. S. (2003). Recall of emotional states in posttraumatic stress disorder: an fMRI investigation. Biological Psychiatry, 53, 204–210.CrossRefPubMedGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. Lanius, R. A., Williamson, P. C., Bluhm, R. L., Densmore, M., Boksman, K., Neufeld, R. W., Gati, J. S., & Menon, R. S. (2005). Functional connectivity of dissociative responses in posttraumatic stress disorder: a functional magnetic resonance imaging investigation. Biological Psychiatry, 57, 873–884.CrossRefPubMedGoogle Scholar
  46. Lanius, R. A., Frewen, P. A., Girotti, M., Neufeld, R. W., Stevens, T. K., & 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, 155, 45–56.CrossRefPubMedGoogle Scholar
  47. Mazza, M., Catalucci, A., Mariano, M., Pino, M. C., Tripaldi, S., Roncone, R., & Gallucci, M. (2012). Neural correlates of automatic perceptual sensitivity to facial affect in posttraumatic stress disorder subjects who survived L’Aquila eartquake of April 6, 2009. Brain Imaging and Behavior, 6, 374–386.CrossRefPubMedGoogle Scholar
  48. Mcnally, R. J., Lasko, N. B., Macklin, M. L., & Pitman, R. K. (1995). Autobiographical memory disturbance in combat-related posttraumatic-stress-disorder. Behaviour Research and Therapy, 33, 619–630.CrossRefPubMedGoogle Scholar
  49. Milad, M. R., & Quirk, G. J. (2012). Fear extinction as a model for translational neuroscience: ten years of progress. Annual Review of Psychology, 63(63), 129–151.CrossRefPubMedGoogle Scholar
  50. Milner, B. (2005). The medial temporal-lobe amnesic syndrome. Psychiatric Clinics of North America, 28, 599.CrossRefPubMedGoogle Scholar
  51. Misra, G., Coombes, S.A. (2014). Neuroimaging evidence of motor control and pain processing in the human midcingulate cortex. Cereb Cortex.Google Scholar
  52. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Morrow, B. A., Elsworth, J. D., Rasmusson, A. M., & Roth, R. H. (1999). The role of mesoprefrontal dopamine neurons in the acquisition and expression of conditioned fear in the rat. Neuroscience, 92, 553–564.CrossRefPubMedGoogle Scholar
  54. Moscovitch, M., Rosenbaum, R. S., Gilboa, A., Addis, D. R., Westmacott, R., Grady, C., McAndrews, M. P., Levine, B., Black, S., Winocur, G., & Nadel, L. (2005). Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. Journal of Anatomy, 207, 35–66.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Moscovitch, M., Nadel, L., Winocur, G., Gilboa, A., & Rosenbaum, R. S. (2006). The cognitive neuroscience of remote episodic, semantic and spatial memory. Current Opinion in Neurobiology, 16, 179–190.CrossRefPubMedGoogle Scholar
  56. Patel, R., Spreng, R. N., Shin, L. M., & Girard, T. A. (2012). Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 36(9), 2130–42.CrossRefPubMedGoogle Scholar
  57. Perrin, M., Vandeleur, C.L., Castelao, E., Rothen, S., Glaus, J., Vollenweider, P., Preisig, M. (2013). Determinants of the development of post-traumatic stress disorder, in the general population. Soc Psychiatry Psychiatr Epidemiol.Google Scholar
  58. Pissiota, A., Frans, O., Fernandez, M., von 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.CrossRefPubMedGoogle Scholar
  59. Pitman, R. K., Rasmusson, A. M., Koenen, K. C., Shin, L. M., Orr, S. P., Gilbertson, M. W., Milad, M. R., & Liberzon, I. (2012). Biological studies of post-traumatic stress disorder. Nature Review Neuroscience, 13, 769–787.CrossRefGoogle Scholar
  60. Polak, A.R., Witteveen, A.B..., Visser, R.S., Opmeer, B.C., Vulink, N., Figee, M., Denys, D., Olff, M. (2012). Comparison of the effectiveness of trauma-focused cognitive behavioral therapy and paroxetine treatment in PTSD patients: Design of a randomized controlled trial. Bmc Psychiatry 12.Google Scholar
  61. Portas, C. M., Rees, G., Howseman, A. M., Josephs, O., Turner, R., & Frith, C. D. (1998). A specific role for the thalamus in mediating the interaction of attention and arousal in humans. Journal of Neuroscience, 18, 8979–8989.PubMedGoogle Scholar
  62. Protopopescu, X., Pan, H., Tuescher, O., Cloitre, M., Goldstein, M., Engelien, W., Epstein, J., Yang, Y., Gorman, J., LeDoux, J., Silbersweig, D., & Stern, E. (2005). Differential time courses and specificity of amygdala activity in posttraumatic stress disorder subjects and normal control subjects. Biological Psychiatry, 57(5), 464–73.CrossRefPubMedGoogle Scholar
  63. Rabinak, C. A., Angstadt, M., Welsh, R. C., Kenndy, A. E., Lyubkin, M., Martis, B., & Phan, K. L. (2011). Altered amygdala resting-state functional connectivity in post-traumatic stress disorder. Front Psychiatry, 2, 62.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Rauch, S. L., Whalen, P. J., Shin, L. M., McInerney, S. C., Macklin, M. L., Lasko, N. B., Orr, S. P., & Pitman, R. K. (2000). Exaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study. Biological Psychiatry, 47(9), 769–76.CrossRefPubMedGoogle Scholar
  65. 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.CrossRefPubMedGoogle Scholar
  66. Rauch, S. A. M., Eftekhari, A., & Ruzek, J. I. (2012). Review of exposure therapy: a gold standard for PTSD treatment. Journal of Rehabilitation Research and Development, 49, 679–687.CrossRefPubMedGoogle Scholar
  67. Robinson, J. L., Laird, A. R., Glahn, D. C., Lovallo, W. R., & Fox, P. T. (2010). Meta-analytic connectivity modeling: delineating the functional connectivity of the human amygdala. Human Brain Mapping, 31, 173–184.PubMedPubMedCentralGoogle Scholar
  68. 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.CrossRefPubMedGoogle Scholar
  69. Santiago, P. N., Ursano, R. J., Gray, C. L., Pynoos, R. S., Spiegel, D., Lewis-Fernandez, R., Friedman, M. J., & Fullerton, C. S. (2013). A systematic review of PTSD prevalence and trajectories in DSM-5 defined trauma exposed populations: intentional and non-intentional traumatic events. Plos One, 8, e59236.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Shaw, M. E., Strother, S. C., McFarlane, A. C., Morris, P., Anderson, J., Clark, C. R., & Egan, G. F. (2002). Abnormal functional connectivity in posttraumatic stress disorder. NeuroImage, 15, 661–674.CrossRefPubMedGoogle Scholar
  71. Shin, L. M., & Liberzon, I. (2010). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology, 35, 169–191.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 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.CrossRefPubMedGoogle Scholar
  73. Shin, L. M., McNally, R. J., Kosslyn, S. M., Thompson, W. L., Rauch, S. L., Alpert, N. M., Metzger, L. J., Lasko, N. B., Orr, S. P., & Pitman, R. K. (1999). Regional cerebral blood flow during script-driven imagery in childhood sexual abuse-related PTSD: a PET investigation. American Journal of Psychiatry, 156, 575–584.PubMedGoogle Scholar
  74. Shin, L. M., Shin, P. S., Heckers, S., Krangel, T. S., Macklin, M. L., Orr, S. P., Lasko, N., Segal, E., Makris, N., Richert, K., Levering, J., Schacter, D. L., Alpert, N. M., Fischman, A. J., Pitman, R. K., & Rauch, S. L. (2004). Hippocampal function in posttraumatic stress disorder. Hippocampus, 14(3), 292–300.CrossRefPubMedGoogle Scholar
  75. Simmons, A. N., Paulus, M. P., Thorp, S. R., Matthews, S. C., Norman, S. B., & Stein, M. B. (2008). Functional activation and neural networks in women with posttraumatic stress disorder related to intimate partner violence. Biological Psychiatry, 64, 681–690.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Simmons, A. N., Matthews, S. C., Strigo, I. A., Baker, D. G., Donovan, H. K., Motezadi, A., Stein, M. B., & Paulus, M. P. (2011). Altered amygdala activation during face processing in Iraqi and Afghanistani war veterans. Biology Mood Anxiety Disorders, 1(1), 6.CrossRefGoogle Scholar
  77. Smith, M. E. (2005). Bilateral hippocampal volume reduction in adults with post-traumatic stress disorder: a meta-analysis of structural MRI studies. Hippocampus, 15, 798–807.CrossRefPubMedGoogle Scholar
  78. Sripada, R. K., King, A. P., Garfinkel, S. N., Wang, X., Sripada, C. S., Welsh, R. C., & Liberzon, I. (2012). Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. Journal of Psychiatry and Neuroscience, 37(4), 241–9.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Stein, M. B., Koverola, C., Hanna, C., Torchia, M. G., & McClarty, B. (1997). Hippocampal volume in women victimized by childhood sexual abuse. Psychological Medicine, 27, 951–959.CrossRefPubMedGoogle Scholar
  80. Sullivan, K., Krengel, M., Proctor, S. P., Devine, S., Heeren, T., & White, R. F. (2003). Cognitive functioning in treatment-seeking Gulf War veterans: pyridostigmine bromide use and PTSD. Journal of Psychopathology and Behavioral Assessment, 25, 95–103.CrossRefGoogle Scholar
  81. Taylor, S. F., Phan, K. L., Decker, L. R., & Liberzon, I. (2003). Subjective rating of emotionally salient stimuli modulates neural activity. NeuroImage, 18, 650–659.CrossRefPubMedGoogle Scholar
  82. Vann, S. D., Aggleton, J. P., & Maguire, E. A. (2009). What does the retrosplenial cortex do? Nature Reviews Neuroscience, 10, 792–U750.CrossRefPubMedGoogle Scholar
  83. Vasterling, J. J., & Brailey, K. (2005). Neuropsychological findings in adults with PTSD. In J. J. Vasterling & C. R. Brewin (Eds.), Neuropsychology of PTSD: Biological, cognitive, and clinical perspectives (pp. 178–207). New York: Guilford Press.Google Scholar
  84. Vasterling, J. J., Brailey, K., Constans, J. I., & Sutker, P. B. (1998). Attention and memory dysfunction in posttraumatic stress disorder. Neuropsychology, 12, 125–133.CrossRefPubMedGoogle Scholar
  85. Vasterling, J. J., Duke, L. M., Brailey, K., Constans, J. I., Allain, A. N., & Stuker, P. B. (2002). Attention, learning, and memory performances and intellectual resources in Vietnam veterans: PTSD and no disorder comparisons. Neuropsychology, 16, 5–14.CrossRefPubMedGoogle Scholar
  86. Vincent, J. L., Snyder, A. Z., Fox, M. D., Shannon, B. J., Andrews, J. R., Raichle, M. E., & Buckner, R. L. (2006). Coherent spontaneous activity identifies a hippocampal-parietal memory network. Journal of Neurophysiology, 96, 3517–3531.CrossRefPubMedGoogle Scholar
  87. Vogt, B. A. (2005). Pain and emotion interactions in subregions of the cingulate gyrus. Nature Review Neuroscience, 6, 533–544.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Maddalena Boccia
    • 1
    • 2
  • Simonetta D’Amico
    • 3
  • Filippo Bianchini
    • 1
    • 2
  • Assunta Marano
    • 3
  • Anna Maria Giannini
    • 2
  • Laura Piccardi
    • 1
    • 3
  1. 1.Neuropsychology UnitIRCCS Fondazione Santa Lucia of RomeRomeItaly
  2. 2.Department of Psychology“Sapienza” University of RomeRomeItaly
  3. 3.Department of Life, Health and Environmental SciencesL’Aquila UniversityL’AquilaItaly

Personalised recommendations