White matter microstructure varies with post-traumatic stress severity following medical trauma

  • Nathaniel G. Harnett
  • Edward W. FerenceIII
  • Amy J. Knight
  • David C. KnightEmail author


The prefrontal cortex, amygdala, hippocampus, and hypothalamus are important components of the neural network that mediates the healthy learning, expression, and regulation of emotion. These brain regions are connected by white matter pathways that include the cingulum bundle, uncinate fasciculus, and fornix/stria terminalis. Individuals with trauma and stress-related disorders show dysfunction of the cognitive-affective processes supported by the brain regions these white matter tracts connect. Therefore, variability in the microstructure of these white matter pathways may play an important role in the cognitive-affective dysfunction related to post-traumatic stress disorder. Thus, the current study used diffusion weighted imaging to assess the white matter microstructure of the cingulum bundle, uncinate fasciculus, and fornix/stria terminalis acutely (< 1 month) following trauma. Further, we assessed both acute (i.e., < 1 month) and subacute (i.e., 3 months post-trauma) post-traumatic stress symptom severity. White matter microstructure (assessed < 1 month post-trauma) of the uncinate fasciculus and fornix/stria terminalis varied with acute post-traumatic stress severity (assessed < 1 month post-trauma). Further, white matter microstructure (assessed < 1 month post-trauma) of the cingulum bundle and fornix/stria terminalis varied with subacute post-traumatic stress severity (assessed 3 months post-trauma). The current results suggest white matter architecture of the prefrontal cortex – amygdala network plays an important role in the development of trauma and stress-related disorders.


Tractography Acute stress PTSD Cingulum bundle Uncinate fasciculus Stria terminalis 



The authors would like to thank Thomas DeRamus and Rajesh Kana for their assistance with this manuscript.


This research was supported by the University of Alabama at Birmingham, Department of Physical Medicine and Rehabilitation’s Functional Neurorecovery Pilot Grants Initiative (A. J. K. & D. C. K.), the University of Alabama at Birmingham, Office of Equity and Diversity’s CMFSDP Fellowship (N. G. H.), the Ford Foundation‘s Predoctoral Fellowship (N. G. H.), and National Institutes of Health [Grant Number: F99NS105171] (N. G. H.).

Compliance with ethical standards

Conflicts of interest

Nathaniel Harnett declares he has no conflicts of interest. Edward Ference declares he has no conflicts of interest. Amy Knight declares she has no conflicts of interest. David Knight declares he has no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

11682_2018_9995_MOESM1_ESM.docx (20 kb)
ESM 1 (DOCX 20 kb)


  1. Amstadter, A. B., & Vernon, L. L. (2008). Emotional reactions during and after trauma: A comparison of trauma types. Journal of Aggression, Maltreatment & Trauma, 16(4), 391–408. Scholar
  2. Atlas, L. Y., Lindquist, M. A., Bolger, N., & Wager, T. D. (2014). Brain mediators of the effects of noxious heat on pain. Pain, 155(8), 1632–1648. Scholar
  3. Avery, S. N., Clauss, J. A., Winder, D. G., Woodward, N., Heckers, S., & Blackford, J. U. (2014). BNST neurocircuitry in humans. NeuroImage, 91, 311–323. Scholar
  4. Basser, P. J., Pajevic, S., Pierpaoli, C., Duda, J., & Aldroubi, A. (2000). In Vivo Fiber Tractography. Magnenetic Resonance in Medicine, 44(4), 625–632. Scholar
  5. Berretta, S., Pantazopoulos, H., Caldera, M., Pantazopoulos, P., & Paré, D. (2005). Infralimbic cortex activation increases c-Fos expression in intercalated neurons of the amygdala. Neuroscience, 132(4), 943–953. Scholar
  6. Boekel, W., Forstmann, B. U., & Keuken, M. C. (2017). A test-retest reliability analysis of diffusion measures of white matter tracts relevant for cognitive control. Psychophysiology, 54(1), 24–33. Scholar
  7. Buijs, R. M., & Van Eden, C. G. (2000). The integration of stress by the hypothalamus, amygdala and prefrontal cortex: Balance between the autonomic nervous system and the neuroendocrine system. Progress in Brain Research, 126, 117–132. Scholar
  8. Catani, M., Howard, R. J., Pajevic, S., & Jones, D. K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. NeuroImage, 17(1), 77–94. Scholar
  9. Chen, L., Lui, S., Wu, Q. Z., Zhang, W., Zhou, D., Chen, H. F., et al. (2013). Impact of acute stress on human brain microstructure: An MR diffusion study of earthquake survivors. Human Brain Mapping, 34(2), 367–373. Scholar
  10. Choi, J. M., Padmala, S., & Pessoa, L. (2012). Impact of state anxiety on the interaction between threat monitoring and cognition. NeuroImage, 59(2), 1912–1923. Scholar
  11. Cohen-Adad, J., Descoteaux, M., Rossignol, S., Hoge, R. D., Deriche, R., & Benali, H. (2008). Detection of multiple pathways in the spinal cord using q-ball imaging. NeuroImage, 42(2), 739–749.CrossRefPubMedGoogle Scholar
  12. Costanzo, M. E., Jovanovic, T., Pham, D., Leaman, S., Highland, K. B., Norrholm, S. D., & Roy, M. J. (2016). White matter microstructure of the uncinate fasciculus is associated with subthreshold posttraumatic stress disorder symptoms and fear potentiated startle during early extinction in recently deployed Service Members. Neuroscience Letters, 618, 66–71. Scholar
  13. Critchley, H. D., Elliott, R., Mathias, C. J., & Dolan, R. J. (2000). Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study. The Journal of Neuroscience, 20(8), 3033–3040.CrossRefPubMedGoogle Scholar
  14. Davenport, N. D., Lim, K. O., & Sponheim, S. R. (2015). White matter abnormalities associated with military PTSD in the context of blast TBI. Human Brain Mapping, 36(3), 1053–1064. Scholar
  15. 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(5), 829–838. Scholar
  16. Denny, B. T., Ochsner, K. N., Weber, J., & Wager, T. D. (2014). Anticipatory brain activity predicts the success or failure of subsequent emotion regulation. Social Cognitive and Affective Neuroscience, 9(4), 403–411. Scholar
  17. Dretsch, M. N., Lange, R. T., Katz, J. S., Goodman, A., Daniel, T. A., Deshpande, G., et al. (2017). Examining microstructural white matter in active duty soldiers with a history of mild traumatic brain injury and traumatic stress. The Open Neuroimaging Journal, 11(1), 46–57. Scholar
  18. Dretsch, M. N., Wood, K. H., Daniel, T. A., Katz, J. S., Deshpande, G., Goodman, A. M., et al. (2016). Exploring the neurocircuitry underpinning predictability of threat in soldiers with PTSD compared to deployment exposed controls. The Open Neuroimaging Journal, 10(1), 111–124. Scholar
  19. Eichenauer, K., Feltz, G., Wilson, J., & Brookings, J. (2010). Measuring psychosocial risk factors in cardiac rehabilitation: Validation of the psychosocial risk factor survey. Journal of Cardiopulmonary Rehabilitation and Prevention, 30(5), 309–318. Scholar
  20. Etkin, A., Egner, T., & Kalisch, R. (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitive Sciences, 15(2), 85–93. Scholar
  21. Etkin, A., & Wager, T. D. (2007). Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. American Journal of Psychiatry, 164(10), 1476–1488. Scholar
  22. Fani, N., King, T. Z., Brewster, R., Srivastava, A., Stevens, J. S., Glover, E. M., et al. (2015). Fear-potentiated startle during extinction is associated with white matter microstructure and functional connectivity. Cortex, 64, 249–259. Scholar
  23. Fani, N., King, T. Z., Shin, J., Srivastava, A., Brewster, R. C., Jovanovic, T., et al. (2016). Structural and functional connectivity in posttraumatic stress disorder: Associations with FKBP5. Depression and Anxiety, 33(4), 300–307. Scholar
  24. Fani, N., Tone, E. B., Phifer, J., Norrholm, S. D., Bradley, B., Ressler, K. J., et al. (2012). Attention bias toward threat is associated with exaggerated fear expression and impaired extinction in PTSD. Psychological Medicine, 42(3), 533–543. Scholar
  25. Foa, E. B. (1995). The posttraumatic diagnostic scale (PDS) manual. Minneapolis: National Computer Systems.Google Scholar
  26. Foa, E. B., Cashman, L., Jaycox, L., & Perry, K. (1997). The Validation of a Self-Report Measure of Posttraumatic Stress Disorder : The Posttraumatic Diagnostic Scale. Psychological Assessment, 9(4), 445–451.CrossRefGoogle Scholar
  27. Fuchs, P. N., Balinsky, M., & Melzack, R. (1996). Electrical stimulation of the cingulum bundle and surrounding cortical tissue reduces formalin-test pain in the rat. Brain Research, 743(1–2), 116–123. Scholar
  28. Hagmann, P., Jonasson, L., Maeder, P., Thiran, J.-P., Wedeen, V. J., & Meuli, R. (2006). Understanding diffusion MR imaging techniques: From scalar diffusion-weighted imaging to diffusion tensor imaging and beyond. RadioGraphics, 26(suppl_1), S205–S223. Scholar
  29. Harnett, N. G., Wood, K. H., Ference, E. W., Reid, M. A., Lahti, A. C., Knight, A. J., & Knight, D. C. (2017). Glutamate/glutamine concentrations in the dorsal anterior cingulate vary with Post-Traumatic Stress Disorder symptoms. Journal of Psychiatric Research, 91, 169–176. Scholar
  30. Helmstetter, F. J. (1992). The amygdala is essential for the expression of conditional hypoalgesia. Behavioral Neuroscience, 106(3), 518–528. Scholar
  31. Helmstetter, F. J., & Bellgowan, P. S. (1993). Lesions of the amygdala block conditional hypoalgesia on the tail flick test. Brain Research, 612(1–2), 253–257. Scholar
  32. Herman, J. P., Schäfer, M. K., & Young, E. A., Thompson, R., Douglass, J., Akil, H., & Watson, S. J. (1989). Evidence for hippocampal regulation of neuroendocrine neurons of the hypothalamo-pituitary-adrenocortical axis. The Journal of Neuroscience, 9(9), 3072–3082. Scholar
  33. Hill, M. N., Campolongo, P., Yehuda, R., & Patel, S. (2018). Integrating endocannabinoid signaling and cannabinoids into the biology and treatment of posttraumatic stress disorder. Neuropsychopharmacology, 43(1), 80–102. Scholar
  34. Hill, M. N., McLaughlin, R. J., Bingham, B., Shrestha, L., Lee, T. T. Y., Gray, J. M., et al. (2010). Endogenous cannabinoid signaling is essential for stress adaptation. Proceedings of the National Academy of Sciences, 107(20), 9406–9411. Scholar
  35. Hoge, C. W., McGurk, D., Thomas, J. L., Cox, A. L., Engel, C. C., & Castro, C. A. (2008). Mild traumatic brain injury in U.S. soldiers returning from Iraq. The New England Journal of Medicine, 358(5), 453–463. Scholar
  36. Hu, H., Zhou, Y., Wang, Q., Su, S., Qiu, Y., Ge, J., et al. (2016). Association of abnormal white matter integrity in the acute phase of motor vehicle accidents with post-traumatic stress disorder. Journal of Affective Disorders, 190, 714–722. Scholar
  37. Jacobson, L., & Sapolsky, R. (1991). The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocrine Reviews, 12(2), 118–134. Scholar
  38. Jakupcak, M., & Tull, M. T. (2005). Effects of trauma exposure on anger, aggression, and violence in a nonclinical sample of men. Violence and Victims, 20(5), 589–598. Scholar
  39. Jansen, A. S. P., Van Nguyen, X., Karpitskiy, V., Mettenleiter, T. C., & Loewy, A. D. (1995). Central command neurons of the sympathetic nervous system: Basis of the fight-or-flight response. Science, 270(5236), 644–646. Scholar
  40. Jenkins, L. M., Barba, A., Campbell, M., Lamar, M., Shankman, S. A., Leow, A. D., et al. (2016). Shared white matter alterations across emotional disorders: A voxel-based meta-analysis of fractional anisotropy. NeuroImage: Clinical, 12, 1022–1034. Scholar
  41. Jovanovic, T., Norrholm, S. D., Blanding, N. Q., Davis, M., Duncan, E., Bradley, B., & Ressler, K. J. (2010). Impaired fear inhibition is a biomarker of PTSD but not depression. Depression and Anxiety, 27(3), 244–251. Scholar
  42. Kennis, M., Van Rooij, S. J. H., Tromp, D. P. M., Fox, A. S., Rademaker, A. R., Kahn, R. S., et al. (2015). Treatment outcome-related white matter differences in veterans with posttraumatic stress disorder. Neuropsychopharmacology, 40(10), 2434–2442. Scholar
  43. Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H.-A., Murison, R., Moser, E. I., & Moser, M.-B. (2002). Reduced fear expression after lesions of the ventral hippocampus. Proceedings of the National Academy of Sciences, 99(16), 10825–10830. Scholar
  44. Knight, D. C., Nguyen, H. T., & Bandettini, P. A. (2005). The role of the human amygdala in the production of conditioned fear responses. NeuroImage, 26(4), 1193–1200. Scholar
  45. Knight, D. C., Smith, C. N., Cheng, D. T., Stein, E. A., & Helmstetter, F. J. (2004). Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning. Cognitive, Affective, & Behavioral Neuroscience, 4(3), 317–325. Scholar
  46. Knight, D. C., Smith, C. N., Stein, E. A., & Helmstetter, F. J. (1999). Functional MRI of human Pavlovian fear conditioning: patterns of activation as a function of learning. Neuroreport, 10(17), 3665–3670.CrossRefPubMedGoogle Scholar
  47. Knight, D. C., Waters, N. S., & Bandettini, P. A. (2009). Neural substrates of explicit and implicit fear memory. NeuroImage, 45(1), 208–214. Scholar
  48. Koch, S. B. J., Van Zuiden, M., Nawijn, L., Frijling, J. L., Veltman, D. J., & Olff, M. (2017). Decreased uncinate fasciculus tract integrity in male and female patients with PTSD: A diffusion tensor imaging study. Journal of Psychiatry and Neuroscience, 42(5), 331–342. Scholar
  49. Kohda, K., Harada, K., Kato, K., Hoshino, A., Motohashi, J., Yamaji, T., et al. (2007). Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: A putative post-traumatic stress disorder model. Neuroscience, 148(1), 22–33. Scholar
  50. LaBar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E., & Phelps, E. A. (1998). Human amygdala activation during conditioned fear acquisition and extinction: A mixed-trial fMRI study. Neuron, 20(5), 937–945. Scholar
  51. LeDoux, J. E., Ciocchetti, P., Xagoraris, A., & Romanski, L. (1990). The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. The Journal of Neuroscience, 10(4), 1062–1069.CrossRefPubMedGoogle Scholar
  52. LeDoux, J. E., Iwata, J., Cicchetti, P., & Reis, D. J. (1988). Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. The Journal of Neuroscience, 8(7), 2517–2529. Scholar
  53. Lerner, J. S., & Keltner, D. (2001). Fear, anger, and risk. Journal of Personality and Social Psychology, 81(1), 146–159. Scholar
  54. Liberzon, I., Abelson, J. L., Flagel, S. B., Raz, J., & Young, E. A. (1999a). Neuroendocrine and psychophysiologic responses in PTSD: A symptom provocation study. Neuropsychopharmacology, 21(1), 40–50. Scholar
  55. Liberzon, I., López, J. F., Flagel, S. B., Vázquez, D. M., & Young, E. A. (1999b). Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: Relevance to post-traumatic stress disorder. Journal of Neuroendocrinology, 11(1), 11–17. Scholar
  56. Likhtik, E. (2005). Prefrontal control of the amygdala. The Journal of Neuroscience, 25(32), 7429–7437. Scholar
  57. Lommen, M. J. J., Engelhard, I. M., van de Schoot, R., & van den Hout, M. A. (2014). Anger: Cause or consequence of posttraumatic stress? A prospective study of Dutch soldiers. Journal of Traumatic Stress, 27(2), 200–207. Scholar
  58. Meibach, R. C., & Siegel, A. (1977). Efferent connections of the hippocampal formation in the rat. Brain Research, 124(2), 197–224.CrossRefPubMedGoogle Scholar
  59. Meyerhoff, D. J., Mon, A., Metzler, T., & Neylan, T. C. (2014). Cortical gamma-aminobutyric acid and glutamate in posttraumatic stress disorder and their relationships to self-reported sleep quality. Sleep, 37(5), 893–900. Scholar
  60. Meythaler, J. M., Peduzzi, J. D., Eleftheriou, E., & Novack, T. A. (2001). Current concepts: Diffuse axonal injury-associated traumatic brain injury. Archives of Physical Medicine and Rehabilitation, 82(10), 1461–1471. Scholar
  61. Milad, M. R., Orr, S. P., Lasko, N. B., Chang, Y., Rauch, S. L., & Pitman, R. K. (2008). Presence and acquired origin of reduced recall for fear extinction in PTSD: Results of a twin study. Journal of Psychiatric Research, 42(7), 515–520. Scholar
  62. Milad, M. R., Pitman, R. K., Ellis, C. B., Gold, A. L., Shin, L. M., Lasko, N. B., et al. (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry, 66(12), 1075–1082. Scholar
  63. Milad, M. R., & Quirk, G. J. (2002). Neurons in medial prefrontal cortex signal memory for fear extinction. Nature, 420(6911), 70–74. Scholar
  64. Milad, M. R., Quirk, G. J., Pitman, R. K., Orr, S. P., Fischl, B., & Rauch, S. L. (2007a). A role for the human dorsal anterior cingulate cortex in fear expression. Biological Psychiatry, 62(10), 1191–1194. Scholar
  65. Milad, M. R., Wright, C. I., Orr, S. P., Pitman, R. K., Quirk, G. J., & Rauch, S. L. (2007b). Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biological Psychiatry, 62(5), 446–454. Scholar
  66. Mobbs, D., Yu, R., Rowe, J. B., Eich, H., FeldmanHall, O., & Dalgleish, T. (2010). Neural activity associated with monitoring the oscillating threat value of a tarantula. Proceedings of the National Academy of Sciences, 107(47), 20582–20586. Scholar
  67. Mori, S., & Aggarwal, M. (2014). In vivo magnetic resonance imaging of the human limbic white matter. Frontiers in Aging. Neuroscience, 6, 321. Scholar
  68. Mori, S., Crain, B. J., Chacko, V. P., & van Zijl, P. C. (1999). Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Annals of Neurology, 45(2), 265–269.<265::AID-ANA21>3.0.CO;2-3.CrossRefPubMedGoogle Scholar
  69. Mori, S., Kageyama, Y., Hou, Z., Aggarwal, M., Patel, J., Brown, T., et al. (2017). Elucidation of white matter tracts of the human amygdala by detailed comparison between high-resolution postmortem magnetic resonance imaging and histology. Frontiers in Neuroanatomy, 11.
  70. Mori, S., Oishi, K., Jiang, H., Jiang, L., Li, X., Akhter, K., et al. (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage, 40(2), 570–582. Scholar
  71. Motzkin, J. C., Philippi, C. L., Wolf, R. C., Baskaya, M. K., & Koenigs, M. (2015). Ventromedial prefrontal cortex is critical for the regulation of amygdala activity in humans. Biological Psychiatry, 77(3), 276–284. Scholar
  72. Olson, E. A., Cui, J., Fukunaga, R., Nickerson, L. D., Rauch, S. L., & Rosso, I. M. (2017). Disruption of white matter structural integrity and connectivity in posttraumatic stress disorder: A TBSS and tractography study. Depression and Anxiety, 34(5), 437–445. Scholar
  73. Orth, U., & Wieland, E. (2006). Anger, hostility, and posttraumatic stress disorder in trauma-exposed adults: A meta-analysis. Journal of Consulting and Clinical Psychology, 74(4), 698–706. Scholar
  74. Petrovich, G. D., Canteras, N. S., & Swanson, L. W. (2001). Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Research Reviews, 38(1–2), 247–289. Scholar
  75. Phillips, R. G., & LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience, 106(2), 274–285. Scholar
  76. Piervincenzi, C., Ben-Soussan, T. D., Mauro, F., Mallio, C. A., Errante, Y., Quattrocchi, C. C., & Carducci, F. (2017). White matter microstructural changes following quadrato motor training: A longitudinal study. Frontiers in Human Neuroscience, 11.
  77. Pitman, R. K., Rasmusson, A. M., Koenen, K. C., Shin, L. M., Orr, S. P., Gilbertson, M. W., et al. (2012). Biological studies of post-traumatic stress disorder. Nature Reviews Neuroscience, 13(11), 769–787. Scholar
  78. Ramikie, T. S., Nyilas, R., Bluett, R. J., Gamble-George, J. C., Hartley, N. D., Mackie, K., et al. (2014). Multiple mechanistically distinct modes of endocannabinoid mobilization at central amygdala glutamatergic synapses. Neuron, 81(5), 1111–1125. Scholar
  79. Redeker, N. S., Smeltzer, S. C., Kirkpatrick, J., & Parchment, S. (1995). Risk factors of adolescent and young adult trauma victims. American Journal of Critical Care, 4(5), 370–378.PubMedGoogle Scholar
  80. Ruehle, S., Rey, A. A., Remmers, F., & Lutz, B. (2012). The endocannabinoid system in anxiety, fear memory and habituation. Journal of Psychopharmacology. Scholar
  81. Sandi, C. (2011). Glucocorticoids act on glutamatergic pathways to affect memory processes. Trends in Neurosciences. Scholar
  82. Sanjuan, P. M., Thoma, R., Claus, E. D., Mays, N., & Caprihan, A. (2013). Reduced white matter integrity in the cingulum and anterior corona radiata in posttraumatic stress disorder in male combat veterans: A diffusion tensor imaging study. Psychiatry Research: Neuroimaging, 214(3), 260–268. Scholar
  83. Seo, J. P., Kim, O. L., Kim, S. H., Chang, M. C., Kim, M. S., Son, S. M., & Jang, S. H. (2012). Neural injury of uncinate fasciculus in patients with diffuse axonal injury. NeuroRehabilitation, 30(4), 323–328. Scholar
  84. Shackman, A. J., Salomons, T. V., Slagter, H. A., Fox, A. S., Winter, J. J., & Davidson, R. J. (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Reviews Neuroscience, 12(3), 154–167. Scholar
  85. Shin, L. M., Bush, G., Milad, M. R., Lasko, N. B., Brohawn, K. H., Hughes, K. C., et al. (2011). Exaggerated activation of dorsal anterior cingulate cortex during cognitive interference: A monozygotic twin study of posttraumatic stress disorder. American Journal of Psychiatry, 168(9), 979–985. Scholar
  86. Shin, L. M., Whalen, P. J., Pitman, R. K., Bush, G., Macklin, M. L., Lasko, N. B., et al. (2001). An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biological Psychiatry, 50(12), 932–942. Scholar
  87. Southwick, S. M., Krystal, J. H., Morgan, C. A., Johnson, D., Nagy, L. M., Nicolaou, A., et al. (1993). Abnormal noradrenergic function in posttraumatic stress disorder. Archives of General Psychiatry, 50(4), 266–274. Scholar
  88. Timpl, P., Spanagel, R., Sillaber, I., Kresse, A., Reul, J. M. H. M., Stalla, G. K., et al. (1998). Impaired stress response and reduced anxiety in mice lacking a functional corticotropin-releasing hormone receptor 1. Nature Genetics, 19(2), 162–166. Scholar
  89. Tuch, D. S. (2004). Q-ball imaging. Magnetic Resonance in Medicine, 52(6), 1358–1372.CrossRefPubMedGoogle Scholar
  90. Urry, H. L., Van Reekum, C. M., Johnstone, T., Kalin, N. H., Thurow, M. E., Schaefer, H. S., et al. (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. The Journal of Neuroscience, 26(16), 4415–4425. Scholar
  91. Wakana, S., Jiang, H., Nagae-Poetscher, L. M., van Zijl, P. C. M., & Mori, S. (2004). Fiber tract–based atlas of human white matter anatomy. Radiology, 230(1), 77–87. Scholar
  92. Wechsler, D. (2001). Wechsler test of adult. Reading: WTAR: Psychological Corporation.Google Scholar
  93. Yang, Z. Y., Quan, H., Peng, Z. L., Zhong, Y., Tan, Z. J., & Gong, Q. Y. (2015). Proton magnetic resonance spectroscopy revealed differences in the glutamate plus glutamine/creatine ratio of the anterior cingulate cortex between healthy and pediatric post-traumatic stress disorder patients diagnosed after 2008 Wenchuan earthquake. Psychiatry and Clinical Neurosciences, 69(12), 782–790. Scholar
  94. Yeh, F. C., & Tseng, W. Y. I. (2011). NTU-90: A high angular resolution brain atlas constructed by q-space diffeomorphic reconstruction. NeuroImage, 58(1), 91–99. Scholar
  95. Yeh, F. C., Verstynen, T. D., Wang, Y., Fernández-Miranda, J. C., & Tseng, W. Y. I. (2013). Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS One, 8(11), e80713. Scholar
  96. Yehuda, R., Lowy, M. T., Southwick, S. M., Shaffer, D., & Giller, E. L. (1991). Lymphocyte glucocorticoid receptor number in posttraumatic stress disorder. American Journal of Psychiatry, 148(4), 499–504. Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Nathaniel G. Harnett
    • 1
  • Edward W. FerenceIII
    • 2
  • Amy J. Knight
    • 2
  • David C. Knight
    • 1
    Email author
  1. 1.Department of PsychologyUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Department of Physical Medicine and RehabilitationUniversity of Alabama at BirminghamBirminghamUSA

Personalised recommendations