Utility of Magnetic Resonance Findings in Elucidating Structural and Functional Brain Impairment in Traumatic Brain Injury

  • Eduardo González-ToledoEmail author
  • Nicolás Fayed Miguel
  • Laura Viguera
  • Kanika Sharma
  • Piyush Kalakoti
  • Navdeep Samra
  • Anil Nanda
  • Hai Sun


Traumatic brain injury (TBI) is a major cause of death and disability in the United States, contributing to about 30% of all injury-related deaths. TBI survivors often develop clinical impairments and long-term disabilities. These include impaired thinking or memory, effects on movement and sensations such as vision, hearing, or emotional functioning including personality changes, depression, burst of anger, abnormal social behavior, and insomnia. These issues not only affect individuals but can have a deleterious impact on families and communities. The advances in computer software applied to a non-invasive acquisition of images containing digital data, provides us with objective examination of brain structure and function. Magnetic resonance (MR) imaging of the brain makes it possible to investigate morphological and functional connectivity without exposing the patient to ionizing radiations. In patients with TBI, computed tomography and conventional MR scans seldom show limited or no abnormalities to explain clinical symptomatology. For these reasons, we propose an “ad hoc” protocol that exploits advances in MR sequences to predict long-term outcomes including evaluation of cortical thickness, detecting hemosiderin deposits via magnetic susceptibility weighted images, to explore indemnity of fiber tracts using diffusion tensor with fractional anisotropy measurement, to assess metabolic changes in the frontal lobe and cingulate cortex by utilizing the properties of magnetic resonance spectroscopy, and lastly to detect abnormal connectivity in the brain networks via resting-state functional magnetic resonance imaging. Meticulous application of our protocol can potentially detect subtle abnormalities in patients with mild TBI such as detection of iron or mineral deposits, abnormal cortical thickness, abnormal metabolites, disruption of white matter tracts, and decreased or loss connectivity in brain networks. Application of special MR sequences as described in our protocol can optimize clinical outcomes, offer predictive capabilities of short and long-term prognosis, and aid in risk-stratification tailored upon individual comorbidities.


Traumatic brain injury Diffuse axonal injury DTI Rs-fMRI Cortical thickness Susceptibility imaging DWI MRS 


  1. 1.
    Kalakoti P, Notarianni C. Revisiting traumatic brain injury in the pediatric population. World Neurosurg. 2016;91:635–7.PubMedCrossRefGoogle Scholar
  2. 2.
    Menon DK, Schwab K, Wright DW, et al. Position statement: definition of traumatic brain injury. Arch Phys Med Rehabil. 2010;91(11):1637–40.PubMedCrossRefGoogle Scholar
  3. 3.
    McAllister TW. Neurobiological consequences of traumatic brain injury. Dialogues Clin Neurosci. 2011;13(3):287–300.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Centers for Disease Control and Prevention. Injury prevention & control: traumatic brain injury & concussion: rates of TBI-related emergency department visits, Hospitalizations, and deaths — United States, 2001–2010. Last accessed: 28 June 2016 [URL:].
  5. 5.
    Hyder AA, Wunderlich CA, Puvanachandra P, Gururaj G, Kobusingye OC. The impact of traumatic brain injuries: a global perspective. NeuroRehabilita​tion. 2007;22(5):341–53.Google Scholar
  6. 6.
    Langlois JA, Rutland-Brown W, Thomas KE. The incidence of traumatic brain injury among children in the United States: differences by race. J Head Trauma Rehabil. 2005;20(3):229–38.PubMedCrossRefGoogle Scholar
  7. 7.
    Reid SR, Roesler JS, Gaichas AM, Tsai AK. The epidemiology of pediatric traumatic brain injury in Minnesota. Arch Pediatr Adolesc Med. 2001;155(7):​784–9.PubMedCrossRefGoogle Scholar
  8. 8.
    Winthrop AL, Brasel KJ, Stahovic L, Paulson J, Schneeberger B, Kuhn EM. Quality of life and functional outcome after pediatric trauma. J Trauma. 2005;58(3):468–73; discussion 473–64.Google Scholar
  9. 9.
    Centers for Disease Control and Prevention. Injury prevention & control: traumatic brain injury & concussion: basic information. Last accessed: 28 June 2016 [URL:].
  10. 10.
    Rutland-Brown W, Langlois JA, Thomas KE, Xi YL. Incidence of traumatic brain injury in the United States, 2003. J Head Trauma Rehabil. 2006;21(6):544–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Centers for Disease Control and Prevention. Injury prevention & control: traumatic brain injury & concussion: basic information. Last accessed: 28 June 2016 [URL:].
  12. 12.
    Centers for Medicare & Medicaid Services, Office of the Actuary, National Health Statistics Group; U.S. Department of Commerce, Bureau of Economic Analysis; and U.S. Bureau of the Census. National health expenditure data. Last acessed: 28 June 2016 [URL:​AccountsHistorical.html].
  13. 13.
    Pangilinan PH, Kelly BM, Hornyak JEI, et al. Classification and complications of traumatic brain injury. Medscape. June 10, 2016 Last accessed: 16 June 2016 [URL:].
  14. 14.
    Adams JH, Graham DI, Jennett B. The structural basis of moderate disability after traumatic brain damage. J Neurol Neurosurg Psychiatry. 2001;71(4):521–4.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Evans SA, Airey MC, Chell SM, Connelly JB, Rigby AS, Tennant A. Disability in young adults following major trauma: 5 year follow up of survivors. BMC Public Health. 2003;3:8.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Chamelian L, Feinstein A. The effect of major depression on subjective and objective cognitive deficits in mild to moderate traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2006;18(1):33–8.PubMedCrossRefGoogle Scholar
  17. 17.
    Jorge RE, Robinson RG, Moser D, Tateno A, Crespo-Facorro B, Arndt S. Major depression following traumatic brain injury. Arch Gen Psychiatry. 2004;61(1):42–50.PubMedCrossRefGoogle Scholar
  18. 18.
    Fann JR, Burington B, Leonetti A, Jaffe K, Katon WJ, Thompson RS. Psychiatric illness following traumatic brain injury in an adult health maintenance organization population. Arch Gen Psychiatry. 2004;61(1):53–61.PubMedCrossRefGoogle Scholar
  19. 19.
    DeKosky ST, Blennow K, Ikonomovic MD, Gandy S. Acute and chronic traumatic encephalopathies: pathogenesis and biomarkers. Nat Rev Neurol. 2013;9(4):192–200.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Deb S, Burns J. Neuropsychiatric consequences of traumatic brain injury: a comparison between two age groups. Brain Inj. 2007;21(3):301–7.PubMedCrossRefGoogle Scholar
  21. 21.
    Till C, Colella B, Verwegen J, Green RE. Postrecovery cognitive decline in adults with traumatic brain injury. Arch Phys Med Rehabil. 2008;89(12 Suppl):S25–34.PubMedCrossRefGoogle Scholar
  22. 22.
    Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet. 1974;2(7872):81–4.PubMedCrossRefGoogle Scholar
  23. 23.
    National Institute for Clinical Excellence. Head injury: Triage, Assessment, Investigation and Early Management of Head Injury in Infants, Children and Adults. National Collaborating Centre for Acute Care (UK). Source London: National Collaborating Centre for Acute Care (UK); 2007.Google Scholar
  24. 24.
    Jones TR, Kaplan RT, Lane B, Atlas SW, Rubin GD. Single- versus multi-detector row CT of the brain: quality assessment. Radiology. 2001;219(3):750–5.PubMedCrossRefGoogle Scholar
  25. 25.
    Newberg AB, Alavi A. Neuroimaging in patients with head injury. Semin Nucl Med. 2003;33(2):136–47.PubMedCrossRefGoogle Scholar
  26. 26.
    Ogawa T, Sekino H, Uzura M, et al. Comparative study of magnetic resonance and CT scan imaging in cases of severe head injury. Acta Neurochir Suppl (Wien). 1992;55:8–10.Google Scholar
  27. 27.
    Levin HS, Amparo E, Eisenberg HM, et al. Magnetic resonance imaging and computerized tomography in relation to the neurobehavioral sequelae of mild and moderate head injuries. J Neurosurg. 1987;66(5):706–13.PubMedCrossRefGoogle Scholar
  28. 28.
    Lee H, Wintermark M, Gean AD, Ghajar J, Manley GT, Mukherjee P. Focal lesions in acute mild traumatic brain injury and neurocognitive outcome: CT versus 3 T MRI. J Neurotrauma. 2008;25(9):1049–56.PubMedCrossRefGoogle Scholar
  29. 29.
    Hammoud DA, Wasserman BA. Diffuse axonal injuries: pathophysiology and imaging. Neuroimaging Clin N Am. 2002;12(2):205–16.PubMedCrossRefGoogle Scholar
  30. 30.
    Hunter JV, Wilde EA, Tong KA, Holshouser BA. J Neurotrauma. 2012;29(4):654–71.Google Scholar
  31. 31.
    Abdelhalim AN, Alberico RA. Pediatric neuroimaging. Neurol Clin. 2009;27(1):285–301, x.Google Scholar
  32. 32.
    Ketonen LM, Valanne L. Neuroimaging of pediatric diseases. Semin Neurol. 2008;28(4):558–69.PubMedCrossRefGoogle Scholar
  33. 33.
    Dill T. Contraindications to magnetic resonance imaging: non-invasive imaging. Heart. 2008;94(7):943–8.PubMedCrossRefGoogle Scholar
  34. 34.
    Hesselink JR, Dowd CF, Healy ME, Hajek P, Baker LL, Luerssen TG. MR imaging of brain contusions: a comparative study with CT. AJR Am J Roentgenol. 1988;150(5):1133–42.PubMedCrossRefGoogle Scholar
  35. 35.
    Hughes DG, Jackson A, Mason DL, Berry E, Hollis S, Yates DW. Abnormalities on magnetic resonance imaging seen acutely following mild traumatic brain injury: correlation with neuropsychological tests and delayed recovery. Neuroradiology. 2004;46(7):550–8.PubMedCrossRefGoogle Scholar
  36. 36.
    Wilberger Jr JE, Rothfus WE, Tabas J, Goldberg AL, Deeb ZL. Acute tissue tear hemorrhages of the brain: computed tomography and clinicopathological correlations. Neurosurgery. 1990;27(2):208–13.PubMedCrossRefGoogle Scholar
  37. 37.
    Yuh EL, Mukherjee P, Lingsma HF, et al. Magnetic resonance imaging improves 3-month outcome prediction in mild traumatic brain injury. Ann Neurol. 2013;73(2):224–35.PubMedCrossRefGoogle Scholar
  38. 38.
    Garnett MR, Cadoux-Hudson TA, Styles P. How useful is magnetic resonance imaging in predicting severity and outcome in traumatic brain injury? Curr Opin Neurol. 2001;14(6):753–7.PubMedCrossRefGoogle Scholar
  39. 39.
    Mittl RL, Grossman RI, Hiehle JF, et al. Prevalence of MR evidence of diffuse axonal injury in patients with mild head injury and normal head CT findings. AJNR. Am J Neuroradiol. 1994;15(8):1583–9.PubMedGoogle Scholar
  40. 40.
    Kampfl A, Franz G, Aichner F, et al. The persistent vegetative state after closed head injury: clinical and magnetic resonance imaging findings in 42 patients. J Neurosurg. 1998;88(5):809–16.PubMedCrossRefGoogle Scholar
  41. 41.
    Kampfl A, Schmutzhard E, Franz G, et al. Prediction of recovery from post-traumatic vegetative state with cerebral magnetic-resonance imaging. Lancet. 1998;351(9118):1763–7.PubMedCrossRefGoogle Scholar
  42. 42.
    Coles JP. Imaging after brain injury. Br J Anaesth. 2007;99(1):49–60.PubMedCrossRefGoogle Scholar
  43. 43.
    Haacke EM, Xu Y, Cheng YC, Reichenbach JR. Susceptibility weighted imaging (SWI). Magn Reson Med. 2004;52(3):612–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Hofer S, Frahm J. Topography of the human corpus callosum revisited – comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. Neuroimage. 2006;32(3):989–94.PubMedCrossRefGoogle Scholar
  45. 45.
    Bigler ED, Bazarian JJ. Diffusion tensor imaging: a biomarker for mild traumatic brain injury? Neurology. 2010;74(8):626–7.PubMedCrossRefGoogle Scholar
  46. 46.
    Mac Donald CL, Johnson AM, Cooper D, et al. Detection of blast-related traumatic brain injury in U.S. military personnel. N Engl J Med. 2011;364(22):2091–100.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Mayer AR, Ling J, Mannell MV, et al. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology. 2010;74(8):643–50.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Wilde EA, McCauley SR, Hunter JV, et al. Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology. 2008;​70(12):948–55.PubMedCrossRefGoogle Scholar
  49. 49.
    Brandstack N, Kurki T, Tenovuo O. Quantitative diffusion-tensor tractography of long association tracts in patients with traumatic brain injury without associated findings at routine MR imaging. Radiology. 2013;267(1):231–9.PubMedCrossRefGoogle Scholar
  50. 50.
    Lipton ML, Gulko E, Zimmerman ME, et al. Diffusion-tensor imaging implicates prefrontal axonal injury in executive function impairment following very mild traumatic brain injury. Radiology. 2009;252(3):816–24.PubMedCrossRefGoogle Scholar
  51. 51.
    Arfanakis K, Haughton VM, Carew JD, Rogers BP, Dempsey RJ, Meyerand ME. Diffusion tensor MR imaging in diffuse axonal injury. AJNR Am J Neuroradiol. 2002;23(5):794–802.PubMedGoogle Scholar
  52. 52.
    Huisman TA, Schwamm LH, Schaefer PW, et al. Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. AJNR Am J Neuroradiol. 2004;25(3):370–6.PubMedGoogle Scholar
  53. 53.
    Perlbarg V, Puybasset L, Tollard E, Lehericy S, Benali H, Galanaud D. Relation between brain lesion location and clinical outcome in patients with severe traumatic brain injury: a diffusion tensor imaging study using voxel-based approaches. Hum Brain Mapp. 2009;30(12):3924–33.PubMedCrossRefGoogle Scholar
  54. 54.
    Greenberg G, Mikulis DJ, Ng K, DeSouza D, Green RE. Use of diffusion tensor imaging to examine subacute white matter injury progression in moderate to severe traumatic brain injury. Arch Phys Med Rehabil. 2008;89(12 Suppl):S45–50.PubMedCrossRefGoogle Scholar
  55. 55.
    Bhadelia RA, Price LL, Tedesco KL, et al. Diffusion tensor imaging, white matter lesions, the corpus callosum, and gait in the elderly. Stroke J Cereb Circ. 2009;40(12):3816–20.CrossRefGoogle Scholar
  56. 56.
    Angelini L, Mazzucchi A, Picciotto F, Nardocci N, Broggi G. Focal lesion of the right cingulum: a case report in a child. J Neurol Neurosurg Psychiatry. 1981;44(4):355–7.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Metzler-Baddeley C, Jones DK, Steventon J, Westacott L, Aggleton JP, O'Sullivan MJ. Cingulum microstructure predicts cognitive control in older age and mild cognitive impairment. J Neurosci. 2012;32(49):17612–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain J Neurol. 1995;118(Pt 1):279–306.CrossRefGoogle Scholar
  59. 59.
    Chanraud S, Zahr N, Sullivan EV, Pfefferbaum A. MR diffusion tensor imaging: a window into white matter integrity of the working brain. Neuropsychol Rev. 2010;20(2):209–25.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Virji-Babul N, Borich MR, Makan N, et al. Diffusion tensor imaging of sports-related concussion in adolescents. Pediatr Neurol. 2013;48(1):24–9.PubMedCrossRefGoogle Scholar
  61. 61.
    Gu L, Li J, Feng DF, et al. Detection of white matter lesions in the acute stage of diffuse axonal injury predicts long-term cognitive impairments: a clinical diffusion tensor imaging study. J Trauma Acute Care Surg. 2013;74(1):242–7.PubMedCrossRefGoogle Scholar
  62. 62.
    Von Der Heide RJ, Skipper LM, Klobusicky E, Olson IR. Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. Brain J Neurol. 2013;136(Pt 6):1692–707.CrossRefGoogle Scholar
  63. 63.
    Barkley JM, Morales D, Hayman LA, Diaz-Marchan PJ. Static neuroimaging in the evaluation of TBI. In: Zasler ND, Katz DI, Zafonte RD, editors. Brain injury medicine: principles and practice. New York: Demos; 2007.Google Scholar
  64. 64.
    Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 1999;9(2):179–94.PubMedCrossRefGoogle Scholar
  65. 65.
    Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A. 2000;97(20):11050–5.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage. 1999;9(2):195–207.PubMedCrossRefGoogle Scholar
  67. 67.
    Kim JS, Singh V, Lee JK, et al. Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification. Neuroimage. 2005;27(1):210–21.PubMedCrossRefGoogle Scholar
  68. 68.
    Palacios EM, Sala-Llonch R, Junque C, et al. Long-term declarative memory deficits in diffuse TBI: correlations with cortical thickness, white matter integrity and hippocampal volume. Cortex. 2013;49(3):646–57.PubMedCrossRefGoogle Scholar
  69. 69.
    Tomaiuolo F, Carlesimo GA, Di Paola M, et al. Gross morphology and morphometric sequelae in the hippocampus, fornix, and corpus callosum of patients with severe non-missile traumatic brain injury without macroscopically detectable lesions: a T1 weighted MRI study. J Neurol Neurosurg Psychiatry. 2004;75(9):1314–22.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Turken AU, Herron TJ, Kang X, et al. Multimodal surface-based morphometry reveals diffuse cortical atrophy in traumatic brain injury. BMC Med Imaging. 2009;9:20.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Yang F, Kruggel F. Automatic segmentation of human brain sulci. Med Image Anal. 2008;12(4):442–51.PubMedCrossRefGoogle Scholar
  72. 72.
    Han X, Xu C, Tosun D, Prince JL. Cortical surface reconstruction using a topology preserving geometric deformable model. In: Proceedings of the IEEE Workshop on Mathematical Methods in Biomedical Image Analysis (MMBIA '01); December 2001; p. 213–20.Google Scholar
  73. 73.
    Han X, Xu C, Prince JL. A topology preserving level set method for geometric deformable models. IEEE Trans Pattern Anal Mach Intell. 2003;25(6):755–68.CrossRefGoogle Scholar
  74. 74.
    Yezzi A, Prince JL. A PDE approach for measuring tissue thickness. In: Proceedings of the IEEE Computer Society Conference on Computer Vision and Pattern Recognition (CVPR '01), vol. 1; December 2001; p. I87–I92.Google Scholar
  75. 75.
    Rocha KR, Yezzi Jr AJ, Prince JL. A hybrid Eulerian–Lagrangian approach for thickness, correspondence, and gridding of annular tissues. IEEE Trans Image Process. 2007;16(3):636–48.PubMedCrossRefGoogle Scholar
  76. 76.
    Kruggel F, von Cramon DY. Measuring the cortical thickness. In: Proceedings of the IEEE Workshop on Mathematical Methods in Biomedical Image Analysis (MMBIA '00); June 2000; p. 154–61.Google Scholar
  77. 77.
    Osechinskiy S, Kruggel F. PDE-based reconstruction of the cerebral cortex from MR images. Conf Proc IEEE Eng Med Biol Soc. 2010;2010:4278–83.PubMedGoogle Scholar
  78. 78.
    Michael AP, Stout J, Roskos PT, et al. Evaluation of cortical thickness after traumatic brain injury in military veterans. J Neurotrauma. 2015;32(22):1751–8.PubMedCrossRefGoogle Scholar
  79. 79.
    Wilde EA, Merkley TL, Bigler ED, et al. Longitudinal changes in cortical thickness in children after traumatic brain injury and their relation to behavioral regulation and emotional control. Int J Dev Neurosci Off J Int Soc Dev Neurosci. 2012;30(3):267–76.CrossRefGoogle Scholar
  80. 80.
    Wilde EA, Newsome MR, Bigler ED, et al. Brain imaging correlates of verbal working memory in children following traumatic brain injury. Int J Psychophysiol Off J Int Organ Psychophysiol. 2011;82(1):86–96.Google Scholar
  81. 81.
    Wang X, Xie H, Cotton AS, et al. Early cortical thickness change after mild traumatic brain injury following motor vehicle collision. J Neurotrauma. 2015;32(7):455–63.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Wintermark M, Sanelli PC, Anzai Y, Tsiouris AJ, Whitlow CT, American College of Radiology Head Injury Institute. Imaging evidence and recommendations for traumatic brain injury: advanced neuro- and neurovascular imaging techniques. AJNR Am J Neuroradiol. 2015;36(2):E1–E11.PubMedCrossRefGoogle Scholar
  83. 83.
    Walz NC, Cecil KM, Wade SL, Michaud LJ. Late proton magnetic resonance spectroscopy following traumatic brain injury during early childhood: relationship with neurobehavioral outcomes. J Neurotrauma. 2008;25(2):94–103.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Babikian T, Freier MC, Ashwal S, Riggs ML, Burley T, Holshouser BA. MR spectroscopy: predicting long-term neuropsychological outcome following pediatric TBI. J Magn Reson Imaging JMRI. 2006;24(4):801–11.PubMedCrossRefGoogle Scholar
  85. 85.
    Parry L, Shores A, Rae C, et al. An investigation of neuronal integrity in severe paediatric traumatic brain injury. Child Neuropsychol J Norm Abnorm Dev Child Adolesc. 2004;10(4):248–61.Google Scholar
  86. 86.
    Ashwal S, Holshouser BA, Shu SK, et al. Predictive value of proton magnetic resonance spectroscopy in pediatric closed head injury. Pediatr Neurol. 2000;23(2):114–25.PubMedCrossRefGoogle Scholar
  87. 87.
    Kasahara M, Menon DK, Salmond CH, et al. Traumatic brain injury alters the functional brain network mediating working memory. Brain Inj. 2011;25(12):1170–87.PubMedCrossRefGoogle Scholar
  88. 88.
    Marquez de la Plata CD, Garces J, Shokri Kojori E, et al. Deficits in functional connectivity of hippocampal and frontal lobe circuits after traumatic axonal injury. Arch Neurol. 2011;68(1):74–84.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Palacios EM, Sala-Llonch R, Junque C, et al. White matter integrity related to functional working memory networks in traumatic brain injury. Neurology. 2012;78(12):852–60.PubMedCrossRefGoogle Scholar
  90. 90.
    Sharp DJ, Beckmann CF, Greenwood R, et al. Default mode network functional and structural connectivity after traumatic brain injury. Brain J Neurol. 2011;134(Pt 8):2233–47.CrossRefGoogle Scholar
  91. 91.
    Arenivas A, Diaz-Arrastia R, Spence J, et al. Three approaches to investigating functional compromise to the default mode network after traumatic axonal injury. Brain Imaging Behav. 2014;8(3):407–19.PubMedCrossRefGoogle Scholar
  92. 92.
    Bonnelle V, Ham TE, Leech R, et al. Salience network integrity predicts default mode network function after traumatic brain injury. Proc Natl Acad Sci U S A. 2012;109(12):4690–5.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Hillary FG, Slocomb J, Hills EC, et al. Changes in resting connectivity during recovery from severe traumatic brain injury. Int J Psychophysiol Off J Int Organ Psychophysiol. 2011;82(1):115–23.Google Scholar
  94. 94.
    Mayer AR, Mannell MV, Ling J, Gasparovic C, Yeo RA. Functional connectivity in mild traumatic brain injury. Hum Brain Mapp. 2011;32(11):1825–35.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Shumskaya E, Andriessen TM, Norris DG, Vos PE. Abnormal whole-brain functional networks in homogeneous acute mild traumatic brain injury. Neurology. 2012;79(2):175–82.PubMedCrossRefGoogle Scholar
  96. 96.
    Slobounov SM, Gay M, Zhang K, et al. Alteration of brain functional network at rest and in response to YMCA physical stress test in concussed athletes: RsFMRI study. Neuroimage. 2011;55(4):1716–27.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Smith SM, Fox PT, Miller KL, et al. Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A. 2009;106(31):13040–5.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Buckner RL, Andrews-Hanna JR, Schacter DL. The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci. 2008;1124:1–38.PubMedCrossRefGoogle Scholar
  99. 99.
    Ding K, Marquez de la Plata C, Wang JY, et al. Cerebral atrophy after traumatic white matter injury: correlation with acute neuroimaging and outcome. J Neurotrauma. 2008;25(12):1433–40.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Gale SD, Baxter L, Roundy N, Johnson SC. Traumatic brain injury and grey matter concentration: a preliminary voxel-based morphometry study. J Neurol Neurosurg Psychiatry. 2005;76(7):984–8.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Lindemer ER, Salat DH, Leritz EC, McGlinchey RE, Milberg WP. Reduced cortical thickness with increased lifetime burden of PTSD in OEF/OIF Veterans and the impact of comorbid TBI. Neuroimage Clin. 2013;2:601–11.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Maxwell WL, MacKinnon MA, Stewart JE, Graham DI. Stereology of cerebral cortex after traumatic brain injury matched to the Glasgow outcome score. Brain J Neurol. 2010;133(Pt 1):139–60.CrossRefGoogle Scholar
  103. 103.
    Merkley TL, Bigler ED, Wilde EA, McCauley SR, Hunter JV, Levin HS. Diffuse changes in cortical thickness in pediatric moderate-to-severe traumatic brain injury. J Neurotrauma. 2008;25(11):1343–5.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Warner MA, Youn TS, Davis T, et al. Regionally selective atrophy after traumatic axonal injury. Arch Neurol. 2010;67(11):1336–44.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Wilde EA, Hunter JV, Newsome MR, et al. Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury. J Neurotrauma. 2005;22(3):333–44.PubMedCrossRefGoogle Scholar
  106. 106.
    Bendlin BB, Ries ML, Lazar M, et al. Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage. 2008;42(2):503–14.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Kim EY, Park HJ, Kim DH, Lee SK, Kim J. Measuring fractional anisotropy of the corpus callosum using diffusion tensor imaging: mid-sagittal versus axial imaging planes. Korean J Radiol. 2008;9(5):391–5.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Gale SD, Johnson SC, Bigler ED, Blatter DD. Nonspecific white matter degeneration following traumatic brain injury. J Int Neuropsychol Soc. 1995;1(1):17–28.PubMedCrossRefGoogle Scholar
  109. 109.
    Kennedy MR, Wozniak JR, Muetzel RL, et al. White matter and neurocognitive changes in adults with chronic traumatic brain injury. J Int Neuropsychol Soc. 2009;15(1):130–6.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Kraus MF, Susmaras T, Caughlin BP, Walker CJ, Sweeney JA, Little DM. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain J Neurol. 2007;130(Pt 10):2508–19.CrossRefGoogle Scholar
  111. 111.
    Kumar R, Husain M, Gupta RK, et al. Serial changes in the white matter diffusion tensor imaging metrics in moderate traumatic brain injury and correlation with neuro-cognitive function. J Neurotrauma. 2009;26(4):481–95.PubMedCrossRefGoogle Scholar
  112. 112.
    Lipton ML, Gellella E, Lo C, et al. Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of diffusion tensor imaging. J Neurotrauma. 2008;25(11):1335–42.PubMedCrossRefGoogle Scholar
  113. 113.
    Mac Donald CL, Dikranian K, Bayly P, Holtzman D, Brody D. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J Neurosci. 2007;27(44):11869–76.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Maller JJ, Thomson RH, Lewis PM, Rose SE, Pannek K, Fitzgerald PB. Traumatic brain injury, major depression, and diffusion tensor imaging: making connections. Brain Res Rev. 2010;64(1):213–40.PubMedCrossRefGoogle Scholar
  115. 115.
    Marsh PD, Keevil CW, McDermid AS, Williamson MI, Ellwood DC. Inhibition by the antimicrobial agent chlorhexidine of acid production and sugar transport in oral streptococcal bacteria. Arch Oral Biol. 1983;28(3):233–40.PubMedCrossRefGoogle Scholar
  116. 116.
    Nakayama N, Okumura A, Shinoda J, et al. Evidence for white matter disruption in traumatic brain injury without macroscopic lesions. J Neurol Neurosurg Psychiatry. 2006;77(7):850–5.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Niogi SN, Mukherjee P, Ghajar J, et al. Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3 T diffusion tensor imaging study of mild traumatic brain injury. AJNR Am J Neuroradiol. 2008;29(5):967–73.PubMedCrossRefGoogle Scholar
  118. 118.
    Wada T, Asano Y, Shinoda J. Decreased fractional anisotropy evaluated using tract-based spatial statistics and correlated with cognitive dysfunction in patients with mild traumatic brain injury in the chronic stage. AJNR Am J Neuroradiol. 2012;33(11):2117–22.PubMedCrossRefGoogle Scholar
  119. 119.
    Westlye LT, Walhovd KB, Bjornerud A, Due-Tonnessen P, Fjell AM. Error-related negativity is mediated by fractional anisotropy in the posterior cingulate gyrus — a study combining diffusion tensor imaging and electrophysiology in healthy adults. Cereb Cortex. 2009;19(2):293–304.PubMedCrossRefGoogle Scholar
  120. 120.
    Zappala G, Thiebaut de Schotten M, Eslinger PJ. Traumatic brain injury and the frontal lobes: what can we gain with diffusion tensor imaging? Cortex. 2012;48(2):156–65.PubMedCrossRefGoogle Scholar
  121. 121.
    Cohen BA, Inglese M, Rusinek H, Babb JS, Grossman RI, Gonen O. Proton MR spectroscopy and MRI-volumetry in mild traumatic brain injury. AJNR Am J Neuroradiol. 2007;28(5):907–13.PubMedGoogle Scholar
  122. 122.
    Garnett MR, Blamire AM, Corkill RG, Cadoux-Hudson TA, Rajagopalan B, Styles P. Early proton magnetic resonance spectroscopy in normal-appearing brain correlates with outcome in patients following traumatic brain injury. Brain J Neurol. 2000;123(Pt 10):2046–54.CrossRefGoogle Scholar
  123. 123.
    Pandit AS, Expert P, Lambiotte R, et al. Traumatic brain injury impairs small-world topology. Neurology. 2013;80(20):1826–33.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    van den Heuvel M, Mandl R, Luigjes J, Hulshoff PH. Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci. 2008;28(43):10844–51.PubMedCrossRefGoogle Scholar
  125. 125.
    Fujiwara E, Schwartz ML, Gao F, Black SE, Levine B. Ventral frontal cortex functions and quantified MRI in traumatic brain injury. Neuropsychologia. 2008;46(2):461–74.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Eduardo González-Toledo
    • 1
    Email author
  • Nicolás Fayed Miguel
    • 2
  • Laura Viguera
    • 3
  • Kanika Sharma
    • 4
  • Piyush Kalakoti
    • 4
  • Navdeep Samra
    • 5
  • Anil Nanda
    • 4
  • Hai Sun
    • 4
  1. 1.Department of Radiology, Neurology, and AnesthesiologyLouisiana State University Health Sciences CenterShreveportUSA
  2. 2.RadiologyHospital QuironMadridSpain
  3. 3.Miguel Servet University Hospital, University of ZaragozaZaragozaSpain
  4. 4.NeurosurgeryLouisiana State University Health Sciences CenterShreveportUSA
  5. 5.Trauma and Surgical Critical CareLouisiana State University Health Sciences CenterShreveportUSA

Personalised recommendations