Advertisement

Subcortical shape and neuropsychological function among U.S. service members with mild traumatic brain injury

  • David F. Tate
  • Benjamin S. C. Wade
  • Carmen S. Velez
  • Ann Marie Drennon
  • Jacob D. Bolzenius
  • Douglas B. Cooper
  • Jan E. Kennedy
  • Matthew W. Reid
  • Amy O. Bowles
  • Paul M. Thompson
  • Boris A. Gutman
  • Jeffrey D. Lewis
  • John L. Ritter
  • Gerald E. York
  • Erin D. Bigler
ORIGINAL RESEARCH

Abstract

In a recent manuscript, our group demonstrated shape differences in the thalamus, nucleus accumbens, and amygdala in a cohort of U.S. Service Members with mild traumatic brain injury (mTBI). Given the significant role these structures play in cognitive function, this study directly examined the relationship between shape metrics and neuropsychological performance. The imaging and neuropsychological data from 135 post-deployed United States Service Members from two groups (mTBI and orthopedic injured) were examined. Two shape features modeling local deformations in thickness (RD) and surface area (JD) were defined vertex-wise on parametric mesh-representations of 7 bilateral subcortical gray matter structures. Linear regression was used to model associations between subcortical morphometry and neuropsychological performance as a function of either TBI status or, among TBI patients, subjective reporting of initial concussion severity (CS). Results demonstrated several significant group-by-cognition relationships with shape metrics across multiple cognitive domains including processing speed, memory, and executive function. Higher processing speed was robustly associated with more dilation of caudate surface area among patients with mTBI who reported more than one CS variables (loss of consciousness (LOC), alteration of consciousness (AOC), and/or post-traumatic amnesia (PTA)). These significant patterns indicate the importance of subcortical structures in cognitive performance and support a growing functional neuroanatomical literature in TBI and other neurologic disorders. However, prospective research will be required before exact directional evolution and progression of shape can be understood and utilized in predicting or tracking cognitive outcomes in this patient population.

Keywords

Mild traumatic brain Injury Subcortical structures Shape analysis Service Members Neuropsychological function Brain behavior relationships 

Notes

Acknowledgements

The view(s) expressed herein are those of the author and do not reflect the official policy or position of the Defense and Veterans Brain Injury Center, Brooke Army Medical Center, the U.S. Army Medical Department, the U.S. Army Office of the Surgeon General, the Department of the Army, Department of Defense, or the U.S. Government.

We also gratefully acknowledge the generous time and effort that the Service Members made in supporting this study. We also gratefully acknowledge the clinical effort and expertise of the Brooke Army Medical Center Brain Injury and Rehabilitation Service staff in the identification, recruitment, consenting, and treatment of Service Members who are a part of this study.

Funding

This work is supported in part by the Defense and Veterans Brain Injury Centers, the U.S. Army Medical Research and Materiel Command (USAMRMC; W81XWH-13-2-0025) and the Chronic Effects of Neurotrauma Consortium (CENC; PT108802-SC104835).

Compliance with ethical standards.

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

Conflict of interest

The authors have no conflicts of interest to disclose.

Supplementary material

11682_2018_9854_MOESM1_ESM.docx (3.5 mb)
Supplementary material 1 (DOCX 3571 KB)

References

  1. Almeida, O. P., Garrido, G. J., Beer, C., Lautenschlager, N. T., Arnolda, L., & Flicker, L. (2012). Cognitive and brain changes associated with ischaemic heart disease and heart failure. European Heart Journal, 33(14), 1769–1776.  https://doi.org/10.1093/eurheartj/ehr467.CrossRefPubMedGoogle Scholar
  2. Arend, I., Rafal, R., & Ward, R. (2008). Spatial and temporal deficits are regionally dissociable in patients with pulvinar lesions. Brain 131(Pt 8):2140–2152.  https://doi.org/10.1093/brain/awn135.CrossRefPubMedGoogle Scholar
  3. Baldo, B. A., Pratt, W. E., Will, M. J., Hanlon, E. C., Bakshi, V. P., & Cador, M. (2013). Principles of motivation revealed by the diverse functions of neuropharmacological and neuroanatomical substrates underlying feeding behavior. Neuroscience and Biobehavioral Reviews, 37(9 Pt A):1985-98.  https://doi.org/10.1016/j.neubiorev.2013.02.017.PubMedGoogle Scholar
  4. Barker-Collo, S., Jones, K., Theadom, A., Starkey, N., Dowell, A., McPherson, K., Ameratunga, S., Dudley, M., Te Ao, B., Feigin, V., & Bionic Research Group. (2015). Neuropsychological outcome and its correlates in the first year after adult mild traumatic brain injury: a population-based New Zealand study. Brain Injury, 29(13–14):1604–1616.  https://doi.org/10.3109/02699052.2015.1075143.CrossRefPubMedGoogle Scholar
  5. Barrett, K., Ward, A. B., Boughey, A., Jones, M., & Mychalkiw, W. (1994). Sequelae of minor head injury: the natural history of post-concussive symptoms and their relationship to loss of consciousness and follow-up. Journal of Accident & Emergency Medicine, 11(2), 79–84.CrossRefGoogle Scholar
  6. Bergsland, N., Zivadinov, R., Dwyer, M. G., Weinstock-Guttman, B., & Benedict, R. H. (2016). Localized atrophy of the thalamus and slowed cognitive processing speed in MS patients. " Mult Scler, 22(10), 1327–1336.  https://doi.org/10.1177/1352458515616204.CrossRefPubMedGoogle Scholar
  7. Bigler, E. D. (2015). Structural image analysis of the brain in neuropsychology using Magnetic Resonance Imaging (MRI) techniques. Neuropsychology Review, 25(3), 224 – 49.  https://doi.org/10.1007/s11065-015-9290-0.CrossRefPubMedGoogle Scholar
  8. Bigler, E. D., Abildskov, T. J., Petrie, J., Farrer, T. J., Dennis, M., Simic, N., Taylor, H. G., Rubin, K. H., Vannatta, K., Gerhardt, C. A., Stancin, T., & Owen Yeates, K. (2013). Heterogeneity of brain lesions in pediatric traumatic brain injury. Neuropsychology, 27(4), 438 – 51.  https://doi.org/10.1037/a0032837.CrossRefPubMedGoogle Scholar
  9. Brenner, L. A., Betthauser, L. M., Bahraini, N., Lusk, J. L., Terrio, H., Scher, A. I., & Schwab, K. A. (2015). Soldiers returning from deployment: a qualitative study regarding exposure, coping, and reintegration. Rehabilitation Psychology, 60(3), 277 – 85.  https://doi.org/10.1037/rep0000048.CrossRefPubMedGoogle Scholar
  10. Churchill, N., Hutchison, M., Richards, D., Leung, G., Graham, S., & Schweizer, T. A. (2016). Brain structure and function associated with a history of sport concussion: a multi-modal magnetic resonance imaging study. Journal of Neurotrauma, 34(4), 765-771.  https://doi.org/10.1089/neu.2016.4531.CrossRefPubMedGoogle Scholar
  11. Clark, A. L., Amick, M. M., Fortier, C., Milberg, W. P., & McGlinchey, R. E. (2014). Poor performance validity predicts clinical characteristics and cognitive test performance of OEF/OIF/OND Veterans in a research setting. The Clinical Neuropsychologist, 28(5), 802 – 25.  https://doi.org/10.1080/13854046.2014.904928.CrossRefPubMedGoogle Scholar
  12. Danziger, S., Ward, R., Owen, V., & Rafal, R. (2004). Contributions of the human pulvinar to linking vision and action. Cognitive, Affective, & Behavioral Neuroscience, 4(1), 89–99.CrossRefGoogle Scholar
  13. Delgado, M. R., Nystrom, L. E., Fissell, C., Noll, D. C., & Fiez, J. A. (2000). Tracking the hemodynamic responses to reward and punishment in the striatum. Journal of Neurophysiology, 84(6), 3072–3077.CrossRefPubMedGoogle Scholar
  14. Delgado, M. R., Stenger, V. A., & Fiez, J. A. (2004). Motivation-dependent responses in the human caudate nucleus. Cerebral Cortex, 14(9), 1022–1030.  https://doi.org/10.1093/cercor/bhh062.CrossRefPubMedGoogle Scholar
  15. Derauf, C., Lester, B. M., Neyzi, N., Kekatpure, M., Gracia, L., Davis, J., Kallianpur, K., Efird, J. T., & Kosofsky, B. (2012). Subcortical and cortical structural central nervous system changes and attention processing deficits in preschool-aged children with prenatal methamphetamine and tobacco exposure. Developmental Neuroscience, 34(4), 327 – 41.  https://doi.org/10.1159/000341119.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Elliott, R., Friston, K. J., & Dolan, R. J. (2000). Dissociable neural responses in human reward systems. The Journal of Neuroscience, 20(16), 6159–6165.PubMedGoogle Scholar
  17. Gale, S. D., Baxter, L., Roundy, N., & Johnson, S. C. (2005). Traumatic brain injury and grey matter concentration: a preliminary voxel based morphometry study. Journal of Neurology, Neurosurgery, and Psychiatry, 76(7), 984–988.  https://doi.org/10.1136/jnnp.2004.036210.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Grahn, J. A., Parkinson, J. A., & Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Progress in Neurobiology, 86(3), 141 – 55.  https://doi.org/10.1016/j.pneurobio.2008.09.004.CrossRefPubMedGoogle Scholar
  19. Grossman, E. J., & Inglese, M. (2016). The Role of thalamic damage in mild traumatic brain injury. Journal of Neurotrauma, 33(2), 163–167.  https://doi.org/10.1089/neu.2015.3965.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Haacke, E. M., Duhaime, A. C., Gean, A. D., Riedy, G., Wintermark, M., Mukherjee, P., Brody, D. L., DeGraba, T., Duncan, T. D., Elovic, E., Hurley, R., Latour, L., Smirniotopoulos, J. G., & Smith, D. H. (2010). Common data elements in radiologic imaging of traumatic brain injury. Journal of Magnetic Resonance Imaging, 32(3), 516 – 43.  https://doi.org/10.1002/jmri.22259.CrossRefPubMedGoogle Scholar
  21. Harrington, D. L., Liu, D., Smith, M. M., Mills, J. A., Long, J. D., Aylward, E. H., & Paulsen, J. S. (2014). Neuroanatomical correlates of cognitive functioning in prodromal Huntington disease. Brain and Behavior, 4(1), 29–40.  https://doi.org/10.1002/brb3.185.CrossRefPubMedGoogle Scholar
  22. Irimia, A., Goh, S. Y., Torgerson, C. M., Vespa, P., & Van Horn, J. D. (2014). Structural and connectomic neuroimaging for the personalized study of longitudinal alterations in cortical shape, thickness and connectivity after traumatic brain injury. Journal of Neurosurgical Sciences, 58(3), 129 – 44.PubMedPubMedCentralGoogle Scholar
  23. Iverson, G. L., Lovell, M. R., & Smith, S. S. (2000). Does brief loss of consciousness affect cognitive functioning after mild head injury? Archives of Clinical Neuropsychology, 15(7), 643–648.CrossRefPubMedGoogle Scholar
  24. Janak, P. H., & Tye, K. M. (2015). From circuits to behaviour in the amygdala. Nature, 517(7534), 284 – 92.  https://doi.org/10.1038/nature14188.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jurick, S. M., Bangen, K. J., Evangelista, N. D., Sanderson-Cimino, M., Delano-Wood, L., & Jak, A. J. (2016). Advanced neuroimaging to quantify myelin in vivo: application to mild TBI. Brain Injury, 30(12), 1452–1457.  https://doi.org/10.1080/02699052.2016.1219064.CrossRefPubMedGoogle Scholar
  26. Jurick, S. M., Twamley, E. W., Crocker, L. D., Hays, C. C., Orff, H. J., Golshan, S., & Jak, A. J. (2016). Postconcussive symptom overreporting in Iraq/Afghanistan Veterans with mild traumatic brain injury. Journal of Rehabilitation Research and Development, 53(5), 571–584.  https://doi.org/10.1682/JRRD.2015.05.0094.CrossRefPubMedGoogle Scholar
  27. Kalivas, P. W., & Volkow, N. D. (2005). The neural basis of addiction: a pathology of motivation and choice. The American Journal of Psychiatry, 162(8), 1403–1413.  https://doi.org/10.1176/appi.ajp.162.8.1403.CrossRefPubMedGoogle Scholar
  28. Kim, G. H., Lee, J. H., Seo, S. W., Kim, J. H., Seong, J. K., Ye, B. S., Cho, H., Noh, Y., Kim, H. J., Yoon, C. W., Oh, S. J., Kim, J. S., Choe, Y. S., Lee, K. H., Kim, S. T., Hwang, J. W., Jeong, J. H., & Na, D. L. (2015). Hippocampal volume and shape in pure subcortical vascular dementia. " Neurobiol Aging, 36(1), 485 – 91.  https://doi.org/10.1016/j.neurobiolaging.2014.08.009.CrossRefPubMedGoogle Scholar
  29. Kirouac, G. J. 2015. Placing the paraventricular nucleus of the thalamus within the brain circuits that control behavior. Neurosci Biobehav Rev 56, 315 – 29.  https://doi.org/10.1016/j.neubiorev.2015.08.005.CrossRefPubMedGoogle Scholar
  30. Koerte, I. K., Hufschmidt, J., Muehlmann, M., Lin, A. P., & Shenton, M. E. (2016). Advanced neuroimaging of mild traumatic brain injury. Translational Research in Traumatic Brain Injury, edited by D. Laskowitz and G. Grant. Boca Raton (FL).Google Scholar
  31. Little, D. M., Kraus, M. F., Joseph, J., Geary, E. K., Susmaras, T., Zhou, X. J., Pliskin, N., & Gorelick, P. B. (2010). Thalamic integrity underlies executive dysfunction in traumatic brain injury. Neurology, 74(7), 558 – 64.  https://doi.org/10.1212/WNL.0b013e3181cff5d5.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Lutkenhoff, E. S., McArthur, D. L., Hua, X., Thompson, P. M., Vespa, P. M., & Monti, M. M. (2013). Thalamic atrophy in antero-medial and dorsal nuclei correlates with six-month outcome after severe brain injury. Neuroimage Clincal, 3, 396–404.  https://doi.org/10.1016/j.nicl.2013.09.010.CrossRefGoogle Scholar
  33. Macfarlane, M. D., Jakabek, D., Walterfang, M., Vestberg, S., Velakoulis, D., Wilkes, F. A., Nilsson, C., van Westen, D., Looi, J. C., & Santillo, A. F. (2015). Striatal atrophy in the behavioural variant of frontotemporal dementia: correlation with diagnosis, negative symptoms and disease severity. PLoS One, 10(6), e0129692.  https://doi.org/10.1371/journal.pone.0129692.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Machts, J., Loewe, K., Kaufmann, J., Jakubiczka, S., Abdulla, S., Petri, S., Dengler, R., Heinze, H. J., Vielhaber, S., Schoenfeld, M. A., & Bede, P. (2015). Basal ganglia pathology in ALS is associated with neuropsychological deficits. Neurology, 85(15), 1301–1309.  https://doi.org/10.1212/WNL.0000000000002017.CrossRefPubMedGoogle Scholar
  35. Martikainen, K. K., Seppa, K., Viita, P. M., Rajala, S. A., Luukkaala, T. H., & Keranen, T. (2011). Outcome and consequences according to the type of transient loss of consciousness: 1-year follow-up study among primary health care patients. Journal of Neurology, 258(1), 132–136.  https://doi.org/10.1007/s00415-010-5687-0.CrossRefPubMedGoogle Scholar
  36. Miskowiak, K. W., Vinberg, M., Macoveanu, J., Ehrenreich, H., Koster, N., Inkster, B., Paulson, O. B., Kessing, L. V., Skimminge, A., & Siebner, H. R. (2015). Effects of erythropoietin on hippocampal volume and memory in mood disorders. Biological Psychiatry, 78(4), 270–277.  https://doi.org/10.1016/j.biopsych.2014.12.013.CrossRefPubMedGoogle Scholar
  37. Murray, R. J., Brosch, T., & Sander, D. (2014). The functional profile of the human amygdala in affective processing: insights from intracranial recordings. Cortex, 60, 10–33.  https://doi.org/10.1016/j.cortex.2014.06.010.CrossRefPubMedGoogle Scholar
  38. Newsome, M. R., Durgerian, S., Mourany, L., Scheibel, R. S., Lowe, M. J., Beall, E. B., Koenig, K. A., Parsons, M., Troyanskaya, M., Reece, C., Wilde, E., Fischer, B. L., Jones, S. E., Agarwal, R., Levin, H. S., & Rao, S. M. (2015). Disruption of caudate working memory activation in chronic blast-related traumatic brain injury. Neuroimage Clincal, 8:543 – 53.  https://doi.org/10.1016/j.nicl.2015.04.024.
  39. Norris, J. N., Sams, R., Lundblad, P., Frantz, E., & Harris, E. (2014). Blast-related mild traumatic brain injury in the acute phase: acute stress reactions partially mediate the relationship between loss of consciousness and symptoms. Brain Injury, 28(8), 1052–1062.  https://doi.org/10.3109/02699052.2014.891761.CrossRefPubMedGoogle Scholar
  40. Phillips, A. G., Ahn, S., & Howland, J. G. (2003). Amygdalar control of the mesocorticolimbic dopamine system: parallel pathways to motivated behavior. Neuroscience and Biobehavioral Reviews, 27(6), 543 – 54.CrossRefPubMedGoogle Scholar
  41. Postle, B. R., & D’Esposito, M. (1999). Dissociation of human caudate nucleus activity in spatial and nonspatial working memory: an event-related fMRI study. Brain Research. Cognitive Brain Research, 8(2), 107 – 15.CrossRefPubMedGoogle Scholar
  42. Postle, B. R., & D’Esposito, M. (2003). Spatial working memory activity of the caudate nucleus is sensitive to frame of reference. Cognitive, Affective, & Behavioral Neuroscience, 3(2), 133 – 44.CrossRefGoogle Scholar
  43. Primus, E. A., Bigler, E. D., Anderson, C. V., Johnson, S. C., Mueller, R. M., & Blatter, D. (1997). Corpus striatum and traumatic brain injury. Brain Injury, 11(8), 577 – 86.CrossRefPubMedGoogle Scholar
  44. Pujol, N., Penades, R., Junque, C., Dinov, I., Fu, C. H., Catalan, R., Ibarretxe-Bilbao, N., Bargallo, N., Bernardo, M., Toga, A., Howard, R. J., & Costafreda, S. G. (2014). Hippocampal abnormalities and age in chronic schizophrenia: morphometric study across the adult lifespan. The British Journal of Psychiatry, 205(5), 369 – 75.  https://doi.org/10.1192/bjp.bp.113.140384.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Quigley, S. J., Scanlon, C., Kilmartin, L., Emsell, L., Langan, C., Hallahan, B., Murray, M., Waters, C., Waldron, M., Hehir, S., Casey, H., McDermott, E., Ridge, J., Kenney, J., O’Donoghue, S., Nannery, R., Ambati, S., McCarthy, P., Barker, G. J., Cannon, D. M., & McDonald, C. (2015). Volume and shape analysis of subcortical brain structures and ventricles in euthymic bipolar I disorder. Psychiatry Research, 233(3), 324 – 30.  https://doi.org/10.1016/j.pscychresns.2015.05.012.CrossRefPubMedGoogle Scholar
  46. Reuber, M., Chen, M., Jamnadas-Khoda, J., Broadhurst, M., Wall, M., Grunewald, R. A., Howell, S. J., Koepp, M., Parry, S., Sisodiya, S., Walker, M., & Hesdorffer, D. (2016). Value of patient-reported symptoms in the diagnosis of transient loss of consciousness. Neurology, 87(6), 625 – 33.  https://doi.org/10.1212/WNL.0000000000002948.PubMedPubMedCentralGoogle Scholar
  47. Roitman, P., Gilad, M., Ankri, Y. L., & Shalev, A. Y. (2013). Head injury and loss of consciousness raise the likelihood of developing and maintaining PTSD symptoms. Journal of Traumatic Stress, 26(6), 727 – 34.  https://doi.org/10.1002/jts.21862.CrossRefPubMedGoogle Scholar
  48. Shenton, M. E., Hamoda, H. M., Schneiderman, J. S., Bouix, S., Pasternak, O., Rathi, Y., Vu, M. A., Purohit, M. P., Helmer, K., Koerte, I., Lin, A. P., Westin, C. F., Kikinis, R., Kubicki, M., Stern, R. A., & Zafonte, R. (2012). A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury. Brain Imaging and Behavior, 6(2), 137 – 92.  https://doi.org/10.1007/s11682-012-9156-5.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Spies, G., Ahmed-Leitao, F., Fennema-Notestine, C., Cherner, M., & Seedat, S. (2016). Effects of HIV and childhood trauma on brain morphometry and neurocognitive function. Journal of Neurovirology, 22(2), 149 – 58.  https://doi.org/10.1007/s13365-015-0379-2.CrossRefPubMedGoogle Scholar
  50. Tate, D. F., Wade, B. S., Velez, C. S., Drennon, A. M., Bolzenius, J., Gutman, B. A., Thompson, P. M., Lewis, J. D., Wilde, E. A., Bigler, E. D., Shenton, M. E., Ritter, J. L., & York, G. E. (2016). Volumetric and shape analyses of subcortical structures in United States service members with mild traumatic brain injury. Journal of Neurology, 263(10), 2065–2079.  https://doi.org/10.1007/s00415-016-8236-7.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Van Boven, R. W., Harrington, G. S., Hackney, D. B., Ebel, A., Gauger, G., Bremner, J. D., D’Esposito, M., Detre, J. A., Haacke, E. M., Jack, C. R. Jr., Jagust, W. J., Le Bihan, D., Mathis, C. A., Mueller, S., Mukherjee, P., Schuff, N., Chen, A. & M. W. Weiner. (2009) Advances in neuroimaging of traumatic brain injury and posttraumatic stress disorder. Journal of Rehabilitation Research and Development, 46(6):717 – 57.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Vasterling, J. J., Verfaellie, M., & Sullivan, K. D. (2009). Mild traumatic brain injury and posttraumatic stress disorder in returning veterans: perspectives from cognitive neuroscience. Clinical Psychology Review, 29(8), 674 – 84.  https://doi.org/10.1016/j.cpr.2009.08.004.CrossRefPubMedGoogle Scholar
  53. Vecera, S. P., & Rizzo, M. (2003). Spatial attention: normal processes and their breakdown. Neurologic Clinics, 21(3), 575–607.CrossRefPubMedGoogle Scholar
  54. Wade, B. S., Valcour, V. G., Wendelken-Riegelhaupt, L., Esmaeili-Firidouni, P., Joshi, S. H., Gutman, B. A., & Thompson, P. M. (2015a). Mapping abnormal subcortical brain morphometry in an elderly HIV+ cohort. NeuroImage: Clinical, 9, 564–73.  https://doi.org/10.1016/j.nicl.2015.10.006.CrossRefGoogle Scholar
  55. Wade, B. S., Valcour, V. G., Wendelken-Riegelhaupt, L., Esmaeili-Firidouni, P., Joshi, S. H., Wang, Y., & Thompson, P. M. (2015b). Mapping abnormal subcortical brain morphometry in an elderly HIV + cohort. Proceedings of IEEE International Symposium on Biomedical, 2015, 971–975.  https://doi.org/10.1109/ISBI.2015.7164033.Google Scholar
  56. Wade, B. S., Joshi, S. H., Njau, S., Leaver, A. M., Vasavada, M., Woods, R. P., Gutman, B. A., Thompson, P. M., Espinoza, R., & Narr, K. L. (2016). Effect of electroconvulsive therapy on striatal morphometry in major depressive disorder. Neuropsychopharmacology, 41(10), 2481–2491.  https://doi.org/10.1038/npp.2016.48.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Wang, L., Swank, J. S., Glick, I. E., Gado, M. H., Miller, M. I., Morris, J. C., & Csernansky, J. G. (2003). Changes in hippocampal volume and shape across time distinguish dementia of the Alzheimer type from healthy aging. Neuroimage, 20(2), 667 – 82.  https://doi.org/10.1016/S1053-8119(03)00361-6.CrossRefPubMedGoogle Scholar
  58. Wang, Y., Zhang, J., Gutman, B., Chan, T. F., Becker, J. T., Aizenstein, H. J., Lopez, O. L., Tamburo, R. J., Toga, A. W., & Thompson, P. M. (2010). Multivariate tensor-based morphometry on surfaces: application to mapping ventricular abnormalities in HIV/AIDS. Neuroimage, 49(3), 2141–2157.  https://doi.org/10.1016/j.neuroimage.2009.10.086.CrossRefPubMedGoogle Scholar
  59. Wilde, E. A., Bouix, S., Tate, D. F., Lin, A. P., Newsome, M. R., Taylor, B. A., Stone, J. R., Montier, J., Gandy, S. E., Biekman, B., Shenton, M. E., & York, G. (2015). Advanced neuroimaging applied to veterans and service personnel with traumatic brain injury: state of the art and potential benefits. Brain Imaging and Behavior, 9(3), 367–402.  https://doi.org/10.1007/s11682-015-9444-y.CrossRefPubMedGoogle Scholar
  60. Xiong, K. L., Zhang, J. N., Zhang, Y. L., Zhang, Y., Chen, H., & Qiu, M. G. (2016). Brain functional connectivity and cognition in mild traumatic brain injury. Neuroradiology, 58(7), 733–739.  https://doi.org/10.1007/s00234-016-1675-0.CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  • David F. Tate
    • 1
    • 2
  • Benjamin S. C. Wade
    • 1
    • 3
    • 4
  • Carmen S. Velez
    • 1
  • Ann Marie Drennon
    • 5
  • Jacob D. Bolzenius
    • 1
  • Douglas B. Cooper
    • 6
  • Jan E. Kennedy
    • 5
  • Matthew W. Reid
    • 5
  • Amy O. Bowles
    • 7
  • Paul M. Thompson
    • 3
  • Boris A. Gutman
    • 3
  • Jeffrey D. Lewis
    • 8
  • John L. Ritter
    • 9
  • Gerald E. York
    • 10
  • Erin D. Bigler
    • 11
  1. 1.Missouri Institute of Mental HealthUniversity of Missouri–St. LouisBerkeleyUSA
  2. 2.Department of Physical Medicine and RehabilitationBaylor College of MedicineHoustonUSA
  3. 3.Imaging Genetics CenterUniversity of Southern CaliforniaMarina del ReyUSA
  4. 4.Ahmanson-Lovelace Brain Mapping Center, Department of NeurologyUCLALos AngelesUSA
  5. 5.Defense and Veterans Brain Injury CenterSan Antonio Military Medical CenterSan AntonioUSA
  6. 6.Defense and Veteran Brain Injury Center (DVBIC); San Antonio Polytrauma Rehabilitation Center, South Texas Veterans Health Care System Department of Psychiatry, UT-Health San AntonioSan AntonioUSA
  7. 7.Department of Rehabilitation MedicineBrooke Army Medical CenterSan AntonioUSA
  8. 8.Department of Neurology, Uniformed Services University of the Health Sciences School of MedicineBethesdaUSA
  9. 9.Austin Radiological AssociationAustinUSA
  10. 10.Alaska Radiology AssociatesTBI Imaging and ResearchAnchorageUSA
  11. 11.Departments of Psychology and NeuroscienceBrigham Young UniversityProvoUSA

Personalised recommendations