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Chronic Effects of Blast-Related TBI on Subcortical Functional Connectivity in Veterans

  • Mary R. Newsome (a1) (a2), Andrew R. Mayer (a3) (a4), Xiaodi Lin (a1) (a2), Maya Troyanskaya (a1) (a2), George R. Jackson (a5) (a6), Randall S. Scheibel (a1) (a2), Annette Walder (a7), Ajithraj Sathiyaraj (a8), Elisabeth A. Wilde (a1) (a2) (a6) (a9), Shalini Mukhi (a9) (a10), Brian A. Taylor (a1) (a2) (a9) (a10) and Harvey S. Levin (a1) (a2)...

Abstract

Objectives: Blast explosions are the most frequent mechanism of traumatic brain injury (TBI) in recent wars, but little is known about their long-term effects. Methods: Functional connectivity (FC) was measured in 17 veterans an average of 5.46 years after their most serious blast related TBI, and in 15 demographically similar veterans without TBI or blast exposure. Subcortical FC was measured in bilateral caudate, putamen, and globus pallidus. The default mode and fronto-parietal networks were also investigated. Results: In subcortical regions, between-groups t tests revealed altered FC from the right putamen and right globus pallidus. However, following analysis of covariance (ANCOVA) with age, depression (Center for Epidemiologic Studies Depression Scale), and posttraumatic stress disorder symptom (PTSD Checklist – Civilian version) measures, significant findings remained only for the right globus pallidus with anticorrelation in bilateral temporal occipital fusiform cortex, occipital fusiform gyrus, lingual gyrus, and cerebellum, as well as the right occipital pole. No group differences were found for the default mode network. Although reduced FC was found in the fronto-parietal network in the TBI group, between-group differences were nonsignificant after the ANCOVA. Conclusions: FC of the globus pallidus is altered years after exposure to blast related TBI. Future studies are necessary to explore the trajectory of changes in FC in subcortical regions after blast TBI, the effects of isolated versus repetitive blast-related TBI, and the relation to long-term outcomes in veterans. (JINS, 2016, 22, 631–642)

Copyright

Corresponding author

Correspondence and reprint requests to: Mary R. Newsome, Michael E. DeBakey VA Medical Center, Department of Physical Medicine & Rehabilitation, Baylor College of Medicine BCM 637, Houston, TX 77030. E-mail: mnewsome@bcm.edu

References

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Ahmed, R.M., Irish, M., Henning, E., Dermody, N., Bartley, L., Kiernan, M.C., & Hodges, J.R. (2016). Assessment of eating behavior disturbance and associated neural networks in frontotemporal dementia. JAMA Neurology, 73, 282290. doi:10.1001/jamaneurol.2015.4478
Akbar, N., Till, C., Sled, J.G., Binns, M.A., Doesburg, S.M., Aubert-Broche, B., & Banwell, B. (2015). Altered resting-state functional connectivity in cognitively preserved pediatric-onset MS patients and relationship to structural damage and cognitive performance. Multiple Sclerosis, doi:10.1177/1352458515602336
Alexander, G.E., DeLong, M.R., & Strick, P.L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S. Research Support, U.S. Gov’t, P.H.S. Review]. Annual Review of Neuroscience, 9, 357381. doi:10.1146/annurev.ne.09.030186.002041
Arnold Anteraper, S., Triantafyllou, C., Sawyer, A.T., Hofmann, S.G., Gabrieli, J.D., & Whitfield-Gabrieli, S. (2014). Hyper-connectivity of subcortical resting-state networks in social anxiety disorder. [Research Support, Non-U.S. Gov’t]. Brain Connect, 4(2), 8190. doi:10.1089/brain.2013.0180
Ashby, F.G. (2011). Processing statistical analysis of MRI data. Cambridge: Cambridge University Press.
Babor, T.F., Higgins-Biddle, J.C., Saunders, J.B., & Monteiro, M.G. (2001). The alcohol use disorders identification test: Guidelines for use in primary care (2nd ed.). Geneva: WHO.
Barona, A., Reynolds, C.R., & Chastain, R. (1984). A demographically based index of premorbid intelligence for the WAIS-R. Journal of Consulting and Clinical Psychology, 52, 885887.
Belanger, H.G., Uomoto, J.M., & Vanderploeg, R.D. (2009). The Veterans Health Administration's (VHA’s) Polytrauma System of Care for mild traumatic brain injury: Costs, benefits, and controversies. [Research Support, U.S. Gov’t, Non-P.H.S. Review]. The Journal of Head Trauma Rehabilitation, 24(1), 413. doi:10.1097/HTR.0b013e3181957032
Biswal, B., Yetkin, F.Z., Haughton, V.M., & Hyde, J.S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. [Research Support, U.S. Gov’t, P.H.S.]. Magnetic Resonance in Medicine, 34(4), 537541.
Bower, J.H., Maraganore, D.M., Peterson, B.J., McDonnell, S.K., Ahlskog, J.E., & Rocca, W.A. (2003). Head trauma preceding PD: A case-control study. [Research Support, U.S. Gov’t, P.H.S. Review]. Neurology, 60(10), 16101615.
Brenner, L.A., Vanderploeg, R.D., & Terrio, H. (2009). Assessment and diagnosis of mild traumatic brain injury, posttraumatic stress disorder, and other polytrauma conditions: Burden of adversity hypothesis. [Review]. Rehabilitation Psychology, 54(3), 239246. doi:10.1037/a0016908
Brown, L., Sherbenou, R.J., & Johnsen, S.K. (2010). Test of nonverbal intelligence— (4th Ed.). Austin, TX: Pro-Ed.
Button, K.S., Ioannidis, J.P., Mokrysz, C., Nosek, B.A., Flint, J., Robinson, E.S., && Munafo, M.R. (2013). Power failure: Why small sample size undermines the reliability of neuroscience. [Research Support, Non-U.S. Gov’t]. Nature Reviews. Neuroscience, 14(5), 365376. doi:10.1038/nrn3475
Cicerone, K.D., & Kalmar, K. (1995). Persistent postconcussion syndrome: The structure of subjective complaints after mTBI. The Journal of Head Trauma Rehabilitation, 10, 117.
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Earlbaum Associates.
Cole, M.W., Reynolds, J.R., Power, J.D., Repovs, G., Anticevic, A., & Braver, T.S. (2013). Multi-task connectivity reveals flexible hubs for adaptive task control. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Nature Neuroscience, 16(9), 13481355. doi:10.1038/nn.3470
Cools, R. (2006). Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson's disease. [Research Support, Non-U.S. Gov’t Review]. Neuroscience and Biobehavioral Reviews, 30(1), 123. doi:10.1016/j.neubiorev.2005.03.024
Crozier, J. C., Wang, L., Huettel, S.A., & De Bellis, M.D. (2014). Neural correlates of cognitive and affective processing in maltreated youth with posttraumatic stress symptoms: does gender matter? [Research Support, N.I.H., Extramural]. Dev Psychopathol, 26(2), 491513. doi: 10.1017/S095457941400008X
Davenport, N.D., Lim, K.O., Armstrong, M.T., & Sponheim, S.R. (2012). Diffuse and spatially variable white matter disruptions are associated with blast-related mild traumatic brain injury. [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.]. Neuroimage, 59(3), 20172024. doi:10.1016/j.neuroimage.2011.10.050
de Rover, M., Petersson, K.M., van der Werf, S.P., Cools, A.R., Berger, H.J., & Fernandez, G. (2008). Neural correlates of strategic memory retrieval: Differentiating between spatial-associative and temporal-associative strategies. [Comparative Study]. Human Brain Mapping, 29(9), 10681079. doi:10.1002/hbm.20445
Derogatis, L.R. (1993). BSI Brief Symptom Inventory: Administration, Scoring, and Procedure Manual (4th ed.). Minneapolis, MN: National Computer Systems.
Eid, L., & Parent, M. (2015). Morphological evidence for dopamine interactions with pallidal neurons in primates. Frontiers in Neuroanatomy, 9, 111. doi:10.3389/fnana.2015.00111
Fischer, B.L., Parsons, M., Durgerian, S., Reece, C., Mourany, L., Lowe, M.J., & Rao, S.M. (2014). Neural activation during response inhibition differentiates blast from mechanical causes of mild to moderate traumatic brain injury. Journal of Neurotrauma, 31(2), 169179. doi:10.1089/neu.2013.2877
Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., & Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. [Comparative Study Research Support, N.I.H., Extramural Research Support, U.S. Gov’t, P.H.S.]. Proc Natl Acad Sci U S A, 102(27), 96739678. doi: 10.1073/pnas.0504136102
Friston, K. (2013). Sample size and the fallacies of classical inference. [Comment Research Support, Non-U.S. Gov’t]. Neuroimage, 81, 503504. doi:10.1016/j.neuroimage.2013.02.057
Gauthier, J., Parent, M., Levesque, M., & Parent, A. (1999). The axonal arborization of single nigrostriatal neurons in rats. [Research Support, Non-U.S. Gov’t]. Brain Research, 834(1–2), 228232.
Green, P., Gervais, R., & Allen, L.M. (2001). Word Memory Test in normal controls and clinical cases simulating impairment. Archives of Clinical Neuropsychology, 16(8), 849850.
Greicius, M.D., Supekar, K., Menon, V., & Dougherty, R.F. (2009). Resting-state functional connectivity reflects structural connectivity in the default mode network. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.]. Cerebral Cortex, 19(1), 7278. doi:10.1093/cercor/bhn059
Gusnard, D.A., & Raichle, M.E. (2001). Searching for a baseline: Functional imaging and the resting human brain. [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, P.H.S. Review]. Nature Reviews. Neuroscience, 2(10), 685694. doi:10.1038/35094500
Han, K., Mac Donald, C.L., Johnson, A.M., Barnes, Y., Wierzechowski, L., Zonies, D., & Brody, D.L. (2014). Disrupted modular organization of resting-state cortical functional connectivity in U.S. military personnel following concussive ‘mild’ blast-related traumatic brain injury. [Research Support, N.I.H., Extramural Research Support, U.S. Gov’t, Non-P.H.S.]. Neuroimage, 84, 7696. doi:10.1016/j.neuroimage.2013.08.017
Helmich, R.C., Janssen, M.J., Oyen, W.J., Bloem, B.R., & Toni, I. (2011). Pallidal dysfunction drives a cerebellothalamic circuit into Parkinson tremor. [Research Support, Non-U.S. Gov’t]. Annals of Neurology, 69(2), 269281. doi:10.1002/ana.22361
Helmick, K.M., Spells, C.A., Malik, S.Z., Davies, C.A., Marion, D.W., & Hinds, S.R. (2015). Traumatic brain injury in the US military: Epidemiology and key clinical and research programs. Brain Imaging and Behavior, 9, 358366. doi:10.1007/s11682-015-9399-z
Hosseini, S.M., & Kesler, S.R. (2013). Comparing connectivity pattern and small-world organization between structural correlation and resting-state networks in healthy adults. [Comparative Study Research Support, N.I.H., Extramural]. Neuroimage, 78, 402414. doi:10.1016/j.neuroimage.2013.04.032
Jorge, R.E., Acion, L., White, T., Tordesillas-Gutierrez, D., Pierson, R., Crespo-Facorro, B., && Magnotta, V.A. (2012). White matter abnormalities in veterans with mild traumatic brain injury. [Research Support, N.I.H., Extramural Research Support, U.S. Gov’t, Non-P.H.S.]. The American Journal of Psychiatry, 169(12), 12841291. doi:10.1176/appi.ajp.2012.12050600
Kang, X., Herron, T.J., Ettlinger, M., & Woods, D.L. (2015). Hemispheric asymmetries in cortical and subcortical anatomy. Laterality, 20(6), 658684. doi:10.1080/1357650X.2015.1032975
Keane, T.M., Fairbank, J.A., Caddell, J.M., Zimering, R.T., Taylor, K.L., & Mora, C.A. (1989). Clinical evaluation of a measure to assess combat exposure. Psychological Assessment: A Journal of Consulting and Clinical Psychology, 1(1), 5355.
Kwon, H.G., & Jang, S.H. (2014). Differences in neural connectivity between the substantia nigra and ventral tegmental area in the human brain. Frontiers in Human Neuroscience, 8, 41. doi:10.3389/fnhum.2014.00041
Levin, H.S., Wilde, E., Troyanskaya, M., Petersen, N.J., Scheibel, R., Newsome, M., & Li, X. (2010). Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.]. Journal of Neurotrauma, 27(4), 683694. doi:10.1089/neu.2009.1073
Lindquist, M.A., Caffo, B., & Crainiceanu, C. (2013). Ironing out the statistical wrinkles in "ten ironic rules". [Comment]. Neuroimage, 81, 499502. doi:10.1016/j.neuroimage.2013.02.056
MacGregor, A.J., Dougherty, A.L., & Galarneau, M.R. (2011). Injury-specific correlates of combat-related traumatic brain injury in Operation Iraqi Freedom. [Comparative Study Research Support, U.S. Gov’t, Non-P.H.S.]. The Journal of Head Trauma Rehabilitation, 26(4), 312318. doi:10.1097/HTR.0b013e3181e94404
Maldjian, J.A., Laurienti, P.J., Kraft, R.A., & Burdette, J.H. (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage, 19(3), 12331239.
Marras, C., Hincapie, C.A., Kristman, V.L., Cancelliere, C., Soklaridis, S., Li, A., & Cassidy, J.D. (2014). Systematic review of the risk of Parkinson’s disease after mild traumatic brain injury: Results of the International Collaboration on Mild Traumatic Brain Injury Prognosis. [Research Support, Non-U.S. Gov’t Review]. Archives of Physical Medicine and Rehabilitation, 95(3 Suppl.), S238S244. doi:10.1016/j.apmr.2013.08.298
Mayer, A.R., Mannell, M.V., Ling, J., Gasparovic, C., & Yeo, R.A. (2011). Functional connectivity in mild traumatic brain injury. [Research Support, N.I.H., Extramural Research Support, U.S. Gov’t, Non-P.H.S.]. Human Brain Mapping, 32(11), 18251835. doi:10.1002/hbm.21151
Middleton, F.A., & Strick, P.L. (2000). Basal ganglia output and cognition: Evidence from anatomical, behavioral, and clinical studies. [Review]. Brain and Cognition, 42(2), 183200. doi:10.1006/brcg.1999.1099
Miller, G. A., & Chapman, J. P. (2001). Misunderstanding analysis of covariance. [Research Support, U.S. Gov’t, P.H.S.]
Morey, R.A., Dolcos, F., Petty, C.M., Cooper, D.A., Hayes, J.P., LaBar, K.S., & McCarthy, G. (2009). The role of trauma-related distractors on neural systems for working memory and emotion processing in posttraumatic stress disorder. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.]. Journal of Psychiatric Research, 43(8), 809817. doi:10.1016/j.jpsychires.2008.10.014
Nathan, D.E., Oakes, T.R., Yeh, P.H., French, L.M., Harper, J.F., Liu, W., & Riedy, G. (2015). Exploring variations in functional connectivity of the resting state default mode network in mild traumatic brain injury. Brain Connectivity, 5(2), 102114. doi:10.1089/brain.2014.0273
Newsome, M.R., Durgerian, S., Mourany, L., Scheibel, R.S., Lowe, M.J., Beall, E.B., & Rao, S.M. (2015). Disruption of caudate working memory activation in chronic blast-related traumatic brain injury. Neuroimage: Clinical, 8, 543553. doi:10.1016/j.nicl.2015.04.024
Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97113.
Pelletier-Baldelli, A., Bernard, J.A., & Mittal, V.A. (2015). Intrinsic functional connectivity in salience and default mode networks and aberrant social processes in youth at ultra-high risk for psychosis. [Research Support, N.I.H., Extramural]. PLoS One, 10(8), e0134936. doi:10.1371/journal.pone.0134936
Power, J.D., Barnes, K.A., Snyder, A.Z., Schlaggar, B.L., & Petersen, S.E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.]. Neuroimage, 59(3), 21422154. doi:10.1016/j.neuroimage.2011.10.018
Radloff, L.S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Applied Psychological Measurement, 1, 385401.
Rao, J.A., Jenkins, L.M., Hymen, E., Feigon, M., Weisenbach, S.L., Zubieta, J.K., && Langenecker, S.A. (2016). Differential resting state connectivity patterns and impaired semantically cued list learning test performance in early course remitted major depressive disorder. Journal of the International Neuropsychological Society, 22(2), 225239. doi:10.1017/S1355617716000011
Readnower, R.D., Chavko, M., Adeeb, S., Conroy, M.D., Pauly, J.R., McCarron, R.M., && Sullivan, P.G. (2010). Increase in blood-brain barrier permeability, oxidative stress, and activated microglia in a rat model of blast-induced traumatic brain injury. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Journal of Neuroscience Research, 88(16), 35303539. doi:10.1002/jnr.22510
Robinson, M.E., Lindemer, E.R., Fonda, J.R., Milberg, W.P., McGlinchey, R.E., & Salat, D.H. (2015). Close-range blast exposure is associated with altered functional connectivity in Veterans independent of concussion symptoms at time of exposure. [Research Support, U.S. Gov’t, Non-P.H.S.]. Human Brain Mapping, 36(3), 911922. doi:10.1002/hbm.22675
Sajja, V.S., Galloway, M., Ghoddoussi, F., Kepsel, A., & VandeVord, P. (2013). Effects of blast-induced neurotrauma on the nucleus accumbens. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Journal of Neuroscience Research, 91(4), 593601. doi:10.1002/jnr.23179
Sakamoto, H., Fukuda, R., Okuaki, T., Rogers, M., Kasai, K., Machida, T., & Kato, N. (2005). Parahippocampal activation evoked by masked traumatic images in posttraumatic stress disorder: A functional MRI study. [Clinical Trial Research Support, Non-U.S. Gov’t]. Neuroimage, 26(3), 813821. doi:10.1016/j.neuroimage.2005.02.032
Scheibel, R.S., Newsome, M.R., Troyanskaya, M., Lin, X., Steinberg, J.L., Radaideh, M., & Levin, H.S. (2012). Altered brain activation in military personnel with one or more traumatic brain injuries following blast. [Research Support, U.S. Gov’t, Non-P.H.S.]. Journal of the International Neuropsychological Society, 18(1), 89100. doi:10.1017/S1355617711001433
Scheibel, R.S., Pastorek, N.J., Troyanskaya, M., Kennedy, J.E., Steinberg, J.L., Newsome, M.R., & Levin, H.S. (2015). The suppression of brain activation in post-deployment military personnel with posttraumatic stress symptoms. Brain Imaging and Behavior, 9(3), 513526. doi:10.1007/s11682-015-9376-6
Shahaduzzaman, M., Acosta, S., Bickford, P.C., & Borlongan, C.V. (2013). alpha-Synuclein is a pathological link and therapeutic target for Parkinson's disease and traumatic brain injury. Medical Hypotheses, 81(4), 675680. doi:10.1016/j.mehy.2013.07.025
Skinner, H.A. (1982). The Drug Abuse Screening Test. Addictive Behavior, 7(4), 363371.
Smith, S.M., Fox, P. T., Miller, K. L., Glahn, D. C., Fox, P. M., Mackay, C. E., & Beckmann, C. F. (2009). Correspondence of the brain’s functional architecture during activation and rest. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Proc Natl Acad Sci U S A, 106(31), 1304013045. doi: 10.1073/pnas.0905267106
Sours, C., Zhuo, J., Janowich, J., Aarabi, B., Shanmuganathan, K., & Gullapalli, R.P. (2013). Default mode network interference in mild traumatic brain injury - A pilot resting state study. [Research Support, U.S. Gov’t, Non-P.H.S.]. Brain Research, 1537, 201215. doi:10.1016/j.brainres.2013.08.034
Spielberg, J.M., McGlinchey, R.E., Milberg, W.P., & Salat, D.H. (2015). Brain network disturbance related to posttraumatic stress and traumatic brain injury in veterans. Biological Psychiatry, 78(3), 210216. doi:10.1016/j.biopsych.2015.02.013
Sponheim, S.R., McGuire, K.A., Kang, S.S., Davenport, N.D., Aviyente, S., Bernat, E.M., && Lim, K.O. (2011). Evidence of disrupted functional connectivity in the brain after combat-related blast injury. [Research Support, U.S. Gov’t, Non-P.H.S.]. Neuroimage, 54(Suppl. 1), S21S29. doi:10.1016/j.neuroimage.2010.09.007
Stevens, M.C., Lovejoy, D., Kim, J., Oakes, H., Kureshi, I., & Witt, S.T. (2012). Multiple resting state network functional connectivity abnormalities in mild traumatic brain injury. [Research Support, Non-U.S. Gov’t]. Brain Imaging and Behavior, 6(2), 293318. doi:10.1007/s11682-012-9157-4
Taylor, P.A., & Ford, C.C. (2009). Simulation of blast-induced early-time intracranial wave physics leading to traumatic brain injury. [Research Support, U.S. Gov’t, Non-P.H.S.]. Journal of Biomechanical Engineering, 131(6), 061007. doi:10.1115/1.3118765
Tumer, N., Svetlov, S., Whidden, M., Kirichenko, N., Prima, V., Erdos, B., & Wang, K.K. (2013). Overpressure blast-wave induced brain injury elevates oxidative stress in the hypothalamus and catecholamine biosynthesis in the rat adrenal medulla. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.]. Neuroscience Letters, 544, 6267. doi:10.1016/j.neulet.2013.03.042
Vakhtin, A.A., Calhoun, V.D., Jung, R.E., Prestopnik, J.L., Taylor, P.A., & Ford, C.C. (2013). Changes in intrinsic functional brain networks following blast-induced mild traumatic brain injury. [Research Support, U.S. Gov’t, Non-P.H.S.]. Brain Injury, 27(11), 13041310. doi:10.3109/02699052.2013.823561
Weathers, F.W., Litz, B.T., Herman, D.S., Huska, J.A., & Keane, T.M. (1993). The PTSD Checklist (PCL): Reliability, validity, and diagnostic utility. Paper presented at the 9th Annual Conference of the ISTSS. San Antonio, TX.
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. [Research Support, Non-U.S. Gov’t]. Brain Connectivity, 2(3), 125141. doi:10.1089/brain.2012.0073
Woods, A.S., Colsch, B., Jackson, S.N., Post, J., Baldwin, K., Roux, A., & Balaban, C. (2013). Gangliosides and ceramides change in a mouse model of blast induced traumatic brain injury. [Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.]. ACS Chemical Neuroscience, 4(4), 594600. doi:10.1021/cn300216h
Yeh, P.H., Wang, B., Oakes, T.R., French, L.M., Pan, H., Graner, J., & Riedy, G. (2014). Postconcussional disorder and PTSD symptoms of military-related traumatic brain injury associated with compromised neurocircuitry. [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.]. Human Brain Mapping, 35(6), 26522673. doi:10.1002/hbm.22358
Yeterian, E.H., & Van Hoesen, G.W. (1978). Cortico-striate projections in the rhesus monkey: The organization of certain cortico-caudate connections. [Research Support, U.S. Gov’t, P.H.S.]. Brain Research, 139(1), 4363.

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