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Predicting Behavioral Deficits in Pediatric Traumatic Brain Injury Through Uncinate Fasciculus Integrity

Published online by Cambridge University Press:  15 April 2011

Chad P. Johnson ,
Jenifer Juranek ,
Larry A. Kramer ,
Mary R. Prasad ,
Paul R. Swank  and
Linda Ewing-Cobbs
Chad P. Johnson
Affiliation:
Department of Psychology, University of Houston, Houston, Texas
Jenifer Juranek
Affiliation:
Department of Pediatrics, University of Texas Health Science Center at Houston, Houston, Texas
Larry A. Kramer
Affiliation:
Department of Radiology, University of Texas Health Science Center at Houston, Houston, Texas
Mary R. Prasad
Affiliation:
Department of Pediatrics, University of Texas Health Science Center at Houston, Houston, Texas
Paul R. Swank
Affiliation:
Department of Pediatrics, University of Texas Health Science Center at Houston, Houston, Texas
Linda Ewing-Cobbs*
Affiliation:
Department of Pediatrics, University of Texas Health Science Center at Houston, Houston, Texas Department of Psychiatry and Behavioral Sciences, University of Texas Health Science Center at Houston, Houston, Texas
*
Correspondence and reprint requests to: Linda Ewing-Cobbs, Dan L Duncan Children's Neurodevelopmental Clinic, Children's Learning Institute, 7000 Fannin, Suite 2401, Houston, TX 77030. E-mail: linda.ewing-cobbs@uth.tmc.edu
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Abstract

Behavioral dysregulation is a common and detrimental consequence of traumatic brain injury (TBI) in children that contributes to poor academic achievement and deficits in social development. Unfortunately, behavioral dysregulation is difficult to predict from either injury severity or early neuropsychological evaluation. The uncinate fasciculus (UF) connects orbitofrontal and anterior temporal lobes, which are commonly implicated in emotional and behavioral regulation. Using probabilistic diffusion tensor tractography (DTT), we examined the relationship between the integrity of the UF 3 months post-injury and ratings of executive functions 12 months post-injury in children with moderate to severe TBI and a comparison group with orthopedic injuries. As expected, fractional anisotropy of the UF was lower in the TBI group relative to the orthopedic injury group. DTT metrics from the UF served as a biomarker and predicted ratings of emotional and behavior regulation, but not metacognition. In contrast, the Glasgow Coma Scale score was not related to either UF integrity or to executive function outcomes. Neuroanatomical biomarkers like the uncinate fasciculus may allow for early identification of behavioral problems and allow for investigation into the relationship of frontotemporal networks to brain-behavior relationships. (JINS, 2011, 17, 663–673)

Keywords

Diffusion tensor imagingExecutive functionNeuropsychologyChildAnisotropyBehavior
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 17 , Issue 4 , 21 June 2011 , pp. 663 - 673
Copyright
Copyright © The International Neuropsychological Society 2011

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References

REFERENCES

Allen, J.S., Brusss, J., Mehta, S., Grabowski, T., Brown, C.K., Damasio, H. (2008). Effects of spatial transformation on regional brain volume estimates. Neuroimage, 42, 535–547. doi:10.1016/j.neuroimage.2008.05.047CrossRefGoogle ScholarPubMed
Amodio, D.M., Firth, C.D. (2006). Meeting of minds: The medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7, 268–277. doi:10.1038/nrn1884CrossRefGoogle ScholarPubMed
Anderson, V., Catroppa, C. (2005). Recovery of executive skills following paediatric traumatic brain injury (TBI): A 2 year follow-up. Brain Injury, 19, 459–470. doi:10.1080/02699050400004823CrossRefGoogle ScholarPubMed
Bachevalier, J., Loveland, K.A. (2006). The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism. Neuroscience & Biobehavioral Review, 30, 97–117. doi:10.1016/j.neubiorev.2005.07.002CrossRefGoogle ScholarPubMed
Barkovich, A.J. (2005). Pediatric neuroimaging. Baltimore: Lippincott Williams & Wilkins.Google Scholar
Barnea-Goraly, N., Kwon, H., Menon, V., Eliez, S., Lotspeich, L., Reiss, A.L. (2004). White matter structure in autism: Preliminary evidence from diffusion tensor imaging. Biological Psychiatry, 55, 323–326. doi:10.1016/j.biopsych.2003.10.022CrossRefGoogle ScholarPubMed
Basser, P.J. (1997). New histological and physiological stains derived from diffusion-tensor MR images. Annals of the New York Academy of Sciences, 820, 123–138. doi:10.1111/j.1749-6632.1997.tb46192.xCrossRefGoogle ScholarPubMed
Bechara, A., Damasio, H., Damasio, A.R. (2000). Emotion, decision making, and the orbitofrontal cortex. Cerebral Cortex, 10, 295–307. doi:10.1093/cercor/10.3.295CrossRefGoogle ScholarPubMed
Bendlin, B.B., Ries, M.L., Lazar, M., Alexander, A.L., Dempsey, R.J., Rowley, H.A., Johnson, S.C. (2008). Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neuroimage, 42, 503–514. doi:10.1016/j.neuroimage.2008.04.254CrossRefGoogle ScholarPubMed
Bigler, E.D. (2007). Anterior and middle cranial fossa in traumatic brain injury: Relevant neuroanatomy and neuropathology in the study of neuropsychological outcome. Neuropsychology, 21, 515–531. doi:10.1037/0894-4105.21.5.515CrossRefGoogle Scholar
Bunge, S.A., Wright, S.B. (2007). Neurodevelopmental changes in working memory and cognitive control. Current Opinion in Neurobiology, 17, 243–250. doi:10.1016/j.conb.2007.02.005CrossRefGoogle ScholarPubMed
Castellanos, F.X., Sonuga-Barke, E.J.S., Milham, M.P., Tannock, R. (2006). Characterizing cognition in ADHD: Beyond executive dysfunction. Trends in Cognitive Science, 10, 117–123. doi:10.1016/j.tics.2006.01.011CrossRefGoogle ScholarPubMed
Chao, Y.P., Chen, J.H., Cho, K.H., Yeh, C.H., Chou, K.H., Lin, C.P. (2008). A multiple streamline approach to high angular resolution diffusion tractography. Medical Engineering & Physics, 30, 989–996.CrossRefGoogle ScholarPubMed
Cook, P.A., Zhang, H., Avants, B.B., Yushkevich, P., Alexander, D.C., Gee, J.C., Thompson, A.J. (2005). An automated approach to connectivity-based partitioning of brain structures. Lecture Notes in Computer Science, 3749, 164–171. doi:10.1007/11566465_21CrossRefGoogle Scholar
Croxson, P.L., Johansen-Berg, H., Behrens, T.E.J., Robson, M.D., Pinsk, M.A., Gross, C.G., Rushworth, M.F.S. (2005). Quantitative investigation of connections of the prefrontal cortex in the human and macaque using probabilistic diffusion tractography. The Journal of Neuroscience, 25, 8854–8866. doi:10.1523/JNEUROSCI.1311-05.2005CrossRefGoogle ScholarPubMed
Damasio, A.R. (1994). Descartes’ error: Emotion, reason, and the human brain. New York: Putnam.Google Scholar
Dennis, M. (1991). Frontal lobe function in childhood and adolescence: A heuristic for assessing attention regulation, executive control, and the intentional states important for social discourse. Developmental Neuropsychology, 7, 327–358.CrossRefGoogle Scholar
Dennis, M., Guger, S., Roncadin, C., Barnes, M., Schachar, R. (2001). Attentional-inhibitory control and social-behavioral regulation after childhood closed head injury: Do biological, developmental, and recovery variables predict outcome? Journal of the International Neuropsychological Society, 7, 683–692.CrossRefGoogle ScholarPubMed
Desikan, R.S., Segonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., Killiany, R.J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31, 968–980. doi:10.1016/j.neuroimage.2006.01.021CrossRefGoogle ScholarPubMed
Di Stefano, G., Bachevalier, J., Levin, H.S., Song, J., Scheibel, R.S., Fletcher, J.M. (2000). Volume of focal brain lesions and hippocampal formation in relation to memory function after closed head injury in children. Journal of Neurology, Neurosurgery, and Psychiatry, 69, 210–216. doi:10.1136/jnnp.69.2.210CrossRefGoogle ScholarPubMed
Diehl, B., Busch, R.M., Duncan, J.S., Piao, Z., Tkach, J., Luders, H.O. (2008). Abnormalities in diffusion tensor imaging of the uncinate fasciculus relate to reduced memory in temporal lobe epilepsy. Epilepsia, 49, 1409–1418. doi:10.1111/j.1528-1167.2008.01596.xCrossRefGoogle ScholarPubMed
Eslinger, P.J., Grattan, L.M., Damasio, H., Damasio, A.R. (1992). Developmental consequences of childhood frontal lobe damage. Archives of Neurology, 49, 764–769.CrossRefGoogle ScholarPubMed
Eluvathingal, T.J., Chugani, H.T., Behen, M.E., Juhasz, C., Muzik, O., Maqbool, M., Makki, M. (2006). Abnormal brain connectivity in children after early severe socioemotional deprivation: A diffusion tensor imaging study. Pediatrics, 117, 2093–2100. doi:10.1542/peds.2005-1727CrossRefGoogle ScholarPubMed
Eluvathingal, T.J., Hasan, K.M., Kramer, L., Fletcher, J.M., Ewing-Cobbs, L. (2007). Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. Cerebral Cortex, 17, 2760–2768. doi:10.1093/cercor/bhm003CrossRefGoogle ScholarPubMed
Ewing-Cobbs, L., Hasan, K.M., Prasad, M.R., Kramer, L., Bachevalier, J. (2006). Corpus callosum diffusion anisotropy correlates with neuropsychological outcomes in twins disconcordant for traumatic brain injury. American Journal of Neuroradiology, 27, 879–881.Google ScholarPubMed
Ewing-Cobbs, L., Prasad, M.R., Landry, S.H., Kramer, L., DeLeon, R. (2004). Executive functions following traumatic brain injury in young children: A preliminary analysis. Developmental Neuropsychology, 26, 487–512. doi:10.1207/s15326942dn2601_7CrossRefGoogle ScholarPubMed
Ewing-Cobbs, L., Prasad, M.R., Swank, P., Kramer, L., Cox, C.S., Fletcher, J.M., Hasan, K.M. (2008). Arrested development and disrupted callosal microstructure following pediatric traumatic brain injury. Neuroimage, 42, 1305–1315. doi:10.1016/j.neuroimage.2008.06.031CrossRefGoogle ScholarPubMed
Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Ségonne, F., Salat, D.H., Dale, A.M. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 11–22. doi:10.1093/cercor/bhg087CrossRefGoogle ScholarPubMed
Fuster, J.M. (1991). The prefrontal cortex and its relation to behavior. Progress in Brain Research, 87, 201–211. doi:10.1016/S0079-6123(08)63053-8CrossRefGoogle ScholarPubMed
Ganesalingam, K., Sanson, A., Anderson, V., Yeates, K.O. (2006). Self-regulation and social and behavioral functioning following childhood traumatic brain injury. Journal of the International Neuropsychological Society, 12, 609–621. doi:10.1017/S1355617706060796CrossRefGoogle ScholarPubMed
Gerring, J., Brady, K., Chen, A., Quinn, C., Herskovits, E., Bandeen-Roche, K., Bryan, R.N. (2000). Neuroimaging variables related to development of secondary attention deficit hyperactivity disorder after closed head injury in children and adolescents. Brain Injury, 14, 205–218.Google ScholarPubMed
Gioia, G.A., Isquith, P.K. (2004). Ecological assessment of executive function in traumatic brain injury. Developmental Neuropsychology, 25, 135–158.CrossRefGoogle ScholarPubMed
Gioia, G.A., Isquith, P.K., Guy, S.C., Kenworthy, L. (2000). Behavior rating inventory of executive function. Odessa, FL: Psychological Assessment Resources.Google Scholar
Goldman, P.S. (1974). An alternative to developmental plasticity: Heterology of CNS structures in infants and adults. In D.G. Stein, J.J. Rosen, & N. Butters (Eds.), Plasticity and recovery of function in the central nervous system (pp. 149–174). New York: Academic.Google Scholar
Goldman-Rakic, P.S. (1988). Topography of cognition: Parallel distributed networks in primate association cortex. Annual Review of Neuroscience, 11, 137–156. doi:10.1146/annurev.ne.11.030188.001033CrossRefGoogle ScholarPubMed
Hanten, G., Wilde, E.A., Menefee, D.S., Li, X., Lane, S., Vasquez, C., Levin, H.S. (2008). Correlates of social problem solving during the first year after traumatic brain injury in children. Neuropsychology, 22, 357–370. doi:10.1037/0894-4105.22.3.357CrossRefGoogle ScholarPubMed
Hasan, K.M. (2006). Diffusion tensor eigenvalues or both mean diffusivity and fractional anisotropy are required in quantitative clinical diffusion tensor MR reports: Fractional anisotropy alone is not sufficient. Radiology, 236, 221–230. doi:10.1148/radiol.2392051172Google Scholar
Hasan, K.M., Narayana, P.A. (2003). DTI parameter optimization at 3.0T: Potential application in entire normal human brain mapping and multiple sclerosis research. Medicamundi, 49, 30–45.Google Scholar
Herskovits, E., Gerring, J.P., Davatzikos, C., Bryan, R.N. (1999). Is the spatial distribution of brain lesions associated with closed-head injury in children predictive of subsequent development of posttraumatic stress disorder? Radiology, 224, 345–351. doi:10.1148/radiol.2242011439CrossRefGoogle Scholar
Highley, J.R., Walker, M.A., Esiri, M.M., Crow, T.J., Harrison, P.J. (2002). Asymmetry of the uncinate fasciculus: A post-mortem study of normal subjects and patients with schizophrenia. Cerebral Cortex, 12, 1218–1224. doi:10.1093/cercor/12.11.1218CrossRefGoogle ScholarPubMed
Huisman, T.A., Schwann, L.H., Schaefer, P.W., Koroshetz, W.J., Shetty-Alva, N., Ozsunar, O.W., Sorensen, A.G. (2004). Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. AJNR American Journal of Neuroradiology, 25, 370–376.Google ScholarPubMed
Kober, H., Barrett, L.F., Joseph, J., Bliss-Moreau, E., Lindquist, K., Wager, T.D. (2008). Functional grouping and cortical-subcortical interactions in emotion: A meta-analysis of neuroimaging studies. Neuroimage, 42, 998–1031. doi:10.1016/j.neuroimage.2008.03.059CrossRefGoogle ScholarPubMed
Kubicki, M., Westin, C.F., Maier, S.E., Mamata, H., Frumin, M., Ersner-Hershfield, H., Shenton, M.E. (2002). Diffusion tensor imaging and its application to neuropsychiatric disorders. Harvard Review of Psychiatry, 10, 324–336. doi:10.1080/10673220216231CrossRefGoogle ScholarPubMed
Johansen-Berg, H., Behrens, T.E.J. (2006). Just pretty pictures? What diffusion tractography can add in clinical neuroscience. Current Opinion in Neurology, 19, 379–385.CrossRefGoogle ScholarPubMed
Le Bihan, D. (2003). Looking into the functional architecture of the brain with diffusion MRI. Nature Reviews Neuroscience, 4, 469–480. doi:10.1016/j.ics.2006.04.006CrossRefGoogle ScholarPubMed
Lee, J.E., Bigler, E.D., Alexander, A.L., Lazar, M., DuBray, M.B., Chung, M.K., Lainhart, J.E. (2007). Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism. Neuroscience Letters, 424, 127–132. doi:10.1016/j.neulet.2007.07.042CrossRefGoogle ScholarPubMed
Levin, H.S. (1993). Head trauma. Current Opinion in Neurology, 6, 841–846.CrossRefGoogle ScholarPubMed
Levin, H.S., Wilde, E.A., Chu, Z., Yallampalli, R., Hanten, G.R., Li, X., Hunter, J.V. (2008). Diffusion tensor imaging in relation to cognitive and functional outcome of traumatic brain injury. Journal of Head Trauma Rehabilitation, 23, 197–208. doi:10.1097/01.HTR.0000327252.54128.7cCrossRefGoogle ScholarPubMed
Levin, H.S., Zhang, L., Dennis, M., Ewing-Cobbs, L., Schachar, R., Max, J., Hunter, J.V. (2004). Psychosocial outcome of TBI in children with unilateral frontal lesions. Journal of the International Neuropsychological Society, 10, 305–316. doi:10.1017/S1355617704102129CrossRefGoogle ScholarPubMed
Lin, J.J., Riley, J.D., Juranek, J., Cramer, S.C. (2008). Vulnerability of the frontal-temporal connections in temporal lobe epilepsy. Epilepsy Research, 82, 162–170. doi:10.1016/j.eplepsyres.2008.07.020CrossRefGoogle ScholarPubMed
Mangeot, S., Armstrong, K., Colvin, A.N., Yeates, K.O., Taylor, H.G. (2002). Long-term executive function deficits in children with traumatic brain injuries: Assessment using the Behavior Rating Inventory of Executive Function (BRIEF). Child Neuropsychology, 8, 271–284. doi:10.1076/chin.8.4.271.13503CrossRefGoogle ScholarPubMed
Max, J.E., Schachar, R.J., Levin, H.S., Ewing-Cobbs, L., Chapman, S.B., Dennis, M., Landis, J. (2005). Predictors of attention-deficit/hyperactivity disorder within 6 months after pediatric traumatic brain injury. Journal of the American Academy of Child & Adolescent Psychiatry, 44, 1032–1040. doi:10.1097/01.chi.0000173293.05817.b1CrossRefGoogle ScholarPubMed
Mori, S., van Zijl, P.C.M. (2002). Fiber tracking: Principles and strategies – a technical review. NMR in Biomedicine, 15, 468–480. doi:10.1002/nbm.781CrossRefGoogle ScholarPubMed
Moseley, M., Bammer, R., Illes, J. (2002). Diffusion-tensor imaging of cognitive performance. Brain and Cognition, 50, 396–413. doi:10.1016/S0278-2626(02)00524-9CrossRefGoogle ScholarPubMed
Ochsner, K.N., Ray, R.R., Hughes, B., McRae, K., Cooper, J.C., Weber, J., Gross, J.J. (2009). Bottom-up and top-down processes in emotion generation: Common and distinct neural mechanisms. Psychological Science, 20, 1322–1331. doi:10.1111/j.1467-9280.2009.02459.xCrossRefGoogle ScholarPubMed
Pierpaoli, C., Barnett, A., Pajevic, S., Chen, R., Penix, L., Virta, A., Basser, P. (2001). Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage, 13, 1174–1185. doi:10.1006/nimg.2001.0765CrossRefGoogle ScholarPubMed
Pierpaoli, C., Basser, P.J. (1996). Toward a quantitative assessment of diffusion anisotropy. Magnetic Resonance in Medicine, 36, 893–906. doi:10.1002/mrm.1910360612CrossRefGoogle Scholar
Pugliese, L., Catani, M., Ameis, S., Dell'Acqua, F., de Schotten, M.T., Murphy, C., Murphy, D.G.M. (2009). The anatomy of extended limbic pathways in Asperger syndrome: A preliminary diffusion tensor imaging tractography study. Neuroimage, 47, 427–434. doi:10.1016/j.neuroimage.2009.05.014CrossRefGoogle ScholarPubMed
Rubia, K., Smith, A.B., Woolley, J., Nosarti, C., Heyman, I., Taylor, E., Brammer, M. (2006). Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Human Brain Mapping, 27, 973–993. doi:10.1002/hbm.20237CrossRefGoogle ScholarPubMed
Rugg-Gunn, F.J., Symms, M.R., Barker, G.J., Greenwood, R., Duncan, J.S. (2001). Diffusion imaging shows abnormalities after blunt head trauma when conventional magnetic resonance imaging is normal. Journal of Neurology, Neurosurgery, & Psychiatry, 70, 530–533. doi:10.1136/jnnp.70.4.530CrossRefGoogle Scholar
Saatman, K.E., Duhaime, A.C., Bullock, R., Maas, A.I., Valadka, A., Manley, G.T. (2008). Classification of traumatic brain injury for targeted therapies. Journal of Neurotrauma, 25, 719–738. doi:10.1089/neu.2008.0586CrossRefGoogle ScholarPubMed
Schwartz, L., Taylor, H.G., Drotar, D., Yeates, K.O., Wade, S.L., Stancin, T. (2003). Long term behavior problems following pediatric traumatic brain injury: Prevalence, predictors, and correlates. Journal of Pediatric Psychology, 28, 251–263. doi:10.1093/jpepsy/jsg013CrossRefGoogle ScholarPubMed
Sesma, H.W., Slomine, B.S., Ding, R., McCarthy, M.L. (2008). Executive functioning in the first year after pediatric traumatic brain injury. Pediatrics, 121, e1686–1695. doi:10.1542/peds.2007-2461CrossRefGoogle ScholarPubMed
Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E., Johansen-Berg, H., Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23, S208–S219. doi:10.1016/j.neuroimage.2004.07.051CrossRefGoogle ScholarPubMed
Somerville, L.H., Casey, B.J. (2010). Developmental neurobiology of cognitive control and motivational systems. Current Opinions in Neurobiology, 20, 236–241. doi:10.1016/j.conb.2010.01.006CrossRefGoogle ScholarPubMed
Steyerberg, E.W., Mushkudiani, N., Perel, P., Butcher, I., Lu, J., McHugh, G.S., Maas, A.I.R. (2008). Predicting outcome after traumatic brain injury: Development and international validation of prognostic scores based on admission characteristics. Public Library of Science Medicine, 5, e165. doi:10.1371/journal.pmed.0050165Google ScholarPubMed
Tasker, R.C. (2006). Changes in white matter late after severe traumatic brain injury in childhood. Developmental Neuroscience, 28, 302–308. doi:10.1159/000094156CrossRefGoogle ScholarPubMed
Taylor, H.G., Yeates, K.O., Wade, S.L., Drotar, D., Stancin, T., Minich, N. (2002). A prospective study of short- and long-term outcomes after traumatic brain injury in children: Behavior and achievement. Neuropsychology, 16, 15–27. doi:10.1037//0894-4105.16.1.15CrossRefGoogle Scholar
Teasdale, G., Jennett, B. (1974). Assessment of coma and impaired consciousness: A practical scale. The Lancet, 304, 81–84. doi:10.1016/S0140-6736(74)91639-0CrossRefGoogle Scholar
Vriezen, E.R., Pigott, S.E. (2002). The relationship between parental report on the BRIEF and performance-based measures of executive function in children with moderate to severe traumatic brain injury. Child Neuropsychology, 8, 296–303. doi:10.1076/chin.8.4.296.13505CrossRefGoogle ScholarPubMed
Wager, T.D., Davidson, M.L., Hughes, B.L., Lindquist, M.A., Ochsner, K.N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron, 59, 1037–1050. doi:10.1016/j.neuron.2008.09.006CrossRefGoogle ScholarPubMed
Wallis, L.I., Widjaja, E., Wignall, E.L., Wilkinson, I.D., Griffiths, P.D. (2006). Misrepresentation of surface rendering of pediatric brain malformations performed following spatial normalization. Acta Radiologica, 47, 1094–1099. doi:10.1080/02841850600979048CrossRefGoogle ScholarPubMed
Wilde, E.A., Chu, Z., Bigler, E.D., Hunter, J.V., Fearing, M.A., Hanten, G., Levin, H.S. (2006). Diffusion tensor imaging in the corpus callosum in children after moderate to severe traumatic brain injury. Journal of Neurotrauma, 23, 1412–1426. doi:10.1089/neu.2006.23.1412CrossRefGoogle ScholarPubMed
Wilde, E.A., Hunter, J.V., Newsome, M.R., Scheibel, R.S., Bigler, E.D., Johnson, J.L., Levin, H.S. (2005). Frontal and temporal morphometric findings on MRI in children after moderate to severe traumatic brain injury. Journal of Neurotrauma, 22, 333–344. doi:10.1089/neu.2005.22.333CrossRefGoogle ScholarPubMed
Wilde, E.A., Ramos, M.A., Yallampali, R., Bigler, E.D., McCauley, S.R., Chu, Z., Levin, H.S. (2010). Diffusion tensor imaging of the cingulum bundle in children after traumatic brain injury. Developmental Neuropsychology, 35, 333–351. doi:10.1080/87565641003696940CrossRefGoogle ScholarPubMed