Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-25T04:26:03.791Z Has data issue: false hasContentIssue false

Disrupted Structural Connectome Is Associated with Both Psychometric and Real-World Neuropsychological Impairment in Diffuse Traumatic Brain Injury

Published online by Cambridge University Press:  07 October 2014

Junghoon Kim*
Affiliation:
Moss Rehabilitation Research Institute, Elkins Park, Pennsylvania
Drew Parker
Affiliation:
Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania
John Whyte
Affiliation:
Moss Rehabilitation Research Institute, Elkins Park, Pennsylvania
Tessa Hart
Affiliation:
Moss Rehabilitation Research Institute, Elkins Park, Pennsylvania
John Pluta
Affiliation:
Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania
Madhura Ingalhalikar
Affiliation:
Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania
H. B. Coslett
Affiliation:
Department of Neurology, University of Pennsylvania, Philadelphia, Pennsylvania
Ragini Verma
Affiliation:
Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania
*
Correspondence and reprint requests to: Junghoon Kim, Department of Physiology, Pharmacology, and Neuroscience, Sophie Davis School of Biomedical Education, The City College of New York, 160 Convent Avenue, New York, NY 10031. E-mail: [email protected]

Abstract

Traumatic brain injury (TBI) is likely to disrupt structural network properties due to diffuse white matter pathology. The present study aimed to detect alterations in structural network topology in TBI and relate them to cognitive and real-world behavioral impairment. Twenty-two people with moderate to severe TBI with mostly diffuse pathology and 18 demographically matched healthy controls were included in the final analysis. Graph theoretical network analysis was applied to diffusion tensor imaging (DTI) data to characterize structural connectivity in both groups. Neuropsychological functions were assessed by a battery of psychometric tests and the Frontal Systems Behavior Scale (FrSBe). Local connection-wise analysis demonstrated reduced structural connectivity in TBI arising from subcortical areas including thalamus, caudate, and hippocampus. Global network metrics revealed that shortest path length in participants with TBI was longer compared to controls, and that this reduced network efficiency was associated with worse performance in executive function and verbal learning. The shortest path length measure was also correlated with family-reported FrSBe scores. These findings support the notion that the diffuse form of neuropathology caused by TBI results in alterations in structural connectivity that contribute to cognitive and real-world behavioral impairment. (JINS, 2014, 20, 1–10)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adnan, A., Crawley, A., Mikulis, D., Moscovitch, M., Colella, B., & Green, R. (2013). Moderate-severe traumatic brain injury causes delayed loss of white matter integrity: Evidence of fornix deterioration in the chronic stage of injury. Brain Injury, 27(12), 14151422.CrossRefGoogle ScholarPubMed
Bassett, D.S., Bullmore, E., Verchinski, B.A., Mattay, V.S., Weinberger, D.R., & Meyer-Lindenberg, A. (2008). Hierarchical organization of human cortical networks in health and schizophrenia. Journal of Neuroscience, 28(37), 92399248.CrossRefGoogle ScholarPubMed
Bazarian, J.J., Zhong, J., Blyth, B., Zhu, T., Kavcic, V., & Peterson, D. (2007). Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: A pilot study. J Neurotrauma, 24(9), 14471459.CrossRefGoogle ScholarPubMed
Behrens, T.E., Woolrich, M.W., Jenkinson, M., Johansen-Berg, H., Nunes, R.G., Clare, S., &Smith, S.M. (2003). Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magnetic Resonance in Medicine, 50(5), 10771088.CrossRefGoogle ScholarPubMed
Bennett, I.J., Madden, D.J., Vaidya, C.J., Howard, D.V., & Howard, J.H. Jr. (2010). Age-related differences in multiple measures of white matter integrity: A diffusion tensor imaging study of healthy aging. Human Brain Mapping, 31(3), 378390.CrossRefGoogle ScholarPubMed
Benton, A.L., & Hamsher, K. (1983). Multilingual Aphasia Examination. Iowa City: AJA Associates.Google Scholar
Blatter, D.D., Bigler, E.D., Gale, S.D., Johnson, S.C., Anderson, C.V., Burnett, B.M., &Bailey, B.J. (1997). MR-based brain and cerebrospinal fluid measurement after traumatic brain injury: Correlation with neuropsychological outcome. AJNR American Journal of Neuroradiology, 18(1), 110.Google ScholarPubMed
Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews. Neuroscience, 10(3), 186198.CrossRefGoogle ScholarPubMed
Burzynska, A.Z., Preuschhof, C., Backman, L., Nyberg, L., Li, S.C., Lindenberger, U., & Heekeren, H.R. (2010). Age-related differences in white matter microstructure: Region-specific patterns of diffusivity. Neuroimage, 49(3), 21042112.CrossRefGoogle ScholarPubMed
Caeyenberghs, K., Leemans, A., Leunissen, I., Gooijers, J., Michiels, K., Sunaert, S., & Swinnen, S.P. (2014). Altered structural networks and executive deficits in traumatic brain injury patients. Brain Structure & Function, 219(1), 193209.CrossRefGoogle ScholarPubMed
Caeyenberghs, K., Leemans, A., Leunissen, I., Michiels, K., & Swinnen, S.P. (2013). Topological correlations of structural and functional networks in patients with traumatic brain injury. Frontiers in Human Neuroscience, 7, 726.CrossRefGoogle ScholarPubMed
Cao, C., & Slobounov, S. (2010). Alteration of cortical functional connectivity as a result of traumatic brain injury revealed by graph theory, ICA, and sLORETA analyses of EEG signals. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 18(1), 1119.CrossRefGoogle ScholarPubMed
Castellanos, N.P., Leyva, I., Buldu, J.M., Bajo, R., Paul, N., Cuesta, P., &del-Pozo, F. (2011). Principles of recovery from traumatic brain injury: Reorganization of functional networks. Neuroimage, 55(3), 11891199.CrossRefGoogle ScholarPubMed
Castellanos, N.P., Paul, N., Ordonez, V.E., Demuynck, O., Bajo, R., Campo, P., &Maestu, F. (2010). Reorganization of functional connectivity as a correlate of cognitive recovery in acquired brain injury. Brain, 133(Pt 8), 23652381.CrossRefGoogle ScholarPubMed
Collette, F., Hogge, M., Salmon, E., & Van der Linden, M. (2006). Exploration of the neural substrates of executive functioning by functional neuroimaging. Neuroscience, 139(1), 209221.CrossRefGoogle ScholarPubMed
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (2000). California Verbal Learning Test: Second Edition. San Antonio, TX: Psychological Corporation.Google Scholar
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(3), 968980.CrossRefGoogle ScholarPubMed
Edlow, B.L., & Wu, O. (2012). Advanced neuroimaging in traumatic brain injury. Seminars in Neurology, 32(4), 374400.Google ScholarPubMed
Faul, M., Xu, L., Wald, M.M., & Coronado, V.G. (2010). Traumatic brain injury in the United States: Emergency department visits, hospitalizations, and deaths. Atlanta, GA: Center for Disease Control and Prevention.Google Scholar
Fischl, B., Sereno, M.I., & Dale, A.M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage, 9(2), 195207.CrossRefGoogle Scholar
Gong, G., He, Y., Concha, L., Lebel, C., Gross, D.W., Evans, A.C., & Beaulieu, C. (2009). Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. Cerebral Cortex, 19(3), 524536.CrossRefGoogle ScholarPubMed
Gong, G., Rosa-Neto, P., Carbonell, F., Chen, Z.J., He, Y., & Evans, A.C. (2009). Age- and gender-related differences in the cortical anatomical network. Journal of Neuroscience, 29(50), 1568415693.CrossRefGoogle ScholarPubMed
Grace, J., Stout, J.C., & Malloy, P.F. (1999). Assessing frontal lobe behavioral syndromes with the frontal lobe personality scale. Assessment, 6(3), 269284.CrossRefGoogle ScholarPubMed
Graham, D.I., Maxwell, W.L., Adams, J.H., & Jennett, B. (2005). Novel aspects of the neuropathology of the vegetative state after blunt head injury. Progress in Brain Research, 150, 445455.CrossRefGoogle ScholarPubMed
Hagmann, P., Sporns, O., Madan, N., Cammoun, L., Pienaar, R., Wedeen, V.J., &Grant, P.E. (2010). White matter maturation reshapes structural connectivity in the late developing human brain. Proceedings of the National Academy of Sciences of the United States America, 107(44), 1906719072.CrossRefGoogle ScholarPubMed
He, Y., & Evans, A. (2010). Graph theoretical modeling of brain connectivity. Current Opinion in Neurology, 23(4), 341350.CrossRefGoogle ScholarPubMed
Huisman, T.A., Schwamm, L.H., Schaefer, P.W., Koroshetz, W.J., Shetty-Alva, N., Ozsunar, Y., &Sorensen, A.G. (2004). Diffusion tensor imaging as potential biomarker of white matter injury in diffuse axonal injury. AJNR American Journal of Neuroradiology, 25(3), 370376.Google ScholarPubMed
Hulkower, M.B., Poliak, D.B., Rosenbaum, S.B., Zimmerman, M.E., & Lipton, M.L. (2013). A decade of DTI in traumatic brain injury: 10 years and 100 articles later. AJNR American Journal of Neuroradiology, 34(11), 20642074.CrossRefGoogle ScholarPubMed
Kim, J., Avants, B., Patel, S., Whyte, J., Coslett, B.H., Pluta, J., &Gee, J.C. (2008). Structural consequences of diffuse traumatic brain injury: A large deformation tensor-based morphometry study. Neuroimage, 39(3), 10141026.CrossRefGoogle ScholarPubMed
Kim, J., Whyte, J., Hart, T., Vaccaro, M., Polansky, M., & Coslett, H.B. (2005). Executive function as a predictor of inattentive behavior after traumatic brain injury. Journal of the International Neuropsychological Society, 11(4), 434445.CrossRefGoogle ScholarPubMed
Kim, J., Whyte, J., Patel, S., Europa, E., Slattery, J., Coslett, H.B., & Detre, J.A. (2012). A perfusion fMRI study of the neural correlates of sustained-attention and working-memory deficits in chronic traumatic brain injury. Neurorehabilitation and Neural Repair, 26(7), 870880.CrossRefGoogle ScholarPubMed
Levin, H.S., Benton, A.L., & Grossman, R.G. (1982). Neurobehavioral consequences of closed head injury. New York: Oxford University Press.Google Scholar
Levine, B., Kovacevic, N., Nica, E.I., Schwartz, M.L., Gao, F., & Black, S.E. (2013). Quantified MRI and cognition in TBI with diffuse and focal damage. Neuroimage. Clinical, 2, 534541.CrossRefGoogle ScholarPubMed
Li, Y., Jewells, V., Kim, M., Chen, Y., Moon, A., Armao, D., &Shen, D. (2013). Diffusion tensor imaging based network analysis detects alterations of neuroconnectivity in patients with clinically early relapsing-remitting multiple sclerosis. Human Brain Mapping, 34, 33763391.CrossRefGoogle ScholarPubMed
Lo, C.Y., Wang, P.N., Chou, K.H., Wang, J., He, Y., & Lin, C.P. (2010). Diffusion tensor tractography reveals abnormal topological organization in structural cortical networks in Alzheimer's disease. Journal of Neuroscience, 30(50), 1687616885.CrossRefGoogle ScholarPubMed
Mendez, C.V., Hurley, R.A., Lassonde, M., Zhang, L., & Taber, K.H. (2005). Mild traumatic brain injury: Neuroimaging of sports-related concussion. The Journal of Neuropsychiatry and Clinical Neurosciences, 17(3), 297303.CrossRefGoogle ScholarPubMed
Morris, S.B., & DeShon, R.P. (2002). Combining effect size estimates in meta-analysis with repeated measures and independent-groups designs. Psychological Methods, 7(1), 105125.CrossRefGoogle ScholarPubMed
Nakamura, T., Hillary, F.G., & Biswal, B.B. (2009). Resting network plasticity following brain injury. PLoS One, 4(12), e8220.CrossRefGoogle ScholarPubMed
Pandit, A.S., Expert, P., Lambiotte, R., Bonnelle, V., Leech, R., Turkheimer, F.E., & Sharp, D.J. (2013). Traumatic brain injury impairs small-world topology. Neurology, 80(20), 18261833.CrossRefGoogle ScholarPubMed
Povlishock, J.T., & Katz, D.I. (2005). Update of neuropathology and neurological recovery after traumatic brain injury. The Journal of Head Trauma Rehabilitation, 20(1), 7694.CrossRefGoogle ScholarPubMed
Quade, D. (1967). Rank analysis of covariance. Journal of the American Statistical Association, 62(320), 11871200.CrossRefGoogle Scholar
Reitan, R.M., & Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery. Tuscon, AZ: Neuropsychology Press.Google Scholar
Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. Neuroimage, 52(3), 10591069.CrossRefGoogle ScholarPubMed
Schwartz, M.F., Brecher, A.R., Whyte, J., & Klein, M.G. (2005). A patient registry for cognitive rehabilitation research: A strategy for balancing patients' privacy rights with researchers' need for access. Archives of Physical Medicine and Rehabilitation, 86(9), 18071814.CrossRefGoogle ScholarPubMed
Sharp, D.J., Scott, G., & Leech, R. (2014). Network dysfunction after traumatic brain injury. Nature Reviews . Neurology, 10(3), 156166.Google Scholar
Simpson, E.H. (1951). The interpretation of interaction in contingency tables. Journal of the Royal Statistical Society, 13, 238241.Google Scholar
Stam, C.J., & Reijneveld, J.C. (2007). Graph theoretical analysis of complex networks in the brain. Nonlinear Biomedical Physics, 1(1), 3.CrossRefGoogle ScholarPubMed
Thurman, D.J., Alverson, C., Dunn, K.A., Guerrero, J., & Sniezek, J.E. (1999). Traumatic brain injury in the United States: A public health perspective. The Journal of Head Trauma Rehabilitation, 14(6), 602615.CrossRefGoogle ScholarPubMed
Trenerry, M.R., Crosson, B., DeBoe, J., & Leber, W.R. (1989). Stroop Neuropsychological Screening Test. Odessa, FL: Psychlogical Assessment Resources, Inc.Google Scholar
Wang, J.Y., Bakhadirov, K., Devous, M.D. Sr., Abdi, H., McColl, R., Moore, C., &Diaz-Arrastia, R. (2008). Diffusion tensor tractography of traumatic diffuse axonal injury. Archives of Neurology, 65(5), 619626.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997a). Wechsler Adult Intelligence Scale - 3rd Edition. New York: Psychological Corporation.Google Scholar
Wechsler, D. (1997b). Wechsler Memory Scale - 3rd Edition. New York: Psychological Corporation.Google Scholar
Wilde, E.A., McCauley, S.R., Hunter, J.V., Bigler, E.D., Chu, Z., Wang, Z.J., &Levin, H.S. (2008). Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology, 70(12), 948955.CrossRefGoogle ScholarPubMed
Supplementary material: File

Kim Supplementary Material

Table S1

Download Kim Supplementary Material(File)
File 111.9 KB
Supplementary material: File

Kim Supplementary Material

Table S2

Download Kim Supplementary Material(File)
File 68.6 KB
Supplementary material: File

Kim Supplementary Material

Table S3

Download Kim Supplementary Material(File)
File 63 KB