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Role of Frontotemporal Fiber Tract Integrity in Task-Switching Performance of Healthy Controls and Patients with Temporal Lobe Epilepsy

Published online by Cambridge University Press:  12 October 2011

N. Erkut Kucukboyaci ,
H.M. Girard ,
D.J. Hagler Jr. ,
J. Kuperman ,
E.S. Tecoma ,
V.J. Iragui ,
E. Halgren  and
C.R. McDonald
N. Erkut Kucukboyaci*
Affiliation:
Department of Psychiatry, University of California, San Diego, California Multimodal Imaging Laboratory, University of California, San Diego, California San Diego State University/University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California
H.M. Girard
Affiliation:
Multimodal Imaging Laboratory, University of California, San Diego, California
D.J. Hagler Jr.
Affiliation:
Multimodal Imaging Laboratory, University of California, San Diego, California Department of Radiology, University of California, San Diego, California
J. Kuperman
Affiliation:
Multimodal Imaging Laboratory, University of California, San Diego, California
E.S. Tecoma
Affiliation:
Department of Neurosciences, University of California, San Diego, California
V.J. Iragui
Affiliation:
Department of Neurosciences, University of California, San Diego, California
E. Halgren
Affiliation:
Multimodal Imaging Laboratory, University of California, San Diego, California Department of Radiology, University of California, San Diego, California
C.R. McDonald
Affiliation:
Department of Psychiatry, University of California, San Diego, California Multimodal Imaging Laboratory, University of California, San Diego, California
*
Correspondence and reprint requests to: N. Erkut Kucukboyaci, Multimodal Imaging Laboratory, Suite C101; 8950 Villa La Jolla Drive, La Jolla, CA 92037. E-mail: [email protected]
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Abstract

The objective of this study is to investigate the relationships among frontotemporal fiber tract compromise and task-switching performance in healthy controls and patients with temporal lobe epilepsy (TLE). We performed diffusion tensor imaging (DTI) on 30 controls and 32 patients with TLE (15 left TLE). Fractional anisotropy (FA) was calculated for four fiber tracts [uncinate fasciculus (UncF), arcuate fasciculus (ArcF), dorsal cingulum (CING), and inferior fronto-occipital fasciculus (IFOF)]. Participants completed the Trail Making Test-B (TMT-B) and Verbal Fluency Category Switching (VFCS) test. Multivariate analyses of variances (MANOVAs) were performed to investigate group differences in fiber FA and set-shifting performances. Canonical correlations were used to examine the overall patterns of structural-cognitive relationships and were followed by within-group bivariate correlations. We found a significant canonical correlation between fiber FA and task-switching performance. In controls, TMT-B correlated with left IFOF, whereas VFCS correlated with FA of left ArcF and left UncF. These correlations were not significant in patients with TLE. We report significant correlations between frontotemporal fiber tract integrity and set-shifting performance in healthy controls that appear to be absent or attenuated in patients with TLE. These findings suggest a breakdown of typical structure-function relationships in TLE that may reflect aberrant developmental or degenerative processes. (JINS, 2012, 18, 57–67)

Keywords

Diffusion tensorUncinateCingulateFrontal lobeArcuateIFOF
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 1 , January 2012 , pp. 57 - 67
Copyright
Copyright © The International Neuropsychological Society 2011

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References

Ahmadi, M.E., Hagler, D.J. Jr., McDonald, C.R., Tecoma, E.S., Iragui, V.J., Dale, A.M., Halgren, E. (2009). Side matters: Diffusion tensor imaging tractography in left and right temporal lobe epilepsy. AJNR American Journal of Neuroradiology, 30(9), 1740–1747. doi:10.3174/ajnr.A1650CrossRefGoogle ScholarPubMed
Basser, P.J., Mattiello, J., LeBihan, D. (1994). MR diffusion tensor spectroscopy and imaging. Journal of Biophysics, 66(1), 259–267.CrossRefGoogle ScholarPubMed
Bernhardt, B.C., Bernasconi, N., Concha, L., Bernasconi, A. (2010). Cortical thickness analysis in temporal lobe epilepsy: Reproducibility and relation to outcome. Neurology, 74(22), 1776–1784. doi:10.1212/WNL.0b013e3181e0f80aCrossRefGoogle ScholarPubMed
Bernhardt, B.C., Worsley, K.J., Kim, H., Evans, A.C., Bernasconi, A., Bernasconi, N. (2009). Longitudinal and cross-sectional analysis of atrophy in pharmacoresistant temporal lobe epilepsy. Neurology, 72(20), 1747–1754. doi:10.1212/01.wnl.0000345969.57574.f5CrossRefGoogle ScholarPubMed
Bonelli, S.B., Powell, R.H., Yogarajah, M., Samson, R.S., Symms, M.R., Thompson, P.J., Duncan, J.S. (2010). Imaging memory in temporal lobe epilepsy: Predicting the effects of temporal lobe resection. Brain, 133(Pt 4), 1186–1199. doi:10.1093/brain/awq006CrossRefGoogle ScholarPubMed
Bonilha, L., Alessio, A., Rorden, C., Baylis, G., Damasceno, B.P., Min, L.L., Cendes, F. (2007). Extrahippocampal gray matter atrophy and memory impairment in patients with medial temporal lobe epilepsy. Human Brain Mapping, 28(12), 1376–1390. doi:10.1002/hbm.20373CrossRefGoogle ScholarPubMed
Burns, J., Job, D., Bastin, M.E., Whalley, H., Macgillivray, T., Johnstone, E.C., Lawrie, S.M. (2003). Structural disconnectivity in schizophrenia: A diffusion tensor magnetic resonance imaging study. The British Journal of Psychiatry, 182, 439–443.CrossRefGoogle ScholarPubMed
Cahn-Weiner, D.A., Wittenberg, D., McDonald, C. (2009). Everyday cognition in temporal lobe and frontal lobe epilepsy. Epileptic Disorders, 11(3), 222–227. doi:10.1684/epd.2009.0265CrossRefGoogle ScholarPubMed
Catani, M., Howard, R.J., Pajevic, S., Jones, D.K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage, 17(1), 77–94.CrossRefGoogle ScholarPubMed
Catani, M., Jones, D.K., Ffytche, D.H. (2005). Perisylvian language networks of the human brain. Annals of Neurology, 57, 8–16.CrossRefGoogle ScholarPubMed
Charlton, R.A., Barrick, T.R., Lawes, I.N., Markus, H.S., Morris, R.G. (2010). White matter pathways associated with working memory in normal aging. Cortex, 46(4), 474–489. doi:10.1016/j.cortex.2009.07.005CrossRefGoogle ScholarPubMed
Coan, A.C., Appenzeller, S., Bonilha, L., Li, L.M., Cendes, F. (2009). Seizure frequency and lateralization affect progression of atrophy in temporal lobe epilepsy. Neurology, 73(11), 834–842. doi:10.1212/WNL.0b013e3181b783ddGoogle Scholar
Delis, D.C., Kaplan, E., Kramer, J.H. (2001). The Delis-Kaplan Executive Function System. San Antonio, TX: The Psychological Corporation.Google Scholar
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(8), 1409–1418. doi:10.1111/j.1528-1167.2008.01596.xCrossRefGoogle ScholarPubMed
Diehl, B., Piao, Z., Tkach, J., Busch, R.M., LaPresto, E., Najm, I., Luders, H. (2010). Cortical stimulation for language mapping in focal epilepsy: Correlations with tractography of the arcuate fasciculus. Epilepsia, 51(4), 639–646. doi:10.1111/j.1528-1167.2009.02421.xCrossRefGoogle ScholarPubMed
Drake, M., Allegri, R.F., Thomson, A. (2000). Executive cognitive alteration of prefrontal type in patients with mesial temporal lobe epilepsy. [Alteracion cognitiva ejecutiva de tipo prefrontal en pacientes con epilepsia del lobulo temporal mesial] Medicina, 60(4), 453–456.Google ScholarPubMed
Dulay, M.F., Verma, A., Karmonik, C., Kawai, M., Xue, Z., Strutt, A.M., Grossman, R.G. (2009). Frontal lobe functional correlates of diffusion tensor imaging in temporal lobe epilepsy (abstract). Epilepsia, 50(Suppl. 11), 79.Google Scholar
Focke, N.K., Yogarajah, M., Bonelli, S.B., Bartlett, P.A., Symms, M.R., Duncan, J.S. (2008). Voxel-based diffusion tensor imaging in patients with mesial temporal lobe epilepsy and hippocampal sclerosis. Neuroimage, 40(2), 728–737. doi:10.1016/j.neuroimage.2007.12.031CrossRefGoogle ScholarPubMed
Garcia Espinosa, A., Andrade Machado, R., Borges Gonzalez, S., Garcia Gonzalez, M.E., Perez Montoto, A., Toledo Sotomayor, G. (2010). Wisconsin card sorting test performance and impulsivity in patients with temporal lobe epilepsy: Suicidal risk and suicide attempts. Epilepsy & Behavior, 17(1), 39–45. doi:10.1016/j.yebeh.2009.09.010Google Scholar
Guimaraes, C.A., Bonilha, L., Franzon, R.C., Li, L.M., Cendes, F., Guerreiro, M.M. (2007). Distribution of regional gray matter abnormalities in a pediatric population with temporal lobe epilepsy and correlation with neuropsychological performance. Epilepsy & Behavior, 11(4), 558–566. doi:10.1016/j.yebeh.2007.07.005CrossRefGoogle Scholar
Hagler, D.J. Jr., Ahmadi, M.E., Kuperman, J., Holland, D., McDonald, C.R., Halgren, E., Dale, A.M. (2009). Automated white-matter tractography using a probabilistic diffusion tensor atlas: Application to temporal lobe epilepsy. Human Brain Mapping, 30(5), 1535–1547. doi:10.1002/hbm.20619CrossRefGoogle ScholarPubMed
Hamberger, M.J., Seidel, W.T. (2003). Auditory and visual naming tests: Normative and patient data for accuracy, response time, and tip-of-the-tongue. Journal of the International Neuropsychological Society, 9(3), 479–489.CrossRefGoogle ScholarPubMed
Hermann, B., Jones, J., Sheth, R., Dow, C., Koehn, M., Seidenberg, M. (2006). Children with new-onset epilepsy: Neuropsychological status and brain structure. Brain, 129, 2609–2619. doi:10.1093/brain/awl196CrossRefGoogle ScholarPubMed
Hermann, B., Seidenberg, M., Lee, E.J., Chan, F., Rutecki, P. (2007). Cognitive phenotypes in temporal lobe epilepsy. Journal of the International Neuropsychological Society, 13(1), 12–20. doi:10.1017/S135561770707004XCrossRefGoogle ScholarPubMed
Holland, D., Kuperman, J.M., Dale, A.M. (2010). Efficient correction of inhomogeneous static magnetic field-induced distortion in echo planar imaging. Neuroimage, 50(1), 175–183.Google Scholar
Hutchinson, E., Pulsipher, D., Dabbs, K., Myers y Gutierrez, A., Sheth, R., Jones, J., Hermann, B. (2010). Children with new-onset epilepsy exhibit diffusion abnormalities in cerebral white matter in the absence of volumetric differences. Epilepsy Research, 88, 208–214. doi:10.1016.j.eplepsyres.2009.11.011CrossRefGoogle ScholarPubMed
Jovicich, J., Czanner, S., Greve, D., Haley, E., Kouwe, A., Gollub, R., Dale, A. (2006). Reliability in multi-site structural MRI studies: Effects of gradient non-linearity correction on phantom and human data. Neuroimage, 30(2), 436–443.CrossRefGoogle ScholarPubMed
Keller, S.S., Roberts, N. (2008). Voxel-based morphometry of temporal lobe epilepsy: An introduction and review of the literature. Epilepsia, 49(5), 741–757. doi:10.1111/j.1528-1167.2007.01485.xCrossRefGoogle ScholarPubMed
Kim, C.H., Lee, S.A., Yoo, H.J., Kang, J.K., Lee, J.K. (2007). Executive performance on the Wisconsin card sorting test in mesial temporal lobe epilepsy. European Neurology, 57, 39–46. doi:10.1159/000097009Google Scholar
Klingler, J., Gloor, P. (1960). The connections of the amygdala and of the anterior temporal cortex in the human brain. Journal of Comparative Neurology, 115, 333–369.CrossRefGoogle 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(2–3), 162–170. doi:10.1016/j.eplepsyres.2008.07.020CrossRefGoogle ScholarPubMed
Lin, J.J., Salamon, N., Lee, A.D., Dutton, R.A., Geaga, J.A., Hayashi, K.M., Thompson, P.M. (2007). Reduced neocortical thickness and complexity mapped in mesial temporal lobe epilepsy with hippocampal sclerosis. Cerebral Cortex, 17, 2007–2018. doi:10.1093/cercor/bhl109CrossRefGoogle ScholarPubMed
Lopes, A.F., Simoes, M.M., Robalo, C.N., Fineza, I., Goncalves, O.B. (2010). Neuropsychological evaluation in children with epilepsy: Attention and executive functions in temporal lobe epilepsy. [Evaluacion neuropsicologica en ninos con epilepsia: atencion y funciones ejecutivas en epilepsia del lobulo temporal] Revista De Neurologia, 50(5), 265–272.CrossRefGoogle ScholarPubMed
Martin, R.C., Sawrie, S.M., Edwards, R., Roth, D.L., Faught, E., Kuzniecky, R.I., Gilliam, F.G. (2000). Investigation of executive function change following anterior temporal lobectomy: Selective normalization of verbal fluency. Neuropsychology, 14(4), 501–508.CrossRefGoogle ScholarPubMed
Martino, J., Brogna, C., Robles, S.G., Vergani, F., Duffau, H. (2010). Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex, 46(5), 691–699. doi:10.1016/j.cortex.2009.07.015CrossRefGoogle ScholarPubMed
McDonald, C.R., Ahmadi, M.E., Hagler, D.J., Tecoma, E.S., Iragui, V.J., Gharapetian, L., Halgren, E. (2008). Diffusion tensor imaging correlates of memory and language impairments in temporal lobe epilepsy. Neurology, 71(23), 1869–1876. doi:10.1212/01.wnl.0000327824.05348.3bCrossRefGoogle ScholarPubMed
McDonald, C.R., Delis, D.C., Kramer, J.H., Tecoma, E.S., Iragui, V.J. (2008). A componential analysis of proverb interpretation in patients with frontal lobe epilepsy and temporal lobe epilepsy: Relationships with disease-related factors. The Clinical Neuropsychologist, 22(3), 480–496. doi:10.1080/13854040701363828CrossRefGoogle ScholarPubMed
McDonald, C.R., Delis, D.C., Norman, M.A., Tecoma, E.S., Iragui-Madoz, V.I. (2005). Is impairment in set-shifting specific to frontal-lobe dysfunction? evidence from patients with frontal-lobe or temporal-lobe epilepsy. Journal of the International Neuropsychological Society, 11(4), 477–481.CrossRefGoogle ScholarPubMed
McDonald, C.R., Hagler, D.J. Jr., Ahmadi, M.E., Tecoma, E., Iragui, V., Gharapetian, L., Halgren, E. (2008). Regional neocortical thinning in mesial temporal lobe epilepsy. Epilepsia, 49(5), 794–803. doi:10.1111/j.1528-1167.2008.01539.xGoogle Scholar
Mueller, S.G., Laxer, K.D., Barakos, J., Cheong, I., Garcia, P., Weiner, M.W. (2009). Widespread neocortical abnormalities in temporal lobe epilepsy with and without mesial sclerosis. Neuroimage, 46(2), 353–359. doi:10.1016/j.neuroimage.2009.02.020CrossRefGoogle ScholarPubMed
Pereira, F.R., Alessio, A., Sercheli, M.S., Pedro, T., Bilevicius, E., Rondina, J.M., Cendes, F. (2010). Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: Evidence from resting state fMRI. BMC Neuroscience, 11, 66. doi:10.1186/1471-2202-11-66CrossRefGoogle ScholarPubMed
Perry, M.E., McDonald, C.R., Hagler, D.J. Jr., Gharapetian, L, Kuperman, J.M., McEvoy, L.K. (2009). White matter tracts associated with set-shifting in healthy aging. Neuropsychologia, 47(13), 2835–2842. doi:10.1016/j.neuropsychologia.2009.06.008Google Scholar
Protzner, A.B., McAndrews, M.P. (2011). Network alterations supporting word retrieval in patients with medial temporal lobe epilepsy. Journal of Cognitive Neuroscience, 23, 2605–2619. doi:10.1162/jocn.2010.21599Google Scholar
Riederer, F., Lanzenberger, R., Kaya, M., Prayer, D., Serles, W., Baumgartner, C. (2008). Network atrophy in temporal lobe epilepsy: A voxel-based morphometry study. Neurology, 71(6), 419–425. doi:10.1212/01.wnl.0000324264.96100.e0CrossRefGoogle ScholarPubMed
Riley, J.D., Franklin, D.L., Choi, V., Kim, R.C., Binder, D.K., Cramer, S., Lin, J.J. (2010). Altered white matter integrity in temporal lobe epilepsy: Association with cognitive and clinical profiles. Epilepsia, 51(4), 536–545. doi:10.1111/j.1528-1167.2009.02508.xGoogle Scholar
Riley, J.D., Moore, S., Cramer, S., Lin, J.J. (2011). Caudate atrophy and impaired frontostriatal connections are linked to executive dysfunction in temporal lobe epilepsy. Epilepsy & Behavior, 21(1), 80–87. doi:10.1016/j.yebeh.2011.03.013Google Scholar
Seidenberg, M., Kelly, K.G., Parrish, J., Geary, E., Dow, C., Rutecki, P., Hermann, B. (2005). Ipsilateral and contralateral MRI volumetric abnormalities in chronic unilateral temporal lobe epilepsy and their clinical correlates. Epilepsia, 46(3), 420–430. doi:10.1111/j.0013-9580.2005.27004.xGoogle Scholar
Trebuchon-Da Fonseca, A., Guedj, E., Alario, F.X., Laguitton, V., Mundler, O., Chauvel, P., Liegeois-Chauvel, C. (2009). Brain regions underlying word finding difficulties in temporal lobe epilepsy. Brain, 132(Pt 10), 2772–2784. doi:10.1093/brain/awp083CrossRefGoogle ScholarPubMed
Urbanski, M., Thiebaut de Schotten, M., Rodrigo, S., Catani, M., Oppenheim, C., Touze, E., Bartolomeo, P. (2008). Brain networks of spatial awareness: Evidence from diffusion tensor imaging tractography. Journal of Neurology, Neurosurgery, and Psychiatry, 79(5), 598–601. doi:10.1136/jnnp.2007.126276Google Scholar
Voineskos, A.N., Lobaugh, N.J., Bouix, S., Rajji, T.K., Miranda, D., Kennedy, J.L., Shenton, M.E. (2010). Diffusion tensor tractography findings in schizophrenia across the adult lifespan. Brain, 133(Pt 5), 1494–1504. doi:10.1093/brain/awq040CrossRefGoogle ScholarPubMed
Wakana, S., Jiang, H., Nagae-Poetscher, L.M., van Zijl, P.C., Mori, S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology, 230, 77–87. doi:10.1148/radiol.2301021640CrossRefGoogle ScholarPubMed
Wang, X.Q., Lang, S.Y., Lu, H., Ma, L., Mao, Y.L., Yang, F. (2007). Executive function impairment in patients with temporal lobe epilepsy: Neuropsychological and diffusion-tensor imaging study. Zhonghua Yi Xue Za Zhi, 87(45), 3183–3187.Google Scholar
Wang, X.Q., Lang, S.Y., Lu, H., Ma, L., Mao, Y.L., Yang, F. (2010). Changes in extratemporal integrity and cognition in temporal lobe epilepsy: a diffusion tensor imaging study. Neurology India, 58(6), 891–899. doi:10.4103/0028-3886.73739Google Scholar
Yogarajah, M., Duncan, J.S. (2008). Diffusion-based magnetic resonance imaging and tractography in epilepsy. Epilepsia, 49, 189–200.Google Scholar
Yogarajah, M., Focke, N.K., Bonelli, S.B., Thompson, P., Vollmar, C., McEvoy, A.W., Duncan, J.S. (2010). The structural plasticity of white matter networks following anterior temporal lobe resection. Brain, 133(Pt 8), 2348–2364. doi:10.1093/brain/awq175CrossRefGoogle ScholarPubMed
Zahr, N.M., Rohlfing, T., Pfefferbaum, A., Sullivan, E.V. (2009). Problem solving, working memory, and motor correlates of association and commissural fiber bundles in normal aging: A quantitative fiber tracking study. NeuroImage, 44(3), 1050–1062. doi:10.1016/j.neuroimage.2008.09.046CrossRefGoogle ScholarPubMed