Hostname: page-component-669899f699-tpknm Total loading time: 0 Render date: 2025-04-28T15:24:13.219Z Has data issue: false hasContentIssue false
  • English
  • Français

White Matter Integrity Dissociates Verbal Memory and Auditory Attention Span in Emerging Adults with Congenital Heart Disease

Published online by Cambridge University Press:  26 January 2015

Ryan C. Brewster ,
Tricia Z. King ,
Thomas G. Burns ,
David M. Drossner  and
William T. Mahle
Ryan C. Brewster
Affiliation:
Georgia State University, Department of Psychology and Neuroscience Institute, Atlanta, Georgia
Tricia Z. King*
Affiliation:
Georgia State University, Department of Psychology and Neuroscience Institute, Atlanta, Georgia
Thomas G. Burns
Affiliation:
Children’s Healthcare of Atlanta, Atlanta, Georgia Emory University School of Medicine, Atlanta, Georgia
David M. Drossner
Affiliation:
Children’s Healthcare of Atlanta, Atlanta, Georgia
William T. Mahle
Affiliation:
Children’s Healthcare of Atlanta, Atlanta, Georgia Emory University School of Medicine, Atlanta, Georgia
*
Correspondence and reprint requests to: Tricia Z. King, Department of Psychology, Georgia State University 140 Decatur Street, Urban Life Building Suite 1150, Atlanta, GA 30303. E-mail: [email protected].
Get access Rights & Permissions [Opens in a new window]

Abstract

White matter disruptions have been identified in individuals with congenital heart disease (CHD). However, no specific theory-driven relationships between microstructural white matter disruptions and cognition have been established in CHD. We conducted a two-part study. First, we identified significant differences in fractional anisotropy (FA) of emerging adults with CHD using Tract-Based Spatial Statistics (TBSS). TBSS analyses between 22 participants with CHD and 18 demographically similar controls identified five regions of normal appearing white matter with significantly lower FA in CHD, and two higher. Next, two regions of lower FA in CHD were selected to examine theory-driven differential relationships with cognition: voxels along the left uncinate fasciculus (UF; a tract theorized to contribute to verbal memory) and voxels along the right middle cerebellar peduncle (MCP; a tract previously linked to attention). In CHD, a significant positive correlation between UF FA and memory was found, r(20)=.42, p=.049 (uncorrected). There was no correlation between UF and auditory attention span. A positive correlation between MCP FA and auditory attention span was found, r(20)=.47, p=.027 (uncorrected). There was no correlation between MCP and memory. In controls, no significant relationships were identified. These results are consistent with previous literature demonstrating lower FA in younger CHD samples, and provide novel evidence for disrupted white matter integrity in emerging adults with CHD. Furthermore, a correlational double dissociation established distinct white matter circuitry (UF and MCP) and differential cognitive correlates (memory and attention span, respectively) in young adults with CHD. (JINS, 2015, 21, 22–33)

Keywords

Congenital heart diseaseDiffusion tensor imagingAdolescentsAdultsMemoryAttention
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 21 , Issue 1 , January 2015 , pp. 22 - 33
Copyright
Copyright © The International Neuropsychological Society 2015 

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.)

Article purchase

Temporarily unavailable

References

Andersson, J.L., Jenkinson, M., & Smith, S. (2007). Non-linear registration, aka Spatial normalisation FMRIB technical report TR07JA2. Oxford: FMRIB Analysis Group of the University of Oxford.Google Scholar
Andropoulos, D.B., Hunter, J.V., Nelson, D.P., Stayer, S.A., Stark, A.R., McKenzie, E.D., … Fraser, C.D. Jr. (2010). Brain immaturity is associated with brain injury before and after neonatal cardiac surgery with high-flow bypass and cerebral oxygenation monitoring. The Journal of Thoracic and Cardiovascular Surgery, 139(3), 543–556. doi: 10.1016/j.jtcvs.2009.08.022 CrossRefGoogle ScholarPubMed
Ashtari, M., Kumra, S., Bhaskar, S.L., Clarke, T., Thaden, E., Cervellione, K.L., … Ardekani, B.A. (2005). Attention-deficit/hyperactivity disorder: A preliminary diffusion tensor imaging study. Biological Psychiatry, 57(5), 448–455. doi: 10.1016/j.biopsych.2004.11.047 CrossRefGoogle ScholarPubMed
Bechtel, N., Kobel, M., Penner, I.K., Klarhofer, M., Scheffler, K., Opwis, K., & Weber, P. (2009). Decreased fractional anisotropy in the middle cerebellar peduncle in children with epilepsy and/or attention deficit/hyperactivity disorder: A preliminary study. Epilepsy and Behavior, 15(3), 294–298. doi: 10.1016/j.yebeh.2009.04.005 CrossRefGoogle ScholarPubMed
Behrens, T.E., Johansen-Berg, H., Woolrich, M.W., Smith, S.M., Wheeler-Kingshott, C.A., Boulby, P.A., … Matthews, P.M. (2003). Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nature Neuroscience, 6(7), 750–757. doi: 10.1038/nn1075 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), 1077–1088. doi: 10.1002/mrm.10609 CrossRefGoogle ScholarPubMed
Bellinger, D.C., Wypij, D., Rivkin, M.J., DeMaso, D.R., Robertson, R.L. Jr., Dunbar-Masterson, C., … Newburger, J.W. (2011). Adolescents with d-transposition of the great arteries corrected with the arterial switch procedure: Neuropsychological assessment and structural brain imaging. Circulation, 124(12), 1361–1369. doi: 10.1161/circulationaha.111.026963 CrossRefGoogle ScholarPubMed
Bellinger, D.C., Wypij, D., duPlessis, A.J., Rappaport, L.A., Jonas, R.A., Wernovsky, G., & Newburger, J.W. (2003). Neurodevelopmental status at eight years in children with dextro-transposition of the great arteries: The Boston Circulatory Arrest Trial. The Journal of Thoracic and Cardiovascular Surgery, 126(5), 1385–1396. doi: 10.1016/s0022 CrossRefGoogle ScholarPubMed
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289–300. doi: 10.2307/2346101 CrossRefGoogle Scholar
Botto, L.D., Correa, A., & Erickson, J.D. (2001). Racial and temporal variations in the prevalence of heart defects. Pediatrics, 107(3), e32. doi: 10.1542/peds.107.3.e32 CrossRefGoogle ScholarPubMed
Christidi, F., Zalonis, I., Kyriazi, S., Rentzos, M., Karavasilis, E., Wilde, E.A., & Evdokimidis, I. (2014). Uncinate fasciculus microstructure and verbal episodic memory in amyotrophic lateral sclerosis: A diffusion tensor imaging and neuropsychological study. Brain Imaging and Behavior, 8, 497–505. doi: 10.1007/s11682-013-9271-y CrossRefGoogle ScholarPubMed
Correa, A., Cragan, J.D., Kucik, J.E., Alverson, C.J., Gilboa, S.M., Balakrishnan, R., … Chitra, J. (2007). Reporting birth defects surveillance data 1968–2003. Birth Defects Research. Part A, Clinical and Molecular Teratology, 79(2), 65–186. doi: 10.1002/bdra.20350 Google ScholarPubMed
Davenport, N.D., Karatekin, C., White, T., & Lim, K.O. (2010). Differential fractional anisotropy abnormalities in adolescents with ADHD or schizophrenia. Psychiatry Research, 181(3), 193–198. doi: 10.1016/j.pscychresns.2009.10.012 CrossRefGoogle ScholarPubMed
Delis, D., Kaplan, E., Kramer, J., & Ober, B. (2000). California Verbal Learning Test-II. San Antonio, TX: The Psychological Corporation.Google Scholar
Dennis, M., Francis, D.J., Cirino, P.T., Schachar, R., Barnes, M.A., & Fletcher, J.M. (2009). Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society, 15(3), 331–343. doi: 10.1017/s1355617709090481 CrossRefGoogle Scholar
Diehl, B., Busch, R.M., Duncan, J.S., Piao, Z., Tkach, J., & Lüders, 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.x CrossRefGoogle ScholarPubMed
Dimitropoulos, A., McQuillen, P.S., Sethi, V., Moosa, A., Chau, V., Xu, D., … Miller, S.P. (2013). Brain injury and development in newborns with critical congenital heart disease. Neurology, 81(3), 241–248. doi: 10.1212/WNL.0b013e31829bfdcf CrossRefGoogle ScholarPubMed
Ellmore, T.M., Li, H., Xue, Z., Wong, S.T., & Frye, R.E. (2013). Tract-based spatial statistics reveal altered relationship between non-verbal reasoning abilities and white matter integrity in autism spectrum disorder. Journal of the International Neuropsychological Society, 19(6), 723–728. doi: 10.1017/s1355617713000325 CrossRefGoogle ScholarPubMed
Fujie, S., Namiki, C., Nishi, H., Yamada, M., Miyata, J., Sakata, D., … Murai, T. (2008). The role of the uncinate fasciculus in memory and emotional recognition in amnestic mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 26(5), 432–439. doi: 10.1159/000165381 CrossRefGoogle ScholarPubMed
Gaynor, J.W., Gerdes, M., Nord, A.S., Bernbaum, J., Zackai, E., Wernovsky, G., … Jarvik, G.P. (2010). Is cardiac diagnosis a predictor of neurodevelopmental outcome after cardiac surgery in infancy? The Journal of Thoracic and Cardiovascular Surgery, 140(6), 1230–1237. doi: 10.1016/j.jtcvs.2010.07.069 CrossRefGoogle ScholarPubMed
Genova, H.M., DeLuca, J., Chiaravalloti, N., & Wylie, G. (2013). The relationship between executive functioning, processing speed, and white matter integrity in multiple sclerosis. Journal of Clinical and Expimental Neuropsychology, 35(6), 631–641. doi: 10.1080/13803395.2013.806649 CrossRefGoogle ScholarPubMed
Grech, V., & Savona-Ventura, C. (1999). Declining mortality from congenital heart disease related to innovations in diagnosis and treatment: A population-based study. Cardiology in the Young, 9(1), 78–80.CrossRefGoogle ScholarPubMed
Hoeft, F., Barnea-Goraly, N., Haas, B.W., Golarai, G., Ng, D., Mills, D., … Reiss, A.L. (2007). More is not always better: Increased fractional anisotropy of superior longitudinal fasciculus associated with poor visuospatial abilities in Williams syndrome. The Journal of Neuroscience, 27(44), 11960–11965. doi: 10.1523/jneurosci.3591-07.2007 CrossRefGoogle Scholar
Hoffman, J.I., Kaplan, S., & Liberthson, R.R. (2004). Prevalence of congenital heart disease. American Heart Journal, 147(3), 425–439. doi: 10.1016/j.ahj.2003.05.003 CrossRefGoogle ScholarPubMed
Hövels-Gürich, H.H., Konrad, K., Skorzenski, D., Herpertz-Dahlmann, B., Messmer, B.J., & Seghaye, M.-C. (2007). Attentional Dysfunction in Children After Corrective Cardiac Surgery in Infancy. The Annals of Thoracic Surgery, 83(4), 1425–1430. doi: http://dx.doi.org/10.1016/j.athoracsur.2006.10.069 CrossRefGoogle ScholarPubMed
Jenkinson, M., Beckmann, C.F., Behrens, T.E., Woolrich, M.W., & Smith, S.M. (2012). FSL. Neuroimage, 62(2), 782–790. doi: 10.1016/j.neuroimage.2011.09.015 CrossRefGoogle ScholarPubMed
Jones, D.K. (2008). Studying connections in the living human brain with diffusion MRI. Cortex, 44(8), 936–952. doi: http://dx.doi.org/10.1016/j.cortex.2008.05.002 CrossRefGoogle ScholarPubMed
Jones, D.K., Symms, M.R., Cercignani, M., & Howard, R.J. (2005). The effect of filter size on VBM analyses of DT-MRI data. Neuroimage, 26(2), 546–554. doi: 10.1016/j.neuroimage.2005.02.013 CrossRefGoogle ScholarPubMed
Kobel, M., Bechtel, N., Specht, K., Klarhofer, M., Weber, P., Scheffler, K., … Penner, I.K. (2010). Structural and functional imaging approaches in attention deficit/hyperactivity disorder: Does the temporal lobe play a key role? Psychiatry Research, 183(3), 230–236. doi: 10.1016/j.pscychresns.2010.03.010 CrossRefGoogle ScholarPubMed
Lande, M.B., Gerson, A.C., Hooper, S.R., Cox, C., Matheson, M., Mendley, S.R., … Flynn, J.T. (2011). Casual blood pressure and neurocognitive function in children with chronic kidney disease: A report of the children with chronic kidney disease cohort study. Clinical Journal of the American Society of Nephrology, 6(8), 1831–1837. doi: 10.2215/cjn.00810111 CrossRefGoogle ScholarPubMed
Li, Y., Gonzalez, P., & Zhang, L. (2012). Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: Mechanisms and possible interventions. Progress in Neurobiology, 98(2), 145–165. doi: 10.1016/j.pneurobio.2012.05.010 CrossRefGoogle ScholarPubMed
Mabbott, D.J., Rovet, J., Noseworthy, M.D., Smith, M.L., & Rockel, C. (2009). The relations between white matter and declarative memory in older children and adolescents. Brain Research, 1294, 80–90. doi: 10.1016/j.brainres.2009.07.046 CrossRefGoogle ScholarPubMed
Mahle, W.T., Clancy, R.R., Moss, E.M., Gerdes, M., Jobes, D.R., & Wernovsky, G. (2000). Neurodevelopmental outcome and lifestyle assessment in school-aged and adolescent children with hypoplastic left heart syndrome. Pediatrics, 105(5), 1082–1089.CrossRefGoogle ScholarPubMed
Mahle, W.T., Tavani, F., Zimmerman, R.A., Nicolson, S.C., Galli, K.K., Gaynor, J.W., … Kurth, C.D. (2002). An MRI study of neurological injury before and after congenital heart surgery. Circulation, 106(12 Suppl 1), I109–I114.CrossRefGoogle ScholarPubMed
Matos, S.M., Sarmento, S., Moreira, S., Pereira, M.M., Quintas, J., Peixoto, B., … Areias, M.E. (2013). Impact of fetal development on neurocognitive performance of adolescents with cyanotic and acyanotic congenital heart disease. Congenital Heart Disease. doi: 10.1111/chd.12152 Google ScholarPubMed
Mellion, K., Uzark, K., Cassedy, A., Drotar, D., Wernovsky, G., Newburger, J.W., … Marino, B.S. (2014). Health-related quality of life outcomes in children and adolescents with congenital heart disease. The Journal of Pediatrics, 164, 781–788.CrossRefGoogle ScholarPubMed
Miatton, M., De Wolf, D., François, K., Thiery, E., & Vingerhoets, G. (2008). Do parental ratings on cognition reflect neuropsychological outcome in congenital heart disease? Acta Paediatricia, 97(1), 41–45. doi: 10.1111/j.1651-2227.2007.00530.x CrossRefGoogle ScholarPubMed
Miatton, M., De Wolf, D., François, K., Thiery, E., & Vingerhoets, G. (2007). Intellectual, neuropsychological, and behavioral functioning in children with tetralogy of Fallot. The Journal of Thoracic and Cardiovascular Surgery, 133(2), 449–455. doi: http://dx.doi.org/10.1016/j.jtcvs.2006.10.006 CrossRefGoogle ScholarPubMed
Miller, S.P., McQuillen, P.S., Hamrick, S., Xu, D., Glidden, D.V., Charlton, N., … Vigneron, D.B. (2007). Abnormal brain development in newborns with congenital heart disease. New England Journal of Medicine, 357(19), 1928–1938. doi:10.1056/NEJMoa067393 CrossRefGoogle ScholarPubMed
Miller, G.A. (1956). The magical number seven plus or minus two: Some limits on our capacity for processing information. Psychology Review, 63(2), 81–97.CrossRefGoogle ScholarPubMed
Mussatto, K.A., Hoffmann, R.G., Hoffman, G.M., Tweddell, J.S., Bear, L., Cao, Y., & Brosig, C. (2014). Risk and prevalence of developmental delay in young children with congenital heart disease. Pediatrics, 133(3), e570–e577. doi: 10.1542/peds.2013-2309 CrossRefGoogle ScholarPubMed
Nestor, P.G., Kubicki, M., Gurrera, R.J., Niznikiewicz, M., Frumin, M., McCarley, R.W., & Shenton, M.E. (2004). Neuropsychological correlates of diffusion tensor imaging in schizophrenia. Neuropsychology, 18(4), 629–637. doi: 10.1037/0894-4105.18.4.629 CrossRefGoogle ScholarPubMed
Neufeld, R.E., Clark, B.G., Robertson, C.M.T., Moddemann, D.M., Dinu, I.A., Joffe, A.R., … Rebeyka, I.M. (2008). Five-year neurocognitive and health outcomes after the neonatal arterial switch operation. The Journal of Thoracic and Cardiovascular Surgery, 136(6), 1413–1421.e1412. doi: http://dx.doi.org/10.1016/j.jtcvs.2008.05.011 CrossRefGoogle ScholarPubMed
Nichols, T.E., & Holmes, A.P. (2002). Nonparametric permutation tests for functional neuroimaging: A primer with examples. Human Brain Mapping, 15(1), 1–25.CrossRefGoogle ScholarPubMed
Niogi, S.N., Mukherjee, P., Ghajar, J., Johnson, C.E., Kolster, R., Lee, H., … McCandliss, B.D. (2008). Structural dissociation of attentional control and memory in adults with and without mild traumatic brain injury. Brain, 131(Pt 12), 3209–3221. doi: 10.1093/brain/awn247 CrossRefGoogle ScholarPubMed
Papagno, C., Miracapillo, C., Casarotti, A., Romero Lauro, L.J., Castellano, A., Falini, A., … Bello, L. (2011). What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain, 134(Pt 2), 405–414. doi: 10.1093/brain/awq283 CrossRefGoogle ScholarPubMed
Partridge, S.C., Vigneron, D.B., Charlton, N.N., Berman, J.I., Henry, R.G., Mukherjee, P., … Miller, S.P. (2006). Pyramidal tract maturation after brain injury in newborns with heart disease. Annals of Neurology, 59(4), 640–651. doi: 10.1002/ana.20772 CrossRefGoogle ScholarPubMed
Quartermain, M.D., Ittenbach, R.F., Flynn, T.B., Gaynor, J.W., Zhang, X., Licht, D.J., … Wernovsky, G. (2010). Neuropsychological status in children after repair of acyanotic congenital heart disease. Pediatrics, 126(2), e351–e359. doi: 10.1542/peds.2009-2822 CrossRefGoogle ScholarPubMed
Reller, M.D., Strickland, M.J., Riehle-Colarusso, T., Mahle, W.T., & Correa, A. (2008). Prevalence of congenital heart defects in metropolitan Atlanta, 1998–2005. The Journal of Pediatrics, 153(6), 807–813. doi: http://dx.doi.org/10.1016/j.jpeds.2008.05.059 CrossRefGoogle ScholarPubMed
Rivkin, M.J., Watson, C.G., Scoppettuolo, L.A., Wypij, D., Vajapeyam, S., Bellinger, D.C., … Newburger, J.W. (2013). Adolescents with D-transposition of the great arteries repaired in early infancy demonstrate reduced white matter microstructure associated with clinical risk factors. The Journal of Thoracic and Cardiovascular Surgery, 146(3), 543–549 e541. doi: 10.1016/j.jtcvs.2012.12.006 CrossRefGoogle ScholarPubMed
Rollins, C.K., Watson, C.G., Asaro, L.A., Wypij, D., Vajapeyam, S., Bellinger, D.C., … Rivkin, M.J. (2014). White matter microstructure and cognition in adolescents with congenital heart disease. The Journal of Pediatrics. doi: 10.1016/j.jpeds.2014.07.028 CrossRefGoogle ScholarPubMed
Sage, C.A., Van Hecke, W., Peeters, R., Sijbers, J., Robberecht, W., Parizel, P., … Sunaert, S. (2009). Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis: Revisited. Human Brain Mapping, 30(11), 3657–3675. doi: 10.1002/hbm.20794 CrossRefGoogle ScholarPubMed
Sananes, R., Manlhiot, C., Kelly, E., Hornberger, L.K., Williams, W.G., MacGregor, D., … McCrindle, B.W. (2012). Neurodevelopmental Outcomes After Open Heart Operations Before 3 Months of Age. The Annals of Thoracic Surgery, 93(5), 1577–1583. doi: http://dx.doi.org/10.1016/j.athoracsur.2012.02.011 CrossRefGoogle ScholarPubMed
Santamarina-Perez, P., Freniche, V., Eiroa-Orosa, F.J., Llobet, G., Saez, N., Alegre, J., & Jacas, C. (2011). [The role of depression in cognitive impairment in patients with chronic fatigue syndrome]. Medicina Clinica, 136(6), 239–243. doi: 10.1016/j.medcli.2010.07.022 Google ScholarPubMed
Sarajuuri, A., Jokinen, E., Mildh, L., Tujulin, A.M., Mattila, I., Valanne, L., & Lonnqvist, T. (2012). Neurodevelopmental burden at age 5 years in patients with univentricular heart. Pediatrics, 130(6), e1636–e1646. doi: 10.1542/peds.2012-0486 CrossRefGoogle ScholarPubMed
Schaefer, C., von Rhein, M., Knirsch, W., Huber, R., Natalucci, G., Caflisch, J., … Latal, B. (2013). Neurodevelopmental outcome, psychological adjustment, and quality of life in adolescents with congenital heart disease. Developmental Medine and Child Neurology, 55(12), 1143–1149. doi: 10.1111/dmcn.12242 CrossRefGoogle ScholarPubMed
Schwarz, C.G., Reid, R.I., Gunter, J.L., Senjem, M.L., Przybelski, S.A., Zuk, S.M., … Jack, C.R. Jr. (2014). Improved DTI registration allows voxel-based analysis that outperforms Tract-Based Spatial Statistics. Neuroimage, 94(0), 65–78. doi: http://dx.doi.org/10.1016/j.neuroimage.2014.03.026 CrossRefGoogle ScholarPubMed
Sethi, V., Tabbutt, S., Dimitropoulos, A., Harris, K.C., Chau, V., Poskitt, K., … McQuillen, P.S. (2013). Single-ventricle anatomy predicts delayed microstructural brain development. Pediatric Research, 73(5), 661–667. doi: 10.1038/pr.2013.29 CrossRefGoogle ScholarPubMed
Shiffrin, R.M., & Nosofsky, R.M. (1994). Seven plus or minus two: A commentary on capacity limitations. Psychology Review, 101(2), 357–361.CrossRefGoogle ScholarPubMed
Shillingford, A.J., Glanzman, M.M., Ittenbach, R.F., Clancy, R.R., Gaynor, J.W., & Wernovsky, G. (2008). Inattention, hyperactivity, and school performance in a population of school-age children with complex congenital heart disease. Pediatrics, 121(4), e759–e767. doi: 10.1542/peds.2007-1066 CrossRefGoogle Scholar
Smith, S.M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143–155. doi: 10.1002/hbm.10062 CrossRefGoogle ScholarPubMed
Smith, S.M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T.E., Mackay, C.E., … Behrens, T.E. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage, 31(4), 1487–1505. doi: 10.1016/j.neuroimage.2006.02.024 CrossRefGoogle ScholarPubMed
Smith, S.M., & Nichols, T.E. (2009). Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage, 44(1), 83–98. doi: 10.1016/j.neuroimage.2008.03.061 CrossRefGoogle ScholarPubMed
Smith, K.M., King, T.Z., Jayakar, R., & Morris, R.D. (2014). Reading skill in adult survivors of childhood brain tumor: A theory-based neurocognitive model. Neuropsychology, 28(3), 448–458. doi: 10.1037/neu0000056 CrossRefGoogle 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(Suppl. 1), S208–S219. doi: 10.1016/j.neuroimage.2004.07.051 CrossRefGoogle ScholarPubMed
Tyagi, M., Austin, K., Stygall, J., Deanfield, J., Cullen, S., & Newman, S.P. (2014). What do we know about cognitive functioning in adult congenital heart disease? Cardiology in the Young, 24(1), 13–19. doi: 10.1017/s1047951113000747 CrossRefGoogle ScholarPubMed
Voets, N.L., Adcock, J.E., Stacey, R., Hart, Y., Carpenter, K., Matthews, P.M., & Beckmann, C.F. (2009). Functional and structural changes in the memory network associated with left temporal lobe epilepsy. Human Brain Mapping, 30(12), 4070–4081. doi: 10.1002/hbm.20830 CrossRefGoogle ScholarPubMed
von Der Heide, R.J., Skipper, L.M., Klobusicky, E., & Olson, I.R. (2013). Dissecting the uncinate fasciculus: Disorders, controversies and a hypothesis. Brain, 136(Pt 6), 1692–1707. doi: 10.1093/brain/awt094 CrossRefGoogle ScholarPubMed
von Rhein, M., Buchmann, A., Hagmann, C., Huber, R., Klaver, P., Knirsch, W., & Latal, B. (2014). Brain volumes predict neurodevelopment in adolescents after surgery for congenital heart disease. Brain, 137(Pt 1), 268–276. doi: 10.1093/brain/awt322 CrossRefGoogle ScholarPubMed
von Rhein, M., Scheer, I., Loenneker, T., Huber, R., Knirsch, W., & Latal, B. (2011). Structural brain lesions in adolescents with congenital heart disease. The Journal of Pediatrics, 158(6), 984–989. doi: http://dx.doi.org/10.1016/j.jpeds.2010.11.040 CrossRefGoogle ScholarPubMed
Wechsler, D. (2009). Wechsler Abbreviated Scale of Intelligence. New York: The Psychological Corporation.Google Scholar
Wechsler, D. (1997). Wechsler Adult Intelligence Scale-III. New York: The Psychological Corporation.Google Scholar
White, D.A., Moinuddin, A., McKinstry, R.C., Noetzel, M., Armstrong, M., & DeBaun, M. (2006). Cognitive screening for silent cerebral infarction in children with sickle cell disease. Journal of Pediatric Hematology/Oncology, 28(3), 166–169. doi: 10.1097/01.mph.0000203720.45448.ea CrossRefGoogle ScholarPubMed
Woolrich, M.W., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T., … Smith, S.M. (2009). Bayesian analysis of neuroimaging data in FSL. Neuroimage, 45(1 Suppl), S173–S186. doi: 10.1016/j.neuroimage.2008.10.055 CrossRefGoogle ScholarPubMed
Yang, Q., Chen, H., Correa, A., Devine, O., Mathews, T.J., & Honein, M.A. (2006). Racial differences in infant mortality attributable to birth defects in the United States, 1989–2002. Birth Defects Research Part A: Clinical and Molecular Teratology, 76(10), 706–713. doi: 10.1002/bdra.20308 CrossRefGoogle ScholarPubMed