Functional significance of atypical cortical organization in spina bifida myelomeningocele: Relations of cortical thickness and gyrification with IQ and fine motor dexterity

Cerebral Cortex

Volumn 23, Issue 10, 2013, Pages 2357-2369

  Treble, Amery ^a   Juranek, Jenifer ^b   Stuebing, Karla K ^a   Dennis, Maureen ^c   Fletcher, Jack M ^a  

^a UNIVERSITY OF HOUSTON   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Atypical cortical organization; Cortical thickness; Gyrification; Neurobehavioral function; Spina bifida

Indexed keywords

ADOLESCENT; ANTERIOR CINGULATE; ARNOLD CHIARI MALFORMATION; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN REGION; CINGULATE GYRUS; COGNITION; CONTROLLED STUDY; CORPUS CALLOSUM; CORTICAL THICKNESS (BRAIN); FEMALE; FINE MOTOR DEXTERITY; FRONTAL LOBE; FUNCTIONAL ASSESSMENT; FUSIFORM GYRUS; HANDEDNESS; HUMAN; HYDROCEPHALUS; INFERIOR FRONTAL GYRUS; INTELLIGENCE QUOTIENT; MAJOR CLINICAL STUDY; MALE; MENINGOMYELOCELE; MIDDLE FRONTAL GYRUS; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL LOBE; PARIETAL LOBE; POSTERIOR CINGULATE; PRIORITY JOURNAL; SEIZURE; SOCIAL STATUS; SPINA BIFIDA MYELOMENINGOCELE; SPINAL DYSRAPHISM; SUPERIOR TEMPORAL SULCUS; TEMPORAL LOBE; WHITE MATTER INJURY;

EID: 84887923492     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs226     Document Type: Article

References (87)

1. Armstrong E, Schleicher A, Omran H., Curtis M, Zilles K. 1995. The ontogeny of human gyrification. Cereb Cortex. 5: 56-63.
2. Awate SP, Win L, Yushkevich P., Schultz RT, Gee JC. 2008. 3D cerebral cortical morphometry in autism: Increased folding in children and adolescents in frontal, parietal, and temporal lobes. Med Image Comput Comput Assist Interv. 11: 559-567.
3. Barkovich J. 2005. Pediatric neuroimaging. Philadelphia (PA): Lippin-cott, Williams & Wilkins.
4. Batty MJ, Liddle EB, Pitiot A, Toro R., Groom MJ, Scerif G, Liotti M, Liddle P.F., Paus T., Hollis C. 2010. Cortical gray matter in attention-deficit/hyperactivity disorder: a structural magnetic resonance imaging study. J Am Acad Child Adolesc Psychiatry. 49: 229-238.
5. Bearden CE, van Erp TG, Dutton RA, Lee AD, Simon TJ, Cannon T.D., Emanuel BS, McDonald-McGinn D, Zackai EH, Thompson PM. 2009. Alterations in midline cortical thickness and gyrification patterns mapped in children with 22q11.2 deletions. Cereb Cortex. 19: 115-126.
6. Bearden CE, van Erp TG, Dutton RA, Tran H, Zimmermann L, Sun D., Geaga JA, Simon TJ, Glahn DC, Cannon TD et al. 2007. Mapping cortical thickness in children with 22q11.2 deletions. Cereb Cortex. 17: 1889-1898.
7. Casanova MF, Araque J, Giedd J., Rumsey JM. 2004. Reduced brain size and gyrification in the brains of dyslexic patients. J Child Neurol. 19: 275-281.
8. Chklovskii DB, Mel BW, Svoboda K. 2004. Cortical rewiring and information storage. Nature. 431: 782-788.
9. Dale AM, Fischl B, Sereno MI. 1999. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage. 9: 179-194.
10. Dale AM, Sereno MI. 1993. Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cognitive Neurosci. 5: 162-176.
11. Del Bigio MR. 2004. Cellular damage and prevention in childhood hydrocephalus. Brain Pathol. 14: 317-324.
12. Del Bigio MR. 2010. Neuropathology and structural changes in hydrocephalus. Dev Disabil Res Rev. 16: 16-22.
13. Dennis M. 2009. The Goldilocks dilemma in neurodevelopmental disorders: A functional brain that is not too big, not too small, but just right. Annual Meeting of the International Neuropsychological Society; 2009 Feb 11-14; Atlanta, GA. J Int Neuropsychol Soc. 15 (SUPPL. 1): 1-249.
14. Desikan RS, Segonne F, Fischl B., Quinn BT, Dickerson BC, Blacker D, Buckner R.L., Dale AM, Maguire RP, Hyman BT et al. 2006. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 31: 968-980.
15. Eliez S, Schmitt JE, White C.D., Reiss AL. 2000. Children and adolescents with velocardiofacial syndrome: A volumetric MRI study. Am J Psychiatr. 157: 409-415.
16. Fischl B, Dale AM. 2000. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA. 97: 11050-11055.
17. Fletcher JM, Copeland K, Frederick J.A., Blaser SE, Kramer LA, Northrup H, Hannay HJ, Brandt M.E., Francis DJ, Villarreal G et al. 2005. Spinal lesion level in spina bifida: A source of neural and cognitive heterogeneity. J Neurosurg. 102: 268-279.
18. Gaser C, Luders E, Thompson P.M., Lee AD, Dutton RA, Geaga JA, Hayashi K.M., Bellugi U., Galaburda AM, Korenberg JR et al. 2006. Increased local gyrification mapped in Williams syndrome. Neuroimage. 33: 46-54.
19. Giedd JN. 2004. Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci. 1021: 77-85.
20. Giedd JN, Blumenthal J, Jeffries N.O., Castellanos FX, Liu H, Zijdenbos A, Paus T., Evans AC, Rapoport JL. 1999. Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci. 2: 861-863.
21. Giza CC, Prins ML. 2006) Is being plastic fantastic? Mechanisms of altered plasticity after developmental traumatic brain injury. Dev Neurosci. 28: 364-379.
22. Gogtay N, Giedd JN, Lusk L, Hayashi K.M., Greenstein D., Vaituzis AC, Nugent TF, 3rd, Herman DH, Clasen LS, Toga AW et al. 2004. Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA. 101: 8174-8179.
23. Goldman-Rakic PS. 1980. Morphological consequences of prenatal injury to the primate brain. Prog Brain Res. 53: 1-19.
24. Hale PM, McAllister JP, 2nd, Katz SD, Wright LC, Lovely TJ, Miller DW, Wolfson BJ, Salotto AG, Shroff DV. 1992. Improvement of cortical morphology in infantile hydrocephalic animals after ven-triculoperitoneal shunt placement. Neurosurgery. 31: 1085-1096.
25. Hannay HJ, Dennis M, Kramer L., Blaser S, Fletcher JM. 2009. Partial agenesis of the corpus callosum in spina bifida meningomyelocele and potential compensatory mechanisms. J Clin Exp Neuropsychol. 31: 180-194.
26. Hartberg CB, Lawyer G, Nyman H., Jonsson EG, Haukvik UK, Saetre P, Bjerkan P.S., Andreassen OA, Hall H, Agartz I. 2010. Investigating relationships between cortical thickness and cognitive performance in patients with schizophrenia and healthy adults. Psychiatr Res. 182: 123-133.
27. Hasan KM, Eluvathingal TJ, Kramer L.A., Ewing-Cobbs L, Dennis M, Fletcher JM. 2008. White matter microstructural abnormalities in children with spina bifida myelomeningocele and hydrocephalus: A diffusion tensor tractography study of the association pathways. J Magn Reson Imaging. 27: 700-709.
28. Hasan KM, Sankar A, Halphen C., Kramer LA, Ewing-Cobbs L, Dennis M, Fletcher JM. 2008. Quantitative diffusion tensor imaging and intellectual outcomes in spina bifida: Laboratory investigation. J Neurosurg Pediatr. 2: 75-82.
29. Hollingshead AB. 1975. Four factor index of social status. New Haven (CT): Yale University.
30. Huttenlocher PR, Dabholkar AS. 1997. Regional differences in synap-togenesis in human cerebral cortex. J Comp Neurol. 387: 167-178.
31. Hyde KL, Lerch JP, Zatorre R.J., Griffiths TD, Evans AC, Peretz I. 2007. Cortical thickness in congenital amusia: When less is better than more. J Neurosci. 27: 13028-13032.
32. Hyde KL, Samson F, Evans A.C., Mottron L. 2010. Neuroanatomical differences in brain areas implicated in perceptual and other core features of autism revealed by cortical thickness analysis and voxel-based morphometry. Hum Brain Mapp. 31: 556-566.
33. Im K, Lee JM, Yoon U, Shin Y.W., Hong SB, Kim IY, Kwon JS, Kim SI. 2006. Fractal dimension in human cortical surface: Multiple regression analysis with cortical thickness, sulcal depth, and folding area. Hum Brain Mapp. 27: 994-1003.
34. Isaacson RL. 1975. The myth of recovery from early brain damage. In: Ellis NR, editor. Aberrant development in infancy: Human and animal studies. Hillsdale (NJ): Lawrence Erlbaum Associates.
35. Jiao Y, Chen R, Ke X., Chu K, Lu Z, Herskovits EH. 2010. Predictive models of autism spectrum disorder based on brain regional cortical thickness. Neuroimage. 50: 589-599.
36. Juranek J, Fletcher JM, Hasan K.M., Breier JI, Cirino PT, Pazo-Alvarez P, Diaz JD, Ewing-Cobbs L, Dennis M., Papanicolaou AC. 2008. Neocortical reorganization in spina bifida. Neuroimage. 40: 1516-1522.
37. Juranek J, Salman MS. 2010. Anomalous development of brain structure and function in spina bifida myelomeningocele. Dev Disabil Res Rev. 16: 23-30.
38. Karama S, Ad-Dab'bagh Y, Haier RJ, Deary IJ, Lyttelton OC, Lepage C, Evans AC, Group TBDC. 2009. Positive association between cognitive ability and cortical thickness in a representative US sample of healthy 6 to 18 year-olds. Intelligence. 37: 145-155.
39. Kates WR, Folley BS, Lanham D.C., Capone GT, Kaufmann WE. 2002. Cerebral growth in Fragile X syndrome: review and comparison with Down syndrome. Microsc Res Tech. 57: 159-167.
40. Kesler SR, Vohr B, Schneider K.C., Katz KH, Makuch RW, Reiss AL, Ment LR. 2006. Increased temporal lobe gyrification in preterm children. Neuropsychologia. 44: 445-453.
41. Kivitie-Kallio S., Autti T, Salonen O., Norio R. 1998. MRI of the brain in the Cohen syndrome: a relatively large corpus callosum in patients with mental retardation and microcephaly. Neuropediatrics. 29: 298-301.
42. Kriebel RM, McAllister JP, 2nd. 2000. Pathology of the hippocampus in experimental feline infantile hydrocephalus. Neurol Res. 22: 29-36.
43. Kriebel RM, Shah AB, McAllister J.P., 2nd. 1993. The microstructure of cortical neuropil before and after decompression in experimental infantile hydrocephalus. Exp Neurol. 119: 89-98.
44. Lafayette Instruments. 1999. Purdue pegboard model #32020 instructions and normative data. Lafayette (IN): Lafayette Instruments.
45. Lin JJ, Salamon N, Lee A.D., Dutton RA, Geaga JA, Hayashi KM, Luders E, Toga A.W., Engel J., Jr, Thompson PM. 2007. Reduced neocortical thickness and complexity mapped in mesial temporal lobe epilepsy with hippocampal sclerosis. Cereb Cortex. 17: 2007-2018.
46. Magnotta VA, Andreasen NC, Schultz S.K., Harris G., Cizadlo T, Heckel D, Nopoulos P., Flaum M. 1999. Quantitative in vivo measurement of gyrification in the human brain: Changes associated with aging. Cereb Cortex. 9: 151-160.
47. Makris N, Biederman J, Valera E.M., Bush G., Kaiser J, Kennedy DN, Caviness V.S., Faraone SV, Seidman LJ. 2007. Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. Cereb Cortex. 17: 1364-1375.
48. Mangin JF, Jouvent E, Cachia A. 2010. In-vivo measurement of cortical morphology: Means and meanings. Curr Opin Neurol. 23: 359-367.
49. McIntosh AM, Moorhead TW, McKirdy J, Hall J., Sussmann JE, Stanfield AC, Harris JM, Johnstone E.C., Lawrie SM. 2009. Prefrontal gyral folding and its cognitive correlates in bipolar disorder and schizophrenia. Acta Psychiatr Scand. 119: 192-198.
50. Mostofsky SH, Burgess MP, Gidley Larson JC. 2007. Increased motor cortex white matter volume predicts motor impairment in autism. Brain. 130: 2117-2122.
51. Mueller SG, Laxer KD, Barakos J, Cheong I., Garcia P, Weiner MW. 2009. Widespread neocortical abnormalities in temporal lobe epilepsy with and without mesial sclerosis. Neuroimage. 46: 353-359.
52. Nagy Z, Lagercrantz H, Hutton C. 2010. Effects of preterm birth on cortical thickness measured in adolescence. Cereb Cortex. 21: 300-306.
53. Narr KL, Woods RP, Lin J, Kim J., Phillips OR, Del'homme M, Caplan R, Toga AW, McCracken JT, Levitt JG. 2009. Widespread cortical thinning is a robust anatomical marker for attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry. 48: 1014-1022.
54. Narr KL, Woods RP, Thompson P.M., Szeszko P., Robinson D, Dimtcheva T, Gurbani M, Toga A.W., Bilder RM. 2007. Relationships between IQ and regional cortical gray matter thickness in healthy adults. Cereb Cortex. 17: 2163-2171.
55. Oyegbile T, Hansen R, Magnotta V., O'Leary D, Bell B, Seidenberg M., Hermann BP. 2004. Quantitative measurement of cortical surface features in localization-related temporal lobe epilepsy. Neuropsychology. 18: 729-737.
56. Rae C, Joy P, Harasty J., Kemp A, Kuan S, Christodoulou J., Cowell CT, Coltheart M. 2004) Enlarged temporal lobes in Turner syndrome: An X-chromosome effect? Cereb Cortex. 14: 156-164.
57. Raznahan A, Cutter W, Lalonde F., Robertson D, Daly E, Conway G.S., Skuse DH, Ross J, Lerch JP, Giedd JN et al. 2010. Cortical anatomy in human X monosomy. Neuroimage. 49: 2915-2923.
58. Raznahan A, Shaw P, Lalonde F., Stockman M, Wallace GL, Greenstein D, Clasen L., Gogtay N, Giedd JN. 2011) How does your cortex grow? J Neurosci. 31: 7174-7177.
59. Reddon JR, Gill DM, Gauk S.E., Maerz MD. 1988. Purdue Pegboard: Test-retest estimates. Percept Mot Skill. 66: 503-506.
60. Salman MS, Dennis M, Sharpe JA. 2009. The cerebellar dysplasia of Chiari II malformation as revealed by eye movements. Can J Neurol Sci. 36: 713-724.
61. Schaer M, Cuadra MB, Tamarit L, Lazeyras F., Eliez S, Thiran JP. 2008. A surface-based approach to quantify local cortical gyrification. IEEE Trans Med Imaging. 27: 161-170.
62. Schaer M, Debbane M, Bach Cuadra M, Ottet MC, Glaser B, Thiran J.P., Eliez S. 2009. Deviant trajectories of cortical maturation in 22q11.2 deletion syndrome (22q11DS): A cross-sectional and longitudinal study. Schizophr Res. 115: 182-190.
63. Schneider GE. 1979) Is it really better to have your brain lesion early? A revision of the "Kennard principle". Neuropsychologia. 17: 557-583.
64. Schneider GE, Jhaveri SR. 1974. Neuroanatomical correlations of spared or altered function after brain lesions in the newborn hamster. In: Stein DG, Rosen JJ, Butters N, editors. Plasticity and recovery of function in the central nervous system. New York: Academic Press.
65. Shaw P, Greenstein D, Lerch J., Clasen L, Lenroot R, Gogtay N., Evans A, Rapoport J, Giedd J. 2006. Intellectual ability and cortical development in children and adolescents. Nature. 440: 676-679
66. Shaw P, Kabani NJ, Lerch J.P., Eckstrand K., Lenroot R, Gogtay N, Greenstein D., Clasen L, Evans A, Rapoport JL et al. 2008. Neuro-developmental trajectories of the human cerebral cortex. J Neurosci. 28: 3586-3594.
67. Simos PG, Papanicolaou AC, Castillo E.M., Juranek J., Cirino PT, Rezaie R, Fletcher JM. 2011. Brain mechanisms for reading and language processing in spina bifida meningomyelocele: A combined magnetic source- and structural magnetic resonance imaging study. Neuropsychology. 25: 590-601.
68. Sowell ER, Mattson SN, Kan E, Thompson P.M., Riley EP, Toga AW. 2008. Abnormal cortical thickness and brain-behavior correlation patterns in individuals with heavy prenatal alcohol exposure. Cereb Cortex. 18: 136-144.
69. Sowell ER, Peterson BS, Thompson P.M., Welcome SE, Henkenius AL, Toga AW. 2003. Mapping cortical change across the human life span. Nat Neurosci. 6: 309-315.
70. Sowell ER, Thompson PM, Leonard C.M., Welcome SE, Kan E, Toga AW. 2004. Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci. 24: 8223-8231.
71. Stanfield AC, Moorhead TW, Harris J.M., Owens DG, Lawrie SM, Johnstone EC. 2008. Increased right prefrontal cortical folding in adolescents at risk of schizophrenia for cognitive reasons. Biol Psychiatry. 63: 80-85.
72. Subramaniam B, Naidu S, Reiss AL. 1997. Neuroanatomy in Rett syndrome: Cerebral cortex and posterior fossa. Neurology. 48: 399-407.
73. Sur M, Rubenstein JL. 2005. Patterning and plasticity of the cerebral cortex. Science. 310: 805-810.
74. Tan WH, Bacino CA, Skinner S.A., Anselm I., Barbieri-Welge R, Bauer-Carlin A, Beaudet A.L., Bichell TJ, Gentile JK, Glaze DG et al. 2011. Angelman syndrome: Mutations influence features in early childhood. Am J Med Genet. 155A: 81-90.
75. Thompson PM, Lee AD, Dutton R.A., Geaga JA, Hayashi KM, Eckert MA, Bellugi U, Galaburda A.M., Korenberg JR, Mills DL et al. 2005. Abnormal cortical complexity and thickness profiles mapped in Williams syndrome. J Neurosci. 25: 4146-4158.
76. Thorndike R, Hagen E, Sattler J. 1986. The Stanford-Binet intelligence scale. Itasca (IL): Riverside.
77. Tiffen J. 1968. Purdue Pegboard test. Chicago (IL): Scientific Research Associates.
78. Vachha B, Adams RC, Rollins NK. 2006. Limbic tract anomalies in pediatric myelomeningocele and Chiari II malformation: anatomic correlations with memory and learning - initial investigation. Radiology. 240: 194-202.
79. Van Essen DC. 1997. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature. 385: 313-318.
80. Voets NL, Bernhardt BC, Kim H, Yoon U., Bernasconi N. 2011. Increased temporolimbic cortical folding complexity in temporal lobe epilepsy. Neurology. 76: 138-144.
81. Weis S, Weber G, Neuhold A., Rett A. 1991. Down syndrome: MR quantification of brain structures and comparison with normal control subjects. Am J Neuroradiol. 12: 1207-1211.
82. White T, Andreasen NC, Nopoulos P, Magnotta V. 2003. Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biol Psychiatry. 54: 418-426.
83. White T, Hilgetag CC. 2011. Gyrification and neural connectivity in schizophrenia. Dev Psychopathol. 23: 339-352.
84. White T, Su S, Schmidt M., Kao CY, Sapiro G. 2010. The development of gyrification in childhood and adolescence. Brain Cogn. 72: 36-45.
85. Wobrock T, Gruber O, McIntosh A.M., Kraft S., Klinghardt A, Scherk H, Reith W., Schneider-Axmann T, Lawrie SM, Falkai P et al. 2010. Reduced prefrontal gyrification in obsessive-compulsive disorder. Eur Arch Psychiatry Clin Neurosci. 260: 455-464.
86. Wolosin SM, Richardson ME, Hennessey J.G., Denckla MB, Mostofsky SH. 2009. Abnormal cerebral cortex structure in children with ADHD. Hum Brain Mapp. 30: 175-184.
87. Zhang Y, Zhou Y, Yu C., Lin L, Li C, Jiang T. 2010. Reduced cortical folding in mental retardation. Am J Neuroradiol. 31: 1063-1067. Development