Atypical development of white matter microstructure of the corpus callosum in males with autism: A longitudinal investigation

Molecular Autism

Volumn 6, Issue 1, 2015, Pages

  Travers, Brittany G ^a,b,c   Tromp, Do P M ^b,c   Adluru, Nagesh ^b,c   Lange, Nicholas ^c,d,e   Destiche, Dan ^b,c   Ennis, Chad ^b,c   Nielsen, Jared A ^c,f   Froehlich, Alyson L ^c,g   Prigge, Molly B D ^c,f,h   Fletcher, P Thomas ^c,g,i   Anderson, Jeffrey S ^c,f   Zielinski, Brandon A ^c,f,h   Bigler, Erin D ^c,j   Lainhart, Janet E ^b,c   Alexander, Andrew L ^b,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e MCLEAN HOSPITAL   (United States)

^f UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF UTAH   (United States)

^h PRIMARY CHILDREN'S MEDICAL CENTER   (United States)

ⁱ Department of Electrical and Computer Engineering   (United States)

^j BRIGHAM YOUNG UNIVERSITY   (United States)

more..

Author keywords

Adolescence; Adulthood; Brain development; Childhood; Developmental disorders; Diffusion tensor imaging

Indexed keywords

ADOLESCENT; ADULT; AGE DISTRIBUTION; ARTICLE; AUTISM; BRAIN MATURATION; BRAIN RADIOGRAPHY; CHILD; COHORT ANALYSIS; CONNECTOME; CONTROLLED STUDY; CORPUS CALLOSUM; CROSS-SECTIONAL STUDY; DEVELOPMENTAL STAGE; DIFFUSION WEIGHTED IMAGING; ECHO PLANAR IMAGING; FRACTIONAL ANISOTROPY; HUMAN; INTELLIGENCE TEST; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SIGNAL NOISE RATIO; WHITE MATTER;

EID: 84928710754     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/s13229-015-0001-8     Document Type: Article

References (97)

1. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, Webb SJ. Autism and abnormal development of brain connectivity. J Neurosci Off J Soc Neurosci. 2004;24:9228-31.
2. Just MA, Cherkassky VL, Keller TA, Kana RK, Minshew NJ. Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cereb Cortex. 2007;17:951-61.
3. Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA. Sentence comprehension in autism: thinking in pictures with decreased functional connectivity. Brain J Neurol. 2006;129(Pt 9):2484-93.
4. Kitzbichler MG, Khan S, Ganesan S, Vangel MG, Herbert MR, Hämäläinen MS, et al. Altered development and multifaceted band-specific abnormalities of resting state networks in autism. Biol Psychiatry 2014
5. Pajevic S, Basser PJ, Fields RD. Role of myelin plasticity in oscillations and synchrony of neuronal activity. Neuroscience. 2014;276:135-47.
6. Paul LK, Brown WS, Adolphs R, Tyszka JM, Richards LJ, Mukherjee P, et al. Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat Rev. 2007;8:287-99.
7. Minshew NJ, Goldstein G, Siegel DJ. Neuropsychologic functioning in autism: profile of a complex information processing disorder. J Int Neuropsychol Soc JINS. 1997;3:303-16.
8. Minshew NJ, Sweeney J, Luna B. Autism as a selective disorder of complex information processing and underdevelopment of neocortical systems. Mol Psychiatry. 2002;7 Suppl 2:S14-5.
9. Williams DL, Goldstein G, Minshew NJ. Neuropsychologic functioning in children with autism: further evidence for disordered complex information-processing. Child Neuropsychol J Norm Abnorm Dev Child Adolesc. 2006;12:279-98.
10. Courchesne E, Press GA, Yeung-Courchesne R. Parietal lobe abnormalities detected with MR in patients with infantile autism. AJR American J Roentgenol. 1993;160:387-93.
11. Belmonte M, Egaas B, Townsend J, Courchesne E. NMR intensity of corpus callosum differs with age but not with diagnosis of autism. Neuroreport. 1995;6:1253-6.
12. Egaas B, Courchesne E, Saitoh O. Reduced size of corpus callosum in autism. Arch Neurol. 1995;52:794-801.
13. Piven J, Bailey J, Ranson BJ, Arndt S. An MRI study of the corpus callosum in autism. Am J Psychiatry. 1997;154:1051-6.
14. Hardan AY, Minshew NJ, Keshavan MS. Corpus callosum size in autism. Neurology. 2000;55:1033-6.
15. Prigge MB, Lange N, Bigler ED, Merkley TL, Neeley ES, Abildskov TJ, et al. Corpus callosum area in children and adults with autism. Res Autism Spectr Disord. 2013;7:221-34.
16. Frazier TW, Hardan AY. A meta-analysis of the corpus callosum in autism. Biol Psychiatry. 2009;66:935-41.
17. Di Martino A, Ross K, Uddin LQ, Sklar AB, Castellanos FX, Milham MP. Functional brain correlates of social and nonsocial processes in autism spectrum disorders: an activation likelihood estimation meta-analysis. Biol Psychiatry. 2009;65:63-74.
18. Anderson JS, Druzgal TJ, Froehlich A, DuBray MB, Lange N, Alexander AL, et al. Decreased interhemispheric functional connectivity in autism. Cereb Cortex. 2011;21:1134-46.
19. Dinstein I, Pierce K, Eyler L, Solso S, Malach R, Behrmann M, et al. Disrupted neural synchronization in toddlers with autism. Neuron. 2011;70:1218-25.
20. Lamantia AS, Rakic P. Cytological and quantitative characteristics of four cerebral commissures in the rhesus monkey. J Comp Neurol. 1990;291:520-37.
21. Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J. 1994;66:259-67.
22. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage. 2002;17:1429-36.
23. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage. 2005;26:132-40.
24. Alexander AL, Hurley SA, Samsonov AA, Adluru N, Hosseinbor AP, Mossahebi P, et al. Characterization of cerebral white matter properties using quantitative magnetic resonance imaging stains. Brain Connect. 2011;1:423-46.
25. Travers BG, Adluru N, Ennis C, Tromp DPM, Destiche D, Doran S, et al. Diffusion tensor imaging in autism spectrum disorder: a review. Autism Res Off J Int Soc Autism Res. 2012;5:289-313.
26. Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurother J Am Soc Exp Neurother. 2007;4:316-29.
27. Alexander AL, Lee JE, Lazar M, Boudos R, DuBray MB, Oakes TR, et al. Diffusion tensor imaging of the corpus callosum in autism. NeuroImage. 2007;34:61-73.
28. Ameis SH, Fan J, Rockel C, Voineskos AN, Lobaugh NJ, Soorya L, et al. Impaired structural connectivity of socio-emotional circuits in autism spectrum disorders: a diffusion tensor imaging study. PLoS One. 2011;6:e28044.
29. Jeong JW, Kumar AK, Sundaram SK, Chugani HT, Chugani DC. Sharp curvature of frontal lobe white matter pathways in children with autism spectrum disorders: tract-based morphometry analysis. AJNR American J Neuroradiol. 2011;32:1600-6.
30. Shukla DK, Keehn B, Lincoln AJ, Muller RA. White matter compromise of callosal and subcortical fiber tracts in children with autism spectrum disorder: a diffusion tensor imaging study. J Am Acad Child Adolesc Psychiatry. 2010;49:1269-78.
31. Shukla DK, Keehn B, Smylie DM, Muller RA. Microstructural abnormalities of short-distance white matter tracts in autism spectrum disorder. Neuropsychologia. 2011;49:1378-82.
32. Weinstein M, Ben-Sira L, Levy Y, Zachor DA, Ben Itzhak E, Artzi M, et al. Abnormal white matter integrity in young children with autism. Hum Brain Mapp. 2011;32:534-43.
33. Harsan LA, Poulet P, Guignard B, Steibel J, Parizel N, de Sousa PL, et al. Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging. J Neurosci Res. 2006;83:392-402.
34. Tyszka JM, Readhead C, Bearer EL, Pautler RG, Jacobs RE. Statistical diffusion tensor histology reveals regional dysmyelination effects in the shiverer mouse mutant. NeuroImage. 2006;29:1058-65.
35. Ben Bashat D, Kronfeld-Duenias V, Zachor DA, Ekstein PM, Hendler T, Tarrasch R, et al. Accelerated maturation of white matter in young children with autism: a high b value DWI study. NeuroImage. 2007;37:40-7.
36. Cheng Y, Chou KH, Chen IY, Fan YT, Decety J, Lin CP. Atypical development of white matter microstructure in adolescents with autism spectrum disorders. NeuroImage. 2010;50:873-82.
37. Cheung C, Chua SE, Cheung V, Khong PL, Tai KS, Wong TK, et al. White matter fractional anisotrophy differences and correlates of diagnostic symptoms in autism. J Child Psychol Psychiatry. 2009;50:1102-12.
38. Ashtari M, Cervellione KL, Hasan KM, Wu J, McIlree C, Kester H, et al. White matter development during late adolescence in healthy males: a cross-sectional diffusion tensor imaging study. NeuroImage. 2007;35:501-10.
39. Barnea-Goraly N, Menon V, Eckert M, Tamm L, Bammer R, Karchemskiy A, et al. White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb Cortex. 2005;15:1848-54.
40. Giorgio A, Watkins KE, Douaud G, James AC, James S, De Stefano N, et al. Changes in white matter microstructure during adolescence. NeuroImage. 2008;39:52-61.
41. Giorgio A, Santelli L, Tomassini V, Bosnell R, Smith S, De Stefano N, et al. Age-related changes in grey and white matter structure throughout adulthood. NeuroImage. 2010;51:943-51.
42. Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C. Microstructural maturation of the human brain from childhood to adulthood. NeuroImage. 2008;40:1044-55.
43. Lebel C, Beaulieu C. Longitudinal development of human brain wiring continues from childhood into adulthood. J Neurosci Off J Soc Neurosci. 2011;31:10937-47.
44. Wolff JJ, Gu H, Gerig G, Elison JT, Styner M, Gouttard S, et al. Differences in white matter fiber tract development present from 6 to 24 months in infants with autism. Am J Psychiatry 2012
45. Innocenti GM. Dynamic interactions between the cerebral hemispheres. Exp Brain Res Exp Hirnforsch Expérimentation Cérébrale. 2009;192:417-23.
46. Pietrasanta M, Restani L, Caleo M. The corpus callosum and the visual cortex: plasticity is a game for two. Neural Plast. 2012;2012:838672.
47. Nesselroade JR, Baltes PB. Longitudinal research in the study of behavior and development. Academic Press; 1979
48. Lord C, Rutter M, Le Couteur A. Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24:659-85.
49. Lord C, Risi S, Lambrecht L, Cook EH, Leventhal BL, DiLavore PC, et al. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000;30:205-23.
50. American Psychiatric Association. Diagnostic criteria from DSM-IV-TR. Arlington, VA: American Psychiatric Association; 2000.
51. Jeste SS, Geschwind DH. Disentangling the heterogeneity of autism spectrum disorder through genetic findings. Nat Rev Neurol. 2014;10:74-81.
52. Elliott C. The nature and structure of children's abilities: evidence from the differential ability scales. J Psychoeduc Assess. 1990;8:376-90.
53. Wechsler D. The Wechsler intelligence scale for children. 3rd ed. San Antonio: The Psychological Corporation; 1991.
54. Wechsler D. Wechsler adult iintelligence scale-III (WAIS-III). San Antonio: Psychological Corporation; 1997.
55. Wechsler D. Wechsler abbreviated scale of intelligence. New York: The Psychological Corporation: Harcourt Brace & Company; 1999.
56. Reese TG, Heid O, Weisskoff RM, Wedeen VJ. Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn Reson Med Off J Soc Magn Reson Med Soc Magn Reson Med. 2003;49:177-82.
57. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. FSL. NeuroImage. 2012;62:782-90.
58. Leemans A, Jones DK. The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med Off J Soc Magn Reson Med Soc Magn Reson Med. 2009;61:1336-49.
59. Chang LC, Jones DK, Pierpaoli C. RESTORE: robust estimation of tensors by outlier rejection. Magn Reson Med Off J Soc Magn Reson Med Soc Magn Reson Med. 2005;53:1088-95.
60. Cook PA, Bai Y, Nedjati-Gilanio S, Seunarine KK, Hall MG, Parker GJ, Alexander DC: Camino: open-source diffusion-MRI reconstruction and processing. Volume Seattle, WA; 2006:2759.
61. Walker L, Chang LC, Koay CG, Sharma N, Cohen L, Verma R, et al. Effects of physiological noise in population analysis of diffusion tensor MRI data. NeuroImage. 2011;54:1168-77.
62. Benner T, van der Kouwe AJW, Sorensen AG. Diffusion imaging with prospective motion correction and reacquisition. Magn Reson Med Off J Soc Magn Reson Med Soc Magn Reson Med. 2011;66:154-67.
63. Yendiki A, Koldewyn K, Kakunoori S, Kanwisher N, Fischl B. Spurious group differences due to head motion in a diffusion MRI study. NeuroImage. 2013;88C:79-90.
64. Zhang H, Yushkevich PA, Alexander DC, Gee JC. Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med Image Anal. 2006;10:764-85.
65. Mori S, Wakana S, Nagae-Poetscher L, Van Zijl PC. MRI atlas of human white matter. Amsterdam: Elsevier; 2005.
66. Avants B, Gee JC. Geodesic estimation for large deformation anatomical shape averaging and interpolation. NeuroImage. 2004;23 Suppl 1:S139-50.
67. Faria AV, Hoon A, Stashinko E, Li X, Jiang H, Mashayekh A, et al. Quantitative analysis of brain pathology based on MRI and brain atlases - applications for cerebral palsy. NeuroImage. 2011;54:1854-61.
68. Walker L, Curry M, Nayak A, Lange N, Pierpaoli C. A framework for the analysis of phantom data in multicenter diffusion tensor imaging studies. Hum Brain Mapp 2012
69. Hastie T. Generalized additive models. Boca Raton, FL: Chapman & Hall/CRC; 1999.
70. Wood SN. Stable and efficient multiple smoothing parameter estimation for generalized additive models. J Am Stat Assoc. 2004;99
71. Wood SN. Generalized additive models: an introduction with R. Boca Raton, FL: Chapman & Hall/CRC; 2006 [Texts in Statistical Science].
72. Wood S, Scheipl F. gamm4: generalized additive mixed models using Mgcv and lme4. 2013.
73. Alexander-Bloch AF, Reiss PT, Rapoport J, McAdams H, Giedd JN, Bullmore ET, et al. Abnormal cortical growth in schizophrenia targets normative modules of synchronized development. Biol Psychiatry. 2014;76:438-46.
74. Harezlak J, Ryan LM, Giedd JN, Lange N. Individual and population penalized regression splines for accelerated longitudinal designs. Biometrics. 2005;61:1037-48.
75. Xiao Z, Qiu T, Ke X, Xiao X, Xiao T, Liang F, et al. Autism spectrum disorder as early neurodevelopmental disorder: evidence from the brain imaging abnormalities in 2-3 years old toddlers. J Autism Dev Disord. 2014;44:1633-40.
76. Billeci L, Calderoni S, Tosetti M, Catani M, Muratori F. White matter connectivity in children with autism spectrum disorders: a tract-based spatial statistics study. BMC Neurol. 2012;12:148.
77. Koldewyn K, Yendiki A, Weigelt S, Gweon H, Julian J, Richardson H, et al. Differences in the right inferior longitudinal fasciculus but no general disruption of white matter tracts in children with autism spectrum disorder. Proc Natl Acad Sci U S A. 2014;111:1981-6.
78. Hanaie R, Mohri I, Kagitani-Shimono K, Tachibana M, Matsuzaki J, Watanabe Y, et al. Abnormal corpus callosum connectivity, socio-communicative deficits, and motor deficits in children with autism spectrum disorder: a diffusion tensor imaging study. J Autism Dev Disord. 2014;44:2209-20.
79. Barnea-Goraly N, Kwon H, Menon V, Eliez S, Lotspeich L, Reiss AL. White matter structure in autism: preliminary evidence from diffusion tensor imaging. Biol Psychiatry. 2004;55:323-6.
80. Barnea-Goraly N, Lotspeich LJ, Reiss AL. Similar white matter aberrations in children with autism and their unaffected siblings: a diffusion tensor imaging study using tract-based spatial statistics. Arch Gen Psychiatry. 2010;67:1052-60.
81. Brito AR, Vasconcelos MM, Domingues RC, da Cruz Hygino LC, Lde Rodrigues S, Gasparetto EL, et al. Diffusion tensor imaging findings in school-aged autistic children. J Neuroimaging Off J Am Soc Neuroimaging. 2009;19:337-43.
82. Cheon KA, Kim YS, Oh SH, Park SY, Yoon HW, Herrington J, et al. Involvement of the anterior thalamic radiation in boys with high functioning autism spectrum disorders: a Diffusion Tensor Imaging study. Brain Res. 2011;1417:77-86.
83. Jou RJ, Jackowski AP, Papademetris X, Rajeevan N, Staib LH, Volkmar FR. Diffusion tensor imaging in autism spectrum disorders: preliminary evidence of abnormal neural connectivity. Aust N Z J Psychiatry. 2011;45:153-62.
84. Kumar A, Sundaram SK, Sivaswamy L, Behen ME, Makki MI, Ager J, et al. Alterations in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. Cereb Cortex. 2010;20:2103-13.
85. Noriuchi M, Kikuchi Y, Yoshiura T, Kira R, Shigeto H, Hara T, et al. Altered white matter fractional anisotropy and social impairment in children with autism spectrum disorder. Brain Res. 2010;1362:141-9.
86. Betzel RF, Byrge L, He Y, Goñi J, Zuo X-N, Sporns O. Changes in structural and functional connectivity among resting-state networks across the human lifespan. NeuroImage. 2014;102P2:345-57.
87. Mason RA, Williams DL, Kana RK, Minshew N, Just MA. Theory of mind disruption and recruitment of the right hemisphere during narrative comprehension in autism. Neuropsychologia. 2008;46:269-80.
88. Damarla SR, Keller TA, Kana RK, Cherkassky VL, Williams DL, Minshew NJ, et al. Cortical underconnectivity coupled with preserved visuospatial cognition in autism: evidence from an fMRI study of an embedded figures task. Autism Res Off J Int Soc Autism Res. 2010;3:273-9.
89. Schipul SE, Williams DL, Keller TA, Minshew NJ, Just MA. Distinctive neural processes during learning in autism. Cereb Cortex. 2012;22:937-50.
90. Zielinski BA, Prigge MBD, Nielsen JA, Froehlich AL, Abildskov TJ, Anderson JS, et al. Longitudinal changes in cortical thickness in autism and typical development. Brain J Neurol. 2014;137:1799-812.
91. Booth R, Wallace GL, Happe F. Connectivity and the corpus callosum in autism spectrum conditions: insights from comparison of autism and callosal agenesis. Prog Brain Res. 2011;189:303-17.
92. Paul LK. Developmental malformation of the corpus callosum: a review of typical callosal development and examples of developmental disorders with callosal involvement. J Neurodev Disord. 2011;3:3-27.
93. Paul LK, Corsello C, Kennedy DP, Adolphs R. Agenesis of the corpus callosum and autism: a comprehensive comparison. Brain J Neurol. 2014;137(Pt 6):1813-29.
94. Hannay HJ, Dennis M, Kramer L, Blaser S, Fletcher JM. Partial agenesis of the corpus callosum in spina bifida meningomyelocele and potential compensatory mechanisms. J Clin Exp Neuropsychol. 2009;31:180-94.
95. Willett JB, Singer JD, Martin NC. The design and analysis of longitudinal studies of development and psychopathology in context: statistical models and methodological recommendations. Dev Psychopathol. 1998;10:395-426.
96. Amundsen LB, Artru AA, Dager SR, Shaw DWW, Friedman S, Sparks B, et al. Propofol sedation for longitudinal pediatric neuroimaging research. J Neurosurg Anesthesiol. 2005;17:180-92.
97. Lee JE, Bigler ED, Alexander AL, Lazar M, DuBray MB, Chung MK, et al. Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism. Neurosci Lett. 2007;424:127-32.