Diffusion Tensor Magnetic Resonance Imaging in Autism

Chapter

Abstract

In this chapter, we describe the methods of diffusion tensor imaging (DTI), and we describe how these imaging methods have been applied to the study of autism spectrum disorder (ASD). This chapter extends upon a recent review of the literature (Travers et al. 2012), by providing information on more recent studies and in-depth information regarding the white matter integrity of the cerebellar, frontal, and thalamic tracts. Therefore, we first review DTI studies of young children with ASD because these children are closest in age to the primary, initiating pathology of autism. Then, we present and discuss results from particular white matter tracts and brain regions of high interest from childhood into adulthood. Specific factors that may potentially influence and at times confound case–control differences in DTI studies are mentioned. We then discuss what DTI findings to date suggest about biological mechanisms involved in autism. Results from the reviewed studies are included in Table 8.7, which is an extension of the table presented in the review by Travers et al. (2012).

Keywords

Autism Spectrum Disorder White Matter Autism Spectrum Disorder Fractional Anisotropy Diffusion Tensor Imaging 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This chapter extended upon the review article (Travers et al. 2012), and we therefore thank Nagesh Adluru PhD, Chad Ennis, Do Tromp, Dan Destiche, Sam Doran, Erin D. Bigler PhD, and Nicholas Lange ScD, who contributed to the Autism Research review. This work was supported by NICHD T32 HD07489 Postdoctoral Training Award (BGT); NICHD P30 HD003352 (ALA); NIMH P50 MH84051 (ALA), NIMH R01 MH080826 (JEL, ALA), NIMH R01 MH084795 (JEL). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIMH, NICHD, or the NIH. The authors would also like to thank Frances Haeberli and Bimi Pangli for their assistance with selecting and reviewing the articles, and Dr. Alyson Froehlich and Annahir Cariello for preparing the chapter for publication.

References

  1. Abe O, Aoki S, Hayashi N, Yamada H, Kunimatsu A, Mori H, Yoshikawa T, Okubo T, Ohtomo K (2002) Normal aging in the central nervous system: quantitative MR diffusion-tensor analysis. Neurobiol Aging 23:433–441PubMedCrossRefGoogle Scholar
  2. Adluru N, Hinrichs C, Chung MK, Lee JE, Singh V, Bigler ED, Lange N, Lainhart JE, Alexander AL (2009) Classification in DTI using shapes of white matter tracts. Conf Proc IEEE Eng Med Biol Soc 2009:2719–2722PubMedGoogle Scholar
  3. Agartz I, Andersson JL, Skare S (2001) Abnormal brain white matter in schizophrenia: a diffusion tensor imaging study. Neuroreport 12:2251–2254PubMedCrossRefGoogle Scholar
  4. Alexander AL, Hasan K, Kindlmann G, Parker DL, Tsuruda JS (2000) A geometric analysis of diffusion tensor measurements of the human brain. Magn Reson Med 44:283–291PubMedCrossRefGoogle Scholar
  5. Alexander AL, Hasan KM, Lazar M, Tsuruda JS, Parker DL (2001a) Analysis of partial volume effects in diffusion-tensor MRI. Magn Reson Med 45:770–780PubMedCrossRefGoogle Scholar
  6. Alexander DC, Pierpaoli C, Basser PJ, Gee JC (2001b) Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans Med Imaging 20:1131–1139PubMedCrossRefGoogle Scholar
  7. Alexander AL, Lee JE, Lazar M, Boudos R, DuBray MB, Oakes TR, Miller JN, Lu J, Jeong EK, McMahon WM, Bigler ED, Lainhart JE (2007) Diffusion tensor imaging of the corpus callosum in Autism. Neuroimage 34:61–73PubMedCrossRefGoogle Scholar
  8. Alexander AL, Hurley SA, Samsonov AA, Adluru N, Hosseinbor AP, Mossahebi P, do Tromp PM, Zakszewski E, Field AS (2011) Characterization of cerebral white matter properties using quantitative magnetic resonance imaging stains. Brain Connect 1:423–446PubMedCrossRefGoogle Scholar
  9. Ameis SH, Fan J, Rockel C, Voineskos AN, Lobaugh NJ, Soorya L, Wang AT, Hollander E, Anagnostou E (2011) Impaired structural connectivity of socio-emotional circuits in autism spectrum disorders: a diffusion tensor imaging study. PLoS One 6:e28044PubMedCrossRefGoogle Scholar
  10. Anderson AW (2001) Theoretical analysis of the effects of noise on diffusion tensor imaging. Magn Reson Med 46:1174–1188PubMedCrossRefGoogle Scholar
  11. Anderson JS, Nielsen JA, Froehlich AL, DuBray MB, Druzgal TJ, Cariello AN, Cooperrider JR, Zielinski BA, Ravichandran C, Fletcher PT, Alexander AL, Bigler ED, Lange N, Lainhart JE (2011) Functional connectivity magnetic resonance imaging classification of autism. Brain 134:3742–3754PubMedCrossRefGoogle Scholar
  12. Ardekani BA, Nierenberg J, Hoptman MJ, Javitt DC, Lim KO (2003) MRI study of white matter diffusion anisotropy in schizophrenia. Neuroreport 14:2025–2029PubMedCrossRefGoogle Scholar
  13. Ashburner J, Friston KJ (2000) Voxel-based morphometry–the methods. Neuroimage 11: 805–821PubMedCrossRefGoogle Scholar
  14. Ashtari M, Cervellione KL, Hasan KM, Wu J, McIlree C, Kester H, Ardekani BA, Roofeh D, Szeszko PR, Kumra S (2007) White matter development during late adolescence in healthy males: a cross-sectional diffusion tensor imaging study. Neuroimage 35:501–510PubMedCrossRefGoogle Scholar
  15. Barnea-Goraly N, Menon V, Krasnow B, Ko A, Reiss A, Eliez S (2003a) Investigation of white matter structure in velocardiofacial syndrome: a diffusion tensor imaging study. Am J Psychiatry 160:1863–1869PubMedCrossRefGoogle Scholar
  16. Barnea-Goraly N, Eliez S, Hedeus M, Menon V, White CD, Moseley M, Reiss AL (2003b) White matter tract alterations in fragile X syndrome: preliminary evidence from diffusion tensor imaging. Am J Med Genet 118B:81–88PubMedCrossRefGoogle Scholar
  17. Barnea-Goraly N, Kwon H, Menon V, Eliez S, Lotspeich L, Reiss AL (2004) White matter structure in autism: preliminary evidence from diffusion tensor imaging. Biol Psychiatry 55:323–326PubMedCrossRefGoogle Scholar
  18. Barnea-Goraly N, Menon V, Eckert M, Tamm L, Bammer R, Karchemskiy A, Dant CC, Reiss AL (2005) White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb Cortex 15:1848–1854PubMedCrossRefGoogle Scholar
  19. Barnea-Goraly N, Lotspeich LJ, Reiss AL (2010) 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 67:1052–1060PubMedCrossRefGoogle Scholar
  20. Basser PJ (1995) Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed 8:333–344PubMedCrossRefGoogle Scholar
  21. Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209–219PubMedCrossRefGoogle Scholar
  22. Basser PJ, Pierpaoli C (1998) A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Imaging 39:928–934Google Scholar
  23. Basser PJ, Mattiello J, LeBihan D (1994a) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103:247–254PubMedCrossRefGoogle Scholar
  24. Basser PJ, Mattiello J, LeBihan D (1994b) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267PubMedCrossRefGoogle Scholar
  25. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44:625–632PubMedCrossRefGoogle Scholar
  26. Batchelor PG, Atkinson D, Hill DL, Calamante F, Connelly A (2003) Anisotropic noise propagation in diffusion tensor MRI sampling schemes. Magn Reson Imaging 49:1143–1151Google Scholar
  27. Beacher FD, Minati L, Baron-Cohen S, Lombardo MV, Lai MC, Gray MA, Harrison NA, Critchley HD (2012) Autism attenuates sex differences in brain structure: a combined voxel-based morphometry and diffusion tensor imaging study. AJNR Am J Neuroradiol 33:83–89PubMedCrossRefGoogle Scholar
  28. Ben Bashat D, Kronfeld-Duenias V, Zachor DA, Ekstein PM, Hendler T, Tarrasch R, Even A, Levy Y, Ben Sira L (2007) Accelerated maturation of white matter in young children with autism: a high b value DWI study. Neuroimage 37:40–47PubMedCrossRefGoogle Scholar
  29. Bloemen OJ, Deeley Q, Sundram F, Daly EM, Barker GJ, Jones DK, van Amelsvoort TA, Schmitz N, Robertson D, Murphy KC, Murphy DG (2010) White matter integrity in Asperger syndrome: a preliminary diffusion tensor magnetic resonance imaging study in adults. Autism Res 3:203–213PubMedCrossRefGoogle Scholar
  30. Bode MK, Mattila ML, Kiviniemi V, Rahko J, Moilanen I, Ebeling H, Tervonen O, Nikkinen J (2011) White matter in autism spectrum disorders – evidence of impaired fiber formation. Acta Radiol 52:1169–1174PubMedCrossRefGoogle Scholar
  31. Bosnell RA, Kincses T, Stagg CJ, Tomassini V, Kischka U, Jbabdi S, Woolrich MW, Andersson J, Matthews PM, Johansen-Berg H (2011) Motor practice promotes increased activity in brain regions structurally disconnected after subcortical stroke. Neurorehabil Neural Repair 25:607–616PubMedCrossRefGoogle Scholar
  32. Brain Development Cooperative Group (2012) Total and regional brain volumes in a population-­based normative sample from 4 to 18 years: the NIH MRI Study of Normal Brain Development. Cereb Cortex 22:1–12CrossRefGoogle Scholar
  33. Brito AR, Vasconcelos MM, Domingues RC, Hygino da Cruz LC Jr, Rodrigues LS, Gasparetto EL, Calçada CABP (2009) Diffusion tensor imaging findings in school-aged autistic children. J Neuroimaging 19:337–343PubMedCrossRefGoogle Scholar
  34. Buchsbaum MS, Tang CY, Peled S, Gudbjartsson H, Lu D, Hazlett EA, Downhill J, Haznedar M, Fallon JH, Atlas SW (1998) MRI white matter diffusion anisotropy and PET metabolic rate in schizophrenia. Neuroreport 9:425–430PubMedCrossRefGoogle Scholar
  35. Casanova MF, Buxhoeveden DP, Switala AE, Roy E (2002) Neuronal density and architecture (Gray Level Index) in the brains of autistic patients. J Child Neurol 17:515–521PubMedCrossRefGoogle Scholar
  36. Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132PubMedCrossRefGoogle Scholar
  37. Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94PubMedCrossRefGoogle Scholar
  38. Catani M, Jones DK, Ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57:8–16PubMedCrossRefGoogle Scholar
  39. Catani M, Allin MP, Husain M, Pugliese L, Mesulam MM, Murray RM, Jones DK (2007) Symmetries in human brain language pathways correlate with verbal recall. Proc Natl Acad Sci USA 104:17163–17168PubMedCrossRefGoogle Scholar
  40. Catani M, Jones DK, Daly E, Embiricos N, Deeley Q, Pugliese L, Curran S, Robertson D, Murphy DG (2008) Altered cerebellar feedback projections in Asperger syndrome. Neuroimage 41:1184–1191PubMedCrossRefGoogle Scholar
  41. Cheng Y, Chou KH, Chen IY, Fan YT, Decety J, Lin CP (2010) Atypical development of white matter microstructure in adolescents with autism spectrum disorders. Neuroimage 50: 873–882PubMedCrossRefGoogle Scholar
  42. Cheon KA, Kim YS, Oh SH, Park SY, Yoon HW, Herrington J, Nair A, Koh YJ, Jang DP, Kim YB, Leventhal BL, Cho ZH, Castellanos FX, Schultz RT (2011) Involvement of the anterior thalamic radiation in boys with high functioning autism spectrum disorders: a diffusion tensor imaging study. Brain Res 1417:77–86PubMedCrossRefGoogle Scholar
  43. Cheung C, Chua SE, Cheung V, Khong PL, Tai KS, Wong TK, Ho TP, McAlonan GM (2009) White matter fractional anisotrophy differences and correlates of diagnostic symptoms in autism. J Child Psychol Psychiatry 50:1102–1112PubMedCrossRefGoogle Scholar
  44. Conturo TE, Lori NF, Cull TS, Akbudak E, Snyder AZ, Shimony JS, McKinstry RC, Burton H, Raichle ME (1999) Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci USA 96:10422–10427PubMedCrossRefGoogle Scholar
  45. Conturo TE, Williams DL, Smith CD, Gultepe E, Akbudak E, Minshew NJ (2008) Neuronal fiber pathway abnormalities in autism: an initial MRI diffusion tensor tracking study of hippocampo-­fusiform and amygdalo-fusiform pathways. J Int Neuropsychol Soc 14:933–946PubMedCrossRefGoogle Scholar
  46. Corrigan NM, Richards TL, Treffert DA, Dager SR (2012) Toward a better understanding of the savant brain. Compr Psychiatry 53:706–717PubMedCrossRefGoogle Scholar
  47. Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, Hallet MJ, Barnes CC, Pierce K (2011) Neuron number and size in prefrontal cortex of children with autism. JAMA 306:2001–2010PubMedCrossRefGoogle Scholar
  48. DuBray Prigge MB, Lange N, Bigler ED, Merkley TL, Neeley ES, Abildskov TJ, Froehlich AL, Nielsen JA, Cooperrider JR, Cariello AN, Ravichandran C, Alexander AL, Lainhart JE (2012) Corpus callosum area in children and adults with autism. Res Autism Spectr Disord 7(2): 221–234CrossRefGoogle Scholar
  49. Engvig A, Fjell AM, Westlye LT, Moberget T, Sundseth O, Larsen VA, Walhovd KB (2011) Memory training impacts short-term changes in aging white matter: a longitudinal diffusion tensor imaging study. Hum Brain Mapp 33(10):2390–2406PubMedCrossRefGoogle Scholar
  50. Filippi CG, Lin DD, Tsiouris AJ, Watts R, Packard AM, Heier LA, Ulug AM (2003) Diffusion-­tensor MR imaging in children with developmental delay: preliminary findings. Radiology 229:44–50PubMedCrossRefGoogle Scholar
  51. Fletcher PT, Whitaker RT, Tao R, DuBray MB, Froehlich A, Ravichandran C, Alexander AL, Bigler ED, Lange N, Lainhart JE (2010) Microstructural connectivity of the arcuate fasciculus in adolescents with high-functioning autism. Neuroimage 51:1117–1125PubMedCrossRefGoogle Scholar
  52. Foong J, Maier M, Barker GJ, Brocklehurst S, Miller DH, Ron MA (2000) In vivo investigation of white matter pathology in schizophrenia with magnetisation transfer imaging. J Neurol Neurosurg Psychiatry 68:70–74PubMedCrossRefGoogle Scholar
  53. Foong J, Symms MR, Barker GJ, Maier M, Miller DH, Ron MA (2002) Investigating regional white matter in schizophrenia using diffusion tensor imaging. Neuroreport 13:333–336PubMedCrossRefGoogle Scholar
  54. Giorgio A, Watkins KE, Douaud G, James AC, James S, De Stefano N, Matthews PM, Smith SM, Johansen-Berg H (2008) Changes in white matter microstructure during adolescence. Neuroimage 39:52–61PubMedCrossRefGoogle Scholar
  55. Giorgio A, Santelli L, Tomassini V, Bosnell R, Smith S, De Stefano N, Johansen-Berg H (2010) Age-related changes in grey and white matter structure throughout adulthood. Neuroimage 51:943–951PubMedCrossRefGoogle Scholar
  56. Gordon EM, Lee PS, Maisog JM, Foss-Feig J, Billington ME, Vanmeter J, Vaidya CJ (2011) Strength of default mode resting-state connectivity relates to white matter integrity in children. Dev Sci 14:738–751PubMedCrossRefGoogle Scholar
  57. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72–78PubMedCrossRefGoogle Scholar
  58. Groen WB, Buitelaar JK, van der Gaag RJ, Zwiers MP (2011) Pervasive microstructural abnormalities in autism: a DTI study. J Psychiatry Neurosci 36:32–40PubMedCrossRefGoogle Scholar
  59. Guo AC, Petrella JR, Kurtzberg J, Provenzale JM (2001) Evaluation of white matter anisotropy in Krabbe disease with diffusion tensor MR imaging: Initial experience. Radiology 218:809–815PubMedGoogle Scholar
  60. Hardan AY, Minshew NJ, Keshavan MS (2000) Corpus callosum size in autism. Neurology 55:1033–1036PubMedCrossRefGoogle Scholar
  61. Harsan LA, Poulet P, Guignard B, Steibel J, Parizel N, de Sousa PL, Boehm N, Grucker D, Ghandour MS (2006) Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging. J Neurosci Res 83:392–402PubMedCrossRefGoogle Scholar
  62. Hasan KM, Parker DL, Alexander AL (2001) Comparison of gradient encoding schemes for diffusion-­tensor MRI. J Magn Reson Imaging 13:769–780PubMedCrossRefGoogle Scholar
  63. Hasan KM, Iftikhar A, Kamali A, Kramer LA, Ashtari M, Cirino PT, Papanicolaou AC, Fletcher JM, Ewing-Cobbs L (2009) Development and aging of the healthy human brain uncinate fasciculus across the lifespan using diffusion tensor tractography. Brain Res 1276:67–76PubMedCrossRefGoogle Scholar
  64. Herbert MR, Ziegler DA, Makris N, Filipek PA, Kemper TL, Normandin JJ, Sanders HA, Kennedy DN, Caviness VS Jr (2004) Localization of white matter volume increase in autism and developmental language disorder. Ann Neurol 55:530–540PubMedCrossRefGoogle Scholar
  65. Hofer S, Merboldt KD, Tammer R, Frahm J (2008) Rhesus monkey and human share a similar topography of the corpus callosum as revealed by diffusion tensor MRI in vivo. Cereb Cortex 18:1079–1084PubMedCrossRefGoogle Scholar
  66. Hong S, Ke X, Tang T, Hang Y, Chu K, Huang H, Ruan Z, Lu Z, Tao G, Liu Y (2011) Detecting abnormalities of corpus callosum connectivity in autism using magnetic resonance imaging and diffusion tensor tractography. Psychiatry Res 194:333–339PubMedCrossRefGoogle Scholar
  67. Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA, Volpe JJ (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44:584–590PubMedCrossRefGoogle Scholar
  68. Imperati D, Colcombe S, Kelly C, Di Martino A, Zhou J, Castellanos FX, Milham MP (2011) Differential development of human brain white matter tracts. PLoS One 6:e23437PubMedCrossRefGoogle Scholar
  69. Ingalhalikar M, Parker D, Bloy L, Roberts TP, Verma R (2011) Diffusion based abnormality markers of pathology: toward learned diagnostic prediction of ASD. Neuroimage 57:918–927PubMedCrossRefGoogle Scholar
  70. Jeong JW, Kumar AK, Sundaram SK, Chugani HT, Chugani DC (2011) Sharp curvature of frontal lobe white matter pathways in children with autism spectrum disorders: tract-based morphometry analysis. AJNR Am J Neuroradiol 32:1600–1606PubMedCrossRefGoogle Scholar
  71. Jones DK (2004) The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med 51:807–815PubMedCrossRefGoogle Scholar
  72. Jones DK, Horsfield MA, Simmons A (1999a) Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn Reson Med 42:515–525PubMedCrossRefGoogle Scholar
  73. Jones DK, Simmons A, Williams SC, Horsfield MA (1999b) Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magn Reson Med 42:37–41PubMedCrossRefGoogle Scholar
  74. Jones DK, Griffin LD, Alexander DC, Catani M, Horsfield MA, Howard R, Williams SC (2002) Spatial normalization and averaging of diffusion tensor MRI data sets. Neuroimage 17: 592–617PubMedCrossRefGoogle Scholar
  75. Jones DK, Catani M, Pierpaoli C, Reeves SJ, Shergill SS, O’Sullivan M, Golesworthy P, McGuire P, Horsfield MA, Simmons A, Williams SC, Howard RJ (2006) Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Hum Brain Mapp 27:230–238PubMedCrossRefGoogle Scholar
  76. Jou RJ, Jackowski AP, Papademetris X, Rajeevan N, Staib LH, Volkmar FR (2011a) Diffusion tensor imaging in autism spectrum disorders: preliminary evidence of abnormal neural connectivity. Aust N Z J Psychiatry 45:153–162PubMedCrossRefGoogle Scholar
  77. Jou RJ, Mateljevic N, Kaiser MD, Sugrue DR, Volkmar FR, Pelphrey KA (2011b) Structural neural phenotype of autism: preliminary evidence from a diffusion tensor imaging study using tract-based spatial statistics. AJNR Am J Neuroradiol 32:1607–1613PubMedCrossRefGoogle Scholar
  78. Kanaan RA, Allin M, Picchioni M, Barker GJ, Daly E, Shergill SS, Woolley J, McGuire PK (2012) Gender differences in white matter microstructure. PLoS One 7:e38272PubMedCrossRefGoogle Scholar
  79. Ke X, Tang T, Hong S, Hang Y, Zou B, Li H, Zhou Z, Ruan Z, Lu Z, Tao G, Liu Y (2009) White matter impairments in autism, evidence from voxel-based morphometry and diffusion tensor imaging. Brain Res 1265:171–177PubMedCrossRefGoogle Scholar
  80. Keary CJ, Minshew NJ, Bansal R, Goradia D, Fedorov S, Keshavan MS, Hardan AY (2009) Corpus callosum volume and neurocognition in autism. J Autism Dev Disord 39:834–841PubMedCrossRefGoogle Scholar
  81. Keller TA, Just MA (2009) Altering cortical connectivity: remediation-induced changes in the white matter of poor readers. Neuron 64:624–631PubMedCrossRefGoogle Scholar
  82. Keller TA, Kana RK, Just MA (2007) A developmental study of the structural integrity of white matter in autism. Neuroreport 18:23–27PubMedCrossRefGoogle Scholar
  83. Kilian S, Brown WS, Hallam BJ, McMahon W, Lu J, Johnson M, Bigler ED, Lainhart J (2008) Regional callosal morphology in autism and macrocephaly. Dev Neuropsychol 33:74–99PubMedCrossRefGoogle Scholar
  84. Klingberg T, Vaidya CJ, Gabrieli JD, Moseley ME, Hedehus M (1999) Myelination and organization of the frontal white matter in children: a diffusion tensor MRI study. Neuroreport 10:2817–2821PubMedCrossRefGoogle Scholar
  85. Knaus TA, Silver AM, Dominick KC, Schuring MD, Shaffer N, Lindgren KA, Joseph RM, Tager-­Flusberg H (2009) Age-related changes in the anatomy of language regions in autism spectrum disorder. Brain Imaging Behav 3:51–63PubMedCrossRefGoogle Scholar
  86. Knaus TA, Silver AM, Kennedy M, Lindgren KA, Dominick KC, Siegel J, Tager-Flusberg H (2010) Language laterality in autism spectrum disorder and typical controls: a functional, volumetric, and diffusion tensor MRI study. Brain Lang 112:113–120PubMedCrossRefGoogle Scholar
  87. Kubicki M, Westin CF, Nestor PG, Wible CG, Frumin M, Maier SE, Kikinis R, Jolesz FA, McCarley RW, Shenton ME (2003) Cingulate fasciculus integrity disruption in schizophrenia: a magnetic resonance diffusion tensor imaging study. Biol Psychiatry 54:1171–1180PubMedCrossRefGoogle Scholar
  88. Kumar A, Sundaram SK, Sivaswamy L, Behen ME, Makki MI, Ager J, Janisse J, Chugani HT, Chugani DC (2010) Alterations in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. Cereb Cortex 20:2103–2113PubMedCrossRefGoogle Scholar
  89. Lai G, Pantazatos SP, Schneider H, Hirsch J (2012) Neural systems for speech and song in autism. Brain 135:961–975PubMedCrossRefGoogle Scholar
  90. Lainhart JE, Lange N (2011) Increased neuron number and head size in autism. JAMA 306:2031–2032PubMedCrossRefGoogle Scholar
  91. Lange N, Dubray MB, Lee JE, Froimowitz MP, Froehlich A, Adluru N, Wright B, Ravichandran C, Fletcher PT, Bigler ED, Alexander AL, Lainhart JE (2010) Atypical diffusion tensor hemispheric asymmetry in autism. Autism Res 3:350–358PubMedCrossRefGoogle Scholar
  92. Langen M, Leemans A, Johnston P, Ecker C, Daly E, Murphy CM, Dell’acqua F, Durston S, Murphy DG (2012) Fronto-striatal circuitry and inhibitory control in autism: findings from diffusion tensor imaging tractography. Cortex 48:183–193PubMedCrossRefGoogle Scholar
  93. Lazar M, Alexander AL (2003) An error analysis of white matter tractography methods: synthetic diffusion tensor field simulations. Neuroimage 20:1140–1153PubMedCrossRefGoogle Scholar
  94. Lebel C, Beaulieu C (2011) Longitudinal development of human brain wiring continues from childhood into adulthood. J Neurosci 31:10937–10947PubMedCrossRefGoogle Scholar
  95. Lebel C, Walker L, Leemans A, Phillips L, Beaulieu C (2008) Microstructural maturation of the human brain from childhood to adulthood. Neuroimage 40:1044–1055PubMedCrossRefGoogle Scholar
  96. Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60:340–352PubMedCrossRefGoogle Scholar
  97. Lee JE, Bigler ED, Alexander AL, Lazar M, DuBray MB, Chung MK, Johnson M, Morgan J, Miller JN, McMahon WM, Lu J, Jeong EK, Lainhart JE (2007) Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism. Neurosci Lett 424:127–132PubMedCrossRefGoogle Scholar
  98. Lee JE, Chung MK, Lazar M, DuBray MB, Kim J, Bigler ED, Lainhart JE, Alexander AL (2009) A study of diffusion tensor imaging by tissue-specific, smoothing-compensated voxel-based analysis. Neuroimage 44:870–883PubMedCrossRefGoogle Scholar
  99. Lewis WW, Sahin M, Scherrer B, Peters JM, Suarez RO, Vogel-Farley VK, Jeste SS, Gregas MC, Prabhu SP, Nelson CA 3rd, Warfield SK (2012) Impaired language pathways in tuberous ­sclerosis complex patients with autism spectrum disorders. Cereb Cortex, epub ahead of print, doi:10.1093/cercor/bhs135Google Scholar
  100. Leyfer OT, Folstein SE, Bacalman S, Davis NO, Dinh E, Morgan J, Tager-Flusberg H, Lainhart JE (2006) Comorbid psychiatric disorders in children with autism: interview development and rates of disorders. J Autism Dev Disord 36:849–861PubMedCrossRefGoogle Scholar
  101. Lezak MD, Howieson DB, Bigler ED, Tranel D (2012) Neuropsychological Assessment, 5th edn. Oxford University Press, New YorkGoogle Scholar
  102. Lim KO, Hedehus M, Moseley M, de Crespigny A, Sullivan EV, Pfefferbaum A (1999) Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. Arch Gen Psychiatry 56:367–374PubMedCrossRefGoogle Scholar
  103. Lo YC, Soong WT, Gau SS, Wu YY, Lai MC, Yeh FC, Chiang WY, Kuo LW, Jaw FS, Tseng WY (2011) The loss of asymmetry and reduced interhemispheric connectivity in adolescents with autism: a study using diffusion spectrum imaging tractography. Psychiatry Res 192:60–66PubMedCrossRefGoogle Scholar
  104. Lori NF, Akbudak E, Shimony JS, Cull TS, Snyder AZ, Guillory RK, Conturo TE (2002) Diffusion tensor fiber tracking of human brain connectivity: aquisition methods, reliability analysis and biological results. NMR Biomed 15:494–515PubMedCrossRefGoogle Scholar
  105. Lovden M, Bodammer NC, Kuhn S, Kaufmann J, Schutze H, Tempelmann C, Heinze HJ, Duzel E, Schmiedek F, Lindenberger U (2010) Experience-dependent plasticity of white-matter microstructure extends into old age. Neuropsychologia 48:3878–3883PubMedCrossRefGoogle Scholar
  106. Mazefsky CA, Oswald DP, Day TN, Eack SM, Minshew NJ, Lainhart JE (2012) ASD, a psychiatric disorder, or both? Psychiatric diagnoses in adolescents with high-functioning ASD. J Clin Child Adolesc Psychol 41:516–523PubMedCrossRefGoogle Scholar
  107. Mori S, van Zijl PC (2002) Fiber tracking: principles and strategies - a technical review. NMR Biomed 15:468–480PubMedCrossRefGoogle Scholar
  108. Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269PubMedCrossRefGoogle Scholar
  109. Mori S, Kaufmann WE, Davatzikos C, Stieltjes B, Amodei L, Fredericksen K, Pearlson GD, Melhem ER, Solaiyappan M, Raymond GV, Moser HW, van Zijl PC (2002) Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med 47:215–223PubMedCrossRefGoogle Scholar
  110. Muetzel RL, Collins PF, Mueller BA, Schissel AM, Lim KO, Luciana M (2008) The development of corpus callosum microstructure and associations with bimanual task performance in healthy adolescents. Neuroimage 39:1918–1925PubMedCrossRefGoogle Scholar
  111. Mukherjee P, Miller JH, Shimony JS, Conturo TE, Lee BC, Almli CR, McKinstry RC (2001) Normal brain maturation during childhood: developmental trends characterized with diffusion-­tensor MR imaging. Radiology 221:349–358PubMedCrossRefGoogle Scholar
  112. Nagae LM, Zarnow DM, Blaskey L, Dell J, Khan SY, Qasmieh S, Levy SE, Roberts TP (2012) Elevated mean diffusivity in the left hemisphere superior longitudinal fasciculus in autism spectrum disorders increases with more profound language impairment. AJNR Am J Neuroradiol 33(9):1720–1725PubMedCrossRefGoogle Scholar
  113. Noriuchi M, Kikuchi Y, Yoshiura T, Kira R, Shigeto H, Hara T, Tobimatsu S, Kamio Y (2010) Altered white matter fractional anisotropy and social impairment in children with autism spectrum disorder. Brain Res 1362:141–149PubMedCrossRefGoogle Scholar
  114. O’Sullivan M, Jones DK, Summers PE, Morris RG, Williams SC, Markus HS (2001) Evidence for cortical “disconnection” as a mechanism of age-related cognitive decline. Neurology 57: 632–638PubMedCrossRefGoogle Scholar
  115. Papadakis NG, Xing D, Huang CL, Hall LD, Carpenter TA (1999) A comparative study of acquisition schemes for diffusion tensor imaging using MRI. J Magn Reson 137:67–82PubMedCrossRefGoogle Scholar
  116. Pardini M, Garaci FG, Bonzano L, Roccatagliata L, Palmieri MG, Pompili E, Coniglione F, Krueger F, Ludovici A, Floris R, Benassi F, Emberti Gialloreti L (2009) White matter reduced streamline coherence in young men with autism and mental retardation. Eur J Neurol 16:1185–1190PubMedCrossRefGoogle Scholar
  117. Pardini M, Elia M, Garaci FG, Guida S, Coniglione F, Krueger F, Benassi F, Emberti Gialloreti L (2012) Long-term cognitive and behavioral therapies, combined with augmentative ­communication, are related to uncinate fasciculus integrity in autism. J Autism Dev Disord 42:585–592PubMedCrossRefGoogle Scholar
  118. Park HJ, Kubicki M, Shenton ME, Guimond A, McCarley RW, Maier SE, Kikinis R, Jolesz FA, Westin CF (2003) Spatial normalization of diffusion tensor MRI using multiple channels. Neuroimage 20:1995–2009PubMedCrossRefGoogle Scholar
  119. Pfefferbaum A, Sullivan EV, Hedehus M, Lim KO, Adalsteinsson E, Moseley M (2000) Age-­related decline in brain white matter anisotropy measured with spatially corrected echo-planar diffusion tensor imaging. Magn Reson Med 44:259–268PubMedCrossRefGoogle Scholar
  120. Poupon C, Clark CA, Frouin V, Regis J, Bloch I, Le Bihan D, Mangin J (2000) Regularization of diffusion-based direction maps for the tracking of brain white matter fascicles. Neuroimage 12:184–195PubMedCrossRefGoogle Scholar
  121. Poustka L, Jennen-Steinmetz C, Henze R, Vomstein K, Haffner J, Sieltjes B (2012) Fronto-­temporal disconnectivity and symptom severity in children with autism spectrum disorder. World J Biol Psychiatry 13:269–280PubMedCrossRefGoogle Scholar
  122. Pugliese L, Catani M, Ameis S, Dell’Acqua F, Thiebaut de Schotten M, Murphy C, Robertson D, Deeley Q, Daly E, Murphy DG (2009) The anatomy of extended limbic pathways in Asperger syndrome: a preliminary diffusion tensor imaging tractography study. Neuroimage 47: 427–434PubMedCrossRefGoogle Scholar
  123. Sahyoun CP, Belliveau JW, Mody M (2010a) White matter integrity and pictorial reasoning in high-functioning children with autism. Brain Cogn 73:180–188PubMedCrossRefGoogle Scholar
  124. Sahyoun CP, Belliveau JW, Soulières I, Schwartz S, Mody M (2010b) Neuroimaging of the functional and structural networks underlying visuospatial vs. linguistic reasoning in high-­functioning autism. Neuropsychologia 48:86–95PubMedCrossRefGoogle Scholar
  125. Schipul SE, Keller TA, Just MA (2011) Inter-regional brain communication and its disturbance in autism. Front Syst Neurosci 5:10PubMedCrossRefGoogle Scholar
  126. Schmithorst VJ, Dardzinski BJ, Holland SK (2001) Simultaneous correction of ghost and geometric distortion artifacts in EPI using a multiecho reference scan. IEEE Trans Med Imaging 20:535–539PubMedCrossRefGoogle Scholar
  127. Schmithorst VJ, Wilke M, Dardzinski BJ, Holland SK (2002) Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: a cross-sectional diffusion-­tensor MR imaging study. Radiology 222:212–218PubMedCrossRefGoogle Scholar
  128. Schneider JF, Il’yasov KA, Boltshauser E, Hennig J, Martin E (2003) Diffusion tensor imaging in cases of adrenoleukodystrophy: preliminary experience as a marker for early demyelination? AJNR Am J Neuroradiol 24:819–824PubMedGoogle Scholar
  129. Shimony JS, McKinstry RC, Akbudak E, Aronovitz JA, Snyder AZ, Lori NF, Cull TS, Conturo TE (1999) Quantitative diffusion-tensor anisotropy brain MR imaging: normative human data and anatomic analysis. Radiology 212:770–784PubMedGoogle Scholar
  130. Shrager RI, Basser PJ (1998) Anisotropically weighted MRI. Magn Reson Med 40:160–165PubMedCrossRefGoogle Scholar
  131. Shukla DK, Keehn B, Lincoln AJ, Muller RA (2010) 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 49(12):1269–1278, e1261-1262PubMedGoogle Scholar
  132. Shukla DK, Keehn B, Muller RA (2011a) Tract-specific analyses of diffusion tensor imaging show widespread white matter compromise in autism spectrum disorder. J Child Psychol Psychiatry 52:286–295PubMedCrossRefGoogle Scholar
  133. Shukla DK, Keehn B, Smylie DM, Müller R-A (2011b) Microstructural abnormalities of short-­distance white matter tracts in autism spectrum disorder. Neuropsychologia 49:1378–1382PubMedCrossRefGoogle Scholar
  134. Sivaswamy L, Kumar A, Rajan D, Behen ME, Muzik O, Chugani DC, Chugani HT (2010) A diffusion tensor imaging study of the cerebellar pathways in children with autism spectrum disorder. J Child Neurol 25:1223–1231PubMedCrossRefGoogle Scholar
  135. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505PubMedCrossRefGoogle Scholar
  136. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436PubMedCrossRefGoogle Scholar
  137. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26:132–140PubMedCrossRefGoogle Scholar
  138. Stieltjes B, Kaufmann WE, van Zijl PC, Fredericksen K, Pearlson GD, Solaiyappan M, Mori S (2001) Diffusion tensor imaging and axonal tracking in the human brainstem. Neuroimage 14:723–735PubMedCrossRefGoogle Scholar
  139. Sundaram SK, Kumar A, Makki MI, Behen ME, Chugani HT, Chugani DC (2008) Diffusion tensor imaging of frontal lobe in autism spectrum disorder. Cereb Cortex 18:2659–2665PubMedCrossRefGoogle Scholar
  140. Supekar K, Uddin LQ, Prater K, Amin H, Greicius MD, Menon V (2010) Development of functional and structural connectivity within the default mode network in young children. Neuroimage 52:290–301PubMedCrossRefGoogle Scholar
  141. Taubert M, Dafotakis M, Sparing R, Eickhoff S, Leuchte S, Fink GR, Nowak DA (2010) Inhibition of the anterior intraparietal area and the dorsal premotor cortex interfere with arbitrary visuo-­motor mapping. Clin Neurophysiol 121:408–413PubMedCrossRefGoogle Scholar
  142. Thakkar KN, Polli FE, Joseph RM, Tuch DS, Hadjikhani N, Barton JJ, Manoach DS (2008) Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD). Brain 131:2464–2478PubMedCrossRefGoogle Scholar
  143. Thomas C, Humphreys K, Jung KJ, Minshew N, Behrmann M (2011) The anatomy of the callosal and visual-association pathways in high-functioning autism: a DTI tractography study. Cortex 47:863–873PubMedCrossRefGoogle Scholar
  144. Tournier JD, Calamante F, King MD, Gadian DG, Connelly A (2002) Limitations and requirements of diffusion tensor fiber tracking: an assessment using simulations. Magn Reson Med 47:701–708PubMedCrossRefGoogle Scholar
  145. Tournier JD, Mori S, Leemans A (2011) Diffusion tensor imaging and beyond. Magn Reson Med 65:1532–1556PubMedCrossRefGoogle Scholar
  146. Travers BG, Adluru N, Ennis C, Tromp DP, Destiche D, Doran S, Bigler ED, Lange N, Lainhart JE, Alexander AL (2012) Diffusion tensor imaging in autism spectrum disorder: a review. Autism Res 5(5):289–313PubMedCrossRefGoogle Scholar
  147. Tuchman R, Cuccaro M (2011) Epilepsy and autism: neurodevelopmental perspective. Curr Neurol Neurosci Rep 11:428–434PubMedCrossRefGoogle Scholar
  148. Tyszka JM, Readhead C, Bearer EL, Pautler RG, Jacobs RE (2006) Statistical diffusion tensor histology reveals regional dysmyelination effects in the shiverer mouse mutant. Neuroimage 29:1058–1065PubMedCrossRefGoogle Scholar
  149. van den Heuvel MP, Mandl RC, Kahn RS, Hulshoff Pol HE (2009) Functionally linked resting-­state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 30:3127–3141PubMedCrossRefGoogle Scholar
  150. Verhoeven JS, Rommel N, Prodi E, Leemans A, Zink I, Vandewalle E, Noens I, Wagemans J, Steyaert J, Boets B, Van de Winckel A, De Cock P, Lagae L, Sunaert S (2012) Is there a common neuroanatomical substrate of language deficit between autism spectrum disorder and specific language impairment? Cereb Cortex 22:2263–2271PubMedCrossRefGoogle Scholar
  151. Vidal CN, Nicolson R, DeVito TJ, Hayashi KM, Geaga JA, Drost DJ, Williamson PC, Rajakumar N, Sui Y, Dutton RA, Toga AW, Thompson PM (2006) Mapping corpus callosum deficits in autism: an index of aberrant cortical connectivity. Biol Psychiatry 60:218–225PubMedCrossRefGoogle Scholar
  152. Vogt BA (2005) Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 6:533–544PubMedCrossRefGoogle Scholar
  153. Wan CY, Marchina S, Norton A, Schlaug G (2012) Atypical hemispheric asymmetry in the arcuate fasciculus of completely nonverbal children with autism. Ann N Y Acad Sci 1252:332–337PubMedCrossRefGoogle Scholar
  154. Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D’Arceuil H, de Crespigny AJ (2008) Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage 41:1267–1277PubMedCrossRefGoogle Scholar
  155. Weinstein M, Ben-Sira L, Levy Y, Zachor DA, Ben Itzhak E, Artzi M, Tarrasch R, Eksteine PM, Hendler T, Ben Bashat D (2011) Abnormal white matter integrity in young children with autism. Hum Brain Mapp 32:534–543PubMedCrossRefGoogle Scholar
  156. Wheeler-Kingshott CA, Cercignani M (2009) About “axial” and “radial” diffusivities. Magn Reson Med 61:1255–1260PubMedCrossRefGoogle Scholar
  157. Wolff JJ, Gu H, Gerig G, Elison JT, Styner M, Gouttard S, Botteron KN, Dager SR, Dawson G, Estes AM, Evans AC, Hazlett HC, Kostopoulos P, McKinstry RC, Paterson SJ, Schultz RT, Zwaigenbaum L, Piven J (2012) Differences in white matter fiber tract development present from 6 to 24 months in infants with autism. Am J Psychiatry 169(6):589–600PubMedGoogle Scholar
  158. Wu YC, Field AS, Whalen PJ, Alexander AL (2011) Age- and gender-related changes in the normal human brain using hybrid diffusion imaging (HYDI). Neuroimage 54:1840–1853PubMedCrossRefGoogle Scholar
  159. Xu D, Mori S, Solaiyappan M, van Zijl PC, Davatzikos C (2002) A framework for callosal fiber distribution analysis. Neuroimage 17:1131–1143PubMedCrossRefGoogle Scholar
  160. Xu D, Mori S, Shen D, van Zijl PC, Davatzikos C (2003) Spatial normalization of diffusion tensor fields. Magn Reson Med 50:175–182PubMedCrossRefGoogle Scholar
  161. Xu J, Kemeny S, Park G, Frattali C, Braun A (2005) Language in context: emergent features of word, sentence, and narrative comprehension. Neuroimage 25:1002–1015PubMedCrossRefGoogle Scholar
  162. Yakovlev P, Lecours A (1967) The myelogenetic cycles of regional maturation of the brain. In: Minkowski A (ed) Regional development of the brain in early life. Blackwell Scientific, Oxford, pp 3–70Google Scholar
  163. Zhang H, Avants BB, Yushkevich PA, Woo JH, Wang S, McCluskey LF, Elman LB, Melhem ER, Gee JC (2007) High-dimensional spatial normalization of diffusion tensor images improves the detection of white matter differences: an example study using amyotrophic lateral sclerosis. IEEE Trans Med Imaging 26:1585–1597PubMedCrossRefGoogle Scholar

Copyright information

© Springer New York 2013

Authors and Affiliations

  1. 1.Waisman CenterUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Waisman CenterUniversity of Wisconsin-MadisonMadisonUSA

Personalised recommendations