Altered white matter integrity in adults with autism spectrum disorder and an IQ >100: a diffusion tensor imaging study

Acta Psychiatrica Scandinavica

Volumn 135, Issue 6, 2017, Pages 573-583

  Nickel, K ^a   Tebartz van Elst, L ^a   Perlov, E ^a,b   Endres, D ^a   Muller G T ^a   Riedel, A ^a   Fangmeier, T ^a   Maier, S ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b Hospital St Urban   (Switzerland)

Author keywords

anterior cingulate cortex; autism spectrum disorder; corpus callosum; diffusion tensor imaging

Indexed keywords

PSYCHOTROPIC AGENT;

ADULT; ANTERIOR CINGULATE; ARTICLE; AUTISM; CLINICAL ARTICLE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CORPUS CALLOSUM; DEPRESSION; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; FUNCTIONAL NEUROIMAGING; HUMAN; INTELLIGENCE QUOTIENT; MALE; PRIORITY JOURNAL; PSYCHOMETRY; RADIOLOGICAL PARAMETERS; WHITE MATTER; ANISOTROPY; CASE CONTROL STUDY; CINGULATE GYRUS; DIAGNOSTIC IMAGING; INTELLIGENCE; NEUROIMAGING; PATHOLOGY;

ADULT; ANISOTROPY; AUTISM SPECTRUM DISORDER; CASE-CONTROL STUDIES; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; FEMALE; GYRUS CINGULI; HUMANS; INTELLIGENCE; MALE; NEUROIMAGING; WHITE MATTER;

EID: 85017464891     PISSN: 0001690X     EISSN: 16000447     Source Type: Journal    
DOI: 10.1111/acps.12731     Document Type: Article

References (68)

1. Ameis SH, Catani M. Altered white matter connectivity as a neural substrate for social impairment in Autism Spectrum Disorder. Cortex 2015;62:158–181.
2. Geschwind DH, Levitt P. Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol 2007;17:103–111.
3. Attwood T. The Complete Guide to Asperger's syndrome. London and Philadelphia: Jessica Kingsley Publishers; 2008.
4. Brugha TS, McManus S, Bankart J et al. Epidemiology of autism spectrum disorders in adults in the community in England. Arch Gen Psychiatry 2011;68:459–465.
5. Kim YS, Leventhal BL, Koh Y-J et al. Prevalence of autism spectrum disorders in a total population sample. Am J Psychiatry 2011;168:904–912.
6. Folstein SE, Rosen-Sheidley B. Genetics of autism: complex aetiology for a heterogeneous disorder. Nat Rev Genet 2001;2:943–955.
7. Alexander AL, Lee JE, Lazar M et al. Diffusion tensor imaging of the corpus callosum in Autism. NeuroImage 2007;34:61–73.
8. Keller TA, Kana RK, Just MA. A developmental study of the structural integrity of white matter in autism. NeuroReport 2007;18:23–27.
9. Lee JE, Bigler ED, Alexander AL et al. Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism. Neurosci Lett 2007;424:127–132.
10. Catani M, Jones DK, Daly E et al. Altered cerebellar feedback projections in Asperger syndrome. NeuroImage 2008;41:1184–1191.
11. Thakkar KN, Polli FE, Joseph RM et al. Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD). Brain J Neurol 2008;131:2464–2478.
12. Bloemen OJN, Deeley Q, Sundram F et al. White matter integrity in Asperger syndrome: a preliminary diffusion tensor magnetic resonance imaging study in adults. Autism Res 2010;3:203–213.
13. Conturo TE, Williams DL, Smith CD, Gultepe E, Akbudak E, Minshew NJ. Neuronal fiber pathway abnormalities in autism: an initial MRI diffusion tensor tracking study of hippocampo-fusiform and amygdalo-fusiform pathways. J Int Neuropsychol Soc 2008;14:933–946.
14. Langen M, Leemans A, Johnston P et al. Fronto-striatal circuitry and inhibitory control in autism: findings from diffusion tensor imaging tractography. Cortex 2012;48:183–193.
15. Lee JE, Chung MK, Lazar M et al. A study of diffusion tensor imaging by tissue-specific, smoothing-compensated voxel-based analysis. NeuroImage 2009;44:870–883.
16. Thomas C, Humphreys K, Jung K-J, Minshew N, Behrmann M. The anatomy of the callosal and visual-association pathways in high-functioning autism: a DTI tractography study. Cortex J Devoted Study Nerv Syst Behav 2011;47:863–873.
17. Pugliese L, Catani M, Ameis S et al. The anatomy of extended limbic pathways in Asperger syndrome: a preliminary diffusion tensor imaging tractography study. NeuroImage 2009;47:427–434.
18. Basser P, Pierpaoli C. Recollections about our 1996 JMR paper on diffusion anisotropy. J Magn Reson 2011;213:571–572.
19. Jeong J-W, Chugani DC, Behen ME, Tiwari VN, Chugani HT. Altered white matter structure of the dentatorubrothalamic pathway in children with autistic spectrum disorders. Cerebellum Lond Engl 2012;11:957–971.
20. McFadden K, Minshew NJ. Evidence for dysregulation of axonal growth and guidance in the etiology of ASD. Front Hum Neurosci 2013;7:671.
21. Zikopoulos B, Barbas H. Altered neural connectivity in excitatory and inhibitory cortical circuits in autism. Front Hum Neurosci 2013;7:609.
22. Tebartz van Elst L, Riedel A, Maier S. Autism as a disorder of altered global functional and structural connectivity. Biol Psychiatry 2016;79:626–627.
23. Koldewyn K, Jiang YV, Weigelt S, Kanwisher N. Global/local processing in autism: not a disability, but a disinclination. J Autism Dev Disord 2013;43:2329–2340.
24. Poustka L, Jennen-Steinmetz C, Henze R, Vomstein K, Haffner J, Sieltjes B. Fronto-temporal disconnectivity and symptom severity in children with autism spectrum disorder. World J Biol Psychiatry 2012;13:269–280.
25. Travers BG, Adluru N, Ennis C et al. Diffusion tensor imaging in autism spectrum disorder: a review. Autism Res 2012;5:289–313.
26. Chen R, Jiao Y, Herskovits EH. Structural MRI in autism spectrum disorder. Pediatr Res 2011;69:63R–68R.
27. Tebartz van Elst L, Maier S, Fangmeier T et al. Disturbed cingulate glutamate metabolism in adults with high-functioning autism spectrum disorder: evidence in support of the excitatory/inhibitory imbalance hypothesis. Mol Psychiatry 2014;19:1314–1325.
28. Wittchen H-U. Strukturiertes klinisches Interview für DSM-IV: Achse I und II, SKID. Göttingen: Hogrefe; 1997.
29. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E. The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 2001;31:5–17.
30. Baron-Cohen S, Wheelwright S. The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord 2004;34:163–175.
31. Melfsen S, Walitza S, Attwood A, Warnke A. Validation of the German version of the Australian Scale of Asperger's Syndrome (ASAS). Z Für Kinder-Jugendpsychiatrie Psychother 2005;33:27–34.
32. Constantino JN, Davis SA, Todd RD et al. Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. J Autism Dev Disord 2003;33:427–433.
33. Vorst HC, Bermond B. Validity and reliability of the Bermond-Vorst alexithymia questionnaire. Personal Individ Differ 2001;30:413–434.
34. Baron-Cohen S, Wheelwright S, Robinson J, Woodbury-Smith M. The Adult Asperger Assessment (AAA): a diagnostic method. J Autism Dev Disord 2005;35:807–819.
35. Retz-Junginger P, Retz W, Blocher D et al. Wender Utah rating scale. The short-version for the assessment of the attention-deficit hyperactivity disorder in adults. Nervenarzt 2002;73:830–838.
36. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry 1961;4:561–571.
37. 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;24:659–685.
38. Lord C, Risi S, Lambrecht L 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;30:205–223.
39. Lehrl S, Triebig G, Fischer B. Multiple choice vocabulary test MWT as a valid and short test to estimate premorbid intelligence. Acta Neurol Scand 1995;91:335–345.
40. Riedel A, Maier S, Ulbrich M et al. No significant brain volume decreases or increases in adults with high-functioning autism spectrum disorder and above average intelligence: a voxel-based morphometric study. Psychiatry Res 2014;223:67–74.
41. Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 1994;103:247–254.
42. Kreher B, Hennig J, Il'yasov K. DTI&FiberTools: a complete toolbox for DTI calculation, fiber tracking, and combined evaluation. In: Proceeding of ISMRM 14th International Scientific Meeting, Seattle, USA, 2006.
43. Friston K, Ashburner J, Kiebel S, Nichols T, Penny W. Statistical parametric mapping: the analysis of functional brain images. London: Lond Acad, 2007, Vii, 647.
44. Ashburner J. A fast diffeomorphic image registration algorithm. NeuroImage 2007;38:95–113.
45. 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;55:323–326.
46. Shukla DK, Keehn B, Lincoln AJ, Müller R-A. 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;49:1269–1278, 1278-2.
47. Hong S, Ke X, Tang T et al. Detecting abnormalities of corpus callosum connectivity in autism using magnetic resonance imaging and diffusion tensor tractography. Psychiatry Res 2011;194:333–339.
48. Frith C. Is autism a disconnection disorder? Lancet Neurol 2004;3:577.
49. Verhoeven JS, De Cock P, Lagae L, Sunaert S. Neuroimaging of autism. Neuroradiology 2010;52:3–14.
50. Witelson SF. Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. Brain J Neurol 1989;112:799–835.
51. Doron KW, Gazzaniga MS. Neuroimaging techniques offer new perspectives on callosal transfer and interhemispheric communication. Cortex 2008;44:1023–1029.
52. Hofer S, Frahm J. Topography of the human corpus callosum revisited–comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. NeuroImage 2006;32:989–994.
53. Schmitz N, Daly E, Murphy D. Frontal anatomy and reaction time in Autism. Neurosci Lett 2007;412:12–17.
54. Vogt BA, Finch DM, Olson CR. Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb Cortex 1992;2:435–443.
55. 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;17:951–961.
56. Just MA, Cherkassky VL, Keller TA, Minshew NJ. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain J Neurol 2004;127:1811–1821.
57. Ozonoff S, Pennington BF, Rogers SJ. Executive function deficits in high-functioning autistic individuals: relationship to theory of mind. J Child Psychol Psychiatry 1991;32:1081–1105.
58. Sundaram SK, Kumar A, Makki MI, Behen ME, Chugani HT, Chugani DC. Diffusion tensor imaging of frontal lobe in autism spectrum disorder. Cereb Cortex 2008;18:2659–2665.
59. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 2000;4:215–222.
60. Remschmidt H, Kamp-Becker I. Asperger-Syndrom. Heidelberg: Springer; 2006.
61. Allman JM, Tetreault NA, Hakeem AY et al. The von Economo neurons in the frontoinsular and anterior cingulate cortex. Ann NY Acad Sci 2011;1225:59–71.
62. Allman JM, Watson KK, Tetreault NA, Hakeem AY. Intuition and autism: a possible role for Von Economo neurons. Trends Cogn Sci 2005;9:367–373.
63. Haznedar MM, Buchsbaum MS, Metzger M, Solimando A, Spiegel-Cohen J, Hollander E. Anterior cingulate gyrus volume and glucose metabolism in autistic disorder. Am J Psychiatry 1997;154:1047–1050.
64. Nakamura K, Sekine Y, Ouchi Y et al. Brain serotonin and dopamine transporter bindings in adults with high-functioning autism. Arch Gen Psychiatry 2010;67:59–68.
65. Ankenman K, Elgin J, Sullivan K, Vincent L, Bernier R. Nonverbal and verbal cognitive discrepancy profiles in autism spectrum disorders: influence of age and gender. Am J Intellect Dev Disabil 2014;119:84–99.
66. Noriuchi M, Kikuchi Y, Yoshiura T et al. Altered white matter fractional anisotropy and social impairment in children with autism spectrum disorder. Brain Res 2010;1362:141–149.
67. Roine U, Roine T, Salmi J et al. Increased coherence of white matter fiber tract organization in adults with Asperger syndrome: a diffusion tensor imaging study. Autism Res 2013;6:642–650.
68. Kirkovski M, Enticott PG, Maller JJ, Rossell SL, Fitzgerald PB. Diffusion tensor imaging reveals no white matter impairments among adults with autism spectrum disorder. Psychiatry Res Neuroimaging 2015;233:64–72.