Atypical functional connectivity in autism spectrum disorder is associated with disrupted white matter microstructural organisation

Frontiers in Human Neuroscience

Volumn , Issue JUL, 2013, Pages

  McGrath, Jane ^a   Johnson, Katherine ^a,b   O'Hanlon, Erik ^c   Garavan, Hugh ^a,d   Leemans, Alexander ^e   Gallagher, Louise ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d UNIVERSITY OF VERMONT   (United States)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Autism Spectrum Disorders; Constrained spherical deconvolution; Diffusion tractography; Functional connectivity; Mental rotation; Neuroimaging; Structural connectivity; Visuospatial processing

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; AUTISM; BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; CAUDATE NUCLEUS; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CUNEUS; DEPTH PERCEPTION; DIFFUSION WEIGHTED IMAGING; HUMAN; MALE; NERVE TRACT; NEURAL CONNECTIVITY; OCCIPITAL LOBE; PRESCHOOL CHILD; SCHOOL CHILD; THALAMUS; TRACTOGRAPHY; UNCUS; WHITE MATTER LESION;

EID: 84933672749     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00434     Document Type: Article

References (74)

1. Agam, Y., Joseph, R.M., Barton, J.J., and Manoach, D.S. (2010). Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders. Neuroimage 52, 336-347.
2. Alexander, A.L., Lee, J.E., Lazar, M., Boudos, R., Dubray, M.B., Oakes, T.R., Miller, J.N., Lu, J., Jeong, E.-K., Mcmahon, W.M., Bigler, E.D., and Lainhart, J.E. (2007). Diffusion tensor imaging of the corpus callosum in Autism. Neuroimage 34, 6173.
3. Alexander, D.C., Barker, G.J., and Arridge, S.R. (2002). Detection and modeling of non-Gaussian apparent diffusion coefficient profiles in human brain data. Magn Reson Med 48, 331-340.
4. Barnea-Goraly, N., Lotspeich, L.J., and Reiss, A.L. (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, 1052-1060.
5. Behrens, T.E., and Sporns, O. (2012). Human connectomics. Curr Opin Neurobiol 22, 144-153.
6. Catani, M., Jones, D.K., Daly, E., Embiricos, N., Deeley, Q., Pugliese, L., Curran, S., Robertson, D., and Murphy, D.G. (2008). Altered cerebellar feedback projections in Asperger syndrome. NeuroImage 41, 1184-1191.
7. Chang, L.C., Jones, D.K., and Pierpaoli, C. (2005). RESTORE: robust estimation of tensors by outlier rejection. Magn Reson Med 53, 1088-1095.
8. Cheon, K.A., Kim, Y.S., Oh, S.H., Park, S.Y., Yoon, H.W., Herrington, J., Nair, A., Koh, Y.J., Jang, D.P., Kim, Y.B., Leventhal, B.L., Cho, Z.H., Castellanos, F.X., and Schultz, R.T. (2011). Involvement of the anterior thalamic radiation in boys with high functioning autism spectrum disorders: a Diffusion Tensor Imaging study. Brain Res 1417, 77-86.
9. Cherkassky, V.L., Kana, R.K., Keller, T.A., and Just, M.A. (2006). Functional connectivity in a baseline resting-state network in autism. NeuroReport 17, 1687-1690.
10. Cheung, C., Chua, S.E., Cheung, V., Khong, P.L., Tai, K.S., Wong, T.K., Ho, T.P., and Mcalonan, G.M. (2009). White matter fractional anisotrophy differences and correlates of diagnostic symptoms in autism. J Child Psychol Psychiatry 50, 1102-1112.
11. Damarla, S.R., Keller, T.A., Kana, R.K., Cherkassky, V.L., Williams, D.L., Minshew, N.J., and Just, M.A. (2010). Cortical underconnectivity coupled with preserved visuospatial cognition in autism: Evidence from an fMRI study of an embedded figures task. Autism Res 3, 273-279.
12. Doidge, N. (2007). The Brain That Changes Itself: Stories of Personal Triumph from the Frontiers of Brain Science. James H. Silberman.
13. Frank, L.R. (2002). Characterization of anisotropy in high angular resolution diffusion-weighted MRI. Magn Reson Med 47, 1083-1099.
14. Friston, K.J., Buechel, C., Fink, G.R., Morris, J., Rolls, E., and Dolan, R.J. (1997). Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6, 218-229.
15. Greicius, M.D., Supekar, K., Menon, V., and Dougherty, R.F. (2009). Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19, 72-78.
16. Hagmann, P., Cammoun, L., Gigandet, X., Meuli, R., Honey, C.J., Wedeen, V.J., and Sporns, O. (2008). Mapping the structural core of human cerebral cortex. PLoS Biol 6, e159.
17. Hermundstad, A.M., Bassett, D.S., Brown, K.S., Aminoff, E.M., Clewett, D., Freeman, S., Frithsen, A., Johnson, A., Tipper, C.M., Miller, M.B., Grafton, S.T., and Carlson, J.M. (2013). Structural foundations of resting-state and task-based functional connectivity in the human brain. Proc Natl Acad Sci U S A 110, 61696174.
18. Honey, C.J., Sporns, O., Cammoun, L., Gigandet, X., Thiran, J.P., Meuli, R., and Hagmann, P. (2009). Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci U S A 106, 2035-2040.
19. Hong, S., Ke, X., Tang, T., Hang, Y., Chu, K., Huang, H., Ruan, Z., Lu, Z., Tao, G., and Liu, Y. (2011). Detecting abnormalities of corpus callosum connectivity in autism using magnetic resonance imaging and diffusion tensor tractography. Psychiatry Res 194, 333-339.
20. Jeurissen, B., Leemans, A., Jones, D.K., Tournier, J.D., and Sijbers, J. (2011). Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution. Hum Brain Mapp 32, 461-479.
21. Jeurissen, B., Leemans, A., Tournier, J.D., Jones, D.K., and Sijbers, J. (2012). Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion MRI. Human Brain Mapping In Press.
22. Johnston, J.M., Vaishnavi, S.N., Smyth, M.D., Zhang, D., He, B.J., Zempel, J.M., Shimony, J.S., Snyder, A.Z., and Raichle, M.E. (2008). Loss of resting interhemispheric functional connectivity after complete section of the corpus callosum. J Neurosci 28, 6453-6458.
23. Jones, D.K., and Cercignani, M. (2010). Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed 23, 803-820.
24. Jones, D.K., and Leemans, A. (2011). Diffusion tensor imaging. Methods Mol Biol 711, 127-144.
25. Jou, R.J., Jackowski, A.P., Papademetris, X., Rajeevan, N., Staib, L.H., and Volkmar, F.R. (2011). Diffusion tensor imaging in autism spectrum disorders: preliminary evidence of abnormal neural connectivity. Aust NZJ Psychiatry 45, 153-162.
26. Just, M.A., Cherkassky, V.L., Keller, T.A., Kana, R.K., and Minshew, N.J. (2007). Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cereb Cortex 17, 951-961.
27. Kana, R.K., Keller, T.A., Cherkassky, V.L., Minshew, N.J., and Just, M.A. (2006). Sentence comprehension in autism: thinking in pictures with decreased functional connectivity. Brain 129, 2484-2493.
28. Keller, T.A., and Just, M.A. (2009). Altering cortical connectivity: remediation-induced changes in the white matter of poor readers. Neuron 64, 624-631.
29. Klein, S., Staring, M., Murphy, K., Viergever, M.A., and Pluim, J.P. (2010). elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imaging 29, 196-205.
30. Koch, M.A., Norris, D.G., and Hund-Georgiadis, M. (2002). An investigation of functional and anatomical connectivity using magnetic resonance imaging. NeuroImage 16, 241-250.
31. Kumar, A., Sundaram, S.K., Sivaswamy, L., Behen, M.E., Makki, M.I., Ager, J., Janisse, J., Chugani, H.T., and Chugani, D.C. (2010). Alterations in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. Cereb Cortex 20, 2103-2113.
32. Lee, P., Foss-Feig, J., Henderson, J., Kenworthy, L., Gilotty, L., Gaillard, W., and Vaidya, C. (2007). Atypical neural substrates of Embedded Figures Task performance in children with Autism Spectrum Disorder. Neuroimage 38, 184193.
33. Leemans, A., Jeurissen, B., Sijbers, J., and Jones, D.K. (2009). ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. Proceedings of the 17th Annual Meeting of International Society for Magnetic Resonance in Medicine, Hawaii, USA., 3536.
34. Leemans, A., and Jones, D.K. (2009). The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61, 1336-1349.
35. Lord, C., Risi, S., Lambrecht, L., Cook, E.H., Jr., Leventhal, B.L., Dilavore, P.C., Pickles, A., and Rutter, M. (2000). The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism & Developmental Disorders 30, 205-223.
36. Lord, C., Rutter, M., and Le Couteur, A. (1994). Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism & Developmental Disorders 24, 659-685.
37. Lowe, M.J., Beall, E.B., Sakaie, K.E., Koenig, K.A., Stone, L., Marrie, R.A., and Phillips, M.D. (2008). Resting state sensorimotor functional connectivity in multiple sclerosis inversely correlates with transcallosal motor pathway transverse diffusivity. Hum Brain Mapp 29, 818-827.
38. Manjaly, Z.M., Bruning, N., Neufang, S., Stephan, K.E., Brieber, S., Marshall, J.C., Kamp-Becker, I., Remschmidt, H., Herpertz-Dahlmann, B., Konrad, K., and Fink, G.R. (2007). Neurophysiological correlates of relatively enhanced local visual search in autistic adolescents. NeuroImage 35, 283-291.
39. Margulies, D.S., Vincent, J.L., Kelly, C., Lohmann, G., Uddin, L.Q., Biswal, B.B., Villringer, A., Castellanos, F.X., Milham, M.P., and Petrides, M. (2009). Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106, 20069-20074.
40. Mason, R.A., Williams, D.L., Kana, R.K., Minshew, N., and Just, M.A. (2008). Theory of Mind disruption and recruitment of the right hemisphere during narrative comprehension in autism. Neuropsychologia 46, 269-280.
41. McGrath, J., Johnson, K., Ecker, C., O'hanlon, E., Gill, M., Gallagher, L., and Garavan, H. (2012). Atypical Visuospatial Processing in Autism: Insights from Functional Connectivity Analysis. Autism Res 5, 314-330.
42. McGrath, J., Johnson, K., O'hanlon, E., Garavan, H., Gallagher, L., and Leemans, A. (2013). White Matter and Visuospatial Processing in Autism: A Constrained Spherical Deconvolution Tractography Study. Autism Res.
43. Metzler-Baddeley, C.M., Hunt, S., Jones, D.K., Leemans, A., Aggleton, J.P., and O'sullivan, M.J. (2012). Temporal association tracts and the breakdown of episodic memory in mild cognitive impairment. Neurology 79, 2233-2240.
44. Monk, C.S., Peltier, S.J., Wiggins, J.L., Weng, S.-J., Carrasco, M., Risi, S., and Lord, C. (2009). Abnormalities of intrinsic functional connectivity in autism spectrum disorders. NeuroImage 47, 764-772.
45. Noriuchi, M., Kikuchi, Y., Yoshiura, T., Kira, R., Shigeto, H., Hara, T., Tobimatsu, S., and Kamio, Y. (2010). Altered white matter fractional anisotropy and social impairment in children with autism spectrum disorder. Brain Res 1362, 141149.
46. Penades, R., Pujol, N., Catalan, R., Massana, G., Rametti, G., Garcia-Rizo, C., Bargallo, N., Gasto, C., Bernardo, M., and Junque, C. (2013). Brain Effects of Cognitive Remediation Therapy in Schizophrenia: A Structural and Functional Neuroimaging Study. Biol Psychiatry.
47. Pluim, J.P., Maintz, J.B., and Viergever, M.A. (2003). Mutual-information-based registration of medical images: a survey. IEEE Trans Med Imaging 22, 9861004.
48. Poustka, L., Jennen-Steinmetz, C., Henze, R., Vomstein, K., Haffner, J., and Sieltjes, B. (2011). Fronto-temporal disconnectivity and symptom severity in children with autism spectrum disorder. World J Biol Psychiatry 13, 269-280.
49. Pruessmann, K.P., Weiger, M., Scheidegger, M.B., and Boesiger, P. (1999). SENSE: sensitivity encoding for fast MRI. Magn Reson Med 42, 952-962.
50. Quigley, M., Cordes, D., Turski, P., Moritz, C., Haughton, V., Seth, R., and Meyerand, M.E. (2003). Role of the corpus callosum in functional connectivity. AJNR Am J Neuroradiol 24, 208-212.
51. Reijmer, Y.D., Brundel, M., De Bresser, J., Kappelle, L.J., Leemans, A., and Biessels, G.J. (2013). Microstructural White Matter Abnormalities and Cognitive Functioning in Type 2 Diabetes: A diffusion tensor imaging study. Diabetes Care 36, 137-144.
52. Reijmer, Y.D., Leemans, A., Heringa, S.M., Wielaard, I., Jeurissen, B., Koek, H.L., and Biessels, G.J. (2012). Improved Sensitivity to Cerebral White Matter Abnormalities in Alzheimer's Disease with Spherical Deconvolution Based Tractography. PLoS one 7, e44074.
53. Sahyoun, C.P., Belliveau, J.W., and Mody, M. (2010). White matter integrity and pictorial reasoning in high-functioning children with autism. Brain Cogn 73, 180-188.
54. Sattler, J.M. (1992). Assessement of Children. Revised and Updated Third Edition (Table L-12). San Diego: Sattler, Jerome M.
55. Scholz, J., Klein, M.C., Behrens, T.E., and Johansen-Berg, H. (2009). Training induces changes in white-matter architecture. Nat Neurosci 12, 1370-1371.
56. Shukla, D.K., Keehn, B., Lincoln, A.J., and Muller, R.A. (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, 1269-1278, 1278 e1261-1262.
57. Skudlarski, P., Jagannathan, K., Calhoun, V.D., Hampson, M., Skudlarska, B.A., and Pearlson, G. (2008). Measuring brain connectivity: diffusion tensor imaging validates resting state temporal correlations. NeuroImage 43, 554-561.
58. Sundaram, S.K., Kumar, A., Makki, M.I., Behen, M.E., Chugani, H.T., and Chugani, D.C. (2008). Diffusion Tensor Imaging of Frontal Lobe in Autism Spectrum Disorder. Cereb. Cortex 18, 2659-2665.
59. Thakkar, K., Polli, F., Joseph, R., Tuch, D., Hadjikhani, N., Barton, J., and Manoach, D. (2008). Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD). Brain 131, 2464-2478.
60. Thomas, C., Humphreys, K., Jung, K.J., Minshew, N., and Behrmann, M. (2011). The anatomy of the callosal and visual-association pathways in high-functioning autism: a DTI tractography study. Cortex 47, 863-873.
61. Tournier, J.D., Calamante, F., and Connelly, A. (2007). Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage 35, 1459-1472.
62. Tournier, J.D., Calamante, F., Gadian, D.G., and Connelly, A. (2004). Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. NeuroImage 23, 1176-1185.
63. Tournier, J.D., Mori, S., and Leemans, A. (2011). Diffusion tensor imaging and beyond. Magn Reson Med 65, 1532-1556.
64. Tournier, J.D., Yeh, C.H., Calamante, F., Cho, K.H., Connelly, A., and Lin, C.P. (2008). Resolving crossing fibres using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. NeuroImage 42, 617-625.
65. Van Den Heuvel, M., Mandl, R., Luigjes, J., and Hulshoff Pol, H. (2008). Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J Neurosci 28, 10844-10851.
66. Vincent, J.L., Patel, G.H., Fox, M.D., Snyder, A.Z., Baker, J.T., Van Essen, D.C., Zempel, J.M., Snyder, L.H., Corbetta, M., and Raichle, M.E. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature 447, 83-86.
67. Vos, S.B., Jones, D.K., Jeurissen, B., Viergever, M.A., and Leemans, A. (2012). The influence of complex white matter architecture on the mean diffusivity in diffusion tensor MRI of the human brain. NeuroImage 59, 2208-2216.
68. Vos, S.B., Jones, D.K., Viergever, M.A., and Leemans, A. (2011). Partial volume effect as a hidden covariate in DTI analyses. NeuroImage 55, 1566-1576.
69. Wechsler, D. (1997). WAIS-II administration and scoring manual. San Antonio, TX: Psychological Corporation.
70. Wechsler, D. (2004). The Wechsler intelligence scale for children-fourth edition. London: Pearson Assessment.
71. Wedeen, V.J., Reese, T.G., Tuch, D.S., Weigel, M.R., Dou, R.M., Weiskoff, R.M., Chessler, D., Cerebral, M.F.O.S.I., and White Matter with Fourier-Transform Diffusion Mri. Ismrm Proc. 8 (Year). "Mapping fibre orientation spectra in cerebral white matter with Fourier-transform diffusion MRI. ", in: International Society of Magnetic Resonance in Medicine).
72. Wedeen, V.J., Wang, R.P., Schmahmann, J.D., Benner, T., Tseng, W.Y., Dai, G., Pandya, D.N., Hagmann, P., D'arceuil, H., and De Crespigny, A.J. (2008). Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage 41, 1267-1277.
73. Weng, S.J., Wiggins, J.L., Peltier, S.J., Carrasco, M., Risi, S., Lord, C., and Monk, C.S. (2010). Alterations of resting state functional connectivity in the default network in adolescents with autism spectrum disorders. Brain Res 1313, 202214.
74. Westin, C.F., Maier, S.E., Mamata, H., Nabavi, A., Jolesz, F.A., and Kikinis, R. (2002). Processing and visualization for diffusion tensor MRI. Med Image Anal 6, 93-108.