Structural and functional underconnectivity as a negative predictor for language in autism

Human Brain Mapping

Volumn 35, Issue 8, 2014, Pages 3602-3615

  Verly, Marjolein ^a   Verhoeven, Judith ^a   Zink, Inge ^a   Mantini, Dante ^a,b,c   Oudenhove, Lukas Van ^d,e   Lagae, Lieven ^a   Sunaert, Stefan ^a   Rommel, Nathalie ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Arcuate fascicle; Autism spectrum disorder; Diffusion tensor imaging; Functional MRI; Language impairment

Indexed keywords

ADOLESCENT; ARCUATE FASCICULUS; ARTICLE; AUTISM; BRAIN FUNCTION; BRAIN REGION; CLINICAL ARTICLE; CLINICAL EVALUATION OF LANGUAGE FUNDAMENTAL; CONNECTOME; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL UNDERCONNECTIVITY; HUMAN; INTELLIGENCE QUOTIENT; INTELLIGENCE TEST; LANGUAGE ABILITY; LANGUAGE DEVELOPMENT; LANGUAGE DISABILITY; LANGUAGE TEST; MALE; NERVOUS SYSTEM PARAMETERS; NEUROPHYSIOLOGY; PEABODY PICTURE VOCABULARY TEST; PREDICTOR VARIABLE; PRIORITY JOURNAL; RESTING STATE NETWORK; RIGHT HEMISPHERE; STRUCTURAL UNDERCONNECTIVITY; TEMPORAL LOBE; TRACTOGRAPHY; VERBAL INTELLIGENCE QUOTIENT; WECHSLER INTELLIGENCE SCALE; ANISOTROPY; BRAIN; CHILD; LANGUAGE; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; REST;

ADOLESCENT; ANISOTROPY; BRAIN; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; INTELLIGENCE TESTS; LANGUAGE; LANGUAGE TESTS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; REST;

EID: 84903965337     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22424     Document Type: Article

References (78)

1. American Psychiatric Association (2000): Diagnostic and Statistical Manual of Mental Disorders. Washington, DC: American Psychiatric Association.
2. 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 55:323-326.
3. Basser PJ, Mattiello J, LeBihan D (1994): MR diffusion tensor spectroscopy and imaging. Biophys J 66:259-267.
4. Beaulieu C (2002): The basis of anisotropic water diffusion in the nervous system-A technical review. NMR Biomed 15:435-455.
5. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, Webb SJ (2004): Autism and abnormal development of brain connectivity. J Neurosci 24:9228-9231.
6. Benson RR, FitzGerald DB, LeSueur LL, Kennedy DN, Kwong KK, Buchbinder BR, Davis TL, Weisskoff RM, Talavage TM, Logan WJ, Cosgrove GR, Belliveau JW, Rosen BR (1999): Language dominance determined by whole brain functional MRI in patients with brain lesions. Neurology 52:798-809.
7. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995): Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537-541.
8. Boddaert N, Chabane N, Gervais H, Good CD, Bourgeois M, Plumet MH, Barthélémy C, Mouren MC, Artiges E, Samson Y, Brunelle F, Frackowiak RS, Zilbovicius M (2004): Superior temporal sulcus anatomical abnormalities in childhood autism: A voxel-based morphometry MRI study. Neuroimage 23:364-369.
9. Carper RA, Courchesne E (2000): Inverse correlation between frontal lobe and cerebellum sizes in children with autism. Brain 123 (Part 4):836-844.
10. Catani M, Mesulam M (2008): The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state. Cortex 44:953-961.
11. Catani M, Howard RJ, Pajevic S, Jones DK (2002): Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77-94.
12. Catani M, Jones DK, Ffytche DH (2005): Perisylvian language networks of the human brain. Ann Neurol 57:8-16.
13. 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 104:17163-17168.
14. Cherkassky VL, Kana RK, Keller TA, Just MA. (2006): Functional connectivity in a baseline resting-state network in autism. Neuroreport 17:1687-1690.
15. Church JA, Fair DA, Dosenbach NU, Cohen AL, Miezin FM, Petersen SE, Schlaggar BL (2009): Control networks in paediatric Tourette syndrome show immature and anomalous patterns of functional connectivity. Brain 132 (Part 1):225-238.
16. Constantino JN, Davis SA, Todd RD, Schindler MK, Gross MM, Brophy SL, Metzger LM, Shoushtari CS, Splinter R, Reich W (2003): 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 33:427-433.
17. Correia S, Lee SY, Voorn T, Tate DF, Paul RH, Zhang S, Salloway SP, Malloy PF, Laidlaw DH (2008): Quantitative tractography metrics of white matter integrity in diffusion-tensor MRI. Neuroimage 42:568-581.
18. Courchesne E (2004): Brain development in autism: Early overgrowth followed by premature arrest of growth. Ment Retard Dev Disabil Res Rev 10:106-111.
19. Courchesne E, Pierce K (2005): Why the frontal cortex in autism might be talking only to itself: Local over-connectivity but long-distance disconnection. Curr Opin Neurobiol 15:225-230.
20. Courchesne E, Carper R, Akshoomoff N (2003): Evidence of brain overgrowth in the first year of life in autism. JAMA 290:337-344.
21. Courchesne E, Redcay E, Morgan JT, Kennedy DP (2005): Autism at the beginning: Microstructural and growth abnormalities underlying the cognitive and behavioral phenotype of autism. Dev Psychopathol 17:577-597.
22. Courchesne E, Pierce K, Schumann CM, Redcay E, Buckwalter JA, Kennedy DP, Morgan J. (2007): Mapping early brain development in autism. Neuron 56:399-413.
23. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF. (2006): Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848-13853.
24. Deco G, Corbetta M (2011): The dynamical balance of the brain at rest. Neuroscientist 17:107-123.
25. Dubois J, Hertz-Pannier L, Cachia A, Mangin JF, Le Bihan D, Dehaene-Lambertz G (2009): Structural asymmetries in the infant language and sensori-motor networks. Cereb Cortex 19:414-423.
26. Dunn LM, Dunn ML, editors (2005): Peabody Picture Vocabulary Test-III-NL. Amsterdam: Pearson Assessment and Information B.V.
27. Ebisch SJ, Gallese V, Willems RM, Mantini D, Groen WB, Romani GL, Buitelaar JK, Bekkering H (2011): Altered intrinsic functional connectivity of anterior and posterior insula regions in high-functioning participants with autism spectrum disorder. Hum Brain Mapp 32:1013-1028.
28. Eluvathingal TJ, Hasan KM, Kramer L, Fletcher JM, Ewing-Cobbs L (2007): Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. Cereb Cortex 17:2760-2768.
29. Fine J, Bartolucci G, Szatmari P, Ginsberg G (1994): Cohesive discourse in pervasive developmental disorders. J Autism Dev Disord 24:315-329.
30. 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 51:1117-1125.
31. Friederici AD, Fiebach CJ, Schlesewsky M, Bornkessel ID, von Cramon DY (2006): Processing linguistic complexity and grammaticality in the left frontal cortex. Cereb Cortex 16:1709-1717.
32. Friston KJ, Holmes AP, Price CJ, Büchel C, Worsley KJ (1999): Multisubject fMRI studies and conjunction analyses. Neuroimage 10:385-396.
33. Glasser MF, Rilling JK (2008): DTI tractography of the human brain's language pathways. Cereb Cortex 18:2471-2482.
34. Greicius MD, Krasnow B, Reiss AL, Menon V (2003): Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proc Natl Acad Sci USA 100:253-258.
35. Groen WB, Zwiers MP, van der Gaag RJ, Buitelaar JK (2008): The phenotype and neural correlates of language in autism: An integrative review. Neurosci Biobehav Rev 32:1416-1425.
36. Harris GJ, Chabris CF, Clark J, Urban T, Aharon I, Steele S, McGrath L, Condouris K, Tager-Flusberg H (2006): Brain activation during semantic processing in autism spectrum disorders via functional magnetic resonance imaging. Brain Cogn 61:54-68.
37. Herbert MR, Ziegler DA, Deutsch CK, O'Brien LM, Lange N, Bakardjiev A, Hodgson J, Adrien KT, Steele S, Makris N, Kennedy D, Harris GJ, Caviness VS Jr (2003): Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. Brain 126 (Part 5):1182-1192.
38. Herbert MR, Ziegler DA, Deutsch CK, O'Brien LM, Kennedy DN, Filipek PA, Bakardjiev AI, Hodgson J, Takeoka M, Makris N, Caviness VS Jr (2005): Brain asymmetries in autism and developmental language disorder: A nested whole-brain analysis. Brain 128 (Part 1):213-226.
39. Hohnen B, Stevenson J (1999): The structure of genetic influences on general cognitive, language, phonological, and reading abilities. Dev Psychol 35:590-603.
40. Jeurissen B, Leemans A, Jones DK, Tournier JD, Sijbers J (2011): Probabilistic fiber tracking using the residual bootstrap with constrained spherical deconvolution. Hum Brain Mapp 32:461-479.
41. Jones TB, Bandettini PA, Kenworthy L, Case LK, Milleville SC, Martin A, Birn RM (2010): Sources of group differences in functional connectivity: An investigation applied to autism spectrum disorder. Neuroimage 49:401-414.
42. Just MA, Cherkassky VL, Keller TA, Minshew NJ (2004): Cortical activation and synchronization during sentence comprehension in high-functioning autism: Evidence of underconnectivity. Brain 127 (Part 8):1811-1821.
43. Kana RK, Keller TA, Cherkassky VL, Minshew NJ, Just MA (2006): Sentence comprehension in autism: Thinking in pictures with decreased functional connectivity. Brain 129 (Part 9):2484-2493.
44. Keller TA, Kana RK, Just MA (2007): A developmental study of the structural integrity of white matter in autism. Neuroreport 18:23-27.
45. Kennedy DP, Courchesne E (2008): The intrinsic functional organization of the brain is altered in autism. Neuroimage 39:1877-1885.
46. Kjelgaard MM, Tager-Flusberg H (2001): An investigation of language impairment in autism: Implications for genetic subgroups. Lang Cogn Process 16:287-308.
47. Knaus TA, Silver AM, Lindgren KA, Hadjikhani N, Tager-Flusberg H (2008): fMRI activation during a language task in adolescents with ASD. J Int Neuropsychol Soc 14:967-979.
48. 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 112:113-120.
49. Kort W, Schittekatte M, Bosmans M, Compaan EL, Dekker PH, Vermeir G, Verhaeghe P, editors (2005): Handleiding en Verantwoording. Wechsler Intelligence Scale for Children. Amsterdam: Harcourt Publishers.
50. Kort W, Schittekatte M, Compaan E, editors (2008): CELF-4-NL: Clinical Evaluation of Language Fundamentals. Amsterdam: Pearson Assessment and Information B.V.
51. Lebel C, Beaulieu C (2009): Lateralization of the arcuate fasciculus from childhood to adulthood and its relation to cognitive abilities in children. Hum Brain Mapp 30:3563-3573.
52. Leemans A, Jones DK (2009): The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61:13.
53. Leemans A, Jeurissen B, Sijbers J, Jones DK (2009):ExploreDTI: A graphical toolbox for processing, analyzing and visualizing diffusion MR data. In: Paper presented at the 17th Annual Meeting of Proceedings of the International Society for Magnetic Resonance in Medicine, Hawaii, USA.
54. Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS Jr, Pandya DN (2005): Segmentation of subcomponents within the superior longitudinal fascicle in humans: A quantitative, in vivo, DT-MRI study. Cereb Cortex 15:854-869.
55. Mizuno A, Villalobos ME, Davies MM, Dahl BC, Müller RA (2006): Partially enhanced thalamocortical functional connectivity in autism. Brain Res 1104:160-174.
56. 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 33:1720-1725.
57. Noonan SK, Haist F, Müller RA (2009): Aberrant functional connectivity in autism: Evidence from low-frequency BOLD signal fluctuations. Brain Res 1262:48-63.
58. Oldfield R (1971): The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9:97-113.
59. Parker GJ, Luzzi S, Alexander DC, Wheeler-Kingshott CA, Ciccarelli O, Lambon Ralph MA. (2005): Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage 24:656-666.
60. Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME (1988): Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature 331:585-589.
61. Powell HW, Parker GJ, Alexander DC, Symms MR, Boulby PA, Wheeler-Kingshott CA, Barker GJ, Noppeney U, Koepp MJ, Duncan JS (2006): Hemispheric asymmetries in language-related pathways: A combined functional MRI and tractography study. Neuroimage 32:388-399.
62. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012): Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142-2154.
63. Rutter M, Le Couteur A, Lord C (2003): Social Communication Questionnaire. Los Angeles, CA: Western Psychological Services.
64. Shih P, Shen M, Ottl B, Keehn B, Gaffrey MS, Müller RA (2010): Atypical network connectivity for imitation in autism spectrum disorder. Neuropsychologia 48:2931-2939.
65. Tournier JD, Yeh CH, Calamante F, Cho KH, Connelly A, Lin CP (2008): Resolving crossing fibres using constrained spherical deconvolution: Validation using diffusion-weighted imaging phantom data. Neuroimage 42:617-625.
66. Turner KC, Frost L, Linsenbardt D, McIlroy JR, Müller RA (2006): Atypically diffuse functional connectivity between caudate nuclei and cerebral cortex in autism. Behav Brain Funct 2:34.
67. Verhoeven JS, De Cock P, Lagae L, Sunaert S (2010): Neuroimaging of autism. Neuroradiology 52:3-14.
68. 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 22:2263-2271.
69. Vernooij MW, Smits M, Wielopolski PA, Houston GC, Krestin GP, van der Lugt A (2007): Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: A combined fMRI and DTI study. Neuroimage 35:1064-1076.
70. Villalobos ME, Mizuno A, Dahl BC, Kemmotsu N, Müller RA (2005): Reduced functional connectivity between V1 and inferior frontal cortex associated with visuomotor performance in autism. Neuroimage 25:916-925.
71. Vos SB, Jones DK, Viergever MA, Leemans A (2011): Partial volume effect as a hidden covariate in DTI analyses. Neuroimage 55:1566-1576.
72. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl P, Mori S (2007): Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36:630-644.
73. Wan CY, Marchina S, Norton A, Schlaug G (2012): Atypical hemispheric asymmetry in the arcuate fasciculus of completely nonverbal children with autism. Ann NY Acad Sci 1252:332-337.
74. 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 41:1267-1277.
75. Weissenbacher A, Kasess C, Gerstl F, Lanzenberger R, Moser E, Windischberger C (2009): Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies. Neuroimage 47:1408-1416.
76. Weng SJ, Wiggins JL, Peltier SJ, Carrasco M, Risi S, Lord C, Monk CS (2010): Alterations of resting state functional connectivity in the default network in adolescents with autism spectrum disorders. Brain Res 1313:202-214.
77. Wicker B, Fonlupt P, Hubert B, Tardif C, Gepner B, Deruelle C (2008): Abnormal cerebral effective connectivity during explicit emotional processing in adults with autism spectrum disorder. Soc Cogn Affect Neurosci 3:135-143.
78. Williams D, Botting N, Boucher J (2008): Language in autism and specific language impairment: Where are the links? Psychol Bull 134:944-963.