Structural and functional connectivity of the human brain in autism spectrum disorders and attention-deficit/hyperactivity disorder: A rich club-organization study

Human Brain Mapping

Volumn 35, Issue 12, 2014, Pages 6032-6048

  Ray, Siddharth ^a,b   Miller, Meghan ^c   Karalunas, Sarah ^b   Robertson, Charles ^b   Grayson, David S ^b,d   Cary, Robert P ^b   Hawkey, Elizabeth ^b   Painter, Julia G ^b   Kriz, Daniel ^b   Fombonne, Eric ^b,e   Nigg, Joel T ^b   Fair, Damien A ^b,e  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Attention deficit hyperactivity disorder; Autism spectrum disorders; Connectivity; Diffusion tensor imaging; DW MRI; High angular resolution diffusion imaging; Rich club organization; Rs fMRI

Indexed keywords

ARTICLE; ATTENTION DEFICIT DISORDER; AUTISM; AXON; BRAIN REGION; CHILD; CLINICAL ARTICLE; COMORBIDITY; CONNECTOME; CONTROLLED STUDY; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IMAGE RECONSTRUCTION; NERVE CELL NETWORK; NEUROIMAGING; NEUROPHYSIOLOGY; VOXEL BASED MORPHOMETRY; ADOLESCENT; BRAIN; COHORT ANALYSIS; COMPARATIVE STUDY; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; SIGNAL PROCESSING;

ADOLESCENT; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; BRAIN; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; COHORT STUDIES; CONNECTOME; HUMANS; MAGNETIC RESONANCE IMAGING; NEURAL PATHWAYS; SIGNAL PROCESSING, COMPUTER-ASSISTED;

EID: 84911445194     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22603     Document Type: Article

References (74)

1. American Psychiatric Association (2000): Diagnostic and Statistical Manual of Mental Disorders, 4th ed. Washington, DC: American Psychiatric Press.
2. American Psychiatric Association (2013): Diagnostic and Statistical Manual of Mental Disorders, 5th ed. Arlington, VA: American Psychiatric Press.
3. Anderson JS, Druzgal TJ, Froehlich A, DuBray MB, Lange N, Alexander AL, Abildskov T, Nielsen JA, Cariello AN, Cooperrider JR, Bigler ED, Lainhart JE (2011): Decreased interhemispheric functional connectivity in autism. Cereb Cortex 21:1134-1146.
4. Aoki Y, Abe O, Nippashi Y, Yamasue H (2013): Comparison of white matter integrity between autism spectrum disorder subjects and typically developing individuals: A meta-analysis of diffusion tensor imaging tractography studies. Mol Autism 4.
5. Assaf M, Jagannathan K, Calhoun VD, Miller L, Stevens MC, Sahl R, O'Boyle JG, Schultz RT, Pearlson GD (2010): Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. Neuroimage 53:247-256.
6. Barnes KA, Cohen AL, Power JD, Nelson SM, Dosenbach YB, Miezin FM, Petersen SE, Schlaggar BL (2010): Identifying Basal Ganglia divisions in individuals using resting-state functional connectivity MRI. Front Syst Neurosci 4.
7. Bassett DS, Bullmore ET (2009): Human brain networks in health and disease. Curr Opin Neurol 22:340-347.
8. Boyle CA, Boulet S, Schieve L, Cohen RA, Blumberg SJ, Yeargin-Allsopp M, Visser S, Kogan MD (2011): Trends in the prevalence of developmental disabilities in US children, 1997-2008. Pediatrics 127:1034-1042.
9. Brieber S, Neufang S, Bruning N, Kamp-Becker I, Remschmidt H, Herpertz-Dahlmann B, Fink GR, Konrad K (2007): Structural brain abnormalities in adolescents with autism spectrum disorder and patients with attention deficit/hyperactivity disorder. J Child Psychol Psychiatry 48:1251-1258.
10. Castellanos FX, Tannock R (2002): Neuroscience of attention-deficit/hyperactivity disorder: The search for endophenotypes. Nat Rev Neurosci 3:617-628.
11. Cherkassky VL, Kana RK, Keller TA, Just MA (2006): Functional connectivity in a baseline resting-state network in autism. Neuroreport 17:1687-1690.
12. 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 50:1102-1112.
13. Christakou A, Murphy CM, Chantiluke K, Cubillo AI, Smith AB, Giampietro V, Daly E, Ecker C, Robertson D, MRC AIMS consortium, Murphy DG, Rubia K (2013): Disorder-specific functional abnormalities during sustained attention in youth with Attention Deficit Hyperactivity Disorder (ADHD) and with autism. Mol Psychiatry 18:236-244.
14. Cohen AL, Fair DA, Miezin FM, Dosenbach NU, Schlaggar BL, Petersen SE (2008): Defining functional areas in individual human brains using resting functional connectivity MRI. Neuroimage 41:45-57.
15. Colizza V, Flammini A, Serrano MA, Vespignani A (2006): Detecting rich-club ordering in complex networks. Nat Phys 2:110-115.
16. 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.
17. Di Martino A, Kelly C, Grzadzinski R, Zuo X-N, Mennes M, Mairena MA, Lord C, Castellanos FX, Milham MP (2011): Aberrant striatal functional connectivity in children with autism. Biol Psychiatry 69:847-856.
18. Di Martino A, Yan C-G, Li Q, Denio E, Castellanos FX, Alaerts K, Anderson JS, Assaf M, Bookheimer SY, Dapretto M, Deen B, Delmonte S, Dinstein I, Ertl-Wagner B, Fair DA, Gallagher L, Kennedy DP, Keown CL, Keysers C, Lainhart JE, Lord C, Luna B, Menon V, Minshew NJ, Monk CS, Mueller S, Muller RA, Nebel MB, Nigg JT, O'Hearn K, Pelphrey KA, Peltier SJ, Rudie JD, Sunaert S, Thioux M, Tyszka JM, Uddin LQ, Verhoeven JS, Wenderoth N, Wiggins JL, Mostofsky SH, Milham MP (2014): The autism brain imaging data exchange: Towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol Psychiatry 19:659-667.
19. Dinstein I, Pierce K, Eyler L, Solso S, Malach R, Behrmann M, Courchesne E (2011): Disrupted neural synchronization in toddlers with autism. Neuron 70:1218-1225.
20. Ebisch SJH, 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.
21. Fair DA, Posner J, Nagel BJ, Bathula D, Dias TGC, Mills K, Blythe MS, Giwa A, Schmitt CF, Nigg JT (2010): Atypical default network connectivity in youth with attention-deficit/hyperactivity disorder. Biol Psychiatry 68:1084-1091.
22. Fair DA, Nigg JT, Iyer S, Bathula D, Mills KL, Dosenbach NUF, Schlaggar BL, Mennes M, Gutman D, Bangaru S, Buitelaar JK, Dickstein DP, DiMartino A, Kennedy DN, Kelly C, Luna B, Schweitzer JB, Velanova K, Wang YF, Mostofsky S, Castellanos FX, Milham MP (2013): Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data. Front Syst Neurosci 6.
23. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Essen DCV, Raichle ME (2005): The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673-9678.
24. Gates KM, Molenaar PCM, Iyer SP, Nigg JT, Fair DA (2014): Organizing heterogeneous samples using community detection of GIMME-derived resting state functional networks. PLoS One 9(3):e91322.
25. Geurts HM, Verte S, Oosterlaan J, Roeyers H, Sergeant JA (2004): How specific are executive functioning deficits in attention deficit hyperactivity disorder and autism? J Child Psychol Psychiatry 45:836-854.
26. Gotts SJ, Simmons WK, Milbury LA, Wallace GL, Cox RW, Martin A (2012): Fractionation of social brain circuits in autism spectrum disorders. Brain 135:2711-2725.
27. Grayson DS, Ray S, Carpenter S, Iyer S, Dias TGC, Stevens C, Nigg JT, Fair DA (2014): Structural and functional rich club organization of the brain in children and adults. PLoS One 9:e88297.
28. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008): Mapping the Structural Core of Human Cerebral Cortex. PLoS Biol 6:e159.
29. Hagmann P, Grant PE, Fair DA (2012): MR connectomics: A conceptual framework for studying the developing brain. Front Syst Neurosci 6.
30. Hallquist MN, Hwang K, Luna B (2013): The nuisance of nuisance regression: Spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. Neuroimage 82:208-225.
31. Happé F, Ronald A, Plomin R (2006): Time to give up on a single explanation for autism. Nat Neurosci 9:1218-1220.
32. Karalunas SL, Geurts HM, Konrad K, Bender S, Nigg JT (2014): Annual Research Review: Reaction time variability in ADHD and autism spectrum disorders: Measurement and mechanisms of a proposed trans-diagnostic phenotype. J Child Psychol Psychiatry 55:685-710.
33. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N (1997): Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): Initial reliability and validity data. J Am Acad Child Adoles Psychiatry 36:980-988.
34. Kennedy DP, Courchesne E (2008): The intrinsic functional organization of the brain is altered in autism. Neuroimage 39:1877-1885.
35. Keown CL, Shih P, Nair A, Peterson N, Mulvey ME, Müller R-A (2013): Local functional overconnectivity in posterior brain regions is associated with symptom severity in autism spectrum disorders. Cell Rep 5:567-572.
36. Lord C, Rutter M, LeCouteur A (1994): Autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24:659-685.
37. Lord C, Risi S, Lambrecht L, Cook EH Jr, Leventhal BL, DiLavore PC, Pickles A, Rutter M (2000): The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord 30:205-223.
38. Lynch CJ, Uddin LQ, Supekar K, Khouzam A, Phillips J, Menon V (2013): Default mode network in childhood autism: Posteromedial cortex heterogeneity and relationship with social deficits. Biol Psychiatry 74:212-219.
39. Maslov S, Sneppen K (2002): Specificity and stability in topology of protein networks. Science 296:910-913.
40. Monk CS, Peltier SJ, Wiggins JL, Weng SJ, Carrasco M, Risi S, Lord C (2009): Abnormalities of intrisic functional connectivity in autism spectrum disorders. Neuroimage 47:764-772.
41. Mori S, Zhang J (2006): Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527-539.
42. Mueller S, Keeser D, Samson AC, Kirsch V, Blautzik J, Grothe M, Erat O, Hegenloh M, Coates U, Reiser MF, Hennig-Fast K, Meindl T (2013): Convergent findings of altered functional and structural brain connectivity in individuals with high functioning autism: A multimodal MRI study. PLoS One 8.
43. Musser ED, Hawkey E, Kachan-Liu SS, Lees P, Roullet J-B, Goddard K, Steiner RD, Nigg JT (2014): Shared familial transmission of autism spectrum and attention-deficit/hyperactivity disorders. J Child Psychol Psychiatry 55:819-827.
44. Nagel BJ, Bathula D, Herting M, Schmitt C, Kroenke CD, Fair D, Nigg JT (2011): Altered white matter microstructure in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 50:283-292.
45. Opsahl T, Colizza V, Panzarasa P, Ramasco JJ (2008): Prominence and control: The weighted rich-club effect. Phys Rev Lett 101.
46. Pavuluri MN, Yang S, Kamineni K, Passarotti AM, Srinivasan G, Harral EM, Sweeney JA, Zhou XJ (2009): Diffusion tensor imaging study of white matter fiber tracts in pediatric bipolar disorder and attention-deficit/hyperactivity disorder. Biol Psychiatry 65:586-593.
47. Pennington BF, Ozonoff S (1996): Executive functions and developmental psychopathology. J Child Psychol Psychiatry 37:51-87.
48. Peterson BS, Potenza MN, Wang ZS, Zhu HT, Martin A, Marsh R, Plessen KJ, Yu S (2009): An fMRI study of the effects of psychostimulants on default-mode processing during Stroop task performance in youths with ADHD. Am J Psychiatry 166:1286-1294.
49. Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, Vogel AC, Laumann TO, Miezin FM, Schlaggar BL, Petersen SE (2011): Functional Network Organization of the Human Brain. Neuron 72:665-678.
50. 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.
51. Rommelse NNJ, Franke B, Geurts HM, Hartman CA, Buitelaar JK (2010): Shared heritability of attention-deficit/hyperactivity disorder and autism spectrum disorder. Eur Child Adolesc Psychiatry 19:281-295.
52. Rommelse NNJ, Geurts HM, Franke B, Buitelaar JK, Hartman CA (2011): A review on cognitive and brain endophenotypes that may be common in autism spectrum disorder and attention-deficit/hyperactivity disorder and facilitate the search for pleiotropic genes. Neurosci Biobehav Rev 35:1363-1396.
53. Ronald A, Simanoff E, Kuntsi J, Asherson P, Plomin R (2008): Evidence for overlapping genetic influences on autistic and ADHD behaviours in a community twin#sample. J Child Psychol Psychiatry 49:535-542.
54. Rudie JD, Hernandez LM, Brown JA, Beck-Pancer D, Colich NL, Gorrindo P, Thompson PM, Geschwind DH, Bookheimer SY, Levitt P, Dapretto M (2012): Autism-associated promoter variant in MET impacts functional and structural brain networks. Neuron 75, 904-915.
55. Rudie JD, Brown JA, Beck-Pancer D, Hernandez LM, Dennis EL, Thompson PM, Bookheimer SY, Dapretto M (2013): Altered functional and structural brain network organization in autism. NeuroImage: Clinical 2:79-94.
56. Silk TJ, Vance A, Rinehart N, Bradshaw JL, Cunnington R (2009): White-matter abnormalities in attention deficit hyperactivity disorder: A diffusion tensor imaging study. Hum Brain Mapp 30:2757-2765.
57. Sinzig J, Morsch D, Bruning N, Schmidt MH, Lehmkuhl G (2008): Inhibition, flexibility, working memory and planning in autism spectrum disorders with and without comorbid ADHD-symptoms. Child Adolesc Psychiatry Ment Health 2.
58. Supekar K, Uddin LQ, Khouzam A, Phillips J, Gaillard WD, Kenworthy LE, Yerys BE, Vaidya CJ, Menon V (2013): Brain hyperconnectivity in children with autism and its links to social deficits. Cell Rep 5:738-747.
59. Tien L, Jiang T, Wang Y, Zang Y, He Y, Liang M, Sui M, Cao Q, Hu S, Peng M, Zhuo Y (2006): Altered resting-state functional connectivity patterns of anterior cingulate cortex in adolescents with attention deficit hyperactivity disorder. Neurosci Lett 400:39-43.
60. Tomasi D, Volkow ND (2012): Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 71:443-450.
61. Tuch DS (2004): Q-ball imaging. Magn Reson Med 52:1358-1372.
62. Uddin LQ, Supekar K, Lynch CJ, Khouzam A, Phillips J, Feinstein C, Ryali S, Menon V (2013): Salience network-based classification and prediction of symptom severity in children with autism. JAMA Psychiatry 70, 869-879.
63. Uddin LQ, Kelly AMC, Biswal BB, Marguiles DS, Shehzad Z, Shaw D, Ghaffari M, Rotrosen J, Adler LA, Castellanos FX, Milham MP (2008): Network homogeneity reveals decreased integrity of default-mode network in ADHD. J Neurosci Methods 169:249-254.
64. van den Heuvel MP, Sporns O (2011): Rich-club organization of the human connectome. J Neurosci 31:15775-15786.
65. van den Heuvel MP, Mandl RCW, Stam CJ, Kahn RS, Pol HEH (2010): Aberrant frontal and temporal complex network structure in schizophrenia: A graph theoretical analysis. J Neurosci 30:15915-15926.
66. van den Heuvel MP, Kahn RS, Goñi J, Sporns O (2012): High-cost, high-capacity backbone for global brain communication. Proc Natl Acad Sci USA 109:11372-11377.
67. van Ewijk H, Heslenfeld DJ, Zwiers MP, Buitelaar JK, Oosterlaan J (2012): Diffusion tensor imaging in attention deficit/hyperactivity disorder: A systematic review and meta-anlysis. Neurosci Biobehav Rev 36:1093-1106.
68. van Wijk BCM, Stam CJ, Daffertshofer A (2010): Comparing brain networks of different size and connectivity density using graph theory. PLoS One 5.
69. von dem Hagen EA, Stoyanova RS, Baron-Cohen S, Calder AJ (2012): Reduced functional connectivity within and between 'social' resting state networks in autism spectrum conditions. Soc Cogn Affect Neurosci 8:694-701.
70. Washington SD, Gordon EM, Brar J, Warburton S, Sawyer AT, Wolfe A, Mease-Ference ER, Girton L, Hailu A, Mbwana J, Gaillard WD, Kalbfleisch ML, Vanmeter JW (2014): Dysmaturation of the default mode network in autism. Hum Brain Mapp 35:1284-1296.
71. Wass S (2011): Distortions and disconnections: disrupted brain connectivity in autism. Brain Cogn 75:18-28.
72. Weng S, 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.
73. Zalesky A, Fornito A, Bullmore E (2012): On the use of correlation as a measure of network connectivity. Neuroimage 60:2096-2106.
74. Zhou S, Mondragon RJ (2004): The rich-club phenomenon in the Internet topology. IEEE Comm Lett 8:180-182.