Disrupted network architecture of the resting brain in attention-deficit/hyperactivity disorder

Human Brain Mapping

Volumn 35, Issue 9, 2014, Pages 4693-4705

  Sripada, Chandra ^a   Kessler, Daniel ^a   Fang, Yu ^a   Welsh, Robert ^a,b   Prem Kumar, Krishan ^a   Angstadt, Michael ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

ADHD 200; Attention deficit hyperactivity disorder; Connectomics; Default network; Frontoparietal network; Functional magnetic resonance imaging; Resting state connectivity; Ventral attention network

Indexed keywords

ADOLESCENT; ATTENTION DEFICIT DISORDER; BRAIN; BRAIN MAPPING; CHILD; CLINICAL TRIAL; CONNECTOME; HEMISPHERIC DOMINANCE; HUMAN; MULTICENTER STUDY; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; REST; THREE DIMENSIONAL IMAGING;

ADOLESCENT; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; BRAIN; BRAIN MAPPING; CHILD; CONNECTOME; FUNCTIONAL LATERALITY; HUMANS; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; NEURAL PATHWAYS; REST;

EID: 84904515849     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22504     Document Type: Article

References (80)

1. American Psychiatric Association, American Psychiatric Association, DSM-5 Task Force (2013): Diagnostic and Statistical Manual of Mental Disorders: DSM-5. Arlington, VA: American Psychiatric Association.
2. Amodio DM, Frith CD (2006): Meeting of minds: The medial frontal cortex and social cognition. Nat Rev Neurosci 7:268-277.
3. Anderson JS, Ferguson MA, Lopez-Larson M, Yurgelun-Todd D (2011): Connectivity gradients between the default mode and attention control networks. Brain Connect 1:147-157.
4. ADHD-200 Consortium (2012): The ADHD-200 Consortium: A model to advance the translational potential of neuroimaging in clinical neuroscience. Front Syst Neurosci 62.
5. Aron AR, Poldrack RA (2005): The cognitive neuroscience of response inhibition: Relevance for genetic research in attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1285-1292.
6. Aron AR, Robbins TW, Poldrack RA (2004): Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170-177.
7. Ashburner J (2007): A fast diffeomorphic image registration algorithm. Neuroimage 38:95-113.
8. Baving L, Laucht M, Schmidt MH (1999): Atypical frontal brain activation in ADHD: Preschool and elementary school boys and girls. J Am Acad Child Adolesc Psychiatry 38:1363-1371.
9. Behzadi Y, Restom K, Liau J, Liu TT (2007): A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37:90-101.
10. Benjamini Y, Hochberg Y (1995): Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289-300.
11. Biswal BB et al. (2010): Toward discovery science of human brain function. Proc Natl Acad Sci 107:4734-4739.
12. Bressler SL, Menon V (2010): Large-scale brain networks in cognition: Emerging methods and principles. Trends Cogn Sci 14:277-290.
13. Buckner RL, Andrews-Hanna JR, Schacter DL (2008): The Brain's Default Network. Ann N Y Acad Sci 1124:1-38.
14. Bullmore E, Brammer M, Harvey I, Ron M (1995): Against the laterality index as a measure of cerebral asymmetry. Psychiatry Res Neuroimaging 61:121-124.
15. Bush G (2009): Attention-deficit/hyperactivity disorder and attention networks. Neuropsychopharmacology 35:278-300.
16. Bush G, Frazier JA, Rauch SL, Seidman LJ, Whalen PJ, Jenike MA, Rosen BR, Biederman J (1999): Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting stroop. Biol Psychiatry 45:1542-1552.
17. Carter CS, Krener P, Chaderjian M, Northcutt C, Wolfe V (1995): Asymmetrical visual-spatial attentional performance in ADHD: Evidence for a right hemispheric deficit. Biol Psychiatry 37:789-797.
18. Casey BJ, Castellanos FX, Giedd JN, Marsh WL, Hamburger SD, Schubert AB, Vauss YC, Vaituzis AC, Dickstein DP, Sarfatti SE, Rapoport JL (1997): Implication of right frontostriatal circuitry in response inhibition and attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 36:374-383.
19. Castellanos FX, Giedd JN, Eckburg P, Marsh WL, Vaituzis AC, Kaysen D, Hamburger SD, Rapoport JL (1994): Quantitative morphology of the caudate nucleus in attention deficit hyperactivity disorder. Am J Psychiatry 151:1791-1796.
20. Castellanos FX, Giedd JN, Marsh WL, Hamburger SD, Catherine A, Dickstein DP, Sarfatti SE, Vauss YC, Snell JW, Lange N, Kaysen D, Krain AL, Ritchie GF, Rajapakse JC, Rapoport JL (1996): Quantitative brain magnetic resonance imaging in attention-deficit hyperactivity disorder. Arch Gen Psychiatry 53:607-616.
21. Castellanos FX, Margulies DS, Kelly C, Uddin LQ, Ghaffari M, Kirsch A, Shaw D, Shehzad Z, Di Martino A, Biswal B, Sonuga-Barke EJS, Rotrosen J, Adler LA, Milham MP (2008): Cingulate-precuneus interactions: A new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biol Psychiatry 63:332-337.
22. Castellanos FX, Proal E (2012): Large-scale brain systems in ADHD: Beyond the prefrontal-striatal model. Trends Cogn Sci 16:17-26.
23. Corbetta M, Shulman GL (2002): Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201-215.
24. Corbetta M, Shulman GL (2011): Spatial neglect and attention networks. Annu Rev Neurosci 34:569-599.
25. Cortese S, Imperati D, Zhou J, Proal E, Klein RG, Mannuzza S, Ramos-Olazagasti MA, Milham MP, Kelly C, Castellanos FX (2013): White matter alterations at 33-year follow-up in adults with childhood attention-deficit/hyperactivity disorder. Biol Psychiatry 74:591-598.
26. Cortese S, Kelly C, Chabernaud C, Proal E, Di Martino A, Milham MP, Castellanos FX (2012): Toward systems neuroscience of ADHD: A meta-analysis of 55 fMRI studies. Am J Psychiatry 169:1038-1055.
27. Damoiseaux JS, Rombouts S a. RB, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006): Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci 103:13848-13853.
28. Dang LC, O'Neil JP, Jagust WJ (2012): Dopamine supports coupling of attention-related networks. J Neurosci 32:9582-9587.
29. Depue BE, Burgess GC, Willcutt EG, Ruzic L, Banich MT (2010): Inhibitory control of memory retrieval and motor processing associated with the right lateral prefrontal cortex: Evidence from deficits in individuals with ADHD. Neuropsychologia 48:3909-3917.
30. Di Martino A, Zuo X-N, Kelly C, Grzadzinski R, Mennes M, Schvarcz A, Rodman J, Lord C, Castellanos FX, Milham MP (2013): Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder. Biol Psychiatry 74:623-632. Available at: http://www.sciencedirect.com/science/article/pii/S0006322313001765. Accessed April 9, 2013.
31. Downar J, Crawley AP, Mikulis DJ, Davis KD (2000): A multimodal cortical network for the detection of changes in the sensory environment. Nat Neurosci 3:277-283.
32. Eckert MA, Menon V, Walczak A, Ahlstrom J, Denslow S, Horwitz A, Dubno JR (2009): At the heart of the ventral attention system: The right anterior insula. Hum Brain Mapp 30:2530-2541.
33. El-Sayed E, Larsson J-O, Persson H, Santosh P, Rydelius P-A (2003): "Maturational lag" hypothesis of attention deficit hyperactivity disorder: An update. Acta Pædiatrica 92:776-784.
34. Fair DA, Cohen AL, Dosenbach NUF, Church JA, Miezin FM, Barch DM, Raichle ME, Petersen SE, Schlaggar BL (2008): The maturing architecture of the brain's default network. Proc Natl Acad Sci 105:4028-4032.
35. Fair DA, Nigg JT, Iyer S, Bathula D, Mills KL, Dosenbach NUF, Schlaggar BL, Mennes M, Dickstein DP, Martino AD, Kennedy DN, Kelly C, Luna B, Schweitzer JB, Velanova K, 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 6:80.
36. Fair DA, Posner J, Nagel BJ, Bathula D, Dias TGC, Mills KL, 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.
37. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005): The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673-9678.
38. Freedman D, Lane D (1983): A nonstochastic interpretation of reported significance levels. J Bus Econ Stat 1:292-298.
39. Gogtay N, Giedd J (2002): Brain development in healthy, hyperactive, and psychotic children. Arch Neurol 59:1244-1248.
40. Good P (2000): Permutation Tests: A Practical Guide to Resampling Methods for Testing Hypotheses, 2nd ed. New York: Springer.
41. Hamilton JP, Furman DJ, Chang C, Thomason ME, Dennis E, Gotlib IH (2011): Default-mode and task-positive network activity in major depressive disorder: Implications for adaptive and maladaptive rumination. Biol Psychiatry 70:327-333.
42. Harpin VA (2005): The effect of ADHD on the life of an individual, their family, and community from preschool to adult life. Arch Child 90 Suppl 1:i2-7.
43. Helps S, James C, Debener S, Karl A, Sonuga-Barke EJS (2008): Very low frequency EEG oscillations and the resting brain in young adults: A preliminary study of localisation, stability and association with symptoms of inattention. J Neural Transm 115:279-285.
44. Kessler RC, Adler L, Barkley R, Biederman J, Conners CK, Demler O, Faraone SV, Greenhill LL, Howes MJ, Secnik K, Spencer T, Ustun TB, Walters EE, Zaslavsky AM (2006): The prevalence and correlates of adult ADHD in the United States: Results from the National Comorbidity Survey Replication. Am J Psychiatry 163:716-723.
45. Kim B-N, Lee J-S, Shin M-S, Cho S-C, Lee D-S (2002): Regional cerebral perfusion abnormalities in attention deficit/hyperactivity disorder. Statistical parametric mapping analysis. Eur Arch Psychiatry Clin Neurosci 252:219-225.
46. Konrad K, Eickhoff SB (2010): Is the ADHD brain wired differently? A review on structural and functional connectivity in attention deficit hyperactivity disorder. Hum Brain Mapp 31:904-916.
47. Laird AR, Fox PM, Eickhoff SB, Turner JA, Ray KL, McKay DR, Glahn DC, Beckmann CF, Smith SM, Fox PT (2011): Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci 23:4022-4037.
48. McKiernan KA, Kaufman JN, Kucera-Thompson J, Binder JR (2003): A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. J Cogn Neurosci 15:394-408.
49. Menon V (2011): Large-scale brain networks and psychopathology: A unifying triple network model. Trends Cogn Sci 15:483-506.
50. Menon V, Uddin LQ (2010): Saliency, switching, attention and control: A network model of insula function. Brain Struct Funct 214:655-667.
51. Nigg JT, Swanson JM, Hinshaw SP (1997): Covert visual spatial attention in boys with attention deficit hyperactivity disorder: Lateral effects, methylphenidate response and results for parents. Neuropsychologia 35:165-176.
52. Polanczyk G, Rohde LA (2007): Epidemiology of attention-deficit/hyperactivity disorder across the lifespan. Curr Opin Psychiatry 20:386-392.
53. 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.
54. 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.
55. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001): A default mode of brain function. Proc Natl Acad Sci 98:676-682.
56. Reid HM, Norvilitis JM (2000): Evidence for anomalous lateralization across domain in ADHD children as well as adults identified with the Wender Utah rating scale. J Psychiatr Res 34:311-316.
57. Rubia K, Halari R, Cubillo A, Smith AB, Mohammad A-M, Brammer M, Taylor E (2011): Methylphenidate normalizes fronto-striatal underactivation during interference inhibition in medication-naïve boys with attention-deficit hyperactivity disorder. Neuropsychopharmacology 36:1575-1586.
58. Rubia K, Overmeyer S, Taylor E, Brammer M R C, Simmons A, Bullmore ET (1999): Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: A study with functional MRI. Am J Psychiatry 156:891-896.
59. Rubia K, Smith AB, Brammer MJ, Toone B, Taylor E (2005): Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. Am J Psychiatry 162:1067-1075.
60. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, Greenstein D, Clasen L, Evans A, Giedd J, Rapoport JL (2007): Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci USA 104:19649-19654.
61. Shaw P, Malek M, Watson B, Greenstein D, de Rossi P, Sharp W (2013): Trajectories of cerebral cortical development in childhood and adolescence and adult attention-deficit/hyperactivity disorder. Biol Psychiatry 74:599-606.
62. Shehzad Z, Kelly AMC, Reiss PT, Gee DG, Gotimer K, Uddin LQ, Lee SH, Margulies DS, Roy AK, Biswal BB, Petkova E, Castellanos FX, Milham MP (2009): The resting brain: Unconstrained yet reliable. Cereb Cortex 19:2209-2229.
63. Smith AB, Taylor E, Brammer M, Halari R, Rubia K (2008): Reduced activation in right lateral prefrontal cortex and anterior cingulate gyrus in medication-naïve adolescents with attention deficit hyperactivity disorder during time discrimination. J Child Psychol Psychiatry 49:977-985.
64. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009): Correspondence of the brain's functional architecture during activation and rest. Proc Natl Acad Sci 106:13040-13045.
65. Sonuga-Barke EJS, Castellanos FX (2007): Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis. Neurosci Biobehav Rev 31:977-986.
66. Sporns O, Chialvo DR, Kaiser M, Hilgetag CC (2004): Organization, development and function of complex brain networks. Trends Cogn Sci 8:418-425.
67. Sridharan D, Levitin DJ, Menon V (2008): A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci USA 105:12569-12574.
68. Sripada C, Angstadt M, Kessler D, Phan KL, Liberzon I, Evans GW, Welsh R, Kim P, Swain JE (2014): Volitional regulation of emotions produces distributed alterations in connectivity between visual, attention control, and default networks. Neuroimage 89:110-121.
69. Sripada C, Kessler D, Angstadt M (under review): Lag in maturation of the brain's intrinsic functional architecture in ADHD.
70. Sripada CS, Kessler D, Welsh R, Angstadt M, Liberzon I, Phan KL, Scott C (2013): Distributed effects of methylphenidate on the network structure of the resting brain: A connectomic pattern classification analysis. Neuroimage 81:213-221.
71. Sripada RK, King AP, Welsh RC, Garfinkel SN, Wang X, Sripada C, Liberzon I (2012): Neural dysregulation in posttraumatic stress disorder: Evidence for disrupted equilibrium between salience and default mode brain networks. Psychosom Med 74:904-911.
72. Tian 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.
73. Tomasi D, Volkow ND (2012): Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 71:443-450.
74. Tu P-C, Lee Y-C, Chen Y-S, Li C-T, Su T-P (2013): Schizophrenia and the brain's control network: Aberrant within- and between-network connectivity of the frontoparietal network in schizophrenia. Schizophr Res 147:339-347.
75. Uddin LQ, Kelly AMC, Biswal BB, Margulies 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.
76. 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-analysis. Neurosci Biobehav Rev 36:1093-1106.
77. Voeller KK, Heilman KM (1988): Attention deficit disorder in children: A neglect syndrome? Neurology 38:806-808.
78. Weissman DH, Roberts KC, Visscher KM, Woldorff MG (2006): The neural bases of momentary lapses in attention. Nat Neurosci 9:971-978.
79. Xia M, Wang J, He Y (2013): BrainNet Viewer: A network visualization tool for human brain connectomics. PLoS ONE 8:e68910.
80. Yeo BTT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zöllei L, Polimeni JR, Fischl B, Liu H, Buckner RL (2011): The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106:1125-1165.