Altered functional brain connectivity in a non-clinical sample of young adults with attention-deficit/hyperactivity disorder

Journal of Neuroscience

Volumn 32, Issue 49, 2012, Pages 17753-17767

  Cocchi, Luca ^a   Bramati, Ivanei E ^b   Zalesky, Andrew ^c   Furukawa, Emi ^d   Fontenelle, Leonardo F ^b,e   Moll, Jorge ^b   Tripp, Gail ^d   Mattos, Paulo ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b D OR INSTITUTE FOR RESEARCH AND EDUCATION IDOR   (Brazil)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; ATTENTION DEFICIT DISORDER; BEHAVIOR; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HUMAN; IMPULSIVENESS; LINGUAL GYRUS; MALE; NERVE CELL NETWORK; OCCIPITAL CORTEX; ORBITAL CORTEX; PRIORITY JOURNAL; TEMPORAL CORTEX;

ADULT; AMYGDALA; ATTENTION; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; BRAIN; CASE-CONTROL STUDIES; CEREBRAL CORTEX; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; IMPULSIVE BEHAVIOR; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; PSYCHIATRIC STATUS RATING SCALES; SELF REPORT;

EID: 84870559098     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3272-12.2012     Document Type: Article

References (86)

1. Ahrendts J, Rüsch N, Wilke M, Philipsen A, Eickhoff SB, Glauche V, Perlov E, Ebert D, Hennig J, van Elst LT (2011) Visual cortex abnormalities in adults with ADHD: a structural MRI study. World J Biol Psychiatry 12: 260-270.CrossRef Medline
2. Amorim P (2000) Validação de entrevista breve para diagnó stico de transtornos mentais. Revista Brasileira de Psiquiatria 22:106-115. CrossRef
3. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, IV-TR Edition. Washington DC: American Psychiatric Association.
4. Bassett DS, Bullmore ET (2009) Human brain networks in health and disease. Curr Opin Neurol 22:340-347.CrossRef Medline
5. Bassett DS, Bullmore E, Verchinski BA, Mattay VS, Weinberger DR, Meyer-Lindenberg A (2008) Hierarchical organization of human cortical networks in health and schizophrenia. J Neurosci 28:9239-9248.CrossRef Medline
6. Biederman J, Newcorn J, Sprich S (1991) Comorbidity of attention deficit hyperactivity disorder with conduct, depressive, anxiety, and other disorders. Am J Psychiatry 148:564-577. Medline
7. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186-198.CrossRef Medline
8. Bush G, Valera EM, Seidman LJ (2005) Functional neuroimaging of attention-deficit/hyperactivity disorder: a review and suggested future directions. Biol Psychiatry 57:1273-1284.CrossRef Medline
9. Cao Q, Zang Y, Sun L, Sui M, Long X, Zou Q, Wang Y (2006) Abnormal neural activity in children with attention deficit hyperactivity disorder: a resting-state functional magnetic resonance imaging study. Neuroreport 17:1033-1036.CrossRef Medline
10. Casey BJ, Nigg JT, Durston S (2007a) New potential leads in the biology and treatment of attention deficit-hyperactivity disorder. Curr Opin Neurol 20:119-124.CrossRef Medline
11. Casey BJ, Epstein JN, Buhle J, Liston C, Davidson MC, Tonev ST, Spicer J, Niogi S, Millner AJ, Reiss A, Garrett A, Hinshaw SP, Greenhill LL, Shafritz KM, Vitolo A, Kotler LA, Jarrett MA, Glover G (2007b) Fronto-striatal connectivity and its role in cognitive control in parent-child dyads with ADHD. Am J Psychiatry 164:1729-1736.CrossRef Medline
12. Castellanos FX, Proal E (2012) Large-scale brain systems in ADHD: beyond the prefrontal-striatal model. Trends Cogn Sci 16:17-26.CrossRef Medline
13. Castellanos FX, Sonuga-Barke EJ, Milham MP, Tannock R (2006) Characterizing cognition in ADHD: beyond executive dysfunction. Trends Cogn Sci 10:117-123.CrossRef Medline
14. Castellanos FX, Margulies DS, Kelly C, Uddin LQ, Ghaffari M, Kirsch A, Shaw D, Shehzad Z, Di Martino A, Biswal B, Sonuga-Barke EJ, 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.CrossRef Medline
15. Chabernaud C, Mennes M, Kelly C, Nooner K, Di Martino A, Castellanos FX, Milham MP (2011) Dimensional brain-behavior relationships in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 71: 434-442.CrossRef Medline
16. Chao-Gan Y, Yu-Feng Z (2010) DPARSF: A MATLAB toolbox for "pipeline" data analysis of resting-state fMRI. Front Syst Neurosci 4:13.CrossRef Medline
17. Chumbley J, Worsley K, Flandin G, Friston K (2010) Topological FDR for neuroimaging. Neuroimage 49:3057-3064.CrossRef Medline
18. Cocchi L, Harrison BJ, Pujol J, Harding IH, Fornito A, Pantelis C, Yücel M (2012a) Functional alterations of large-scale brain networks related to cognitive control in obsessive-compulsive disorder. Hum Brain Mapp 33:1089-1106. Medline
19. Cocchi L, Zalesky A, Fontenelle LF (2012b) How can connectomics advance our knowledge of psychiatric disorders? Rev Bras Psiquiatr 34:131-132.CrossRef Medline
20. De Ridder A, De Graeve D (2006) Healthcare use, social burden and costs of children with and without ADHD in Flanders, Belgium. Clin Drug Investig 26:75-90.CrossRef Medline
21. Fair DA, Posner J, Nagel BJ, Bathula D, Dias TG, 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.CrossRef Medline
22. Fassbender C, Zhang H, Buzy WM, Cortes CR, Mizuiri D, Beckett L, Schweitzer JB (2009) A lack of default network suppression is linked to increased distractibility in ADHD. Brain Res 1273:114-128.CrossRef Medline
23. Frazier TW, Youngstrom EA, Glutting JJ, Watkins MW (2007) ADHD and achievement: meta-analysis of the child, adolescent, and adult literatures and a concomitant study with college students. J Learn Disabil 40:49-65.CrossRef Medline
24. Grevet EH, Bau CH, Salgado CA, Ficher A, Victor MM, Garcia C, de Sousa NO, Nerung L, Belmonte-De-Abreu P (2005) Interrater reliability for diagnosis in adults of attention deficit hyperactivity disorder and oppositional defiant disorder using K-SADS-E (in Portuguese). Arq Neuropsiquiatr 63:307-310.CrossRef Medline
25. Guye M, Bettus G, Bartolomei F, Cozzone PJ (2010) Graph theoretical analysis of structural and functional connectivity MRI in normal and pathological brain networks. MAGMA 23:409-421.CrossRef Medline
26. He Y, Evans A (2010) Graph theoretical modeling of brain connectivity. Curr Opin Neurol 23:341-350.CrossRef Medline
27. Hill DE, Yeo RA, Campbell RA, Hart B, Vigil J, Brooks W (2003) Magnetic resonance imaging correlates of attention-deficit/hyperactivity disorder in children. Neuropsychology 17:496-506.CrossRef Medline
28. Hinnenthal JA, Perwien AR, Sterling KL (2005) A comparison of service use and costs among adults with ADHD and adults with other chronic diseases. Psychiatr Serv 56:1593-1599.CrossRef Medline
29. Huettel SA, Song AW, McCarthy G (2009) Functional magnetic resonance imaging, Ed 2. Sunderland, MA: Sinauer Associates.
30. Humphries MD, Gurney K (2008) Network 'small-world-ness': a quantitative method for determining canonical network equivalence. PLoS One 3:e0002051.CrossRef Medline
31. Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2008) Competition between functional brain networks mediates behavioral variability. Neuroimage 39:527-537.CrossRef Medline
32. 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.CrossRef Medline
33. Krain AL, Castellanos FX (2006) Brain development and ADHD. Clin Psychol Rev 26:433-444.CrossRef Medline
34. Liddle EB, Hollis C, Batty MJ, Groom MJ, Totman JJ, Liotti M, Scerif G, Liddle PF (2011) Task-related default mode network modulation and inhibitory control in ADHD: effects of motivation and methylphenidate. J Child Psychol Psychiatry 52:761-771.CrossRef Medline
35. Liston C, Malter Cohen MM, Teslovich T, Levenson D, Casey BJ (2011) Atypical prefrontal connectivity in attention-deficit/hyperactivity disorder: pathway to disease or pathological end point? Biol Psychiatry 69: 1168-1177.CrossRef Medline
36. Liu D, Yan C, Ren J, Yao L, Kiviniemi VJ, Zang Y (2010) Using coherence to measure regional homogeneity of resting-state fMRI signal. Front Syst Neurosci 4:24.CrossRef Medline
37. Luman M, Tripp G, Scheres A (2010) Identifying the neurobiology of altered reinforcement sensitivity in ADHD: a review and research agenda. Neurosci Biobehav Rev 34:744-754.CrossRef Medline
38. Lynall ME, Bassett DS, Kerwin R, McKenna PJ, Kitzbichler M, Muller U, Bullmore E (2010) Functional connectivity and brain networks in schizophrenia. J Neurosci 30:9477-9487.CrossRef Medline
39. Makris N, Biederman J, Valera EM, Bush G, Kaiser J, Kennedy DN, Caviness VS, Faraone SV, Seidman LJ (2007) Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. Cereb Cortex 17:1364-1375.CrossRef Medline
40. Makris N, Biederman J, Monuteaux MC, Seidman LJ (2009) Towards conceptualizing a neural systems-based anatomy of attention-deficit/hyperactivity disorder. Dev Neurosci 31:36-49.CrossRef Medline
41. Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164:177-190.CrossRef Medline
42. Marrelec G, Kim J, Doyon J, Horwitz B (2009) Large-scale neural model validation of partial correlation analysis for effective connectivity investi-gation in functional MRI. Hum Brain Mapp 30:941-950.CrossRef Medline
43. Maslov S, Sneppen K (2002) Specificity and stability in topology of protein networks. Science 296:910-913.CrossRef Medline
44. Mattos P, Segenreich D, Saboya E, Louzã M, Dias G, Romano M (2006) Transcultural adaptation of the adult self-report scale into Portuguese for evaluation of adult attention deficit hyperactivity disorder (ADHD). Rev Psiquiatr Clin 33:188-194.
45. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1-25.CrossRef Medline
46. Nigg JT, Casey BJ (2005) An integrative theory of attention-deficit/hyperactivity disorder based on the cognitive and affective neurosciences. Dev Psychopathol 17:785-806.CrossRef Medline
47. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113.CrossRef Medline
48. 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.CrossRef Medline
49. Proal E, Reiss PT, Klein RG, Mannuzza S, Gotimer K, Ramos-Olazagasti MA, Lerch JP, He Y, Zijdenbos A, Kelly C, Milham MP, Castellanos FX (2011) Brain gray matter deficits at 33-Year Follow-up in adults with attentiondeficit/ hyperactivity disorder established in childhood. Arch Gen Psychiatry 68:1122-1134.CrossRef Medline
50. Qiu MG, Ye Z, Li QY, Liu GJ, Xie B, Wang J (2011) Changes of brain structure and function in ADHD children. Brain Topogr 24:243-252.CrossRef Medline
51. Rubia K (2011) "Cool" inferior fronto-striatal dysfunction in attention-deficit/ hyperactivity disorder versus "hot" ventromedial orbitofrontal-limbic dysfunction in conduct disorder: a review. Biol Psychiatry 69:e69-e87.CrossRef Medline
52. Rubia K, Smith AB, Halari R, Matsukura F, Mohammad M, Taylor E, Brammer MJ (2009) Disorder-specific dissociation of orbitofrontal dysfunction in boys with pure conduct disorder during reward and ventrolateral prefrontal dysfunction in boys with pure ADHD during sustained attention. Am J Psychiatry 166:83-94.CrossRef Medline
53. Rubia K, Cubillo A, Woolley J, Brammer MJ, Smith A (2011) Disorderspecific dysfunctions in patients with attention-deficit/hyperactivity disorder compared to patients with obsessive-compulsive disorder during interference inhibition and attention allocation. Hum Brain Mapp 32: 601-611.CrossRef Medline
54. Rubinov M, Bassett DS (2011) Emerging evidence of connectomic abnormalities in schizophrenia. J Neurosci 31:6263-6265.CrossRef Medline
55. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059-1069.CrossRef Medline
56. Rubinov M, Sporns O (2011) Weight-conserving characterization of complex functional brain networks. Neuroimage 56:2068-2079.CrossRef Medline
57. Salvador R, Suckling J, Coleman MR, Pickard JD, Menon D, Bullmore E (2005) Neurophysiological architecture of functional magnetic resonance images of human brain. Cereb Cortex 15:1332-1342.CrossRef Medline
58. Satterthwaite TD, Wolf DH, Loughead J, Ruparel K, Elliott MA, Hakonarson H, Gur RC, Gur RE (2012) Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 60:623-632.CrossRef Medline
59. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry [59 Suppl] 20:22-33;quiz 34-57.
60. Sibley MH, Pelham WE, Molina BS, Gnagy EM, Waxmonsky JG, Waschbusch DA, Derefinko KJ, Wymbs BT, Garefino AC, Babinski DE, Kuriyan AB (2012) When diagnosing ADHD in young adults emphasize informant reports, DSM items, and impairment. J Consult Clin Psychol. Advance online publication. Retrieved July 9, 2012.CrossRef Medline.
61. Simon V, Czobor P, Bálint S, Meszaros A, Bitter I (2009) Prevalence and correlates of adult attention-deficit hyperactivity disorder: meta-analysis. Br J Psychiatry 194:204-211.CrossRef Medline
62. Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031.CrossRef Medline
63. Sonuga-Barke EJ, Castellanos FX (2007) Spontaneous attentional fluctuations in impaired states and pathological conditions: a neurobiological hypothesis. Neurosci Biobehav Rev 31:977-986. CrossRef
64. Sporns O (2011) Networks of the brain, Ed 1. Cambridge, MA: MIT.
65. Swanson JM, Sergeant JA, Taylor E, Sonuga-Barke EJ, Jensen PS, Cantwell DP (1998) Attention-deficit hyperactivity disorder and hyperkinetic disorder. Lancet 351:429-433.CrossRef Medline
66. Tian L, Jiang T, Liang M, Zang Y, He Y, Sui M, Wang Y (2008) Enhanced resting-state brain activities in ADHD patients: a fMRI study. Brain Dev 30:342-348.CrossRef Medline
67. Tomasi D, Volkow ND (2012) Abnormal functional connectivity in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 71: 443-450.CrossRef Medline
68. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273-289.CrossRef Medline
69. Van Dijk KR, Sabuncu MR, Buckner RL (2012) The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59:431-438.CrossRef Medline
70. Vloet TD, Gilsbach S, Neufang S, Fink GR, Herpertz-Dahlmann B, Konrad K (2010) Neural mechanisms of interference control and time discrimination in attention-deficit/hyperactivity disorder. J AmAcad Child Adolesc Psychiatry 49:356-367.CrossRef Medline
71. Volkow ND, Wang GJ, Tomasi D, Kollins SH, Wigal TL, Newcorn JH, Telang FW, Fowler JS, Logan J, Wong CT, Swanson JM (2012) Methylphenidate-elicited dopamine increases in ventral striatum are associated with long-term symptom improvement in adults with attention deficit hyperactivity disorder. J Neurosci 32:841-849.CrossRef Medline
72. Wang J, Wang L, Zang Y, Yang H, Tang H, Gong Q, Chen Z, Zhu C, He Y (2009a) Parcellation-dependent small-world brain functional networks: a resting-state fMRI study. Hum Brain Mapp 30:1511-1523.CrossRef Medline
73. Wang J, Zuo X, He Y (2010) Graph-based network analysis of resting-state functional MRI. Front Syst Neurosci 4:16.CrossRef Medline
74. Wang L, Zhu C, He Y, Zang Y, Cao Q, Zhang H, Zhong Q, Wang Y (2009b) Altered small-world brain functional networks in children with attentiondeficit/hyperactivity disorder. Hum Brain Mapp 30:638-649.CrossRef Medline
75. Wechsler D (1999) Wechsler abbreviated scale of intelligence (WASI). San Antonio, TX: Harcourt Assessment.
76. Wig GS, Schlaggar BL, Petersen SE (2011) Concepts and principles in the analysis of brain networks. Ann NY Acad Sci 1224:126-146.CrossRef Medline
77. Wilson TW, Franzen JD, Heinrichs-Graham E, White ML, Knott NL, Wetzel MW (2012) Broadband neurophysiological abnormalities in the medial prefrontal region of the default-mode network in adults with ADHD. Hum Brain Mapp. Advance online publication. Retrieved Nov 18, 2011.CrossRef Medline.
78. Wolf RC, Plichta MM, Sambataro F, Fallgatter AJ, Jacob C, Lesch KP, Herrmann MJ, Schönfeldt-Lecuona C, Connemann BJ, Grön G, Vasic N (2009) Regional brain activation changes and abnormal functional connectivity of the ventrolateral prefrontal cortex during working memory processing in adults with attention-deficit/hyperactivity disorder. Hum Brain Mapp 30:2252-2266.CrossRef Medline
79. Xia M, He Y (2011) Magnetic resonance imaging and graph theoretical analysis of complex brain networks in neuropsychiatric disorders. Brain Connectivity 1:349-365.CrossRef Medline
80. Yates DB, Trentini CM, Tosi SD, Corrêa SK, Poggere LC, Valli F (2006) Apresentação da Escala de Inteligência Wechsler abreviada (WASI). Avaliação Psicológica 5:227-233.
81. Zalesky A, Fornito A, Harding IH, Cocchi L, Yücel M, Pantelis C, Bullmore ET (2010a) Whole-brain anatomical networks: does the choice of nodes matter? Neuroimage 50:970-983.CrossRef Medline
82. Zalesky A, Fornito A, Bullmore ET (2010b) Network-based statistic: identifying differences in brain networks. Neuroimage 53:1197-1207.CrossRef Medline
83. Zalesky A, Cocchi L, Fornito A, Murray MM, Bullmore E (2012a) Connec-tivity differences in brain networks. Neuroimage 60:1055-1062.CrossRef Medline
84. Zalesky A, Fornito A, Egan GF, Pantelis C, Bullmore ET (2012b) The relationship between regional and inter-regional functional connectivity deficits in schizophrenia. Hum Brain Mapp. Advance online publication. Retrieved Sep 16, 2012. doi:10.1002/hbm.21379. CrossRef
85. Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22:394-400.CrossRef Medline
86. Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, Tian LX, Jiang TZ, Wang YF (2007) Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev 29:83-91.CrossRef Medline