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Surface-based shared and distinct resting functional connectivity in attention-deficit hyperactivity disorder and autism spectrum disorder

  • Minyoung Jung (a1), Yiheng Tu (a2), Joel Park (a3), Kristen Jorgenson (a3), Courtney Lang (a3), Wenwen Song (a4) and Jian Kong (a5)...
Abstract
Background

Both attention-deficit hyperactivity disorder (ADHD) and autism spectrum disorder (ASD) are neurodevelopmental disorders with a high prevalence. They are often comorbid and both exhibit abnormalities in sustained attention, yet common and distinct neural patterns of ASD and ADHD remain unidentified.

Aims

To investigate shared and distinct functional connectivity patterns in a relatively large sample of boys (7- to 15-year-olds) with ADHD, ASD and typical development matched by age, gender and IQ.

Method

We applied machine learning techniques to investigate patterns of surface-based brain resting-state connectivity in 86 boys with ASD, 83 boys with ADHD and 125 boys with typical development.

Results

We observed increased functional connectivity within the limbic and somatomotor networks in boys with ASD compared with boys with typical development. We also observed increased functional connectivity within the limbic, visual, default mode, somatomotor, dorsal attention, frontoparietal and ventral attention networks in boys with ADHD compared with boys with ASD. In addition, using a machine learning approach, we were able to discriminate typical development from ASD, typical development from ADHD and ASD from ADHD with accuracy rates of 76.3%, 84.1%, and 79.3%, respectively.

Conclusions

Our results may shed new light on the underlying mechanisms of ASD and ADHD and facilitate the development of new diagnostic methods for these disorders.

Declaration of interest

J.K. holds equity in a startup company, MNT.

Copyright
Corresponding author
Correspondence: Jian Kong, MD, MS, MPH, Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Charlestown, MA 02129, USA. Email: kongj@nmr.mgh.harvard.edu
References
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1Moffitt, TE, Houts, R, Asherson, P, Belsky, DW, Corcoran, DL, Hammerle, M, et al. Is adult ADHD a childhood-onset neurodevelopmental disorder? Evidence from a four-decade longitudinal cohort study. Am J Psychiatry 2015; 172: 967–77.
2Lai, M-C, Lombardo, M V, Baron-Cohen, S. Autism. Lancet 2014; 383: 896910.
3Simonoff, E, Pickles, A, Charman, T, Chandler, S, Loucas, T, Baird, G. Psychiatric disorders in children with autism spectrum disorders: prevalence, comorbidity, and associated factors in a population-derived sample. J Am Acad Child Adolesc Psychiatry 2008; 47: 921–9.
4Park, B, Hong, J, Lee, S-H, Park, H. Functional connectivity of child and adolescent attention deficit hyperactivity disorder patients: correlation with IQ. Front Hum Neurosci 2016; 10: 3140.
5Lynch, CJ, Uddin, LQ, Supekar, K, Khouzam, A, Phillips, J, Menon, V. Default mode network in childhood autism: posteromedial cortex heterogeneity and relationship with social deficits. Biol Psychiatry 2013; 74: 212–9.
6Di Martino, A, Zuo, X-N, Kelly, C, Grzadzinski, R, Mennes, M, Schvarcz, A, et al. Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder. Biol Psychiatry 2013; 74: 623–32.
7Kyeong, S, Kim, JJ, Kim, E. Novel subgroups of attention-deficit/hyperactivity disorder identified by topological data analysis and their functional network modular organizations. PLoS One 2017; 12: e0182603.
8Francx, W, Oldehinkel, M, Oosterlaan, J, Heslenfeld, D, Hartman, CA, Hoekstra, PJ, et al. The executive control network and symptomatic improvement in attention-deficit/hyperactivity disorder. Cortex 2015; 73: 6272.
9Supekar, K, Uddin, LQ, Khouzam, A, Phillips, J, Gaillard, WD, Kenworthy, LE, et al. Brain hyperconnectivity in children with autism and its links to social deficits. Cell Rep 2013; 5: 738–47.
10Christakou, A, Murphy, CM, Chantiluke, K, Cubillo, AI, Smith, AB, Giampietro, V, et al. Disorder-specific functional abnormalities during sustained attention in youth with attention deficit hyperactivity disorder (ADHD) and with autism. Mol Psychiatry 2013; 18: 236–44.
11Ray, S, Miller, M, Karalunas, S, Robertson, C, Grayson, DS, Cary, RP, et al. Structural and functional connectivity of the human brain in autism spectrum disorders and attention-deficit/hyperactivity disorder: a rich club-organization study. Hum Brain Mapp 2014; 35: 6032–48.
12Cerliani, L, Mennes, M, Thomas, RM, Di Martino, A, Thioux, M, Keysers, C. Increased functional connectivity between subcortical and cortical resting-state networks in autism spectrum disorder. JAMA Psychiatry 2015; 72: 111.
13Smith, SM, Vidaurre, D, Beckmann, CF, Glasser, MF, Jenkinson, M, Miller, KL, et al. Functional connectomics from resting-state fMRI. Trends Cogn Sci 2013; 17: 666–82.
14Dickstein, DP, Pescosolido, MF, Reidy, BL, Galvan, T, Kim, KL, Seymour, KE, et al. Developmental meta-analysis of the functional neural correlates of autism spectrum disorders. J Am Acad Child Adolesc Psychiatry 2013; 52: 27989.e16.
15Friedman, L, Stern, H, Brown, GG, Mathalon, DH, Turner, J, Glover, GH, et al. Test-retest and between-site reliability in a multicenter fMRI study. Hum Brain Mapp 2008; 29: 958–72.
16American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (4th edn, revised) (DSM-IV-TR). APA, 2000.
17Lord, C, Rutter, M, DiLavore, PC, Risi, S, Gotham, K, Bishop, SL. Autism Diagnostic Observation Schedule, Second Edition (ADOS-2) Modules 1-4. Western Psychological Services, 2012.
18Lord, C, Rutter, M, Le Couteur, A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 1994; 24: 659–85.
19Constantino, JN, Davis, SA, Todd, RD, Schindler, MK, Gross, MM, Brophy, SL, et al. 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 2003; 33: 427–33.
20Fischl, B, Sereno, MI, Tootell, RBH, Dale, AM. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 1999; 8: 272–84.
21Whitfield-Gabrieli, S, Nieto-Castanon, A. CONN: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect 2012; 2: 125–41.
22Muschelli, J, Nebel, MB, Caffo, BS, Barber, AD, Pekar, JJ, Mostofsky, SH. Reduction of motion-related artifacts in resting state fMRI using aCompCor. Neuroimage 2014; 96: 2235.
23Desikan, RS, Ségonne, F, Fischl, B, Quinn, BT, Dickerson, BC, Blacker, D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 2006; 31: 968–80.
24Guyon, I, Weston, J, Barnhill, S, Vapnik, V. Gene selection for cancer classification using support vector machines. Mach Learn 2002; 46: 389422.
25Tu, Y, Zhang, Z, Tan, A, Peng, W, Hung, YS, Moayedi, M, et al. Alpha and gamma oscillation amplitudes synergistically predict the perception of forthcoming nociceptive stimuli. Hum Brain Mapp 2016; 37: 501–14.
26Zeng, L-L, Shen, H, Liu, L, Wang, L, Li, B, Fang, P, et al. Identifying major depression using whole-brain functional connectivity: a multivariate pattern analysis. Brain 2012; 135: 1498–507.
27Leech, R, Sharp, DJ. The role of the posterior cingulate cortex in cognition and disease. Brain 2014; 137: 1232.
28Buckner, RL, Andrews-Hanna, JR, Schacter, DL. The brain's default network: anatomy, function and relevance to disease. Ann N Y Acad Sci 2008; 1124: 138.
29Leech, R, Kamourieh, S, Beckmann, CF, Sharp, DJ. Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. J Neurosci 2011; 31: 3217–24.
30Rubia, K, Smith, AB, Brammer, MJ, Taylor, E. Temporal lobe dysfunction in medication-naive boys with attention-deficit/hyperactivity disorder during attention allocation and its relation to response variability. Biol Psychiatry 2007; 62: 9991006.
31Gschwind, M, Pourtois, G, Schwartz, S, Van De Ville, D, Vuilleumier, P. White-matter connectivity between face-responsive regions in the human brain. Cereb Cortex 2012; 22: 1564–76.
32Jonas, J, Rossion, B, Krieg, J, Koessler, L, Colnat-Coulbois, S, Vespignani, H, et al. Intracerebral electrical stimulation of a face-selective area in the right inferior occipital cortex impairs individual face discrimination. Neuroimage 2014; 99: 487–97.
33Jung, M, Tu, Y, Lang, CA, Ortiz, A, Park, J, Jorgenson, K, et al. Decreased structural connectivity and resting-state brain activity in the lateral occipital cortex is associated with social communication deficits in boys with autism spectrum disorder. Neuroimage 2017; Sept 18 : pii S1053-8119(17)30779-6, DOI 10.1016/j.neuroimage.2017.09.031.
34Hubbard, AL, Mcnealy, K, Scott-Van Zeeland, AA, Callan, DE, Bookheimer, SY, Dapretto, M. Altered integration of speech and gesture in children with autism spectrum disorders. Brain Behav 2012; 2: 606–19.
35Di Martino, A, Kelly, C, Grzadzinski, R, Zuo, XN, Mennes, M, Mairena, MA, et al. Aberrant striatal functional connectivity in children with autism. Biol Psychiatry 2011; 69: 847–56.
36Hoekzema, E, Carmona, S, Ramos-Quiroga, JA, Richarte Fernández, V, Bosch, R, Soliva, JC, et al. An independent components and functional connectivity analysis of resting state FMRI data points to neural network dysregulation in adult ADHD. Hum Brain Mapp 2014; 35: 1261–72.
37Anderson, A, Douglas, PK, Kerr, WT, Haynes, VS, Yuille, AL, Xie, J, et al. Non-negative matrix factorization of multimodal MRI, fMRI and phenotypic data reveals differential changes in default mode subnetworks in ADHD. Neuroimage. 2014; 102: 207–19.
38Nielsen, JA, Zielinski, BA, Fletcher, PT, Alexander, AL, Lange, N, Bigler, ED, et al. Multisite functional connectivity MRI classification of autism: ABIDE results. Front Hum Neurosci 2013; 7: 599.
39Yahata, N, Morimoto, J, Hashimoto, R, Lisi, G, Shibata, K, Kawakubo, Y, et al. A small number of abnormal brain connections predicts adult autism spectrum disorder. Nat Commun 2016; 7: 11254.
40Mazefsky, CA, Herrington, J, Siegel, M, Scarpa, A, Maddox, BB, Scahill, L, et al. The role of emotion regulation in autism spectrum disorder. J Am Acad Child Adolesc Psychiatry 2013; 52: 679–88.
41Kosaka, H, Omori, M, Munesue, T, Ishitobi, M, Matsumura, Y, Takahashi, T, et al. Smaller insula and inferior frontal volumes in young adults with pervasive developmental disorders. Neuroimage 2010; 50: 1357–63.
42Mayer, JL. The relationship between autistic traits and atypical sensory functioning in neurotypical and ASD adults: a spectrum approach. J Autism Dev Disord 2017; 47: 316–27.
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Surface-based shared and distinct resting functional connectivity in attention-deficit hyperactivity disorder and autism spectrum disorder

  • Minyoung Jung (a1), Yiheng Tu (a2), Joel Park (a3), Kristen Jorgenson (a3), Courtney Lang (a3), Wenwen Song (a4) and Jian Kong (a5)...
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