Altered Resting-State Frontoparietal Control Network in Children with Attention-Deficit/Hyperactivity Disorder

Abstract The frontoparietal control network, anatomically and functionally interposed between the dorsal attention network and default mode network, underpins executive control functions. Individuals with attention-deficit/hyperactivity disorder (ADHD) commonly exhibit deficits in executive functions, which are mainly mediated by the frontoparietal control network. Involvement of the frontoparietal control network based on the anterior prefrontal cortex in neurobiological mechanisms of ADHD has yet to be tested. We used resting-state functional MRI and seed-based correlation analyses to investigate functional connectivity of the frontoparietal control network in a sample of 25 children with ADHD (7–14 years; mean 9.94±1.77 years; 20 males), and 25 age-, sex-, and performance IQ-matched typically developing (TD) children. All participants had limited in-scanner head motion. Spearman’s rank correlations were used to test the associations between altered patterns of functional connectivity with clinical symptoms and executive functions, measured by the Conners’ Continuous Performance Test and Spatial Span in the Cambridge Neuropsychological Test Automated Battery. Compared with TD children, children with ADHD demonstrated weaker connectivity between the right anterior prefrontal cortex (PFC) and the right ventrolateral PFC, and between the left anterior PFC and the right inferior parietal lobule. Furthermore, this aberrant connectivity of the frontoparietal control network in ADHD was associated with symptoms of impulsivity and opposition-defiance, as well as impaired response inhibition and attentional control. The findings support potential integration of the disconnection model and the executive dysfunction model for ADHD. Atypical frontoparietal control network may play a pivotal role in the pathophysiology of ADHD. (JINS, 2015, 21, 271–284)

[1]  H. Jeffreys.  The Theory of Probability , 1922 .

[2]  T. Malti,et al.  Interpretive Understanding, Sympathy, and Moral Emotion Attribution in Oppositional Defiant Disorder Symptomatology , 2013, Child Psychiatry & Human Development.

[3]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[4]  Michael P. Milham,et al.  Resting State Functional Connectivity Correlates of Inhibitory Control in Children with Attention-Deficit/Hyperactivity Disorder , 2012, Front. Psychiatry.

[5]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[6]  H. Hart,et al.  Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. , 2013, JAMA psychiatry.

[7]  Michael P. Milham,et al.  Dimensional Brain-Behavior Relationships in Children with Attention-Deficit/Hyperactivity Disorder , 2012, Biological Psychiatry.

[8]  Daniel L. Schacter,et al.  Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition , 2010, NeuroImage.

[9]  Rupert Lanzenberger,et al.  Correlations and anticorrelations in resting-state functional connectivity MRI: A quantitative comparison of preprocessing strategies , 2009, NeuroImage.

[10]  J. Posner,et al.  Connecting the Dots: A Review of Resting Connectivity MRI Studies in Attention-Deficit/Hyperactivity Disorder , 2014, Neuropsychology Review.

[11]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[12]  Dirk J. Heslenfeld,et al.  Diffusion tensor imaging in attention deficit/hyperactivity disorder: A systematic review and meta-analysis , 2012, Neuroscience & Biobehavioral Reviews.

[13]  K. Mcburnett,et al.  A Review of Attention-Deficit/Hyperactivity Disorder Complicated by Symptoms of Oppositional Defiant Disorder or Conduct Disorder , 2010, Journal of developmental and behavioral pediatrics : JDBP.

[14]  Deanna Greenstein,et al.  Developmental Trajectories of the Corpus Callosum in Attention-Deficit/Hyperactivity Disorder , 2011, Biological Psychiatry.

[15]  G D Logan,et al.  Response inhibition in AD/HD, CD, comorbid AD/HD + CD, anxious, and control children: a meta-analysis of studies with the stop task. , 1998, Journal of child psychology and psychiatry, and allied disciplines.

[16]  Purang Abolmaesumi,et al.  Reducing inter-subject anatomical variation: Effect of normalization method on sensitivity of functional magnetic resonance imaging data analysis in auditory cortex and the superior temporal region , 2009, NeuroImage.

[17]  Yufeng Zang,et al.  Abnormal neural activity in children with attention deficit hyperactivity disorder: a resting-state functional magnetic resonance imaging study , 2006, Neuroreport.

[18]  Ellen Leibenluft,et al.  Emotion dysregulation in attention deficit hyperactivity disorder. , 2014, The American journal of psychiatry.

[19]  Michael P Milham,et al.  Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies. , 2012, The American journal of psychiatry.

[20]  Xi-Nian Zuo,et al.  REST: A Toolkit for Resting-State Functional Magnetic Resonance Imaging Data Processing , 2011, PloS one.

[21]  Chaozhe Zhu,et al.  Abnormal resting-state functional connectivity patterns of the putamen in medication-naïve children with attention deficit hyperactivity disorder , 2009, Brain Research.

[22]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[23]  Chad E. Forbes,et al.  The role of the human prefrontal cortex in social cognition and moral judgment. , 2010, Annual review of neuroscience.

[24]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[25]  Hang Joon Jo,et al.  The perils of global signal regression for group comparisons: a case study of Autism Spectrum Disorders , 2013, Front. Hum. Neurosci..

[26]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[27]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[28]  A. Baddeley,et al.  Executive functions and self-regulation , 2012, Trends in Cognitive Sciences.

[29]  Swathi P. Iyer,et al.  Reward circuit connectivity relates to delay discounting in children with attention-deficit/hyperactivity disorder , 2013, European Neuropsychopharmacology.

[30]  Tianzi Jiang,et al.  Altered resting-state functional connectivity patterns of anterior cingulate cortex in adolescents with attention deficit hyperactivity disorder , 2006, Neuroscience Letters.

[31]  Oscar Vilarroya,et al.  An independent components and functional connectivity analysis of resting state fMRI data points to neural network dysregulation in adult ADHD , 2014, Human brain mapping.

[32]  Noah D. Brenowitz,et al.  Integrated strategy for improving functional connectivity mapping using multiecho fMRI , 2013, Proceedings of the National Academy of Sciences.

[33]  E. Sonuga-Barke,et al.  Neuroeconomics of Attention-Deficit/Hyperactivity Disorder: Differential Influences of Medial, Dorsal, and Ventral Prefrontal Brain Networks on Suboptimal Decision Making? , 2012, Biological Psychiatry.

[34]  F. Castellanos,et al.  Characterizing cognition in ADHD: beyond executive dysfunction , 2006, Trends in Cognitive Sciences.

[35]  J. Schweitzer,et al.  Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature. , 2006, Clinical psychology review.

[36]  Bradley S. Peterson,et al.  Dissociable attentional and affective circuits in medication-naïve children with attention-deficit/hyperactivity disorder , 2013, Psychiatry Research: Neuroimaging.

[37]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[38]  Z. Dienes.  Bayesian Versus Orthodox Statistics: Which Side Are You On? , 2011, Perspectives on psychological science : a journal of the Association for Psychological Science.

[39]  I. Toni,et al.  Anterior Prefrontal Cortex Inhibition Impairs Control over Social Emotional Actions , 2011, Current Biology.

[40]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[41]  M. Barnes,et al.  Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders , 2009, Journal of the International Neuropsychological Society.

[42]  Daeyeol Lee,et al.  Prefrontal Cortex and Impulsive Decision Making , 2011, Biological Psychiatry.

[43]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[44]  B. Pennington,et al.  Validity of the Executive Function Theory of Attention-Deficit/Hyperactivity Disorder: A Meta-Analytic Review , 2005, Biological Psychiatry.

[45]  R. Haier,et al.  The Parieto-Frontal Integration Theory (P-FIT) of intelligence: Converging neuroimaging evidence , 2007, Behavioral and Brain Sciences.

[46]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[47]  Yong He,et al.  Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. , 2007, Brain & development.

[48]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[49]  M. J. Emerson,et al.  The Unity and Diversity of Executive Functions and Their Contributions to Complex “Frontal Lobe” Tasks: A Latent Variable Analysis , 2000, Cognitive Psychology.

[50]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[51]  Katya Rubia,et al.  “Cool” Inferior Frontostriatal Dysfunction in Attention-Deficit/Hyperactivity Disorder Versus “Hot” Ventromedial Orbitofrontal-Limbic Dysfunction in Conduct Disorder: A Review , 2011, Biological Psychiatry.

[52]  J. Grafman,et al.  Opinion: the neural basis of human moral cognition. , 2005, Nature reviews. Neuroscience.

[53]  Jared A. Nielsen,et al.  Multisite functional connectivity MRI classification of autism: ABIDE results , 2013, Front. Hum. Neurosci..

[54]  Katya Rubia,et al.  Gray matter volume abnormalities in ADHD: voxel-based meta-analysis exploring the effects of age and stimulant medication. , 2011, The American journal of psychiatry.

[55]  R. Cameron Craddock,et al.  A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics , 2013, NeuroImage.

[56]  Y. Zang,et al.  Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI , 2007, Brain and Development.

[57]  Jin Fan,et al.  Development of attentional networks: An fMRI study with children and adults , 2005, NeuroImage.

[58]  Daniel L. Schacter,et al.  Intrinsic Architecture Underlying the Relations among the Default, Dorsal Attention, and Frontoparietal Control Networks of the Human Brain , 2013, Journal of Cognitive Neuroscience.

[59]  A. Evans,et al.  Development of Cortical Surface Area and Gyrification in Attention-Deficit/Hyperactivity Disorder , 2012, Biological Psychiatry.

[60]  S. Gau,et al.  Associations of symptoms and subtypes of attention-deficit hyperactivity disorder with visuospatial planning ability in youth. , 2013, Research in developmental disabilities.

[61]  R. Cameron Craddock,et al.  Clinical applications of the functional connectome , 2013, NeuroImage.

[62]  Deepti R. Bathula,et al.  Atypical Default Network Connectivity in Youth with Attention-Deficit/Hyperactivity Disorder , 2010, Biological Psychiatry.

[63]  Marko Wilke,et al.  An alternative approach towards assessing and accounting for individual motion in fMRI timeseries , 2012, NeuroImage.

[64]  S. Bunge,et al.  Neurodevelopmental changes in working memory and cognitive control , 2007, Current Opinion in Neurobiology.

[65]  Liang Wang,et al.  Altered small‐world brain functional networks in children with attention‐deficit/hyperactivity disorder , 2009, Human brain mapping.

[66]  R. Barkley.  Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. , 1997, Psychological bulletin.

[67]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[68]  M. Martel,et al.  Research review: a new perspective on attention-deficit/hyperactivity disorder: emotion dysregulation and trait models. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

[69]  Jian Wang,et al.  Changes of Brain Structure and Function in ADHD Children , 2011, Brain Topography.

[70]  J. Grafman,et al.  The neural basis of human moral cognition , 2005, Nature Reviews Neuroscience.

[71]  Eric J. Johnson,et al.  Lateral prefrontal cortex and self-control in intertemporal choice , 2010, Nature Neuroscience.

[72]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[73]  J. Swanson,et al.  Psychometric properties of the Chinese version of the Swanson, Nolan, and Pelham, version IV scale – parent form , 2008, International journal of methods in psychiatric research.

[74]  Yufeng Zang,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010 .

[75]  E. Koechlin,et al.  Anterior Prefrontal Function and the Limits of Human Decision-Making , 2007, Science.

[76]  Scott Holland,et al.  Template-O-Matic: A toolbox for creating customized pediatric templates , 2008, NeuroImage.

[77]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[78]  T. Klingberg.  Development of a superior frontal–intraparietal network for visuo-spatial working memory , 2006, Neuropsychologia.

[79]  S. Gau,et al.  Executive functions as endophenotypes in ADHD: evidence from the Cambridge Neuropsychological Test Battery (CANTAB). , 2010, Journal of child psychology and psychiatry, and allied disciplines.

[80]  Kristen A. Lindquist,et al.  A functional architecture of the human brain: emerging insights from the science of emotion , 2012, Trends in Cognitive Sciences.

[81]  Wenjun Li,et al.  A method to determine the necessity for global signal regression in resting‐state fMRI studies , 2012, Magnetic resonance in medicine.

[82]  T. Heatherton,et al.  Cognitive neuroscience of self-regulation failure , 2011, Trends in Cognitive Sciences.

[83]  S. Gau,et al.  Validation of Attention-Deficit–Hyperactivity Disorder Subtypes Among Taiwanese Children Using Neuropsychological Functioning , 2008, The Australian and New Zealand journal of psychiatry.

[84]  A. Arnsten,et al.  Neurobiological circuits regulating attention, cognitive control, motivation, and emotion: disruptions in neurodevelopmental psychiatric disorders. , 2012, Journal of the American Academy of Child and Adolescent Psychiatry.

[85]  R. Barkley.  The Executive Functions and Self-Regulation: An Evolutionary Neuropsychological Perspective , 2001, Neuropsychology Review.

[86]  H. Geurts,et al.  The top and the bottom of ADHD: a neuropsychological perspective , 2003, Neuroscience & Biobehavioral Reviews.

[87]  R. Veit,et al.  The truth about lying: inhibition of the anterior prefrontal cortex improves deceptive behavior. , 2010, Cerebral cortex.

[88]  B. Biswal,et al.  Cingulate-Precuneus Interactions: A New Locus of Dysfunction in Adult Attention-Deficit/Hyperactivity Disorder , 2008, Biological Psychiatry.

[89]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[90]  Chaogan Yan,et al.  DPARSF: A MATLAB Toolbox for “Pipeline” Data Analysis of Resting-State fMRI , 2010, Front. Syst. Neurosci..

[91]  R. Davidson,et al.  Dysfunction in the neural circuitry of emotion regulation--a possible prelude to violence. , 2000, Science.

[92]  F. Xavier Castellanos,et al.  Large-scale brain systems in ADHD: beyond the prefrontal–striatal model , 2012, Trends in Cognitive Sciences.

[93]  S. Gau,et al.  Executive Function in Adolescence Among Children With Attention-Deficit/Hyperactivity Disorder in Taiwan , 2009, Journal of developmental and behavioral pediatrics : JDBP.

[94]  Iroise Dumontheil,et al.  Development of rostral prefrontal cortex and cognitive and behavioural disorders , 2008, Developmental medicine and child neurology.

[95]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[96]  R. Kahn,et al.  Efficiency of Functional Brain Networks and Intellectual Performance , 2009, The Journal of Neuroscience.

[97]  Z. Diénès.  Understanding Psychology as a Science: An Introduction to Scientific and Statistical Inference , 2008 .

[98]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[99]  Maarten Mennes,et al.  Abnormal amygdala functional connectivity associated with emotional lability in children with attention-deficit/hyperactivity disorder. , 2014, Journal of the American Academy of Child and Adolescent Psychiatry.

[100]  Richard F. Betzel,et al.  Resting-brain functional connectivity predicted by analytic measures of network communication , 2013, Proceedings of the National Academy of Sciences.

[101]  Kathryn L. Mills,et al.  Altered Cortico-Striatal–Thalamic Connectivity in Relation to Spatial Working Memory Capacity in Children with ADHD , 2012, Front. Psychiatry.

[102]  Beatriz Luna,et al.  Brain Basis of Developmental Change in Visuospatial Working Memory , 2006, Journal of Cognitive Neuroscience.

[103]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[104]  Nicole M Dudukovic,et al.  Altered neural substrates of cognitive control in childhood ADHD: evidence from functional magnetic resonance imaging. , 2005, The American journal of psychiatry.