Connectivity supporting attention in children with attention deficit hyperactivity disorder

Intra-subject variability (ISV) is the most consistent behavioral deficit in Attention Deficit Hyperactivity Disorder (ADHD). ISV may be associated with networks involved in sustaining task control (cingulo-opercular network: CON) and self-reflective lapses of attention (default mode network: DMN). The current study examined whether connectivity supporting attentional control is atypical in children with ADHD. Group differences in full-brain connection strength and brain–behavior associations with attentional control measures were examined for the late-developing CON and DMN in 50 children with ADHD and 50 typically-developing (TD) controls (ages 8–12 years). Children with ADHD had hyper-connectivity both within the CON and within the DMN. Full-brain behavioral associations were found for a number of between-network connections. Across both groups, more anti-correlation between DMN and occipital cortex supported better attentional control. However, in the TD group, this brain–behavior association was stronger and occurred for a more extensive set of DMN–occipital connections. Differential support for attentional control between the two groups occurred with a number of CON–DMN connections. For all CON–DMN connections identified, increased between-network anti-correlation was associated with better attentional control for the ADHD group, but worse attentional control in the TD group. A number of between-network connections with the medial frontal cortex, in particular, showed this relationship. Follow-up analyses revealed that these associations were specific to attentional control and were not due to individual differences in working memory, IQ, motor control, age, or scan motion. While CON–DMN anti-correlation is associated with improved attention in ADHD, other circuitry supports improved attention in TD children. Greater CON–DMN anti-correlation supported better attentional control in children with ADHD, but worse attentional control in TD children. On the other hand, greater DMN–occipital anti-correlation supported better attentional control in TD children.

[1]  N. Volkow,et al.  Dopamine Transporters in Striatum Correlate with Deactivation in the Default Mode Network during Visuospatial Attention , 2009, PloS one.

[2]  Deanna Greenstein,et al.  Trajectories of Cerebral Cortical Development in Childhood and Adolescence and Adult Attention-Deficit/Hyperactivity Disorder , 2013, Biological Psychiatry.

[3]  G. Bush,et al.  Functional Neuroimaging of Attention-Deficit/Hyperactivity Disorder: A Review and Suggested Future Directions , 2005, Biological Psychiatry.

[4]  James D. A. Parker,et al.  The Revised Conners' Parent Rating Scale (CPRS-R): Factor Structure, Reliability, and Criterion Validity , 1998, Journal of abnormal child psychology.

[5]  Brian S Caffo,et al.  fMRI of intrasubject variability in ADHD: anomalous premotor activity with prefrontal compensation. , 2008, Journal of the American Academy of Child and Adolescent Psychiatry.

[6]  W. Reich.  Diagnostic interview for children and adolescents (DICA) , 2000, Journal of the American Academy of Child and Adolescent Psychiatry.

[7]  Michael P Milham,et al.  The Restless Brain: Attention-Deficit Hyperactivity Disorder, Resting—State Functional Connectivity, and Intrasubject Variability , 2009, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[8]  G. Sartori,et al.  Striatal dopamine transporter alterations in ADHD: pathophysiology or adaptation to psychostimulants? A meta-analysis. , 2012, The American journal of psychiatry.

[9]  Michelle E. Hwang,et al.  Examining predictors of reaction times in children with ADHD and normal controls , 2009, Journal of the International Neuropsychological Society.

[10]  Michael Gill,et al.  Attention network hypoconnectivity with default and affective network hyperconnectivity in adults diagnosed with attention-deficit/hyperactivity disorder in childhood. , 2013, JAMA psychiatry.

[11]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[12]  F. Castellanos,et al.  Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis , 2007, Neuroscience & Biobehavioral Reviews.

[13]  Katherine A. Johnson,et al.  Increased Response-Time Variability Across Different Cognitive Tasks in Children With ADHD , 2014, Journal of attention disorders.

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

[15]  Samuel D. Carpenter,et al.  Structural and Functional Rich Club Organization of the Brain in Children and Adults , 2014, PloS one.

[16]  Annie A. Garner,et al.  The Relationship Between ADHD Symptom Dimensions, Clinical Correlates, and Functional Impairments , 2013, Journal of developmental and behavioral pediatrics : JDBP.

[17]  Katya Rubia,et al.  Imaging the ADHD brain: disorder-specificity, medication effects and clinical translation , 2014, Expert review of neurotherapeutics.

[18]  Karl J. Friston,et al.  Robust Smoothness Estimation in Statistical Parametric Maps Using Standardized Residuals from the General Linear Model , 1999, NeuroImage.

[19]  Hongtu Zhu,et al.  An FMRI study of the effects of psychostimulants on default-mode processing during Stroop task performance in youths with ADHD. , 2009, The American journal of psychiatry.

[20]  C Leth-Steensen,et al.  Mean response times, variability, and skew in the responding of ADHD children: a response time distributional approach. , 2000, Acta psychologica.

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

[22]  F Xavier Castellanos,et al.  Brain development and ADHD. , 2006, Clinical psychology review.

[23]  Mary Beth Nebel,et al.  Reduction of motion-related artifacts in resting state fMRI using aCompCor , 2014, NeuroImage.

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

[25]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[26]  Denis Cousineau,et al.  Fitting distributions using maximum likelihood: Methods and packages , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[27]  Denckla Mb,et al.  Revised Neurological Examination for Subtle Signs (1985). , 1985 .

[28]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  B. Biswal,et al.  Network homogeneity reveals decreased integrity of default-mode network in ADHD , 2008, Journal of Neuroscience Methods.

[30]  F. Petermann,et al.  Neuropsychological Profiles on the WAIS-IV of Adults With ADHD , 2016, Journal of attention disorders.

[31]  H. Caci,et al.  A systematic review and analysis of long-term outcomes in attention deficit hyperactivity disorder: effects of treatment and non-treatment , 2012, BMC Medicine.

[32]  Sabine Kastner,et al.  Functional heterogeneity of conflict, error, task-switching, and unexpectedness effects within medial prefrontal cortex , 2011, NeuroImage.

[33]  V. Giampietro,et al.  Disorder-specific functional abnormalities during sustained attention in youth with Attention Deficit Hyperactivity Disorder (ADHD) and with Autism , 2013, Molecular Psychiatry.

[34]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[35]  Danielle Mizuiri,et al.  A lack of default network suppression is linked to increased distractibility in ADHD , 2009, Brain Research.

[36]  P. Liddle,et al.  Task-related default mode network modulation and inhibitory control in ADHD: effects of motivation and methylphenidate. , 2011, Journal of child psychology and psychiatry, and allied disciplines.

[37]  Yufeng Zang,et al.  Abnormal functional connectivity between the anterior cingulate and the default mode network in drug-naïve boys with attention deficit hyperactivity disorder , 2012, Psychiatry Research: Neuroimaging.

[38]  F. Castellanos,et al.  Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes , 2002, Nature Reviews Neuroscience.

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

[40]  F. Castellanos,et al.  Varieties of Attention-Deficit/Hyperactivity Disorder-Related Intra-Individual Variability , 2005, Biological Psychiatry.

[41]  F. Castellanos,et al.  Obesity in Men With Childhood ADHD: A 33-Year Controlled, Prospective, Follow-up Study , 2013, Pediatrics.

[42]  Bharat B. Biswal,et al.  Competition between functional brain networks mediates behavioral variability , 2008, NeuroImage.

[43]  M. Denckla,et al.  Revised Neurological Examination for Subtle Signs (1985). , 1985, Psychopharmacology bulletin.

[44]  L. Hawk,et al.  Reaction Time Variability in ADHD: A Review , 2012, Neurotherapeutics.

[45]  George Bush,et al.  Attention-Deficit/Hyperactivity Disorder and Attention Networks , 2010, Neuropsychopharmacology.

[46]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[47]  Alan C. Evans,et al.  Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. , 2002, JAMA.

[48]  Stewart H. Mostofsky,et al.  Increased intra-individual reaction time variability in attention-deficit/hyperactivity disorder across response inhibition tasks with different cognitive demands , 2009, Neuropsychologia.

[49]  G. Gioia,et al.  Response-Time Variability Is Related to Parent Ratings of Inattention, Hyperactivity, and Executive Function , 2011, Journal of attention disorders.

[50]  Brian S. Caffo,et al.  Developmental changes in within- and between-network connectivity between late childhood and adulthood , 2013, Neuropsychologia.

[51]  S. Rauch,et al.  Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting stroop , 1999, Biological Psychiatry.