Latent resting-state network dynamics in boys and girls with attention-deficit/hyperactivity disorder

Neuroimaging studies of subjects with ADHD typically show altered functional connectivity in prefrontal, striatal, and several temporal brain regions. While the majority of studies have focused on connectivity that is averaged over time, we investigated the temporal dynamics of brain network changes in resting-state fMRI. Using the ADHD-200 consortium, we characterized the time course of latent state changes using Hidden Markov Modeling, and compared state changes between boys and girls with ADHD along with typically developing controls. Sex differences were found in latent state switching, with boys dwelling longer in a given state than girls, and concurrently having fewer overall state transitions. These sex differences were found in children with ADHD and in typically developing controls. Children with ADHD were also found to be more variable in terms of state transitions than controls. These findings add to the growing literature on neural sex differences and may be related to the sex difference in focal versus diffuse attention.

[1]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[2]  Stephen M. Smith,et al.  Brain network dynamics are hierarchically organized in time , 2017, Proceedings of the National Academy of Sciences.

[3]  P F Renshaw,et al.  Using MRI to examine brain-behavior relationships in males with attention deficit disorder with hyperactivity. , 2000, Journal of the American Academy of Child and Adolescent Psychiatry.

[4]  Jin Fan,et al.  Response inhibition in adolescents diagnosed with attention deficit hyperactivity disorder during childhood: an event-related FMRI study. , 2004, The American journal of psychiatry.

[5]  G H Glover,et al.  Selective effects of methylphenidate in attention deficit hyperactivity disorder: a functional magnetic resonance study. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Rucklidge.  Gender differences in attention-deficit/hyperactivity disorder. , 2010, The Psychiatric clinics of North America.

[7]  Fabio Sambataro,et al.  Regional brain activation changes and abnormal functional connectivity of the ventrolateral prefrontal cortex during working memory processing in adults with attention‐deficit/hyperactivity disorder , 2009, Human brain mapping.

[8]  M. Chun,et al.  A neuromarker of sustained attention from whole-brain functional connectivity , 2015, Nature Neuroscience.

[9]  H. Feldman,et al.  Academic and educational outcomes of children with ADHD. , 2007, Journal of pediatric psychology.

[10]  M. Raichle.  The brain's default mode network. , 2015, Annual review of neuroscience.

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

[12]  Steven M Boker,et al.  Issues in intraindividual variability: individual differences in equilibria and dynamics over multiple time scales. , 2009, Psychology and aging.

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

[14]  Wei Li,et al.  Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[15]  J N Giedd,et al.  Cerebellum in attention-deficit hyperactivity disorder , 1998, Neurology.

[16]  Jan K Buitelaar,et al.  Magnetic resonance imaging of boys with attention-deficit/hyperactivity disorder and their unaffected siblings. , 2004, Journal of the American Academy of Child and Adolescent Psychiatry.

[17]  Larry J. Seidman,et al.  Functional MRI in attention-deficit hyperactivity disorder: Evidence for hypofrontality , 2005, Brain and Development.

[18]  Kerstin Konrad,et al.  Is the ADHD brain wired differently? A review on structural and functional connectivity in attention deficit hyperactivity disorder , 2010, Human brain mapping.

[19]  Andrew J. Bulpitt,et al.  A Primer on Learning in Bayesian Networks for Computational Biology , 2007, PLoS Comput. Biol..

[20]  Jonathan Gershon,et al.  A Meta-Analytic Review of Gender Differences in ADHD , 2002, Journal of attention disorders.

[21]  C. Carlson,et al.  Gender differences in ADHD: a meta-analysis and critical review. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[22]  Joseph Biederman,et al.  The age-dependent decline of attention deficit hyperactivity disorder: a meta-analysis of follow-up studies , 2005, Psychological Medicine.

[23]  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.

[24]  S. Rombouts,et al.  Structural and functional connectivity in children and adolescents with and without attention deficit/hyperactivity disorder , 2017, Journal of child psychology and psychiatry, and allied disciplines.

[25]  D. Louis Collins,et al.  Unbiased average age-appropriate atlases for pediatric studies , 2011, NeuroImage.

[26]  E. DeYoe,et al.  Reduction of physiological fluctuations in fMRI using digital filters , 1996, Magnetic resonance in medicine.

[27]  R. Barkley.  Issues in the diagnosis of attention-deficit/hyperactivity disorder in children , 2003, Brain and Development.

[28]  Daniel S. Margulies,et al.  The Neuro Bureau ADHD-200 Preprocessed repository , 2016, NeuroImage.

[29]  E. Bullmore,et al.  Hypofrontality in attention deficit hyperactivity disorder during higher-order motor control: a study with functional MRI. , 1999, The American journal of psychiatry.

[30]  M. Kogan,et al.  Trends in the parent-report of health care provider-diagnosed and medicated attention-deficit/hyperactivity disorder: United States, 2003-2011. , 2014, Journal of the American Academy of Child and Adolescent Psychiatry.

[31]  Peter C. M. Molenaar,et al.  The New Person-Specific Paradigm in Psychology , 2009 .

[32]  W. Johnson,et al.  Sex differences in mental abilities: g masks the dimensions on which they lie , 2007 .

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

[34]  Lain L. MacDonald,et al.  Hidden Markov and Other Models for Discrete- valued Time Series , 1997 .

[35]  Yong He,et al.  Imaging Functional and Structural Brain Connectomics in Attention-Deficit/Hyperactivity Disorder , 2014, Molecular Neurobiology.

[36]  R Cameron Craddock,et al.  A whole brain fMRI atlas generated via spatially constrained spectral clustering , 2012, Human brain mapping.

[37]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[38]  Tianzi Jiang,et al.  Enhanced resting-state brain activities in ADHD patients: A fMRI study , 2008, Brain and Development.

[39]  S. P. Pederson,et al.  Hidden Markov and Other Models for Discrete-Valued Time Series , 1998 .

[40]  P. Molenaar.  A Manifesto on Psychology as Idiographic Science: Bringing the Person Back Into Scientific Psychology, This Time Forever , 2004 .

[41]  Gustavo Deco,et al.  Can sliding-window correlations reveal dynamic functional connectivity in resting-state fMRI? , 2016, NeuroImage.

[42]  J. Morton,et al.  Tracking the Brain's Functional Coupling Dynamics over Development , 2015, The Journal of Neuroscience.

[43]  Ingmar Visser,et al.  Seven things to remember about hidden Markov models: A tutorial on Markovian models for time series , 2011 .

[44]  David A. Leopold,et al.  Dynamic functional connectivity: Promise, issues, and interpretations , 2013, NeuroImage.

[45]  N. Volkow,et al.  Abnormal Functional Connectivity in Children with Attention-Deficit/Hyperactivity Disorder , 2012, Biological Psychiatry.

[46]  R. Halari,et al.  A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with Attention Deficit Hyperactivity Disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention , 2012, Cortex.

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

[48]  Ernesto Pereda,et al.  The variability of EEG functional connectivity of young ADHD subjects in different resting states , 2016, Clinical Neurophysiology.

[49]  Brian Caffo,et al.  Comparing test-retest reliability of dynamic functional connectivity methods , 2017, NeuroImage.

[50]  U. Müller,et al.  Occupational issues of adults with ADHD , 2013, BMC Psychiatry.

[51]  L. Hedges,et al.  Sex differences in mental test scores, variability, and numbers of high-scoring individuals. , 1995, Science.

[52]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[53]  R. Todd,et al.  Sex and age differences in attention-deficit/hyperactivity disorder symptoms and diagnoses: implications for DSM-V and ICD-11. , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[54]  S. Bálint,et al.  Prevalence and correlates of adult attention-deficit hyperactivity disorder: meta-analysis , 2009, British Journal of Psychiatry.

[55]  Mark E Bastin,et al.  Sex Differences in the Adult Human Brain: Evidence from 5216 UK Biobank Participants , 2017, bioRxiv.

[56]  L. Wolf,et al.  College Students with ADHD and Other Hidden Disabilities , 2001, Annals of the New York Academy of Sciences.

[57]  P. Prins,et al.  Social incompetence in children with ADHD: possible moderators and mediators in social-skills training. , 2007, Clinical psychology review.

[58]  Aaron Kucyi,et al.  Disrupted functional connectivity of cerebellar default network areas in attention‐deficit/hyperactivity disorder , 2015, Human brain mapping.

[59]  David G. Norris,et al.  Characterising resting-state functional connectivity in a large sample of adults with ADHD , 2016, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

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

[61]  B. J. Casey,et al.  Differential patterns of striatal activation in young children with and without ADHD , 2003, Biological Psychiatry.

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

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

[64]  M. Greicius.  Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[65]  Chao Zhang,et al.  Functional connectivity predicts gender: Evidence for gender differences in resting brain connectivity , 2018, Human brain mapping.

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

[67]  G. Salum,et al.  ADHD prevalence estimates across three decades: an updated systematic review and meta-regression analysis. , 2013, International journal of epidemiology.