Decreased frontostriatal microstructural organization in attention deficit/hyperactivity disorder

Frontostriatal brain areas have been implicated in the neurobiology of attention deficit/hyperactivity disorder (ADHD), but little work has directly addressed the white matter connections between these regions. The present study investigates the microstructural organization and myelination of frontostriatal white matter in children with ADHD and controls. Diffusion tensor imaging and magnetization transfer imaging scans were acquired in 30 children with ADHD and 34 controls. A study specific volume of interest (VOI) of frontostriatal white matter was created using a tractography based statistical group map. Fractional anisotropy (FA, indexing microstructural organization) and magnetization transfer ratio (MTR, indexing macromolecular content, myelin in particular) were computed for the frontostriatal VOI and for total cerebral white matter. Exploratory analyses were conducted investigating the effect of stimulant use on these measures. Frontostriatal FA but not MTR was decreased in ADHD compared with controls. There were no differences in FA or MTR for total cerebral white matter. Frontostriatal FA correlated negatively with teacher‐rated attention problems in controls but not children with ADHD. The duration of stimulant use did not affect the main results. Changes in frontostriatal connectivity in ADHD appear to be related to changes in microstructural organization rather than myelination per se. A correlation with attention problems for controls suggests that frontostriatal organization is relevant to ADHD‐related behaviors. Hum Brain Mapp, 2012. © 2011 Wiley Periodicals, Inc

[1]  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.

[2]  Hugo G. Schnack,et al.  Changes in the Developmental Trajectories of Striatum in Autism , 2009, Biological Psychiatry.

[3]  H. van Engeland,et al.  Trends in incidence and characteristics of children, adolescents, and adults initiating immediate- or extended-release methylphenidate or atomoxetine in the Netherlands during 2001-2006. , 2010, Journal of child and adolescent psychopharmacology.

[4]  John L Bradshaw,et al.  White‐matter abnormalities in attention deficit hyperactivity disorder: A diffusion tensor imaging study , 2009, Human brain mapping.

[5]  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.

[6]  D. Louis Collins,et al.  Automatic 3‐D model‐based neuroanatomical segmentation , 1995 .

[7]  J. Lancaster,et al.  Volumetric MRI differences in treatment-naïve vs chronically treated children with ADHD , 2006, Neurology.

[8]  D. Cantwell,et al.  Comorbidity in ADHD: implications for research, practice, and DSM-V. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[9]  L. Westlye,et al.  Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. , 2010, Cerebral cortex.

[10]  Matthew K Nock,et al.  Lifetime prevalence, correlates, and persistence of oppositional defiant disorder: results from the National Comorbidity Survey Replication. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[11]  D. Shaffer,et al.  NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): description, differences from previous versions, and reliability of some common diagnoses. , 2000, Journal of the American Academy of Child and Adolescent Psychiatry.

[12]  N. Makris,et al.  Structural Brain Imaging of Attention-Deficit/Hyperactivity Disorder , 2005, Biological Psychiatry.

[13]  S. Debener,et al.  Default-mode brain dysfunction in mental disorders: A systematic review , 2009, Neuroscience & Biobehavioral Reviews.

[14]  Gady Agam,et al.  Development of a human brain diffusion tensor template , 2009, NeuroImage.

[15]  L. Bickman,et al.  Assessing the Impact of Parent and Teacher Agreement on Diagnosing Attention-Deficit Hyperactivity Disorder , 2004, Journal of developmental and behavioral pediatrics : JDBP.

[16]  C. Liston,et al.  Frontostriatal microstructure modulates efficient recruitment of cognitive control. , 2006, Cerebral cortex.

[17]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[18]  John A. Sweeney,et al.  Diffusion Tensor Imaging Study of White Matter Fiber Tracts in Pediatric Bipolar Disorder and Attention-Deficit/Hyperactivity Disorder , 2009, Biological Psychiatry.

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

[20]  Arthur W. Toga,et al.  Atlas-based whole brain white matter analysis using large deformation diffeomorphic metric mapping: Application to normal elderly and Alzheimer's disease participants , 2009, NeuroImage.

[21]  S. Haber The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[22]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

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

[24]  Marieke Langen,et al.  Caudate Nucleus Is Enlarged in High-Functioning Medication-Naive Subjects with Autism , 2007, Biological Psychiatry.

[25]  Michael P Milham,et al.  The neural correlates of attention deficit hyperactivity disorder: an ALE meta-analysis. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

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

[27]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[28]  Vincent Giampietro,et al.  Reduced activation and inter-regional functional connectivity of fronto-striatal networks in adults with childhood Attention-Deficit Hyperactivity Disorder (ADHD) and persisting symptoms during tasks of motor inhibition and cognitive switching. , 2010, Journal of psychiatric research.

[29]  Kelvin O. Lim,et al.  Differential fractional anisotropy abnormalities in adolescents with ADHD or schizophrenia , 2010, Psychiatry Research: Neuroimaging.

[30]  Rozmin Halari,et al.  Methylphenidate normalises activation and functional connectivity deficits in attention and motivation networks in medication-naïve children with ADHD during a rewarded continuous performance task , 2009, Neuropharmacology.

[31]  Nikos Makris,et al.  Towards Conceptualizing a Neural Systems-Based Anatomy of Attention-Deficit/Hyperactivity Disorder , 2009, Developmental Neuroscience.

[32]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[33]  Rachel M. Brouwer,et al.  Segmentation of MRI brain scans using non-uniform partial volume densities , 2010, NeuroImage.

[34]  Sarah Durston,et al.  Imaging genetics in ADHD: A focus on cognitive control , 2009, Neuroscience & Biobehavioral Reviews.

[35]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[36]  B. Horta,et al.  The worldwide prevalence of ADHD: a systematic review and metaregression analysis. , 2007, The American journal of psychiatry.

[37]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[38]  Stefan Skare,et al.  A Model-Based Method for Retrospective Correction of Geometric Distortions in Diffusion-Weighted EPI , 2002, NeuroImage.

[39]  Marieke Langen,et al.  Magnetic resonance simulation is effective in reducing anxiety related to magnetic resonance scanning in children. , 2009, Journal of the American Academy of Child and Adolescent Psychiatry.

[40]  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.

[41]  Alan C. Evans,et al.  Psychostimulant treatment and the developing cortex in attention deficit hyperactivity disorder. , 2009, The American journal of psychiatry.

[42]  Nikos Makris,et al.  Attention and executive systems abnormalities in adults with childhood ADHD: A DT-MRI study of connections. , 2008, Cerebral cortex.

[43]  S. Faraone,et al.  Meta-Analysis of Structural Imaging Findings in Attention-Deficit/Hyperactivity Disorder , 2007, Biological Psychiatry.

[44]  R S Balaban,et al.  Magnetization transfer imaging: practical aspects and clinical applications. , 1994, Radiology.

[45]  Derek K. Jones,et al.  RESTORE: Robust estimation of tensors by outlier rejection , 2005, Magnetic resonance in medicine.

[46]  Peter Stoeter,et al.  Disturbed structural connectivity is related to inattention and impulsivity in adult attention deficit hyperactivity disorder , 2010, The European journal of neuroscience.

[47]  Alexander Leemans,et al.  Microstructural maturation of the human brain from childhood to adulthood , 2008, NeuroImage.

[48]  D. Le Bihan,et al.  Diffusion tensor imaging: Concepts and applications , 2001, Journal of magnetic resonance imaging : JMRI.

[49]  J. Nigg,et al.  An integrative theory of attention-deficit/ hyperactivity disorder based on the cognitive and affective neurosciences , 2005, Development and Psychopathology.

[50]  J. Shuster,et al.  Utilization of Pharmacologic Treatment in Youths with Attention Deficit/Hyperactivity Disorder in Medicaid Database , 2008, The Annals of pharmacotherapy.

[51]  Gary Glover,et al.  Frontostriatal connectivity and its role in cognitive control in parent-child dyads with ADHD. , 2007, The American journal of psychiatry.

[52]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[53]  D. Louis Collins,et al.  Focal white matter density changes in schizophrenia: reduced inter-hemispheric connectivity , 2004, NeuroImage.

[54]  M. Bronskill,et al.  Characterizing white matter with magnetization transfer and T2 , 1999, Magnetic resonance in medicine.

[55]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[56]  P. Boesiger,et al.  SENSE‐DTI at 3 T , 2004, Magnetic resonance in medicine.

[57]  Sarah Durston,et al.  A shift from diffuse to focal cortical activity with development. , 2006, Developmental science.

[58]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[59]  R. Kahn,et al.  Tract-based analysis of magnetization transfer ratio and diffusion tensor imaging of the frontal and frontotemporal connections in schizophrenia. , 2010, Schizophrenia bulletin.

[60]  Gareth J. Barker,et al.  Diffusion tractography based group mapping of major white-matter pathways in the human brain , 2003, NeuroImage.

[61]  Alan C. Evans,et al.  Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation , 2007, Proceedings of the National Academy of Sciences.

[62]  R. Kahn,et al.  Automated Separation of Gray and White Matter from MR Images of the Human Brain , 2001, NeuroImage.

[63]  R. S. Kahn,et al.  Automatic Segmentation of the Ventricular System from MR Images of the Human Brain , 2001, NeuroImage.

[64]  Babak A. Ardekani,et al.  ttention-Deficit/Hyperactivity Disorder: Preliminary Diffusion Tensor Imaging Study , 2005 .