Diffusion tensor imaging in attention deficit/hyperactivity disorder: A systematic review and meta-analysis

Diffusion tensor imaging (DTI) allows in vivo examination of the microstructural integrity of white matter brain tissue. A systematic review and quantitative meta-analysis using GingerALE were undertaken to compare current DTI findings in patients with ADHD and healthy controls to further unravel the neurobiological underpinnings of the disorder. Online databases were searched for DTI studies comparing white matter integrity between ADHD patients and healthy controls. Fifteen studies met inclusion criteria. Alterations in white matter integrity were found in widespread areas, most consistently so in the right anterior corona radiata, right forceps minor, bilateral internal capsule, and left cerebellum, areas previously implicated in the pathophysiology of the disorder. Current literature is critically discussed in terms of its important methodological limitations and challenges, and guidelines for future DTI research are provided. While more research is needed, DTI proves to be a promising technique, providing new prospects and challenges for future research into the pathophysiology of ADHD.

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

[2]  B. Ardekani,et al.  Diffusion tensor imaging reliably differentiates patients with schizophrenia from healthy volunteers , 2011, Human brain mapping.

[3]  Acosta Mt,et al.  [The neuroanatomy of attention deficit/hyperactivity disorder]. , 2004 .

[4]  Karl J. Friston,et al.  Topological FDR for neuroimaging , 2010, NeuroImage.

[5]  S. Hogg-Johnson,et al.  Using the Conners' Teacher Rating Scale—Revised in School Children Referred for Assessment , 2009, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[6]  Heikki Lyytinen,et al.  Corpus Callosum Morphology in Attention Deficit-Hyperactivity Disorder: Morphometric Analysis of MRI , 1991, Journal of learning disabilities.

[7]  S. Mostofsky,et al.  Abnormal cerebral cortex structure in children with ADHD , 2009, Human brain mapping.

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

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

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

[11]  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.

[12]  R. Kessler,et al.  The prevalence and correlates of adult ADHD in the United States: results from the National Comorbidity Survey Replication. , 2006, The American journal of psychiatry.

[13]  K. Lim,et al.  Advances in white matter imaging: A review of in vivo magnetic resonance methodologies and their applicability to the study of development and aging , 2006, Neuroscience & Biobehavioral Reviews.

[14]  Luke Bloy,et al.  Diffusion based abnormality markers of pathology: Toward learned diagnostic prediction of ASD , 2011, NeuroImage.

[15]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

[16]  G. Marchal,et al.  Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis: Revisited , 2009, Human brain mapping.

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

[18]  J. Hebebrand,et al.  Genetic aspects in attention-deficit/hyperactivity disorder , 2008, Journal of Neural Transmission.

[19]  G. Kindlmann,et al.  Orthogonal tensor invariants and the analysis of diffusion tensor magnetic resonance images , 2006, Magnetic resonance in medicine.

[20]  Alan C. Evans,et al.  Genetic Contributions to Human Brain Morphology and Intelligence , 2006, The Journal of Neuroscience.

[21]  Alan C. Evans,et al.  Development of cortical asymmetry in typically developing children and its disruption in attention-deficit/hyperactivity disorder. , 2009, Archives of general psychiatry.

[22]  Thomas E. Nichols,et al.  Controlling the familywise error rate in functional neuroimaging: a comparative review , 2003, Statistical methods in medical research.

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

[24]  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.

[25]  Sterling C. Johnson,et al.  Microstructural diffusion changes are independent of macrostructural volume loss in moderate to severe Alzheimer's disease. , 2010, Journal of Alzheimer's disease : JAD.

[26]  P. Basser,et al.  Comprehensive approach for correction of motion and distortion in diffusion‐weighted MRI , 2004, Magnetic resonance in medicine.

[27]  Ross Cunnington,et al.  Structural development of the basal ganglia in attention deficit hyperactivity disorder: A diffusion tensor imaging study , 2009, Psychiatry Research: Neuroimaging.

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

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

[30]  Daniel C Alexander,et al.  Multiple‐Fiber Reconstruction Algorithms for Diffusion MRI , 2005, Annals of the New York Academy of Sciences.

[31]  Alan C. Evans,et al.  Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder. , 2006, Archives of general psychiatry.

[32]  André J. W. van der Kouwe,et al.  The relationship between diffusion tensor imaging and volumetry as measures of white matter properties , 2008, NeuroImage.

[33]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

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

[35]  Fred L. Bookstein,et al.  “Voxel-Based Morphometry” Should Not Be Used with Imperfectly Registered Images , 2001, NeuroImage.

[36]  Eileen Luders,et al.  Reduced white matter integrity in attention-deficit hyperactivity disorder , 2008, Neuroreport.

[37]  Suzanne E. Welcome,et al.  Cortical abnormalities in children and adolescents with attention-deficit hyperactivity disorder , 2003, The Lancet.

[38]  S. Faraone,et al.  Age-dependent decline of symptoms of attention deficit hyperactivity disorder: impact of remission definition and symptom type. , 2000, The American journal of psychiatry.

[39]  Luis Concha,et al.  In Vivo Diffusion Tensor Imaging and Histopathology of the Fimbria-Fornix in Temporal Lobe Epilepsy , 2010, The Journal of Neuroscience.

[40]  B. Peterson.  Conceptual, methodological, and statistical challenges in brain imaging studies of developmentally based psychopathologies , 2003, Development and Psychopathology.

[41]  Joanna Jacobus,et al.  Sex differences in adolescent white matter architecture , 2011, Brain Research.

[42]  Stephen M. Smith,et al.  DTI measures in crossing-fibre areas: Increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease , 2011, NeuroImage.

[43]  R. Kraft,et al.  Relating imaging indices of white matter integrity and volume in healthy older adults. , 2008, Cerebral cortex.

[44]  W. Kaufmann,et al.  Increased Regional Fractional Anisotropy in Highly Screened Attention-Deficit Hyperactivity Disorder (ADHD) , 2011, Journal of child neurology.

[45]  M. Gill,et al.  The impact of study design and diagnostic approach in a large multi-centre ADHD study: Part 2: Dimensional measures of psychopathology and intelligence , 2011, BMC psychiatry.

[46]  N. Leeds,et al.  Assessing Glioma Cell Infiltration Using A Fiber Coherence Index: A DTI Study , 2005 .

[47]  B. Hart,et al.  Magnetic resonance imaging correlates of attention-deficit/hyperactivity disorder in children. , 2003, Neuropsychology.

[48]  Yufeng Zang,et al.  The macrostructural and microstructural abnormalities of corpus callosum in children with attention deficit/hyperactivity disorder: A combined morphometric and diffusion tensor MRI study , 2010, Brain Research.

[49]  G. Bush,et al.  Cortical thinning of the attention and executive function networks in adults with attention-deficit/hyperactivity disorder. , 2007, Cerebral cortex.

[50]  T. Ptak,et al.  Investigation of apparent diffusion coefficient and diffusion tensor anisotrophy in acute and chronic multiple sclerosis lesions. , 1999, AJNR. American journal of neuroradiology.

[51]  P. Renshaw,et al.  Volumetric MRI analysis comparing subjects having attention-deficit hyperactivity disorder with normal controls , 1997, Neurology.

[52]  T. Nakada,et al.  Absolute eigenvalue diffusion tensor analysis for human brain maturation , 2003, NMR in biomedicine.

[53]  Jan Sijbers,et al.  The effect of template selection on diffusion tensor voxel-based analysis results , 2011, NeuroImage.

[54]  Agatha D. Lee,et al.  Genetics of Brain Fiber Architecture and Intellectual Performance , 2009, The Journal of Neuroscience.

[55]  Brian B. Avants,et al.  High-Dimensional Spatial Normalization of Diffusion Tensor Images Improves the Detection of White Matter Differences: An Example Study Using Amyotrophic Lateral Sclerosis , 2007, IEEE Transactions on Medical Imaging.

[56]  Philip Shaw,et al.  Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. , 2007, The American journal of psychiatry.

[57]  K. Scheffler,et al.  Decreased fractional anisotropy in the middle cerebellar peduncle in children with epilepsy and/or attention deficit/hyperactivity disorder: A preliminary study , 2009, Epilepsy & Behavior.

[58]  Godfrey D Pearlson,et al.  MRI parcellation of the frontal lobe in boys with attention deficit hyperactivity disorder or Tourette syndrome , 2002, Psychiatry Research: Neuroimaging.

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

[60]  K. Konrad,et al.  Integrating genetic, psychopharmacological and neuroimaging studies: A converging methods approach to understanding the neurobiology of ADHD , 2007 .

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

[62]  J. Tsuruda,et al.  Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. , 1990, Radiology.

[63]  Conor Liston,et al.  Atypical Prefrontal Connectivity in Attention-Deficit/Hyperactivity Disorder: Pathway to Disease or Pathological End Point? , 2011, Biological Psychiatry.

[64]  Stewart H Mostofsky,et al.  Smaller prefrontal and premotor volumes in boys with attention-deficit/hyperactivity disorder , 2002, Biological Psychiatry.

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

[66]  U. Mödder,et al.  Age-dependent changes in magnetization transfer contrast of white matter in the pediatric brain. , 1998, AJNR. American journal of neuroradiology.

[67]  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.

[68]  Peter Dechent,et al.  Modeling the influence of TR and excitation flip angle on the magnetization transfer ratio (MTR) in human brain obtained from 3D spoiled gradient echo MRI , 2010, Magnetic resonance in medicine.

[69]  M. Gill,et al.  The impact of study design and diagnostic approach in a large multi-centre ADHD study. Part 1: ADHD symptom patterns , 2011, BMC psychiatry.

[70]  A Pfefferbaum,et al.  Genetic regulation of regional microstructure of the corpus callosum in late life , 2001, Neuroreport.

[71]  Glenn D. Rosen,et al.  Planum temporale asymmetry, reappraisal since Geschwind and Levitsky , 1987, Neuropsychologia.

[72]  Paul M. Thompson,et al.  journal homepage: www.elsevier.com/locate/ynimg Genetic influences on brain asymmetry: A DTI study of 374 twins and siblings , 2022 .

[73]  R. Woods,et al.  Widespread cortical thinning is a robust anatomical marker for attention-deficit/hyperactivity disorder. , 2009, Journal of the American Academy of Child and Adolescent Psychiatry.

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

[75]  John Russell,et al.  Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water , 2002, NeuroImage.

[76]  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.

[77]  R. Tannock,et al.  Diagnostic Instability of DSM–IV ADHD Subtypes: Effects of Informant Source, Instrumentation, and Methods for Combining Symptom Reports , 2010, Journal of clinical child and adolescent psychology : the official journal for the Society of Clinical Child and Adolescent Psychology, American Psychological Association, Division 53.

[78]  G. Bush,et al.  Dorsolateral Prefrontal and Anterior Cingulate Cortex Volumetric Abnormalities in Adults with Attention-Deficit/Hyperactivity Disorder Identified by Magnetic Resonance Imaging , 2006, Biological Psychiatry.

[79]  B. Franke,et al.  Integrated genome-wide association study findings: identification of a neurodevelopmental network for attention deficit hyperactivity disorder. , 2011, The American journal of psychiatry.

[80]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[81]  Walter H Backes,et al.  Assessing and minimizing the effects of noise and motion in clinical DTI at 3 T , 2009, Human brain mapping.

[82]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[83]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

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

[85]  A. Alexander,et al.  Diffusion tensor imaging of the brain , 2007, Neurotherapeutics.

[86]  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.

[87]  T. Paus,et al.  Cortical Gray Matter in Attention-Deficit/Hyperactivity Disorder: A Structural Magnetic Resonance Imaging Study , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[88]  M E Moseley,et al.  Comparison of diffusion‐ and T2‐weighted MRI for the early detection of cerebral ischemia and reperfusion in rats , 1991, Magnetic resonance in medicine.

[89]  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.

[90]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .

[91]  Karl J. Friston,et al.  False discovery rate revisited: FDR and topological inference using Gaussian random fields , 2009, NeuroImage.

[92]  Xiaoqi Huang,et al.  Increased fractional anisotropy in white matter of the right frontal region in children with attention-deficit/hyperactivity disorder: a diffusion tensor imaging study. , 2010, Neuro endocrinology letters.

[93]  Deepti Bathula,et al.  Altered white matter microstructure in children with attention-deficit/hyperactivity disorder. , 2011, Journal of the American Academy of Child and Adolescent Psychiatry.

[94]  A. Mayer,et al.  Head injury or head motion? Assessment and quantification of motion artifacts in diffusion tensor imaging studies , 2012, Human brain mapping.

[95]  Klaus Scheffler,et al.  Structural and functional imaging approaches in attention deficit/hyperactivity disorder: Does the temporal lobe play a key role? , 2010, Psychiatry Research: Neuroimaging.

[96]  John Suckling,et al.  Mapping brain structure in attention deficit-hyperactivity disorder: A voxel-based MRI study of regional grey and white matter volume , 2007, Psychiatry Research: Neuroimaging.

[97]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.