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      Regional brain network organization distinguishes the combined and inattentive subtypes of Attention Deficit Hyperactivity Disorder

      research-article
      a , b , a , a , c , a , c , d , e , a , b , *
      NeuroImage : Clinical
      Elsevier
      ACC, anterior cingulate cortex, ADHD, Attention Deficit Hyperactivity Disorder, ADHD-I, predominantly inattentive presentation, ADHD-C, combined presentation, ADHD-HI, predominantly hyperactive-impulsive, ADHD-RS-IV, Attention Deficit/Hyperactivity Disorder Rating Scale, CPRS-LV, Conners' Parent Rating Scale–Revised: Long Version, DSM-V, Diagnostic Manual of Statistical Disorders fifth edition, DICA, Diagnostic Interview for Children and Adolescents, DMN, default mode network, GM, gray matter, iSPOT-A, international study to predict optimized treatment in ADHD, MINI Kid, Mini International Neuropsychiatric Interview, MPH, methylphenidate, ADHD, Predominantly inattentive type, Combined type, Structural connectome, Volume, Graph theory

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          Abstract

          Attention Deficit Hyperactivity Disorder (ADHD) is characterized clinically by hyperactive/impulsive and/or inattentive symptoms which determine diagnostic subtypes as Predominantly Hyperactive-Impulsive (ADHD-HI), Predominantly Inattentive (ADHD-I), and Combined (ADHD-C). Neuroanatomically though we do not yet know if these clinical subtypes reflect distinct aberrations in underlying brain organization.

          We imaged 34 ADHD participants defined using DSM-IV criteria as ADHD-I ( n = 16) or as ADHD-C ( n = 18) and 28 matched typically developing controls, aged 8–17 years, using high-resolution T1 MRI. To quantify neuroanatomical organization we used graph theoretical analysis to assess properties of structural covariance between ADHD subtypes and controls (global network measures: path length, clustering coefficient, and regional network measures: nodal degree). As a context for interpreting network organization differences, we also quantified gray matter volume using voxel-based morphometry.

          Each ADHD subtype was distinguished by a different organizational profile of the degree to which specific regions were anatomically connected with other regions (i.e., in “nodal degree”). For ADHD-I (compared to both ADHD-C and controls) the nodal degree was higher in the hippocampus. ADHD-I also had a higher nodal degree in the supramarginal gyrus, calcarine sulcus, and superior occipital cortex compared to ADHD-C and in the amygdala compared to controls. By contrast, the nodal degree was higher in the cerebellum for ADHD-C compared to ADHD-I and in the anterior cingulate, middle frontal gyrus and putamen compared to controls. ADHD-C also had reduced nodal degree in the rolandic operculum and middle temporal pole compared to controls. These regional profiles were observed in the context of no differences in gray matter volume or global network organization.

          Our results suggest that the clinical distinction between the Inattentive and Combined subtypes of ADHD may also be reflected in distinct aberrations in underlying brain organization.

          Highlights

          • Structural connectome study of ADHD Inattentive and Combined subtypes.

          • Neurobiological mechanisms underlying the ADHD subtypes remain unclear.

          • Different profile of regional network measures characterized each subtype.

          • Network organization differences were observed in context of preserved volume.

          • Alterations of default mode network in ADHD Combined type than controls

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          Most cited references57

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          Small-world anatomical networks in the human brain revealed by cortical thickness from MRI.

          An important issue in neuroscience is the characterization for the underlying architectures of complex brain networks. However, little is known about the network of anatomical connections in the human brain. Here, we investigated large-scale anatomical connection patterns of the human cerebral cortex using cortical thickness measurements from magnetic resonance images. Two areas were considered anatomically connected if they showed statistically significant correlations in cortical thickness and we constructed the network of such connections using 124 brains from the International Consortium for Brain Mapping database. Significant short- and long-range connections were found in both intra- and interhemispheric regions, many of which were consistent with known neuroanatomical pathways measured by human diffusion imaging. More importantly, we showed that the human brain anatomical network had robust small-world properties with cohesive neighborhoods and short mean distances between regions that were insensitive to the selection of correlation thresholds. Additionally, we also found that this network and the probability of finding a connection between 2 regions for a given anatomical distance had both exponentially truncated power-law distributions. Our results demonstrated the basic organizational principles for the anatomical network in the human brain compatible with previous functional networks studies, which provides important implications of how functional brain states originate from their structural underpinnings. To our knowledge, this study provides the first report of small-world properties and degree distribution of anatomical networks in the human brain using cortical thickness measurements.
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            Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation.

            There is controversy over the nature of the disturbance in brain development that underpins attention-deficit/hyperactivity disorder (ADHD). In particular, it is unclear whether the disorder results from a delay in brain maturation or whether it represents a complete deviation from the template of typical development. Using computational neuroanatomic techniques, we estimated cortical thickness at >40,000 cerebral points from 824 magnetic resonance scans acquired prospectively on 223 children with ADHD and 223 typically developing controls. With this sample size, we could define the growth trajectory of each cortical point, delineating a phase of childhood increase followed by adolescent decrease in cortical thickness (a quadratic growth model). From these trajectories, the age of attaining peak cortical thickness was derived and used as an index of cortical maturation. We found maturation to progress in a similar manner regionally in both children with and without ADHD, with primary sensory areas attaining peak cortical thickness before polymodal, high-order association areas. However, there was a marked delay in ADHD in attaining peak thickness throughout most of the cerebrum: the median age by which 50% of the cortical points attained peak thickness for this group was 10.5 years (SE 0.01), which was significantly later than the median age of 7.5 years (SE 0.02) for typically developing controls (log rank test chi(1)(2) = 5,609, P < 1.0 x 10(-20)). The delay was most prominent in prefrontal regions important for control of cognitive processes including attention and motor planning. Neuroanatomic documentation of a delay in regional cortical maturation in ADHD has not been previously reported.
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              Meta-analysis of structural imaging findings in attention-deficit/hyperactivity disorder.

              Although there are many structural neuroimaging studies of attention-deficit/hyperactivity disorder (ADHD) in children, there are inconsistencies across studies and no consensus regarding which brain regions show the most robust area or volumetric reductions relative to control subjects. Our goal was to statistically analyze structural imaging data via a meta-analysis to help resolve these issues. We searched the MEDLINE and PsycINFO databases through January 2005. Studies must have been written in English, used magnetic resonance imaging, and presented the means and standard deviations of regions assessed. Data were extracted by one of the authors and verified independently by another author. Analyses were performed using STATA with metan, metabias, and metainf programs. A meta-analysis including all regions across all studies indicated global reductions for ADHD subjects compared with control subjects, standardized mean difference=.408, p<.001. Regions most frequently assessed and showing the largest differences included cerebellar regions, the splenium of the corpus callosum, total and right cerebral volume, and right caudate. Several frontal regions assessed in only two studies also showed large significant differences. This meta-analysis provides a quantitative analysis of neuroanatomical abnormalities in ADHD and information that can be used to guide future studies.
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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                22 May 2017
                2017
                22 May 2017
                : 15
                : 383-390
                Affiliations
                [a ]Brain Dynamics Centre, The Westmead Institute for Medical Research, The University of Sydney, Australia
                [b ]The Discipline of Psychiatry, University of Sydney Medical School: Western, Westmead Hospital, Australia
                [c ]Centre for Research into Adolescents' Health, Department of Adolescent and Young Adult Medicine, Westmead Hospital, Australia
                [d ]Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA, USA
                [e ]MIRECC, Palo Alto VA, Palo Alto, CA, USA
                Author notes
                [* ]Corresponding author at: Brain Dynamics Centre, The Westmead Institute for Medical Research, 176 Hawkesbury Road, Westmead, NSW 2145, Australia.Brain Dynamics CentreThe Westmead Institute for Medical Research176 Hawkesbury RoadWestmeadNSW2145Australia m.korgaonkar@ 123456sydney.edu.au
                Article
                S2213-1582(17)30121-3
                10.1016/j.nicl.2017.05.016
                5447655
                c86792d2-c8fd-484f-b3d0-282b96a8f88b
                © 2017 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 28 October 2016
                : 10 April 2017
                : 21 May 2017
                Categories
                Regular Article

                acc, anterior cingulate cortex,adhd, attention deficit hyperactivity disorder,adhd-i, predominantly inattentive presentation,adhd-c, combined presentation,adhd-hi, predominantly hyperactive-impulsive,adhd-rs-iv, attention deficit/hyperactivity disorder rating scale,cprs-lv, conners' parent rating scale–revised: long version,dsm-v, diagnostic manual of statistical disorders fifth edition,dica, diagnostic interview for children and adolescents,dmn, default mode network,gm, gray matter,ispot-a, international study to predict optimized treatment in adhd,mini kid, mini international neuropsychiatric interview,mph, methylphenidate,adhd,predominantly inattentive type,combined type,structural connectome,volume,graph theory

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