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Cited by 249Attention Deficit Hyperactivity DisorderHemispheric Asymmetry in NeuroscienceAutism Spectrum Disorder Research

Development of cortical asymmetry in typically developing children and its disruption in attention-deficit/hyperactivity disorder

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Shaw, Philip, Lalonde, Francois, Lepage, Claude, Rabin, Cara, Eckstrand, Kristen, Sharp, Wendy, Greenstein, Deanna, Evans, Alan +2 more·2009·Archives of General Psychiatry
DOI 10.1001/archgenpsychiatry.2009.103PMC PMC2948210
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Abstract

CONTEXT: Just as typical development of anatomical asymmetries in the human brain has been linked with normal lateralization of motor and cognitive functions, disruption of asymmetry has been implicated in the pathogenesis of neurodevelopmental disorders such as attention-deficit/hyperactivity disorder (ADHD). No study has examined the development of cortical asymmetry using longitudinal neuroanatomical data. OBJECTIVE: To delineate the development of cortical asymmetry in children with and without ADHD. DESIGN: Longitudinal study. SETTING: Government Clinical Research Institute. PARTICIPANTS: A total of 218 children with ADHD and 358 typically developing children, from whom 1133 neuroanatomical magnetic resonance images were acquired prospectively. MAIN OUTCOME MEASURES: Cortical thickness was estimated at 40 962 homologous points in the left and right hemispheres, and the trajectory of change in asymmetry was defined using mixed-model regression. RESULTS: In right-handed typically developing individuals, a mean (SE) increase in the relative thickness of the right orbitofrontal and inferior frontal cortex with age of 0.011 (0.0018) mm per year (t(337) = 6.2, P < .001) was balanced against a relative left-hemispheric increase in the occipital cortical regions of 0.013 (0.0015) mm per year (t(337) = 8.1, P < .001). Age-related change in asymmetry in non-right-handed typically developing individuals was less extensive and was localized to different cortical regions. In ADHD, the posterior component of this evolving asymmetry was intact, but the prefrontal component was lost. CONCLUSIONS: These findings explain the way that, in typical development, the increased dimensions of the right frontal and left occipital cortical regions emerge in adulthood from the reversed pattern of childhood cortical asymmetries. Loss of the prefrontal component of this evolving asymmetry in ADHD is compatible with disruption of prefrontal function in the disorder and demonstrates the way that disruption of typical processes of asymmetry can inform our understanding of neurodevelopmental disorders.

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  1. [1]Toga AW Thompson PM Mapping brain asymmetry Nat Rev Neurosci 2003 4 1 37 48 12511860
  2. [2]Galaburda AM LeMay M Kemper TL Geschwind N Right-left asymmetrics in the brain Science 1978 199 4331 852 856 341314
  3. [3]Crow TJ Schizophrenia as failure of hemispheric dominance for language Trends Neurosci 1997 20 8 339 343 9246721
  4. [4]Herbert MR Ziegler DA Deutsch CK O'Brien LM Kennedy DN Filipek PA Bakard-jiev AI Hodgson J Takeoka M Makris N Caviness VS Jr Brain asymmetries in autism and developmental language disorder: a nested whole-brain analysis Brain 2005 128 pt 1 213 226 15563515
  5. [5]Rubia K Overmeyer S Taylor E Brammer M Williams SC Simmons A Andrew C Bullmore ET Functional frontalisation with age: mapping neurodevelopmental trajectories with fMRI Neurosci Biobehav Rev 2000 24 1 13 19 10654655
  6. [6]Le May M Kido DK Asymmetries of the cerebral hemispheres on computed tomograms J Comput Assist Tomogr 1978 2 4 471 476 708500
  7. [7]Bilder RM Wu H Bogerts B Degreef G Ashtari M Alvir JM Snyder PJ Lieberman JA Absence of regional hemispheric volume asymmetries in first-episode schizophrenia Am J Psychiatry 1994 151 10 1437 1447 8092337
  8. [8]Bear D Schiff D Saver J Greenberg M Freeman R Quantitative analysis of cerebral asymmetries: fronto-occipital correlation, sexual dimorphism, and association with handedness Arch Neurol 1986 43 6 598 603 3718289
  9. [10]Watkins KE Paus T Lerch JP Zijdenbos A Collins DL Neelin P Taylor J Worsley KJ Evans AC Structural asymmetries in the human brain: a voxel-based statistical analysis of 142 MRI scans Cereb Cortex 2001 11 9 868 877 11532891
  10. [11]LeMay M Morphological cerebral asymmetries of modern man, fossil man, and nonhuman primate Ann N Y Acad Sci 1976 280 349 366 827951
  11. [12]Giedd JN Snell JW Lange N Rajapakse JC Casey BJ Kozuch PL Vaituzis AC Vauss YC Hamburger SD Kaysen D Rapoport JL Quantitative magnetic resonance imaging of human brain development: ages 4-18 Cereb Cortex 1996 6 4 551 560 8670681
  12. [13]Reiss AL Abrams MT Singer HS Ross JL Denckla MB Brain development, gender and IQ in children: a volumetric imaging study Brain 1996 119 pt 5 1763 1774 8931596
  13. [14]Matsuzawa J Matsui M Konishi T Noguchi K Gur RC Bilker W Miyawaki T Age-related volumetric changes of brain gray and white matter in healthy infants and children Cereb Cortex 2001 11 4 335 342 11278196
  14. [15]Gilmore JH Lin W Prastawa MW Looney CB Vetsa YSK Knickmeyer RC Evans DD Smith JK Hamer RM Lieberman JA Gerig G Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain J Neurosci 2007 27 6 1255 1260 17287499 PMC2886661
  15. [16]Woods RP Dodrill CB Ojemann GA Brain injury, handedness, and speech lateralization in a series of amobarbital studies Ann Neurol 1988 23 5 510 518 3389757
  16. [17]Narr KL Bilder RM Luders E Thompson PM Woods RP Robinson D Szeszko PR Dimtcheva T Gurbani M Toga AW Asymmetries of cortical shape: effects of handedness, sex and schizophrenia Neuroimage 2007 34 3 939 948 17166743 PMC3299195
  17. [19]Shapleske J Rossell SL Woodruff PW David AS The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance Brain Res Brain Res Rev 1999 29 1 26 49 9974150
  18. [20]Barrick TR Mackay CE Prima S Maes F Vandermeulen D Crow TJ Roberts N Automatic analysis of cerebral asymmetry: an exploratory study of the relationship between brain torque and planum temporale asymmetry Neuroimage 2005 24 3 678 691 15652303
  19. [21]Geschwind N Levitsky W Human brain: left-right asymmetries in temporal speech region Science 1968 161 837 186 187 5657070
  20. [22]Steinmetz H Structure, functional and cerebral asymmetry: in vivo morphometry of the planum temporale Neurosci Biobehav Rev 1996 20 4 587 591 8994197
  21. [23]Foundas AL Eure KF Luevano LF Weinberger DR MRI asymmetries of Broca's area: the pars triangularis and pars opercularis Brain Lang 1998 64 3 282 296 9743543
  22. [24]Falzi G Perrone P Vignolo LA Right-left asymmetry in anterior speech region Arch Neurol 1982 39 4 239 240 7073534
  23. [25]Luders E Narr KL Thompson PM Rex DE Jancke L Toga AW Hemispheric asymmetries in cortical thickness Cereb Cortex 2006 16 8 1232 1238 16267139
  24. [26]Amunts K Schlaug G Schleicher A Steinmetz H Dabringhaus A Roland PE Zilles K Asymmetry in the human motor cortex and handedness Neuroimage 1996 4 3, pt 1 216 222 9345512
  25. [27]McManus IC Bryden MP Geschwind's theory of cerberal lateralization: developing a formal, causal model Psychol Bull 1991 110 2 237 253 1946868
  26. [28]Geschwind DH Miller BL DeCarli C Carmelli D Heritability of lobar brain volumes in twins supports genetic models of cerebral laterality and handedness Proc Natl Acad Sci U S A 2002 99 5 3176 3181 11867730 PMC122492
  27. [29]Annett M Handedness in the children of two left-handed parents Br J Psychol 1974 65 1 129 131 4822769
  28. [32]Rubia K Smith AB Brammer MJ Toone B Taylor E Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD Am J Psychiatry 2005 162 6 1067 1075 15930054
  29. [33]Langleben DD Austin G Krikorian G Ridlehuber HW Goris ML Strauss HW Interhemispheric asymmetry of regional cerebral blood flow in prepubescent boys with attention deficit hyperactivity disorder Nucl Med Commun 2001 22 12 1333 1340 11711904
  30. [34]Shaw P Lerch JP Pruessner JC Taylor KN Rose AB Greenstein D Clasen L Evans A Rapoport JL Giedd JN Cortical morphology in children and adolescents with different apolipoprotein E gene polymorphisms: an observational study Lancet Neurol 2007 6 6 494 500 17509484
  31. [35]Giedd JN Blumenthal J Jeffries NO Castellanos FX Liu H Zijdenbos A Paus T Evans AC Rapoport JL Brain development during childhood and adolescence: a longitudinal MRI study Nat Neurosci 1999 2 10 861 863 10491603
  32. [37]Denckla MB Revised neurological examination for subtle signs Psychopharmacol Bull 1985 21 4 773 800 4089106
  33. [38]Shaw P Eckstrand K Sharp W Blumenthal J Lerch JP Greenstein D Clasen L Evans A Giedd J Rapoport JL Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation Proc Natl Acad Sci U S A 2007 104 49 19649 19654 18024590 PMC2148343
  34. [39]Shaw P Lerch J Greenstein D Sharp W Clasen L Evans A Giedd J Castellanos FX Rapoport J Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit /hyperactivity disorder Arch Gen Psychiatry 2006 63 5 540 549 16651511
  35. [41]Reich W Diagnostic Interview for Children and Adolescents (DICA) J Am Acad Child Adolesc Psychiatry 2000 39 1 59 66 10638068
  36. [42]Werry JS Sprague RL Cohen MN Conners' Teacher Rating Scale for use in drug studies with children: an empirical study J Abnorm Child Psychol 1975 3 3 217 229 1214032
  37. [44]Smith SM Fast robust automated brain extraction Hum Brain Mapp 2002 17 3 143 155 12391568 PMC6871816
  38. [45]Grabner G Janke AL Budge MM Smith D Pruessner J Collins DL Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults Med Image Comput Comput Assist Interv Int Conf Med Image Comput Comput Assist Interv 2006 9 pt 2 58 66 17354756
  39. [47]Sled JG Zijdenbos AP Evans AC A nonparametric method for automatic correction of intensity nonuniformity in MRI data IEEE Trans Med Imaging 1998 17 1 87 97 9617910
  40. [48]Zijdenbos AP Forghani R Evans AC Automatic “pipeline” analysis of 3-D MRI data for clinical trials: application to multiple sclerosis IEEE Trans Med Imaging 2002 21 10 1280 1291 12585710
  41. [49]Tohka J Zijdenbos A Evans A Fast and robust parameter estimation for statistical partial volume models in brain MRI Neuroimage 2004 23 1 84 97 15325355
  42. [50]Kim JS Singh V Lee JK Lerch J Ad-Dab'bagh Y MacDonald D Lee JM Kim SI Evans AC Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification Neuroimage 2005 27 1 210 221 15896981
  43. [51]MacDonald D Kabani N Avis D Evans AC Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI Neuroimage 2000 12 3 340 356 10944416
  44. [52]Robbins S Evans AC Collins DL Whitesides S Tuning and comparing spatial normalization methods Med Image Anal 2004 8 3 311 323 15450225
  45. [53]Lyttelton O Boucher M Robbins S Evans A An unbiased iterative group registration template for cortical surface analysis Neuroimage 2007 34 4 1535 1544 17188895
  46. [54]Chung MK Worsley KJ Robbins S Paus T Taylor J Giedd JN Rapoport JL Evans AC Deformation-based surface morphometry applied to gray matter deformation Neuroimage 2003 18 2 198 213 12595176
  47. [55]Lerch JP Evans AC Cortical thickness analysis examined through power analysis and a population simulation Neuroimage 2005 24 1 163 173 15588607
  48. [56]Lee JK Lee JM Kim JS Kim IY Evans AC Kim SI A novel quantitative cross-validation of different cortical surface reconstruction algorithms using MRI phantom Neuroimage 2006 31 2 572 584 16503170
  49. [57]Singh V Chertkow H Lerch JP Evans AC Dorr AE Kabani NJ Spatial patterns of cortical thinning in mild cognitive impairment and Alzheimer's disease Brain 2006 129 pt 11 2885 2893 17008332
  50. [58]Pinheiro JC Bates DM Mixed-Effects Models in S and S-PLUS New York, NY Springer Publishing Company 2000
  51. [59]Genovese CR Lazar NA Nichols T Thresholding of statistical maps in functional neuroimaging using the false discovery rate Neuroimage 2002 15 4 870 878 11906227
  52. [61]Lancaster JL Kochunov PV Thompson PM Toga AW Fox PT Asymmetry of the brain surface from deformation field analysis Hum Brain Mapp 2003 19 2 79 89 12768532 PMC6872049
  53. [63]Lu L Leonard CM Thompson PM Kan E Jolley J Welcome SE Toga AW Sowell ER Normal developmental changes in inferior frontal gray matter are associated with improvement in phonological processing: a longitudinal MRI analysis Cereb Cortex 2007 17 5 1092 1099 16782757
  54. [64]O'Donnell S Noseworthy MD Levine B Dennis M Cortical thickness of the frontopolar area in typically developing children and adolescents Neuroimage 2005 24 4 948 954 15670671
  55. [65]Sowell ER Peterson BS Thompson PM Welcome SE Henkenius AL Toga AW Mapping cortical change across the human life span Nat Neurosci 2003 6 3 309 315 12548289
  56. [66]Sowell ER Thompson PM Leonard CM Welcome SE Kan E Toga AW Longitudinal mapping of cortical thickness and brain growth in normal children J Neurosci 2004 24 38 8223 8231 15385605 PMC6729679
  57. [67]Thompson-Schill SL Bedny M Goldberg RF The frontal lobes and the regulation of mental activity Curr Opin Neurobiol 2005 15 2 219 224 15831406
  58. [68]Rubia K Smith AB Taylor E Brammer M Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes Hum Brain Mapp 2007 28 11 1163 1177 17538951 PMC6871440
  59. [69]Aron AR Robbins TW Poldrack RA Inhibition and the right inferior frontal cortex Trends Cogn Sci 2004 8 4 170 177 15050513
  60. [70]Aron AR Poldrack RA The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder Biol Psychiatry 2005 57 11 1285 1292 15950000
  61. [71]Vallortigara G Rogers LJ Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization Behav Brain Sci 2005 28 4 575 589 discussion 589-633 16209828
  62. [72]Melsbach G Wohlschlager A Spiess M Gunturkun O Morphological asymmetries of motoneurons innervating upper extremities: clues to the anatomical foundations of handedness? Int J Neurosci 1996 86 3-4 217 224 8884392
  63. [73]Amunts K Jancke L Mohlberg H Steinmetz H Zilles K Interhemispheric asymmetry of the human motor cortex related to handedness and gender Neuropsychologia 2000 38 3 304 312 10678696
  64. [74]Zilles K Dabringhaus A Geyer S Amunts K Qu M Schleicher A Gilissen E Schlaug G Steinmetz H Structural asymmetries in the human forebrain and the forebrain of non-human primates and rats Neurosci Biobehav Rev 1996 20 4 593 605 8994198
  65. [75]McManus IC Bryden MP Geschwind's theory of cerebral lateralization: developing a formal, causal model Psychol Bull 1991 110 2 237 253 1946868
  66. [76]Sun T Patoine C Abu-Khalil A Visvader J Sum E Cherry TJ Orkin SH Geschwind DH Walsh CA Early asymmetry of gene transcription in embryonic human left and right cerebral cortex Science 2005 308 5729 1794 1798 15894532 PMC2756725
  67. [77]Luders E Gaser C Jancke L Schlaug G A voxel-based approach to gray matter asymmetries Neuroimage 2004 22 2 656 664 15193594
  68. [78]Smith AB Taylor E Brammer M Toone B Rubia K Task-specific hypoactivation in prefrontal and temporoparietal brain regions during motor inhibition and task switching in medication-naive children and adolescents with attention deficit hyperactivity disorder Am J Psychiatry 2006 163 6 1044 1051 16741205
  69. [79]Garrett A Penniman L Epstein J Casey BJ Hinshaw SP Glover GP Tonev SP Vitolo AP Davidson MPD Spicer JBA Greenhill LL Reiss AL Neuroanatomical abnormalities in adolescents with attention-deficit /hyperactivity disorder J Am Acad Child Adolesc Psychiatry 2008 47 11 1321 1328 18827721 PMC2644065
  70. [80]Glicksohn J Myslobodsky MS The representation of patterns of structural brain asymmetry in normal individuals Neuropsychologia 1993 31 2 145 159 8455784
  71. [81]Shaw P Sharp WS Morrison M Eckstrand K Greenstein DK Clasen LS Evans AC Rapoport JL Psychostimulant treatment and the developing cortex in attention deficit hyperactivity disorder Am J Psychiatry 2009 166 1 58 63 18794206 PMC2700349

Cited by

Sorted by citations

Authors
Shaw, P., Lalonde, F., Lepage, C., Rabin, C., Eckstrand, K., Sharp, W., Greenstein, D., Evans, A., Giedd, J. N., & Rapoport, J.
Affiliations
National Institute of Mental Health (US)
ORCID
Venue
Archives of General Psychiatry
Publisher
American Medical Association (AMA)
Published
2009-08-01
Volume
66
Issue
8
Pages
888
ISSN
0003-990X (ISSN-L)
DOI
10.1001/archgenpsychiatry.2009.103
PMC
PMC2948210
OpenAlex
W2055703423
Cited by
249
References
81
Citations by year
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FWCI
13.61
Type
journal article
Language
en
Open access
Locations
  • Archives of General Psychiatry (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health
  • National Institute of Mental Health (ZIAMH002240, ZIAMH002794)
Topics
  • Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Hemispheric Asymmetry in Neuroscience
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Keywords
cortical asymmetry, attention deficit hyperactivity disorder, hemispheric lateralization, cortical thickness, brain development, children, prefrontal cortex, orbitofrontal cortex, inferior frontal cortex, occipital cortex, handedness
MeSH terms
Adolescent, Adult, Attention Deficit Disorder with Hyperactivity, Brain, Brain Mapping, Cerebral Cortex, Child, Child Development, Child, Preschool, Frontal Lobe, Humans, Functional Laterality, Longitudinal Studies, Magnetic Resonance Imaging, Prospective Studies, Prefrontal Cortex

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