Background
Delineation of the cortical anomalies underpinning attention-deficit/hyperactivity
disorder (ADHD) can powerfully inform pathophysiological models. We previously found
that ADHD is characterized by a delayed maturation of prefrontal cortical thickness.
We now ask if this extends to the maturation of cortical surface area and gyrification.
Methods
Two hundred thirty-four children with ADHD and 231 typically developing children participated
in the study, with 837 neuroanatomic magnetic resonance images acquired longitudinally.
We defined the developmental trajectories of cortical surfaces and gyrification and
the sequence of cortical maturation, as indexed by the age at which each cortical
vertex attained its peak surface area.
Results
In both groups, the maturation of cortical surface area progressed in centripetal
waves, both lateral (starting at the central sulcus and frontopolar regions, sweeping
toward the mid and superior frontal gyrus) and medial (descending down the medial
prefrontal cortex, toward the cingulate gyrus). However, the surface area developmental
trajectory was delayed in ADHD. For the right prefrontal cortex, the median age by
which 50% of cortical vertices attained peak area was 14.6 years (SE = .03) in ADHD,
significantly later than in typically developing group at 12.7 years (SE = .03) [log-rank
test χ(1)2 = 1300, p < .00001]. Similar, but less pronounced, delay was found in the left hemispheric
lobes. There were no such diagnostic differences in the developmental trajectories
of cortical gyrification.
Conclusions
The congruent delay in cortical thickness and surface area direct attention away from
processes that selectively affect one cortical component toward mechanisms controlling
the maturation of multiple cortical dimensions.
Key Words
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Biological PsychiatryAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation.Proc Natl Acad Sci U S A. 2007; 104: 19649-19654
- Surface area accounts for the relation of gray matter volume to reading-related skills and history of dyslexia.Cereb Cortex. 2010; 20: 2625-2635
- Cortical anatomy in autism spectrum disorder: An in vivo MRI study on the effect of age.Cereb Cortex. 2010; 20: 1332-1340
- Abnormal cerebral cortex structure in children with ADHD.Hum Brain Mapp. 2009; 30: 175-184
- Differential effects of aging and Alzheimer's disease on medial temporal lobe cortical thickness and surface area.Neurobiol Aging. 2009; 30: 432-440
- Role of intermediate progenitor cells in cerebral cortex development.Dev Neurosci. 2008; 30: 24-32
- Distinct genetic influences on cortical surface area and cortical thickness.Cereb Cortex. 2009; 19: 2728-2735
- Cortical thickness or grey matter volume?.Neuroimage. 2010; 53: 1135-1146
- Genetic and environmental contributions to regional cortical surface area in humans: A magnetic resonance imaging twin study.Cereb Cortex. 2011; 21: 2313-2321
- Surface area and cortical thickness descriptors reveal different attributes of the structural human brain networks.Neuroimage. 2010; 50: 1497-1510
- How does your cortex grow?.J Neurosci. 2011; 31: 7174-7177
- Longitudinal mapping of cortical thickness and clinical outcome in children and adolescents with attention-deficit/hyperactivity disorder.Arch Gen Psychiatry. 2006; 63: 540-549
- Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder.JAMA. 2002; 288: 1740-1748
- Diagnostic Interview for Children and Adolescents (DICA).J Am Acad Child Adolesc Psychiatry. 2000; 39: 59-66
- Conners' Teacher Rating Scale for use in drug studies with children–an empirical study.J Abnorm Child Psychol. 1975; 3: 217-229
- Brain development during childhood and adolescence: A longitudinal MRI study.Nat Neurosci. 1999; 2: 861-863
- Intellectual ability and cortical development in children and adolescents.Nature. 2006; 440: 676-679
- Quantitative magnetic resonance imaging of human brain development: Ages 4-18.Cereb Cortex. 1996; 6: 551-560
- The CIVET image-processing environment: A fully automated comprehensive pipeline for anatomical neuroimaging research.Presented at the 12th Annual Meeting of the Organization for Human Brain Mapping. 2006;
- Fast robust automated brain extraction.Hum Brain Mapp. 2002; 17: 143-155
- Symmetric atlasing and model based segmentation: An application to the hippocampus in older adults.Med Image Comput Comput Assist Interv. 2006; 9: 58-66
- Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space.J Comput Assist Tomogr. 1994; 18: 192-205
- A nonparametric method for automatic correction of intensity nonuniformity in MRI data.IEEE Trans Med Imaging. 1998; 17: 87-97
- Automatic “pipeline” analysis of 3-D MRI data for clinical trials: Application to multiple sclerosis.IEEE Trans Med Imaging. 2002; 21: 1280-1291
- Fast and robust parameter estimation for statistical partial volume models in brain MRI.Neuroimage. 2004; 23: 84-97
- 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: 210-221
- Deformation-based surface morphometry applied to gray matter deformation.Neuroimage. 2003; 18: 198-213
- Symmetry of cortical folding abnormalities in Williams syndrome revealed by surface-based analyses.J Neurosci. 2006; 26: 5470-5483
- Brain size and cortical structure in the adult human brain.Cereb Cortex. 2008; 18: 2181-2191
- Structural and functional analyses of human cerebral cortex using a surface-based atlas.J Neurosci. 1997; 17: 7079-7102
- Association study of 10 genes encoding neurotrophic factors and their receptors in adult and child attention-deficit/hyperactivity disorder.Biol Psychiatry. 2008; 63: 935-945
- An investigation of the neurotrophic factor genes GDNF, NGF, and NT3 in susceptibility to ADHD.Am J Med Genet B Neuropsychiatr Genet. 2007; 144B: 375-378
- Neurodevelopmental trajectories of the human cerebral cortex.J Neurosci. 2008; 28: 3586-3594
- Dynamic mapping of human cortical development during childhood through early adulthood.Proc Natl Acad Sci U S A. 2004; 101: 8174-8179
- Cortical gray matter in attention-deficit/hyperactivity disorder: A structural magnetic resonance imaging study.J Am Acad Child Adolesc Psychiatry. 2010; 49: 229-238
- Reduced right frontal cortical thickness in children, adolescents and adults with ADHD and its correlation to clinical variables: A cross-sectional study.J Psychiatr Res. 2010; 44: 1214-1223
- Widespread cortical thinning is a robust anatomical marker for attention-deficit/hyperactivity disorder.J Am Acad Child Adolesc Psychiatry. 2009; 48: 1014-1022
- Abnormal amygdalar activation and connectivity in adolescents with attention-deficit/hyperactivity disorder.J Am Acad Child Adolesc Psychiatry. 2011; 50: 828-837.e3
- Hippocampus and amygdala morphology in attention-deficit/hyperactivity disorder.Arch Gen Psychiatry. 2006; 63: 795-807
- Amygdala activation during emotion processing of neutral faces in children with severe mood dysregulation versus ADHD or bipolar disorder.Am J Psychiatry. 2009; 167: 61-69
- The neural correlates of attention deficit hyperactivity disorder: An ALE meta-analysis.J Child Psychol Psychiatry. 2006; 47: 1051-1062
- Activation in ventral prefrontal cortex is sensitive to genetic vulnerability for attention-deficit hyperactivity disorder.Biol Psychiatry. 2006; 60: 1062-1070
- Disorder-specific dysfunction in right inferior prefrontal cortex during two inhibition tasks in boys with attention-deficit hyperactivity disorder compared to boys with obsessive-compulsive disorder.Hum Brain Mapp. 2010; 31: 287-299
- Alerting deficits in children with attention deficit/hyperactivity disorder: Event-related fMRI evidence.Brain Res. 2008; 1219: 159-168
- Functional magnetic resonance imaging evidence for abnormalities in response selection in attention deficit hyperactivity disorder: Differences in activation associated with response inhibition but not habitual motor response.J Cogn Neurosci. 2008; 20: 478-493
- Temporal lobe dysfunction in medication-naive boys with attention-deficit/hyperactivity disorder during attention allocation and its relation to response variability.Biol Psychiatry. 2007; 62: 999-1006
- Right parietal dysfunction in children with attention deficit hyperactivity disorder, combined type: A functional MRI study.Mol Psychiatry. 2007; 12: 826-832
- Functional neuroanatomy of working memory in adults with attention-deficit/hyperactivity disorder.Biol Psychiatry. 2005; 57: 439-447
- Cingulate-precuneus interactions: A new locus of dysfunction in adult attention-deficit/hyperactivity disorder.Biol Psychiatry. 2008; 63: 332-337
- Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI.Brain Dev. 2007; 29: 83-91
- Cerebellar development and clinical outcome in attention deficit hyperactivity disorder.Am J Psychiatry. 2007; 164: 647-655
- Brain gray matter deficits at 33-year follow-up in adults with attention-deficit/hyperactivity disorder established in childhood.Arch Gen Psychiatry. 2011; 68: 1122-1134
- Gyrification abnormalities in childhood- and adolescent-onset schizophrenia.Biol Psychiatry. 2003; 54: 418-426
- A magnetic resonance imaging study of the cerebellar vermis in chronically treated and treatment-naïve children with attention-deficit/hyperactivity disorder combined type.Biol Psychiatry. 2009; 65: 620-624
- Volumetric MRI differences in treatment-naive vs chronically treated children with ADHD.Neurology. 2006; 67: 1023-1027
- Psychostimulant treatment and the developing cortex in attention deficit hyperactivity disorder.Am J Psychiatry. 2009; 166: 58-63
- Gray matter volume abnormalities in ADHD: Voxel-based meta-analysis exploring the effects of age and stimulant medication.Am J Psychiatry. 2011; 168: 1154-1163
- Sex differences in the functional neuroanatomy of working memory in adults with ADHD.Am J Psychiatry. 2010; 167: 86-94
- Sex differences in adolescent ADHD: Findings from concurrent EEG and EDA.Clin Neurophysiol. 2005; 116: 1455-1463
Article info
Publication history
Published online: March 15, 2012
Accepted:
January 6,
2012
Received in revised form:
January 6,
2012
Received:
August 31,
2011
Identification
Copyright
© 2012 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.