Adolescent Development of Cortical and White Matter Structure in the NCANDA Sample: Role of Sex, Ethnicity, Puberty, and Alcohol Drinking.

Brain structural development continues throughout adolescence, when experimentation with alcohol is often initiated. To parse contributions from biological and environmental factors on neurodevelopment, this study used baseline National Consortium on Alcohol and NeuroDevelopment in Adolescence (NCANDA) magnetic resonance imaging (MRI) data, acquired in 674 adolescents meeting no/low alcohol or drug use criteria and 134 adolescents exceeding criteria. Spatial integrity of images across the 5 recruitment sites was assured by morphological scaling using Alzheimer's disease neuroimaging initiative phantom-derived volume scalar metrics. Clinical MRI readings identified structural anomalies in 11.4%. Cortical volume and thickness were smaller and white matter volumes were larger in older than in younger adolescents. Effects of sex (male > female) and ethnicity (majority > minority) were significant for volume and surface but minimal for cortical thickness. Adjusting volume and area for supratentorial volume attenuated or removed sex and ethnicity effects. That cortical thickness showed age-related decline and was unrelated to supratentorial volume is consistent with the radial unit hypothesis, suggesting a universal neural development characteristic robust to sex and ethnicity. Comparison of NCANDA with PING data revealed similar but flatter, age-related declines in cortical volumes and thickness. Smaller, thinner frontal, and temporal cortices in the exceeds-criteria than no/low-drinking group suggested untoward effects of excessive alcohol consumption on brain structural development.

[1]  Surya N. Gupta,et al.  Intracranial incidental findings on brain MR images in a pediatric neurology practice: A retrospective study , 2008, Journal of the Neurological Sciences.

[2]  Alan C. Evans,et al.  Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI , 2006, NeuroImage.

[3]  Richard Frayne,et al.  Reliability of neuroanatomical measurements in a multisite longitudinal study of youth at risk for psychosis , 2014, Human brain mapping.

[4]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[5]  I Feinberg,et al.  Changes in sleep cycle patterns with age. , 1974, Journal of psychiatric research.

[6]  Peter Kochunov,et al.  Heritable changes in regional cortical thickness with age , 2014, Brain Imaging and Behavior.

[7]  Daisuke Tanaka,et al.  A study of the standard brain in Japanese children: Morphological comparison with the MNI template , 2013, Brain and Development.

[8]  S. Wood.  Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models , 2011 .

[9]  H. Chugani.  A critical period of brain development: studies of cerebral glucose utilization with PET. , 1998, Preventive medicine.

[10]  A. Addington,et al.  Longitudinally mapping the influence of sex and androgen signaling on the dynamics of human cortical maturation in adolescence , 2010, Proceedings of the National Academy of Sciences.

[11]  M. J. Meloy,et al.  Brain development in heavy-drinking adolescents. , 2015, The American journal of psychiatry.

[12]  Kilian M. Pohl,et al.  Neuroinformatics Software Applications Supporting Electronic Data Capture, Management, and Sharing for the Neuroimaging Community , 2015, Neuropsychology Review.

[13]  Torsten Rohlfing,et al.  Developmental change in regional brain structure over 7 months in early adolescence: Comparison of approaches for longitudinal atlas-based parcellation , 2011, NeuroImage.

[14]  J. Haxby,et al.  Longitudinal changes in lateral ventricular volume in Datients with dementia of the Alzheimer type , 1992, Neurology.

[15]  S. Wood.  Low‐Rank Scale‐Invariant Tensor Product Smooths for Generalized Additive Mixed Models , 2006, Biometrics.

[16]  W. van den Brink,et al.  Incidental Head and Neck Findings on MRI in Young Healthy Volunteers: Prevalence and Clinical Implications , 2012, American Journal of Neuroradiology.

[17]  Norbert Schuff,et al.  Measurement of MRI scanner performance with the ADNI phantom. , 2009, Medical physics.

[18]  Shantanu H. Joshi,et al.  Mapping ventricular expansion onto cortical gray matter in older adults , 2015, Neurobiology of Aging.

[19]  Anatol C. Kreitzer,et al.  Plasticity in gray and white: neuroimaging changes in brain structure during learning , 2012, Nature Neuroscience.

[20]  Dinggang Shen,et al.  Puberty-related influences on brain development , 2006, Molecular and Cellular Endocrinology.

[21]  A. Choudhri,et al.  Incidental pineal cysts in children who undergo 3-T MRI , 2013, Pediatric Radiology.

[22]  Michael C Neale,et al.  The dynamic role of genetics on cortical patterning during childhood and adolescence , 2014, Proceedings of the National Academy of Sciences.

[23]  R. Woods,et al.  Sex differences in cortical thickness mapped in 176 healthy individuals between 7 and 87 years of age. , 2007, Cerebral cortex.

[24]  Alan C. Evans,et al.  Neurodevelopmental Trajectories of the Human Cerebral Cortex , 2008, The Journal of Neuroscience.

[25]  Paul M. Thompson,et al.  Robust Brain Extraction Across Datasets and Comparison With Publicly Available Methods , 2011, IEEE Transactions on Medical Imaging.

[26]  P. Rakic.  A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution , 1995, Trends in Neurosciences.

[27]  John D. Van Horn,et al.  Quantitative in vivo evidence for broad regional gradients in the timing of white matter maturation during adolescence , 2011, NeuroImage.

[28]  P. Tobias.  Brain-size, grey matter and race--fact or fiction? , 1970, American journal of physical anthropology.

[29]  Torsten Rohlfing,et al.  The National Consortium on Alcohol and NeuroDevelopment in Adolescence (NCANDA): A Multisite Study of Adolescent Development and Substance Use. , 2015, Journal of studies on alcohol and drugs.

[30]  Terry L. Jernigan,et al.  The Basics of Brain Development , 2010, Neuropsychology Review.

[31]  Linda Chang,et al.  The NIH Toolbox Cognition Battery: results from a large normative developmental sample (PING). , 2014, Neuropsychology.

[32]  S. Tapert,et al.  The effect of alcohol use on human adolescent brain structures and systems. , 2014, Handbook of clinical neurology.

[33]  Vijay K. Venkatraman,et al.  Multimodal imaging of the self-regulating developing brain , 2012, Proceedings of the National Academy of Sciences.

[34]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[35]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[36]  H C Thode,et al.  Gamma distribution model describes maturational curves for delta wave amplitude, cortical metabolic rate and synaptic density. , 1990, Journal of theoretical biology.

[37]  N. Minshew,et al.  Maturation of Widely Distributed Brain Function Subserves Cognitive Development , 2001, NeuroImage.

[38]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

[39]  T. Jernigan,et al.  Maturation of human cerebrum observed in vivo during adolescence. , 1991, Brain : a journal of neurology.

[40]  B. Casey,et al.  Neurobiology of the adolescent brain and behavior: implications for substance use disorders. , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[41]  H. Hakonarson,et al.  Incidental Findings in Youths Volunteering for Brain MRI Research , 2013, American Journal of Neuroradiology.

[42]  Larson J. Hogstrom,et al.  The structure of the cerebral cortex across adult life: age-related patterns of surface area, thickness, and gyrification. , 2013, Cerebral cortex.

[43]  Alan C. Evans,et al.  Brain size and cortical structure in the adult human brain. , 2008, Cerebral cortex.

[44]  Vijay K. Venkatraman,et al.  Neuroanatomical Assessment of Biological Maturity , 2012, Current Biology.

[45]  Tomáš Paus,et al.  Sex differences in the human brain: a developmental perspective. , 2010, Progress in brain research.

[46]  Bruce Fischl,et al.  Genetic topography of brain morphology , 2013, Proceedings of the National Academy of Sciences.

[47]  R. Tibshirani,et al.  Exploring the nature of covariate effects in the proportional hazards model. , 1990, Biometrics.

[48]  A. Pfefferbaum,et al.  Dissociation of preparatory attention and response monitoring maturation during adolescence , 2014, Clinical Neurophysiology.

[49]  Anders M. Dale,et al.  A Geographic Cline of Skull and Brain Morphology among Individuals of European Ancestry , 2011, Human Heredity.

[50]  N. Makris,et al.  Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. , 2001, Cerebral cortex.

[51]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[52]  Matcheri S Keshavan,et al.  Prefrontal cortex, thalamus, and cerebellar volumes in adolescents and young adults with adolescent-onset alcohol use disorders and comorbid mental disorders. , 2005, Alcoholism, clinical and experimental research.

[53]  Anders M. Dale,et al.  Modeling the 3D Geometry of the Cortical Surface with Genetic Ancestry , 2015, Current Biology.

[54]  Jeffrey T Duda,et al.  Associations between children's socioeconomic status and prefrontal cortical thickness. , 2013, Developmental science.

[55]  Ulman Lindenberger,et al.  Trajectories of brain aging in middle-aged and older adults: Regional and individual differences , 2010, NeuroImage.

[56]  R. Bartha,et al.  Ventricular enlargement as a possible measure of Alzheimer's disease progression validated using the Alzheimer's disease neuroimaging initiative database. , 2008, Brain : a journal of neurology.

[57]  Anders M. Dale,et al.  A web-portal for interactive data exploration, visualization, and hypothesis testing , 2014, Front. Neuroinform..

[58]  J. Mazziotta,et al.  Positron emission tomography study of human brain functional development , 1987, Annals of neurology.

[59]  Lin Shi,et al.  Intensity and sulci landmark combined brain atlas construction for Chinese pediatric population , 2014, Human brain mapping.

[60]  R. Fields,et al.  Oligodendrocytes Changing the Rules: Action Potentials in Glia and Oligodendrocytes Controlling Action Potentials , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[61]  B. J. Casey,et al.  Family Income, Parental Education and Brain Structure in Children and Adolescents , 2015, Nature Neuroscience.

[62]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[63]  Adolf Pfefferbaum,et al.  The SRI24 multichannel atlas of normal adult human brain structure , 2009, Human brain mapping.

[64]  M. Rietschel,et al.  Neuropsychosocial profiles of current and future adolescent alcohol misusers , 2014, Nature.

[65]  K. Merikangas,et al.  Use and abuse of alcohol and illicit drugs in US adolescents: results of the National Comorbidity Survey-Adolescent Supplement. , 2012, Archives of general psychiatry.

[66]  F. Crews,et al.  Current hypotheses on the mechanisms of alcoholism. , 2014, Handbook of clinical neurology.

[67]  Linda Chang,et al.  Long-term influence of normal variation in neonatal characteristics on human brain development , 2012, Proceedings of the National Academy of Sciences.

[68]  Eric Kan,et al.  Neural correlates of socioeconomic status in the developing human brain. , 2012, Developmental science.

[69]  J. Illes,et al.  Incidental findings on pediatric MR images of the brain. , 2002, AJNR. American journal of neuroradiology.

[70]  Michael W. L. Chee,et al.  Brain Structure in Young and Old East Asians and Westerners: Comparisons of Structural Volume and Cortical Thickness , 2011, Journal of Cognitive Neuroscience.

[71]  Torsten Rohlfing,et al.  Variation in longitudinal trajectories of regional brain volumes of healthy men and women (ages 10 to 85years) measured with atlas-based parcellation of MRI , 2013, NeuroImage.

[72]  P. Fox,et al.  Influence of age, sex and genetic factors on the human brain , 2013, Brain Imaging and Behavior.

[73]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[74]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[75]  Terry L. Jernigan,et al.  Longitudinal characterization of white matter maturation during adolescence , 2010, Brain Research.

[76]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[77]  A. Dekaban,et al.  Changes in brain weights during the span of human life: Relation of brain weights to body heights and body weights , 1978, Annals of neurology.

[78]  Sherif Karama,et al.  Cortical Thickness, Cortico-Amygdalar Networks, and Externalizing Behaviors in Healthy Children , 2014, Biological Psychiatry.

[79]  Andrew Meade,et al.  Detecting Regular Sound Changes in Linguistics as Events of Concerted Evolution , 2015, Current Biology.

[80]  Alan C. Evans,et al.  Maturation of white matter in the human brain: a review of magnetic resonance studies , 2001, Brain Research Bulletin.

[81]  Torsten Rohlfing,et al.  Performance-based classifier combination in atlas-based image segmentation using expectation-maximization parameter estimation , 2004, IEEE Transactions on Medical Imaging.

[82]  Michel A. Hofman,et al.  Evolution of the human brain: when bigger is better , 2014, Front. Neuroanat..

[83]  A. Dale,et al.  Distinct genetic influences on cortical surface area and cortical thickness. , 2009, Cerebral cortex.

[84]  P. Rakic.  Evolution of the neocortex: Perspective from developmental biology , 2010 .

[85]  R. Dahl,et al.  Pubertal development: correspondence between hormonal and physical development. , 2009, Child development.

[86]  A. Toga,et al.  Mapping Changes in the Human Cortex throughout the Span of Life , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[87]  Deanna Greenstein,et al.  Prenatal growth in humans and postnatal brain maturation into late adolescence , 2012, Proceedings of the National Academy of Sciences.

[88]  Rhoshel K. Lenroot,et al.  Anatomic Magnetic Resonance Imaging of the Developing Child and Adolescent Brain and Effects of Genetic Variation , 2010, Neuropsychology Review.

[89]  E. Behnke,et al.  Inter-racial, gender and aging influences in the length of anterior commissure-posterior commissure line. , 2008, Journal of Korean Neurosurgical Society.

[90]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

[91]  Tal Kenet,et al.  The Pediatric Imaging, Neurocognition, and Genetics (PING) Data Repository , 2016, NeuroImage.

[92]  Edith V. Sullivan,et al.  Callosal microstructural abnormalities in Alzheimer's disease and alcoholism: same phenotype, different mechanisms , 2010, Psychiatry Research: Neuroimaging.

[93]  P. Huttenlocher.  Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[94]  Arthur W. Toga,et al.  The construction of a Chinese MRI brain atlas: A morphometric comparison study between Chinese and Caucasian cohorts , 2010, NeuroImage.

[95]  A. Toga,et al.  Mapping brain maturation , 2006, Trends in Neurosciences.

[96]  J. Lerch,et al.  Patterns of Coordinated Anatomical Change in Human Cortical Development: A Longitudinal Neuroimaging Study of Maturational Coupling , 2011, Neuron.

[97]  J. Rapoport,et al.  Child Psychiatry Branch of the National Institute of Mental Health Longitudinal Structural Magnetic Resonance Imaging Study of Human Brain Development , 2015, Neuropsychopharmacology.

[98]  Edward K. Vogel,et al.  Electrophysiological Evidence for Immature Processing Capacity and Filtering in Visuospatial Working Memory in Adolescents , 2012, PloS one.

[99]  L. Westlye,et al.  Differential Longitudinal Changes in Cortical Thickness, Surface Area and Volume across the Adult Life Span: Regions of Accelerating and Decelerating Change , 2014, The Journal of Neuroscience.

[100]  S. Blakemore,et al.  The role of puberty in the developing adolescent brain , 2010, Human brain mapping.

[101]  Torsten Rohlfing,et al.  N-CANDA data integration: anatomy of an asynchronous infrastructure for multi-site, multi-instrument longitudinal data capture , 2013, J. Am. Medical Informatics Assoc..

[102]  Amanda Wood,et al.  Do children really recover better? Neurobehavioural plasticity after early brain insult. , 2011, Brain : a journal of neurology.

[103]  Suzanne E. Welcome,et al.  Longitudinal Mapping of Cortical Thickness and Brain Growth in Normal Children , 2022 .

[104]  Judy Illes,et al.  Incidental Findings in Brain Imaging Research , 2006, Science.

[105]  Anders M. Dale,et al.  When does brain aging accelerate? Dangers of quadratic fits in cross-sectional studies , 2010, NeuroImage.

[106]  Yoshito Tsushima,et al.  Incidental findings on brain magnetic resonance imaging: systematic review and meta-analysis , 2009, BMJ : British Medical Journal.

[107]  Michael Weiner,et al.  Comparison of phantom and registration scaling corrections using the ADNI cohort , 2009, NeuroImage.

[108]  Judy Illes,et al.  Discovery and disclosure of incidental findings in neuroimaging research , 2004, Journal of magnetic resonance imaging : JMRI.

[109]  Lara M. Wierenga,et al.  Unique developmental trajectories of cortical thickness and surface area , 2014, NeuroImage.