Development and aging of cortical thickness correspond to genetic organization patterns

Significance Here we show that developmental and adult aging-related changes in cortical thickness follow closely the genetic organization of the cerebral cortex. A total of 1,633 MRI scans from 974 participants from 4.1 to 88.5 y of age were used to measure longitudinal changes in cortical thickness, and the topographic pattern of change was compared with the genetic relationship between cortical subdivisions of maximal shared genetic influence, obtained from an independent sample of 406 middle-aged twins. Cortical changes due to maturation and adult age changes adhered to the genetic organization of the cortex, indicating that individual differences in cortical architecture in middle-aged adults have a neurodevelopmental origin and that genetic factors affect cortical changes through life. There is a growing realization that early life influences have lasting impact on brain function and structure. Recent research has demonstrated that genetic relationships in adults can be used to parcellate the cortex into regions of maximal shared genetic influence, and a major hypothesis is that genetically programmed neurodevelopmental events cause a lasting impact on the organization of the cerebral cortex observable decades later. Here we tested how developmental and lifespan changes in cortical thickness fit the underlying genetic organizational principles of cortical thickness in a longitudinal sample of 974 participants between 4.1 and 88.5 y of age with a total of 1,633 scans, including 773 scans from children below 12 y. Genetic clustering of cortical thickness was based on an independent dataset of 406 adult twins. Developmental and adult age-related changes in cortical thickness followed closely the genetic organization of the cerebral cortex, with change rates varying as a function of genetic similarity between regions. Cortical regions with overlapping genetic architecture showed correlated developmental and adult age change trajectories and vice versa for regions with low genetic overlap. Thus, effects of genes on regional variations in cortical thickness in middle age can be traced to regional differences in neurodevelopmental change rates and extrapolated to further adult aging-related cortical thinning. This finding suggests that genetic factors contribute to cortical changes through life and calls for a lifespan perspective in research aimed at identifying the genetic and environmental determinants of cortical development and aging.

[1]  Håkon Grydeland,et al.  Organizing Principles of Human Cortical Development--Thickness and Area from 4 to 30 Years: Insights from Comparative Primate Neuroanatomy. , 2016, Cerebral cortex.

[2]  A. Dale,et al.  The Genetic Association Between Neocortical Volume and General Cognitive Ability Is Driven by Global Surface Area Rather Than Thickness. , 2015, Cerebral cortex.

[3]  J. Gilmore,et al.  Dynamic Development of Regional Cortical Thickness and Surface Area in Early Childhood. , 2015, Cerebral cortex.

[4]  Atle Bjørnerud,et al.  Maturation of Cortico-Subcortical Structural Networks-Segregation and Overlap of Medial Temporal and Fronto-Striatal Systems in Development. , 2015, Cerebral cortex.

[5]  Alan C. Evans,et al.  Changes in thickness and surface area of the human cortex and their relationship with intelligence. , 2015, Cerebral cortex.

[6]  Torkel Klingberg,et al.  The role of fronto-parietal and fronto-striatal networks in the development of working memory: a longitudinal study. , 2015, Cerebral cortex.

[7]  A. Dale,et al.  Genetic and Environmental Contributions to the Relationships Between Brain Structure and Average Lifetime Cigarette Use , 2015, Behavior genetics.

[8]  M. Dylan Tisdall,et al.  Head motion during MRI acquisition reduces gray matter volume and thickness estimates , 2015, NeuroImage.

[9]  J B Poline,et al.  Single nucleotide polymorphism in the neuroplastin locus associates with cortical thickness and intellectual ability in adolescents , 2014, Molecular Psychiatry.

[10]  P. Matthews,et al.  A common brain network links development, aging, and vulnerability to disease , 2014, Proceedings of the National Academy of Sciences.

[11]  Stine K. Krogsrud,et al.  Development of hippocampal subfield volumes from 4 to 22 years , 2014, Human brain mapping.

[12]  Nicholas Lange,et al.  Longitudinal changes in cortical thickness in autism and typical development. , 2014, Brain : a journal of neurology.

[13]  Martin Styner,et al.  Common variants in psychiatric risk genes predict brain structure at birth. , 2014, Cerebral cortex.

[14]  K. Walhovd,et al.  Brain structural maturation and the foundations of cognitive behavioral development. , 2014, Current opinion in neurology.

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

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

[17]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[18]  L Penke,et al.  Childhood cognitive ability accounts for associations between cognitive ability and brain cortical thickness in old age , 2013, Molecular Psychiatry.

[19]  S. Blakemore,et al.  Developmental changes in the structure of the social brain in late childhood and adolescence. , 2014, Social cognitive and affective neuroscience.

[20]  Ingrid Agartz,et al.  Age-related cortical thickness differences in adolescents with early-onset schizophrenia compared with healthy adolescents , 2013, Psychiatry Research: Neuroimaging.

[21]  Stephan Eliez,et al.  Sex differences in thickness, and folding developments throughout the cortex , 2013, NeuroImage.

[22]  J. Gilmore,et al.  Mapping region-specific longitudinal cortical surface expansion from birth to 2 years of age. , 2013, Cerebral cortex.

[23]  Chi-Hua Chen,et al.  Genetics of brain structure: Contributions from the vietnam era twin study of aging , 2013, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

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

[25]  Monica Luciana,et al.  Associations between cortical thickness and general intelligence in children, adolescents and young adults. , 2013, Intelligence.

[26]  Terry L. Jernigan,et al.  Early Adolescent Cortical Thinning Is Related to Better Neuropsychological Performance , 2013, Journal of the International Neuropsychological Society.

[27]  Maria Kharitonova,et al.  Cortical gray-matter thinning is associated with age-related improvements on executive function tasks , 2013, Developmental Cognitive Neuroscience.

[28]  Knut Jørgen Bjuland,et al.  Cortical thickness and cognition in very-low-birth-weight late teenagers. , 2013, Early human development.

[29]  M. Rietschel,et al.  Cortical thickness of superior frontal cortex predicts impulsiveness and perceptual reasoning in adolescence , 2013, Molecular Psychiatry.

[30]  Vincent Frouin,et al.  FTO, obesity and the adolescent brain. , 2013, Human molecular genetics.

[31]  George Richardson,et al.  Brain development and aging: Overlapping and unique patterns of change , 2013, NeuroImage.

[32]  Mert R. Sabuncu,et al.  Statistical analysis of longitudinal neuroimage data with Linear Mixed Effects models , 2013, NeuroImage.

[33]  Alan C. Evans,et al.  Testosterone-related cortical maturation across childhood and adolescence. , 2012, Cerebral cortex.

[34]  R. Mayeux,et al.  Genetic Variants in the Fat and Obesity Associated (FTO) Gene and Risk of Alzheimer's Disease , 2012, PloS one.

[35]  Carol E. Franz,et al.  VETSA: The Vietnam Era Twin Study of Aging , 2012, Twin Research and Human Genetics.

[36]  T. Brown,et al.  Brain Development During the Preschool Years , 2012, Neuropsychology Review.

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

[38]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[39]  A. Dale,et al.  Hierarchical Genetic Organization of Human Cortical Surface Area , 2012, Science.

[40]  Ian J. Deary,et al.  Genetic contributions to stability and change in intelligence from childhood to old age , 2012, Nature.

[41]  P. Due-Tønnessen,et al.  Normal variation in behavioral adjustment relates to regional differences in cortical thickness in children , 2012, European Child & Adolescent Psychiatry.

[42]  Ylva Østby,et al.  Dissociating memory processes in the developing brain: the role of hippocampal volume and cortical thickness in recall after minutes versus days. , 2012, Cerebral cortex.

[43]  Anders M. Dale,et al.  Genetic influences on hippocampal volume differ as a function of testosterone level in middle-aged men , 2012, NeuroImage.

[44]  Alan C. Evans,et al.  Decreased regional cortical thickness and thinning rate are associated with inattention symptoms in healthy children. , 2012, Journal of the American Academy of Child and Adolescent Psychiatry.

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

[46]  K. Walhovd,et al.  Morphometry and connectivity of the fronto-parietal verbal working memory network in development , 2011, Neuropsychologia.

[47]  Anders M. Dale,et al.  Genetic Influences on Cortical Regionalization in the Human Brain , 2011, Neuron.

[48]  L. Westlye,et al.  The brain dynamics of intellectual development: Waxing and waning white and gray matter , 2011, Neuropsychologia.

[49]  Kelly N. Botteron,et al.  Right Anterior Cingulate Cortical Thickness and Bilateral Striatal Volume Correlate with Child Behavior Checklist Aggressive Behavior Scores in Healthy Children , 2011, Biological Psychiatry.

[50]  G. Šimić,et al.  Extraordinary neoteny of synaptic spines in the human prefrontal cortex , 2011, Proceedings of the National Academy of Sciences.

[51]  Bruce Fischl,et al.  Avoiding asymmetry-induced bias in longitudinal image processing , 2011, NeuroImage.

[52]  Armin Raznahan,et al.  How Does Your Cortex Grow? , 2011, The Journal of Neuroscience.

[53]  Rex E. Jung,et al.  Cortical thickness correlates of specific cognitive performance accounted for by the general factor of intelligence in healthy children aged 6 to 18 , 2011, NeuroImage.

[54]  Bruce Fischl,et al.  Presence of ApoE ε4 allele associated with thinner frontal cortex in middle age. , 2011, Journal of Alzheimer's disease : JAD.

[55]  Bruce Fischl,et al.  Highly accurate inverse consistent registration: A robust approach , 2010, NeuroImage.

[56]  Anders M. Dale,et al.  Salivary cortisol and prefrontal cortical thickness in middle-aged men: A twin study , 2010, NeuroImage.

[57]  Andreas Engvig,et al.  Effects of memory training on cortical thickness in the elderly , 2010, NeuroImage.

[58]  A M Dale,et al.  Testosterone modifies the effect of APOE genotype on hippocampal volume in middle-aged men , 2010, Neurology.

[59]  A. Dale,et al.  Life-span changes of the human brain white matter: diffusion tensor imaging (DTI) and volumetry. , 2010, Cerebral cortex.

[60]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[61]  A. Dale,et al.  Multi-modal imaging predicts memory performance in normal aging and cognitive decline , 2010, Neurobiology of Aging.

[62]  K. Walhovd,et al.  Structural Brain Changes in Aging: Courses, Causes and Cognitive Consequences , 2010, Reviews in the neurosciences.

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

[64]  Michael W. Weiner,et al.  A commonly carried allele of the obesity-related FTO gene is associated with reduced brain volume in the healthy elderly , 2010, Proceedings of the National Academy of Sciences.

[65]  L. Westlye,et al.  Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. , 2010, Cerebral cortex.

[66]  廣瀬雄一,et al.  Neuroscience , 2019, Workplace Attachments.

[67]  Bruce Fischl,et al.  Minute Effects of Sex on the Aging Brain: A Multisample Magnetic Resonance Imaging Study of Healthy Aging and Alzheimer's Disease , 2009, The Journal of Neuroscience.

[68]  André J. W. van der Kouwe,et al.  Reliability of MRI-derived cortical and subcortical morphometric measures: Effects of pulse sequence, voxel geometry, and parallel imaging , 2009, NeuroImage.

[69]  B. Hyman,et al.  Preservation of Neuronal Number Despite Age-Related Cortical Brain Atrophy in Elderly Subjects Without Alzheimer Disease , 2008, Journal of neuropathology and experimental neurology.

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

[71]  Milos Judas,et al.  Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. , 2008, Cerebral cortex.

[72]  Jean-Loup Guillaume,et al.  Fast unfolding of communities in large networks , 2008, 0803.0476.

[73]  André J. W. van der Kouwe,et al.  Detection of cortical thickness correlates of cognitive performance: Reliability across MRI scan sessions, scanners, and field strengths , 2008, NeuroImage.

[74]  C. Jack,et al.  Alzheimer's Disease Neuroimaging Initiative , 2008 .

[75]  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.

[76]  Anders M. Dale,et al.  Volumetric cerebral characteristics of children exposed to opiates and other substances in utero , 2007, NeuroImage.

[77]  Deanna Greenstein,et al.  Cortical brain development in nonpsychotic siblings of patients with childhood-onset schizophrenia. , 2007, Archives of general psychiatry.

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

[79]  Dae-Shik Kim,et al.  Diffusion tensor studies dissociated two fronto-temporal pathways in the human memory system , 2007, NeuroImage.

[80]  Corwin Boake,et al.  Genes, Environment, and Time: The Vietnam Era Twin Study of Aging (VETSA) , 2006, Twin Research and Human Genetics.

[81]  P. Magnus,et al.  Cohort profile: the Norwegian Mother and Child Cohort Study (MoBa). , 2006, International journal of epidemiology.

[82]  Anders M. Dale,et al.  Regional cortical thickness matters in recall after months more than minutes , 2006, NeuroImage.

[83]  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.

[84]  Alan C. Evans,et al.  Intellectual ability and cortical development in children and adolescents , 2006, Nature.

[85]  S. Wood.  Generalized Additive Models: An Introduction with R , 2006 .

[86]  R. Peters,et al.  Ageing and the brain , 2006, Postgraduate Medical Journal.

[87]  A. Dale,et al.  Cerebral cortex thickness in 15-year-old adolescents with low birth weight measured by an automated MRI-based method. , 2005, Brain : a journal of neurology.

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

[89]  Marianna D. Eddy,et al.  Regionally localized thinning of the cerebral cortex in schizophrenia , 2003, Schizophrenia Research.

[90]  Suzanne E. Welcome,et al.  Mapping cortical change across the human life span , 2003, Nature Neuroscience.

[91]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[92]  A. Dale,et al.  Regional and progressive thinning of the cortical ribbon in Huntington’s disease , 2002, Neurology.

[93]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[94]  X. Lin,et al.  Inference in generalized additive mixed modelsby using smoothing splines , 1999 .

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

[96]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[97]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[98]  B. Jacobs,et al.  Life‐span dendritic and spine changes in areas 10 and 18 of human cortex: A quantitative golgi study , 1997, The Journal of comparative neurology.

[99]  A. Dale,et al.  Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach , 1993, Journal of Cognitive Neuroscience.

[100]  P. Huttenlocher,et al.  Synaptic development in human cerebral cortex. , 1982, International journal of neurology.

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

[102]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[103]  H. Akaike.  A new look at the statistical model identification , 1974 .

[104]  N. Mantel.  The detection of disease clustering and a generalized regression approach. , 1967, Cancer research.