Aberrant parietal cortex developmental trajectories in girls with turner syndrome and related visual–spatial cognitive development: A preliminary study

Turner syndrome (TS) arises from partial or complete absence of the X‐chromosome in females. Girls with TS show deficits in visual–spatial skills as well as reduced brain volume and surface area in the parietal cortex which supports these cognitive functions. Thus, measuring the developmental trajectory of the parietal cortex and the associated visual–spatial cognition in TS may provide novel insights into critical brain‐behavior associations. In this longitudinal study, we acquired structural MRI data and assessed visual–spatial skills in 16 (age: 8.23 ± 2.5) girls with TS and 13 age‐matched controls over two time‐points. Gray and white matter volume, surface area and cortical thickness were calculated from surfaced based segmentation of bilateral parietal cortices, and the NEPSY Arrows subtest was used to assess visual–spatial ability. Volumetric and cognitive scalars were modeled to obtain estimates of age‐related change. The results show aberrant growth of white matter volume (P = 0.011, corrected) and surface area (P = 0.036, corrected) of the left superior parietal regions during childhood in girls with TS. Other parietal sub‐regions were significantly smaller in girls with TS at both time‐points but did not show different growth trajectories relative to controls. Furthermore, we found that visual–spatial skills showed a widening deficit for girls with TS relative to controls (P = 0.003). Young girls with TS demonstrate an aberrant trajectory of parietal cortical and cognitive development during childhood. Elucidating aberrant neurodevelopmental trajectories in this population is critical for determining specific stages of brain maturation that are particularly dependent on TS‐related genetic and hormonal factors. © 2014 Wiley Periodicals, Inc.

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

[2]  A. Reiss,et al.  Aberrant functional network recruitment of posterior parietal cortex in turner syndrome , 2013, Human brain mapping.

[3]  Michael F. Green,et al.  Structural abnormalities in cortical volume, thickness, and surface area in 22q11.2 microdeletion syndrome: Relationship with psychotic symptoms☆ , 2013, NeuroImage: Clinical.

[4]  Allan L Reiss,et al.  Cortical brain morphology in young, estrogen-naive, and adolescent, estrogen-treated girls with Turner syndrome. , 2013, Cerebral cortex.

[5]  Tricia A. Thornton-Wells,et al.  Regional Brain Differences in Cortical Thickness, Surface Area and Subcortical Volume in Individuals with Williams Syndrome , 2012, PloS one.

[6]  Allan L Reiss,et al.  Changes in frontal-parietal activation and math skills performance following adaptive number sense training: Preliminary results from a pilot study , 2011, Neuropsychological rehabilitation.

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

[8]  A. Reiss,et al.  Reduced functional connectivity during working memory in Turner syndrome. , 2011, Cerebral cortex.

[9]  Allan L. Reiss,et al.  Neuroanatomical spatial patterns in Turner syndrome , 2011, NeuroImage.

[10]  J. Rapoport,et al.  Structural MRI of Pediatric Brain Development: What Have We Learned and Where Are We Going? , 2010, Neuron.

[11]  Joel Stoddard,et al.  Atypical functional brain activation during a multiple object tracking task in girls with Turner syndrome: neurocorrelates of reduced spatiotemporal resolution. , 2010, American journal on intellectual and developmental disabilities.

[12]  Declan G. M. Murphy,et al.  Cortical anatomy in human X monosomy , 2010, NeuroImage.

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

[14]  Bruce Fischl,et al.  Regional white matter volume differences in nondemented aging and Alzheimer's disease , 2009, NeuroImage.

[15]  John O. Willis,et al.  NEPSY: A Developmental Neuropsychological Assessment , 2008 .

[16]  J. Giedd,et al.  Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging , 2006, Neuroscience & Biobehavioral Reviews.

[17]  C. Disteche,et al.  High expression of the mammalian X chromosome in brain , 2006, Brain Research.

[18]  Svend Juul,et al.  Prevalence, incidence, diagnostic delay, and mortality in Turner syndrome. , 2006, The Journal of clinical endocrinology and metabolism.

[19]  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.

[20]  Vinod Menon,et al.  Neuro-functional differences associated with arithmetic processing in Turner syndrome. , 2006, Cerebral cortex.

[21]  Sarah J. Hart,et al.  Visuospatial executive function in Turner syndrome: functional MRI and neurocognitive findings , 2006, Brain : a journal of neurology.

[22]  Andrew Simmons,et al.  Influence of X Chromosome and Hormones on Human Brain Development: A Magnetic Resonance Imaging and Proton Magnetic Resonance Spectroscopy Study of Turner Syndrome , 2006, Biological Psychiatry.

[23]  Kiralee M. Hayashi,et al.  Abnormal Cortical Complexity and Thickness Profiles Mapped in Williams Syndrome , 2005, The Journal of Neuroscience.

[24]  J. Rovet Turner Syndrome: A Review of Genetic and Hormonal Influences on Neuropsychological Functioning , 2004, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[25]  Stephan Eliez,et al.  A volumetric study of parietal lobe subregions in Turner syndrome. , 2004, Developmental medicine and child neurology.

[26]  D. LeBihan,et al.  Brain anatomy in Turner syndrome: evidence for impaired social and spatial-numerical networks. , 2004, Cerebral cortex.

[27]  V. Menon,et al.  Functional neuroanatomy of spatial orientation processing in Turner syndrome. , 2004, Cerebral cortex.

[28]  S. Dehaene,et al.  Functional and Structural Alterations of the Intraparietal Sulcus in a Developmental Dyscalculia of Genetic Origin , 2003, Neuron.

[29]  Stephan Eliez,et al.  Brain development in Turner syndrome: a magnetic resonance imaging study , 2002, Psychiatry Research: Neuroimaging.

[30]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[31]  G. Glover,et al.  Functional neuroanatomy of visuo‐spatial working memory in turner syndrome , 2001, Human brain mapping.

[32]  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.

[33]  H. Kraemer,et al.  How can we learn about developmental processes from cross-sectional studies, or can we? , 2000, The American journal of psychiatry.

[34]  J. Ross,et al.  Use of estrogen in young girls with Turner syndrome , 2000, Neurology.

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

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

[37]  G. Stefanatos,et al.  Transition to young adulthood in Ullrich-Turner syndrome: neurodevelopmental changes. , 1998, American journal of medical genetics.

[38]  M. Corbetta,et al.  Human cortical mechanisms of visual attention during orienting and search. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  M. Corbetta,et al.  Superior Parietal Cortex Activation During Spatial Attention Shifts and Visual Feature Conjunction , 1995, Science.

[40]  A L Reiss,et al.  Neurodevelopmental effects of X monosomy: A volumetric imaging study , 1995, Annals of neurology.

[41]  G. Stefanatos,et al.  Ullrich-Turner syndrome: neurodevelopmental changes from childhood through adolescence. , 1995, American journal of medical genetics.

[42]  B Horwitz,et al.  X-chromosome effects on female brain: a magnetic resonance imaging study of Turner's syndrome , 1993, The Lancet.

[43]  A. Benton,et al.  Visuospatial judgment. A clinical test. , 1978, Archives of neurology.

[44]  S. Kesler,et al.  Cognitive profile of Turner syndrome. , 2009, Developmental disabilities research reviews.

[45]  C. Bondy,et al.  Care of girls and women with Turner syndrome: a guideline of the Turner Syndrome Study Group. , 2007, The Journal of clinical endocrinology and metabolism.

[46]  Christine M Disteche,et al.  Dosage compensation of the active X chromosome in mammals , 2006, Nature Genetics.

[47]  K. Klein,et al.  Estradiol Levels and Secretory Dynamics in Normal Girls and Boys as Determined by an Ultrasensitive Bioassay: A 10 Year Experience , 2006, Journal of pediatric endocrinology & metabolism : JPEM.

[48]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[49]  Alan C. Evans,et al.  Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. , 1996, Cerebral cortex.

[50]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[51]  T Mori,et al.  [Turner syndrome]. , 1993, Ryoikibetsu shokogun shirizu.

[52]  S. Bloch Visuospatial judgment. , 1979, Archives of neurology.