Symmetry of Cortical Folding Abnormalities in Williams Syndrome Revealed by Surface-Based Analyses

We analyzed folding abnormalities in the cerebral cortex of subjects with Williams syndrome (WS), a genetically based developmental disorder, using surface-based analyses applied to structural magnetic resonance imaging data. Surfaces generated from each individual hemisphere were registered to a common atlas target (the PALS-B12 atlas). Maps of sulcal depth (distance from the cerebral hull) were combined across individuals to generate maps of average sulcal depth for WS and control subjects, along with depth-difference maps and t-statistic maps that accounted for within-group variability. Significant structural abnormalities were identified in 33 locations, arranged as 16 bilaterally symmetric pairs plus a lateral temporal region in the right hemisphere. Discrete WS folding abnormalities extended across a broad swath from dorsoposterior to ventroanterior regions of each hemisphere, in cortical areas associated with multiple sensory modalities as well as regions implicated in cognitive and emotional behavior. Hemispheric asymmetry in the temporal cortex is reduced in WS compared with control subjects. These findings provide insights regarding possible developmental mechanisms that give rise to folding abnormalities and to the spectrum of behavioral characteristics associated with WS.

[1]  Janette Atkinson,et al.  Dorsal-stream motion processing deficits persist into adulthood in Williams syndrome , 2006, Neuropsychologia.

[2]  K. Amunts,et al.  The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. , 2006, Cerebral cortex.

[3]  A. Schleicher,et al.  The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. , 2006, Cerebral cortex.

[4]  A. Karmiloff-Smith,et al.  Love Is… AN ABSTRACT WORD: THE INFLUENCE OF LEXICAL SEMANTICS ON VERBAL SHORT-TERM MEMORY IN WILLIAMS SYNDROME , 2005, Cortex.

[5]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[6]  M A Frens,et al.  Increased Prevalences of Left-handedness and Left-eye Sighting Dominance in Individuals with Williams-Beuren Syndrome , 2005, Journal of clinical and experimental neuropsychology.

[7]  Andreas Meyer-Lindenberg,et al.  Genetic Contributions to Human Gyrification: Sulcal Morphometry in Williams Syndrome , 2005, The Journal of Neuroscience.

[8]  C. Mervis,et al.  Neural correlates of genetically abnormal social cognition in Williams syndrome , 2005, Nature Neuroscience.

[9]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Paul Koch,et al.  Functional, structural, and metabolic abnormalities of the hippocampal formation in Williams syndrome. , 2005, The Journal of clinical investigation.

[11]  M. Corbetta,et al.  An Event-Related Functional Magnetic Resonance Imaging Study of Voluntary and Stimulus-Driven Orienting of Attention , 2005, The Journal of Neuroscience.

[12]  K. Tsapkini,et al.  Expressive and receptive vocabulary in children with Williams and Down syndromes. , 2005, Journal of intellectual disability research : JIDR.

[13]  Ursula Bellugi,et al.  Aversion, awareness, and attraction: investigating claims of hyperacusis in the Williams syndrome phenotype. , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[14]  A. Karmiloff-Smith,et al.  Asynchrony in the cognitive and lexical development of young children with Williams syndrome , 2005, Journal of Child Language.

[15]  Agatha D. Lee,et al.  Abnormal Cortical Complexity and Thickness Profiles Mapped in Williams Syndrome , 2005, The Journal of Neuroscience.

[16]  Allan L. Reiss,et al.  Relative sparing of primary auditory cortex in Williams Syndrome , 2005, Brain Research.

[17]  U Bellugi,et al.  Evidence for superior parietal impairment in Williams syndrome , 2005, Neurology.

[18]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[19]  R. Zatorre,et al.  Behavioral and neural correlates of perceived and imagined musical timbre , 2004, Neuropsychologia.

[20]  Ursula Bellugi,et al.  Characterizing the Musical Phenotype in Individuals With Williams Syndrome , 2004, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[21]  Abraham Z. Snyder,et al.  A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume , 2004, NeuroImage.

[22]  C. Mervis,et al.  Neural Basis of Genetically Determined Visuospatial Construction Deficit in Williams Syndrome , 2004, Neuron.

[23]  V Menon,et al.  Anomalous brain activation during face and gaze processing in Williams syndrome , 2004, Neurology.

[24]  A. Galaburda,et al.  An Experiment of Nature: Brain Anatomy Parallels Cognition and Behavior in Williams Syndrome , 2004, The Journal of Neuroscience.

[25]  Simon B. Eickhoff,et al.  Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—The roles of Brodmann areas 44 and 45 , 2004, NeuroImage.

[26]  U. Bellugi,et al.  “Frog, where are you?” Narratives in children with specific language impairment, early focal brain injury, and Williams syndrome , 2004, Brain and Language.

[27]  Ursula Bellugi,et al.  “Everybody in the world is my friend” hypersociability in young children with Williams syndrome , 2004, American journal of medical genetics. Part A.

[28]  D. V. van Essen,et al.  Surface-based approaches to spatial localization and registration in primate cerebral cortex. , 2004, NeuroImage.

[29]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[30]  S. Petersen,et al.  A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging , 2003, Neuropsychologia.

[31]  Jeffrey M. Zacks,et al.  Neural correlates of incongruous visual information An event-related fMRI study , 2003, NeuroImage.

[32]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[33]  C. Mervis.  Williams Syndrome: 15 Years of Psychological Research , 2003, Developmental neuropsychology.

[34]  E. Dykens.  Anxiety, Fears, and Phobias in Persons With Williams Syndrome , 2003, Developmental neuropsychology.

[35]  Annette Karmiloff-Smith,et al.  Dethroning the Myth: Cognitive Dissociations and Innate Modularity in Williams Syndrome , 2003, Developmental neuropsychology.

[36]  Gary H. Glover,et al.  Neural Correlates of Auditory Perception in Williams Syndrome: An fMRI Study , 2003, NeuroImage.

[37]  Rumiko Matsuoka,et al.  Williams syndrome deficits in visual spatial processing linked to GTF2IRD1 and GTF2I on Chromosome 7q11.23 , 2003, Genetics in Medicine.

[38]  John W. Harwell,et al.  Surface-Based Atlases and a Database of Cortical Structure and Function , 2003 .

[39]  A. Toga,et al.  Mapping brain asymmetry , 2003, Nature Reviews Neuroscience.

[40]  A. Karmiloff-Smith,et al.  Early categorization abilities in young children with Williams syndrome , 2002, Neuroreport.

[41]  Y. Miyashita,et al.  Hemispheric asymmetry in human lateral prefrontal cortex during cognitive set shifting , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Stephan Eliez,et al.  Increased gyrification in Williams syndrome: evidence using 3D MRI methods. , 2002, Developmental medicine and child neurology.

[43]  R. Adolphs.  Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

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

[45]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[46]  Neurosciences,et al.  Organization of Visual Areas in Macaque and Human Cerebral Cortex , 2002 .

[47]  U Bellugi,et al.  Dorsal forebrain anomaly in Williams syndrome. , 2001, Archives of neurology.

[48]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

[49]  R. Adolphs.  The neurobiology of social cognition , 2001, Current Opinion in Neurobiology.

[50]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[51]  P. Morosan,et al.  Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System , 2001, NeuroImage.

[52]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: I. During cognitive task performance. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[53]  M. Raichle,et al.  Emotion-induced changes in human medial prefrontal cortex: II. During anticipatory anxiety. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[54]  D. V. van Essen,et al.  Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto‐occipital cortex , 2000, The Journal of comparative neurology.

[55]  Carolyn B. Mervis,et al.  The Williams Syndrome Cognitive Profile , 2000, Brain and Cognition.

[56]  N. Kanwisher,et al.  Mental Imagery of Faces and Places Activates Corresponding Stimulus-Specific Brain Regions , 2000, Journal of Cognitive Neuroscience.

[57]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[58]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[59]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[60]  Rumiko Matsuoka,et al.  VI. Genome Structure and Cognitive Map of Williams Syndrome , 2000, Journal of Cognitive Neuroscience.

[61]  Ursula Bellugi,et al.  I. The Neurocognitive Profile of Williams Syndrome: A Complex Pattern of Strengths and Weaknesses , 2000, Journal of Cognitive Neuroscience.

[62]  Lawrence G. Appelbaum,et al.  III. Electrophysiological Studies of Face Processing in Williams Syndrome , 2000, Journal of Cognitive Neuroscience.

[63]  Stephan Eliez,et al.  IV. Neuroanatomy of Williams Syndrome: A High-Resolution MRI Study , 2000, Journal of Cognitive Neuroscience.

[64]  C. Mervis,et al.  Williams syndrome: cognition, personality, and adaptive behavior. , 2000, Mental retardation and developmental disabilities research reviews.

[65]  J. Marshall,et al.  The neural consequences of conflict between intention and the senses. , 1999, Brain : a journal of neurology.

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

[67]  S. Petersen,et al.  The effects of practice on the functional anatomy of task performance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[68]  A. Damasio,et al.  Deciding Advantageously Before Knowing the Advantageous Strategy , 1997, Science.

[69]  D. V. van Essen,et al.  A tension-based theory of morphogenesis and compact wiring in the central nervous system. , 1997, Nature.

[70]  S. Carmichael,et al.  Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. , 1996, The Journal of comparative neurology.

[71]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[72]  R. Buckner,et al.  Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups. , 1995, Journal of neurophysiology.

[73]  Jack L. Lancaster,et al.  A modality‐independent approach to spatial normalization of tomographic images of the human brain , 1995 .

[74]  P S Goldman-Rakic,et al.  Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[75]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[77]  K. Brodmann.  Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[78]  F. Gilles,et al.  TELENCEPHALIC DEVELOPMENT: CHANGING GYRAL PATTERNS , 1983 .