Anomalous brain activation during face and gaze processing in Williams syndrome

Objective: To investigate the discrete neural systems that underlie relatively preserved face processing skills in Williams syndrome (WS). Methods: The authors compared face and eye-gaze direction processing abilities in 11 clinically and genetically diagnosed WS subjects with 11 healthy age- and sex-matched controls, using functional MRI (fMRI). Results: Compared to controls, WS subjects showed a strong trend toward being less accurate in determining the direction of gaze and had significantly longer response latencies. Significant increases in activation were observed in the right fusiform gyrus (FuG) and several frontal and temporal regions for the WS group. By comparison, controls showed activation in the bilateral FuG, occipital, and temporal lobes. Between-group analysis showed WS subjects to have more extensive activation in the right inferior, superior, and medial frontal gyri, anterior cingulate, and several subcortical regions encompassing the anterior thalamus and caudate. Conversely, controls had greater activation in the primary and secondary visual cortices. Conclusion: The observed patterns of activation in WS subjects suggest a preservation of neural functioning within frontal and temporal regions, presumably resulting from task difficulty or compensatory mechanisms. Persons with WS may possess impairments in visual cortical regions, possibly disrupting global-coherence and visuospatial aspects of face and gaze processing.

[1]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[2]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[3]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[4]  M. D’Esposito,et al.  Activity in fusiform face area modulated as a function of working memory load. , 2001, Brain research. Cognitive brain research.

[5]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[6]  Ursula Bellugi,et al.  Williams syndrome: neuronal size and neuronal-packing density in primary visual cortex. , 2002, Archives of neurology.

[7]  R. Adolphs,et al.  Towards the neural basis for hypersociability in a genetic syndrome. , 1999, Neuroreport.

[8]  R. Campbell,et al.  Annotation: the cognitive neuroscience of face recognition: implications for developmental disorders. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

[9]  E. Courchesne,et al.  Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. , 2001, Brain : a journal of neurology.

[10]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[11]  H. Tager-Flusberg,et al.  People with Williams syndrome process faces holistically , 2003, Cognition.

[12]  Ursula Bellugi,et al.  Face and place processing in Williams syndrome: evidence for a dorsal-ventral dissociation , 2002, Neuroreport.

[13]  Anthony R. McIntosh,et al.  Age-Related Changes in Regional Cerebral Blood Flow during Working Memory for Faces , 1998, NeuroImage.

[14]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[15]  Ursula Bellugi,et al.  Seeing either the forest or the trees: Dissociation in visuospatial processing , 1989, Brain and Cognition.

[16]  Ursula Bellugi,et al.  Bridging cognition, the brain and molecular genetics: evidence from Williams syndrome , 1999, Trends in Neurosciences.

[17]  D. Maurer,et al.  The many faces of configural processing , 2002, Trends in Cognitive Sciences.

[18]  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 .

[19]  W. Yule,et al.  A cognitive and behavioural phenotype in Williams syndrome. , 1991, Journal of clinical and experimental neuropsychology.

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

[21]  C. Deruelle,et al.  Configural and Local Processing of Faces in Children with Williams Syndrome , 1999, Brain and Cognition.

[22]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[23]  U. Bellugi,et al.  Musical Abilities in Individuals with Williams Syndrome , 1998 .

[24]  Attentional Characteristics of Infants and Toddlers With Williams Syndrome During Triadic Interactions , 2003, Developmental neuropsychology.

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

[26]  C A Morris,et al.  Natural history of Williams syndrome: physical characteristics. , 1988, The Journal of pediatrics.

[27]  Isabel Gauthier,et al.  Social interest and the development of cortical face specialization: what autism teaches us about face processing. , 2002, Developmental psychobiology.

[28]  C. Mervis,et al.  Visuospatial construction. , 1999, American journal of human genetics.

[29]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[30]  R. Adolphs,et al.  II. Hypersociability in Williams Syndrome , 2000, Journal of Cognitive Neuroscience.

[31]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[32]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[33]  N. Logothetis,et al.  Integration of Local Features into Global Shapes Monkey and Human fMRI Studies , 2003, Neuron.

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

[35]  K. Sullivan,et al.  A componential view of theory of mind: evidence from Williams syndrome , 2000, Cognition.

[36]  Ursula Bellugi,et al.  V. Multi-Level Analysis of Cortical Neuroanatomy in Williams Syndrome , 2000, Journal of Cognitive Neuroscience.

[37]  M. Tarr,et al.  Becoming a “Greeble” Expert: Exploring Mechanisms for Face Recognition , 1997, Vision Research.

[38]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[39]  Patricia Spallone,et al.  Hemizygosity at the elastin locus in a developmental disorder, Williams syndrome , 1993, Nature Genetics.

[40]  C. Mervis,et al.  Global Spatial Organization by Individuals with Williams Syndrome , 1999 .

[41]  F. Volkmar,et al.  Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. , 2000, Archives of general psychiatry.

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

[43]  N. Kanwisher,et al.  The fusiform face area is selective for faces not animals. , 1999, Neuroreport.

[44]  Karl J. Friston,et al.  Combining Spatial Extent and Peak Intensity to Test for Activations in Functional Imaging , 1997, NeuroImage.

[45]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[46]  U Bellugi,et al.  Cerebral morphologic distinctions between Williams and Down syndromes. , 1993, Archives of neurology.

[47]  C D Frith,et al.  Neural mechanisms involved in the processing of global and local aspects of hierarchically organized visual stimuli. , 1997, Brain : a journal of neurology.

[48]  J. Atkinson,et al.  Visual and visuospatial development in young children with Williams syndrome , 2001, Developmental medicine and child neurology.

[49]  Doris Y. Tsao,et al.  Faces and objects in macaque cerebral cortex , 2003, Nature Neuroscience.

[50]  P. Skudlarski,et al.  The role of the fusiform face area in social cognition: implications for the pathobiology of autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[51]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .