Functional Differentiation of Posterior Superior Temporal Sulcus in Autism: A Functional Connectivity Magnetic Resonance Imaging Study

BACKGROUND Socio-communicative impairments are salient features of autism spectrum disorder (ASD). Abnormal development of posterior superior temporal sulcus (pSTS)--a key processing area for language, biological motion, and social context--could play a role in these deficits. METHODS Functional connectivity magnetic resonance imaging was used to examine the synchronization of low-frequency blood oxygen level-dependent fluctuations during continuous performance on a visual search task. Twenty-one children and adolescents with ASD and 26 typically developing individuals-matched on age and IQ-participated in the study. Three subregions of pSTS were delineated with a data-driven approach, and differentiation of pSTS was examined by comparing the connectivity of each subregion. RESULTS In typically developing individuals, differentiation of networks was positively associated with age and anatomical maturation (cortical thinning in pSTS, greater white matter volume). In the ASD group, differentiation of pSTS connectivity was significantly reduced, and correlations with anatomical measures were weak or absent. Moreover, pSTS differentiation was inversely correlated with autism symptom severity. CONCLUSIONS Atypical maturation of pSTS suggests altered trajectories for functional segregation and integration of networks in ASD, potentially related to impaired cognitive and sensorimotor development. Furthermore, our findings provide a novel explanation for atypically increased connectivity in ASD that has been observed in some functional connectivity magnetic resonance imaging studies.

[1]  Baxter P. Rogers,et al.  Empirical Comparison of Sources of Variation for FMRI Connectivity Analysis , 2008, PloS one.

[2]  Justin L. Vincent,et al.  Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior , 2007, Neuron.

[3]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[4]  H. Tager-Flusberg,et al.  Identifying neurocognitive phenotypes in autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[6]  Mark H Johnson,et al.  Sensitive periods in functional brain development: problems and prospects. , 2005, Developmental psychobiology.

[7]  Peter A. Bandettini,et al.  Sources of group differences in functional connectivity: An investigation applied to autism spectrum disorder , 2010, NeuroImage.

[8]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[9]  Ina Bornkessel-Schlesewsky,et al.  Setting the frame: the human brain activates a basic low-frequency network for language processing. , 2010, Cerebral cortex.

[10]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[11]  E. Bullmore,et al.  Functional disconnectivity of the medial temporal lobe in Asperger’s syndrome , 2005, Biological Psychiatry.

[12]  D. Schacter,et al.  Correlated low-frequency BOLD fluctuations in the resting human brain are modulated by recent experience in category-preferential visual regions. , 2010, Cerebral cortex.

[13]  Ruth A. Carper,et al.  Unusual brain growth patterns in early life in patients with autistic disorder , 2001, Neurology.

[14]  L. Cronbach Coefficient alpha and the internal structure of tests , 1951 .

[15]  G. Jackson,et al.  Effect of prior cognitive state on resting state networks measured with functional connectivity , 2005, Human brain mapping.

[16]  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.

[17]  E. Redcay The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism , 2008, Neuroscience & Biobehavioral Reviews.

[18]  Biyu J. He,et al.  Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect , 2007, Neuron.

[19]  Vince D. Calhoun,et al.  Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations , 2008, NeuroImage.

[20]  M. Just,et al.  From the Selectedworks of Marcel Adam Just Atypical Frontal-posterior Synchronization of Theory of Mind Regions in Autism during Mental State Attribution Atypical Frontal-posterior Synchronization of Theory of Mind Regions in Autism during Mental State Attribution , 2022 .

[21]  T. Sejnowski,et al.  Irresistible environment meets immovable neurons , 1997, Behavioral and Brain Sciences.

[22]  Mark H Johnson,et al.  Mapping functional brain development: Building a social brain through interactive specialization. , 2009, Developmental psychology.

[23]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[24]  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.

[25]  Andrew E. Switala,et al.  Minicolumnar pathology in autism , 2002, Neurology.

[26]  S. Schultz Principles of Neural Science, 4th ed. , 2001 .

[27]  Marcel Adam Just,et al.  Functional connectivity in an fMRI working memory task in high-functioning autism , 2005, NeuroImage.

[28]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[29]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[30]  Audrey R. Nath,et al.  fMRI-Guided Transcranial Magnetic Stimulation Reveals That the Superior Temporal Sulcus Is a Cortical Locus of the McGurk Effect , 2010, The Journal of Neuroscience.

[31]  Jonathan D. Power,et al.  Functional Brain Networks Develop from a “Local to Distributed” Organization , 2009, PLoS Comput. Biol..

[32]  Kaustubh Supekar,et al.  Development of Large-Scale Functional Brain Networks in Children , 2009, NeuroImage.

[33]  Geraldine Dawson,et al.  Abnormal functional connectivity in autism spectrum disorders during face processing. , 2008, Brain : a journal of neurology.

[34]  C. J. Honeya,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009 .

[35]  U. Frith,et al.  Sampling the form of inner experience in three adults with Asperger syndrome , 1994, Psychological Medicine.

[36]  K. Pelphrey,et al.  Charting the typical and atypical development of the social brain , 2008, Development and Psychopathology.

[37]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[38]  A. Klin,et al.  Two-year-olds with autism orient to nonsocial contingencies rather than biological motion , 2009, Nature.

[39]  Daniel P. Kennedy,et al.  Mapping Early Brain Development in Autism , 2007, Neuron.

[40]  Marcel Adam Just,et al.  Theory of Mind disruption and recruitment of the right hemisphere during narrative comprehension in autism , 2008, Neuropsychologia.

[41]  M. Raichle,et al.  Cortical network functional connectivity in the descent to sleep , 2009, Proceedings of the National Academy of Sciences.

[42]  Eric Courchesne,et al.  Cerebral Lobes in Autism: Early Hyperplasia and Abnormal Age Effects , 2002, NeuroImage.

[43]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[44]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[45]  Daniel P. Kennedy,et al.  Functional abnormalities of the default network during self- and other-reflection in autism. , 2008, Social cognitive and affective neuroscience.

[46]  Scott Peltier,et al.  Abnormalities of intrinsic functional connectivity in autism spectrum disorders, , 2009, NeuroImage.

[47]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[48]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[49]  Maria Gavrilescu,et al.  Functional connectivity estimation in fMRI data: Influence of preprocessing and time course selection , 2008, Human brain mapping.

[50]  B. Leventhal,et al.  The Autism Diagnostic Observation Schedule—Generic: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism , 2000, Journal of autism and developmental disorders.

[51]  Ralph-Axel Müller,et al.  Atypical network connectivity for imitation in autism spectrum disorder , 2010, Neuropsychologia.

[52]  Ralph-Axel Müller,et al.  Underconnected, but how? A survey of functional connectivity MRI studies in autism spectrum disorders. , 2011, Cerebral cortex.

[53]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

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

[55]  Guido Gerig,et al.  Cortical Gray and White Brain Tissue Volume in Adolescents and Adults with Autism , 2006, Biological Psychiatry.

[56]  Daniel P. Kennedy,et al.  Failing to deactivate: resting functional abnormalities in autism. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Ruth A. Carper,et al.  Longitudinal Magnetic Resonance Imaging Study of Cortical Development through Early Childhood in Autism , 2010, The Journal of Neuroscience.

[58]  H. Nusbaum,et al.  Task-dependent organization of brain regions active during rest , 2009, Proceedings of the National Academy of Sciences.

[59]  Abraham Z. Snyder,et al.  A method for using blocked and event-related fMRI data to study “resting state” functional connectivity , 2007, NeuroImage.

[60]  C. Frith,et al.  Comment on "Wandering Minds: The Default Network and Stimulus-Independent Thought" , 2007, Science.

[61]  Karl J. Friston,et al.  Dynamic representations and generative models of brain function , 2001, Brain Research Bulletin.

[62]  J. Pekar,et al.  Decreased connectivity and cerebellar activity in autism during motor task performance. , 2009, Brain : a journal of neurology.

[63]  D. Amaral,et al.  Neuroanatomy of autism , 2008, Trends in Neurosciences.

[64]  R. Müller,et al.  Aberrant functional connectivity in autism: Evidence from low-frequency BOLD signal fluctuations , 2009, Brain Research.

[65]  M. Just,et al.  Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. , 2007, Cerebral cortex.

[66]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[67]  Mark H. Johnson Interactive Specialization: A domain-general framework for human functional brain development? , 2011, Developmental Cognitive Neuroscience.

[68]  Mark H. Johnson,et al.  Atypical eye contact in autism: Models, mechanisms and development , 2009, Neuroscience & Biobehavioral Reviews.

[69]  Fumitaka Homae,et al.  General to specific development of functional activation in the cerebral cortexes of 2- to 3-month-old infants , 2010, NeuroImage.

[70]  M E Meyerand,et al.  Combining independent component analysis and correlation analysis to probe interregional connectivity in fMRI task activation datasets. , 2000, Magnetic resonance imaging.

[71]  V. Calhoun,et al.  Changes in the interaction of resting‐state neural networks from adolescence to adulthood , 2009, Human brain mapping.

[72]  Ralph-Axel Müller,et al.  Partially enhanced thalamocortical functional connectivity in autism , 2006, Brain Research.

[73]  Uta Frith,et al.  Theory of mind and self consciousness: what is it like to be autistic? , 1999 .

[74]  David A. Ziegler,et al.  Localization of white matter volume increase in autism and developmental language disorder , 2004, Annals of neurology.

[75]  A. Karmiloff-Smith Atypical epigenesis. , 2007, Developmental science.

[76]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[77]  F. Happé,et al.  Time to give up on a single explanation for autism , 2006, Nature Neuroscience.

[78]  M. Just,et al.  Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. , 2004, Brain : a journal of neurology.

[79]  J. Fawcett,et al.  Regressive events in neurogenesis. , 1984, Science.

[80]  B. Harrison,et al.  Modulation of Brain Resting-State Networks by Sad Mood Induction , 2008, PloS one.

[81]  Antonio Y Hardan,et al.  An MRI study of increased cortical thickness in autism. , 2006, The American journal of psychiatry.

[82]  J. Buitelaar,et al.  The phenotype and neural correlates of language in autism: An integrative review , 2008, Neuroscience & Biobehavioral Reviews.

[83]  Archana Venkataraman,et al.  Intrinsic functional connectivity as a tool for human connectomics: theory, properties, and optimization. , 2010, Journal of neurophysiology.

[84]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[85]  N. Hadjikhani,et al.  Anatomical differences in the mirror neuron system and social cognition network in autism. , 2006, Cerebral cortex.

[86]  Doris Y. Tsao,et al.  Functional Connectivity of the Macaque Brain across Stimulus and Arousal States , 2009, The Journal of Neuroscience.

[87]  Klaas E. Stephan,et al.  The anatomical basis of functional localization in the cortex , 2002, Nature Reviews Neuroscience.

[88]  Jeffrey M. Zacks,et al.  Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses , 2006, Nature Neuroscience.

[89]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[90]  Roberto Toro,et al.  Cortical anatomy in autism spectrum disorder: an in vivo MRI study on the effect of age. , 2010, Cerebral cortex.

[91]  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.

[92]  C. Frith,et al.  Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. , 2002, Brain : a journal of neurology.