The Development of the Neural Substrates of Cognitive Control in Adolescents with Autism Spectrum Disorders

BACKGROUND Autism spectrum disorders (ASDs) involve impairments in cognitive control. In typical development (TYP), neural systems underlying cognitive control undergo substantial maturation during adolescence. Development is delayed in adolescents with ASD. Little is known about the neural substrates of this delay. METHODS We used event-related functional magnetic resonance imaging and a cognitive control task involving overcoming a prepotent response tendency to examine the development of cognitive control in young (ages 12-15; n = 13 with ASD and n = 13 with TYP) and older (ages 16-18; n = 14 with ASD and n = 14 with TYP) adolescents with whole-brain voxelwise univariate and task-related functional connectivity analyses. RESULTS Older ASD and TYP showed reduced activation in sensory and premotor areas relative to younger ones. The older ASD group showed reduced left parietal activation relative to TYP. Functional connectivity analyses showed a significant age by group interaction with the older ASD group exhibiting increased functional connectivity strength between the ventrolateral prefrontal cortex and the anterior cingulate cortex, bilaterally. This functional connectivity strength was related to task performance in ASD, whereas that between dorsolateral prefrontal cortex and parietal cortex (Brodmann areas 9 and 40) was related to task performance in TYP. CONCLUSIONS Adolescents with ASD rely more on reactive cognitive control, involving last-minute conflict detection and control implementation by the anterior cingulate cortex and ventrolateral prefrontal cortex, versus proactive cognitive control requiring processing by dorsolateral prefrontal cortex and parietal cortex. Findings await replication in larger longitudinal studies that examine their functional consequences and amenability to intervention.

[1]  Catalina J. Hooper,et al.  The development of nonverbal working memory and executive control processes in adolescents. , 2005, Child Development.

[2]  M. Dulcan Comprar Dulcan's Textbook of Child and Adolescent Psychiatry | Mina K. Dulcan | 9781585623235 | American Psychiatric Publishing , 2010 .

[3]  Stewart H Mostofsky,et al.  Increased motor cortex white matter volume predicts motor impairment in autism. , 2007, Brain : a journal of neurology.

[4]  Beatriz Luna,et al.  Maturation of Executive Function in Autism , 2007, Biological Psychiatry.

[5]  Early Childhood Predictors of the Social Competence of Adults with Autism , 2011, Journal of autism and developmental disorders.

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

[7]  C. Dissanayake,et al.  Annotation: The similarities and differences between autistic disorder and Asperger's disorder: a review of the empirical evidence. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[8]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[9]  M. Just,et al.  From the Selectedworks of Marcel Adam Just Inhibitory Control in High Functioning Autism: Decreased Activation and Underconnectivity in Inhibition Networks Inhibitory Control in High-functioning Autism: Decreased Activation and Underconnectivity in Inhibition Networks , 2022 .

[10]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[11]  Cameron S Carter,et al.  Development of action monitoring through adolescence into adulthood: ERP and source localization. , 2007, Developmental science.

[12]  E. Lenneberg Biological Foundations of Language , 1967 .

[13]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[14]  Cameron S Carter,et al.  Cognitive control involved in overcoming prepotent response tendencies and switching between tasks. , 2005, Cerebral cortex.

[15]  S Arndt,et al.  An MRI study of the corpus callosum in autism. , 1997, The American journal of psychiatry.

[16]  Kaustubh Supekar,et al.  Developmental Maturation of Dynamic Causal Control Signals in Higher-Order Cognition: A Neurocognitive Network Model , 2012, PLoS Comput. Biol..

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

[18]  P. Thompson,et al.  Neurobiology of intelligence: science and ethics , 2004, Nature Reviews Neuroscience.

[19]  M. D’Esposito,et al.  Longitudinal Evidence for Functional Specialization of the Neural Circuit Supporting Working Memory in the Human Brain , 2010, The Journal of Neuroscience.

[20]  C. Rosano,et al.  Functional neuroimaging indicators of successful executive control in the oldest old , 2005, NeuroImage.

[21]  D. Szűcs,et al.  Delayed development of proactive response preparation in adolescents: ERP and EMG evidence , 2013, Developmental Cognitive Neuroscience.

[22]  S Arndt,et al.  Course of behavioral change in autism: a retrospective study of high-IQ adolescents and adults. , 1996, Journal of the American Academy of Child and Adolescent Psychiatry.

[23]  B. J. Casey,et al.  What have we learned about cognitive development from neuroimaging? , 2006, Neuropsychologia.

[24]  Ruth A. Carper,et al.  Autism and Abnormal Development of Brain Connectivity , 2004, The Journal of Neuroscience.

[25]  B. Pennington,et al.  Brief Report: Impaired Flexible Item Selection Task (FIST) in School-Age Children with Autism Spectrum Disorders , 2012, Journal of autism and developmental disorders.

[26]  Gender differentiations of cognitive-motor functioning in prepubertal and pubertal children. , 2012, Collegium antropologicum.

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

[28]  A Pickles,et al.  Autism screening questionnaire: Diagnostic validity , 1999, British Journal of Psychiatry.

[29]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[30]  T. Hare,et al.  Changes in cerebral functional organization during cognitive development , 2005, Current Opinion in Neurobiology.

[31]  E T Bullmore,et al.  Dopaminergic drug effects on physiological connectivity in a human cortico-striato-thalamic system. , 2003, Brain : a journal of neurology.

[32]  Mark D'Esposito,et al.  From cognitive to neural models of working memory , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[33]  C. Carter,et al.  The neural substrates of cognitive control deficits in autism spectrum disorders , 2009, Neuropsychologia.

[34]  J. Baio Prevalence of autism spectrum disorders--Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008. , 2012, Morbidity and mortality weekly report. Surveillance summaries.

[35]  M. Rutter,et al.  Adult outcome for children with autism. , 2004, Journal of child psychology and psychiatry, and allied disciplines.

[36]  Matti S Hämäläinen,et al.  Disconnectivity of the cortical ocular motor control network in autism spectrum disorders , 2012, NeuroImage.

[37]  Jason J. S. Barton,et al.  Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders , 2010, NeuroImage.

[38]  D. Stuss,et al.  Principles of frontal lobe function , 2002 .

[39]  M. Brammer,et al.  Linear age‐correlated functional development of right inferior fronto‐striato‐cerebellar networks during response inhibition and anterior cingulate during error‐related processes , 2007, Human brain mapping.

[40]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

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

[42]  Mary Beth Nebel,et al.  Disruption of functional organization within the primary motor cortex in children with autism , 2014, Human brain mapping.

[43]  T. Braver The variable nature of cognitive control: a dual mechanisms framework , 2012, Trends in Cognitive Sciences.

[44]  T. Charman The prevalence of autism spectrum disorders , 2002, European Child & Adolescent Psychiatry.

[45]  S. Rombouts,et al.  A comprehensive study of whole-brain functional connectivity in children and young adults. , 2011, Cerebral cortex.

[46]  A. Couteur,et al.  Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders , 1994, Journal of autism and developmental disorders.

[47]  Serge A R B Rombouts,et al.  Developmental differences in prefrontal activation during working memory maintenance and manipulation for different memory loads. , 2011, Developmental science.

[48]  N. Minshew,et al.  Corpus callosum size in autism , 2000, Neurology.

[49]  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.

[50]  E. Claus,et al.  Cognitive Control in Adolescence: Neural Underpinnings and Relation to Self-Report Behaviors , 2011, PloS one.

[51]  Jonathan D. Cohen,et al.  The Role of Prefrontal Cortex in Normal and Disordered Cognitive Control: A Cognitive Neuroscience Perspective , 2009 .

[52]  C. Rice,et al.  Autism and Developmental Disabilities Monitoring Network Surveillance Year 2000 Principal Investigators , 2012 .

[53]  N. Minshew,et al.  Effects of age on brain volume and head circumference in autism , 2002, Neurology.

[54]  Chandan J. Vaidya,et al.  Functional imaging of developmental and adaptive changes in neurocognition , 2006, NeuroImage.

[55]  Vicente L. Malave,et al.  Autism as a neural systems disorder: A theory of frontal-posterior underconnectivity , 2012, Neuroscience & Biobehavioral Reviews.

[56]  Jonathan D. Cohen,et al.  Lateral and medial hypofrontality in first-episode schizophrenia: functional activity in a medication-naive state and effects of short-term atypical antipsychotic treatment. , 2005, The American journal of psychiatry.

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

[58]  J. Pekar,et al.  Children with high functioning autism show increased prefrontal and temporal cortex activity during error monitoring , 2011, Developmental Cognitive Neuroscience.

[59]  Jonathan D. Power,et al.  Prediction of Individual Brain Maturity Using fMRI , 2010, Science.

[60]  T. Sanger,et al.  Harnessing neuroplasticity for clinical applications , 2011, Brain : a journal of neurology.

[61]  Jay N Giedd,et al.  The teen brain: insights from neuroimaging. , 2008, The Journal of adolescent health : official publication of the Society for Adolescent Medicine.

[62]  Patricia Howlin,et al.  Outcome in High-Functioning Adults with Autism with and Without Early Language Delays: Implications for the Differentiation Between Autism and Asperger Syndrome , 2003, Journal of autism and developmental disorders.

[63]  Katharine N. Thakkar,et al.  Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD) , 2008, Brain : a journal of neurology.

[64]  William D Gaillard,et al.  Functional connectivity of the inferior frontal cortex changes with age in children with autism spectrum disorders: a fcMRI study of response inhibition. , 2009, Cerebral cortex.

[65]  S. Bunge,et al.  Neurodevelopmental changes in working memory and cognitive control , 2007, Current Opinion in Neurobiology.

[66]  Carter Wendelken,et al.  Neurocognitive development of the ability to manipulate information in working memory. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[67]  J. Sinzig,et al.  Attention Deficit/Hyperactivity Disorder in Children and Adolescents With Autism Spectrum Disorder , 2009, Journal of attention disorders.

[68]  D. Margulies,et al.  Development of anterior cingulate functional connectivity from late childhood to early adulthood. , 2009, Cerebral cortex.

[69]  Erik Blaser,et al.  Toddlers with Autism Spectrum Disorder are more successful at visual search than typically developing toddlers. , 2011, Developmental science.

[70]  M. Rutter,et al.  Autism and developmental receptive language disorder--a comparative follow-up in early adult life. I: Cognitive and language outcomes. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[71]  S. Petersen,et al.  Development of distinct control networks through segregation and integration , 2007, Proceedings of the National Academy of Sciences.

[72]  H. Barbas,et al.  Changes in Prefrontal Axons May Disrupt the Network in Autism , 2010, The Journal of Neuroscience.

[73]  S. Baron-Cohen,et al.  Superior visual search in autism. , 2001, Journal of experimental psychology. Human perception and performance.

[74]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[75]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[76]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[77]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[78]  Sarah Durston,et al.  A shift from diffuse to focal cortical activity with development. , 2006, Developmental science.

[79]  Kimberly L. Ray,et al.  Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions , 2012, Cognitive, affective & behavioral neuroscience.

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

[81]  Peter E. Clayson,et al.  Cognitive control and conflict adaptation in youth with high-functioning autism. , 2012, Journal of child psychology and psychiatry, and allied disciplines.

[82]  S. Petersen,et al.  Developmental changes in human cerebral functional organization for word generation. , 2005, Cerebral cortex.

[83]  M. Dulcan Dulcan's Textbook of Child and Adolescent Psychiatry , 2009 .

[84]  Moo K. Chung,et al.  Less white matter concentration in autism: 2D voxel-based morphometry , 2004, NeuroImage.

[85]  Claire Hughes,et al.  Executive function deficits in autism spectrum disorders and attention-deficit/hyperactivity disorder: Examining profiles across domains and ages , 2006, Brain and Cognition.

[86]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[87]  Stewart H. Mostofsky,et al.  Motor Signs Distinguish Children with High Functioning Autism and Asperger’s Syndrome from Controls , 2006, Journal of autism and developmental disorders.

[88]  C. Carter,et al.  ERP Correlates of Action Monitoring in Adolescence , 2004, Annals of the New York Academy of Sciences.

[89]  S. Ozonoff,et al.  A longitudinal study of executive function and theory of mind development in autism , 1994, Development and Psychopathology.

[90]  Conor V. Dolan,et al.  Source (or Part of the following Source): Type Article Title Age-related Change in Executive Function: Developmental Trends and a Latent Variable Analysis Author(s) Age-related Change in Executive Function: Developmental Trends and a Latent Variable Analysis , 2022 .

[91]  K. R. Ridderinkhof,et al.  The developing brain: From theory to neuroimaging and back , 2011, Developmental Cognitive Neuroscience.

[92]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[93]  Laurent Mottron,et al.  The Level and Nature of Autistic Intelligence , 2007, Psychological science.

[94]  Adam Gazzaley,et al.  Measuring functional connectivity during distinct stages of a cognitive task , 2004, NeuroImage.

[95]  R. Müller,et al.  Developmental Changes of Cortical and Cerebellar Motor Control: A Clinical Positron Emission Tomography Study With Children and Adults , 1998, Journal of child neurology.

[96]  H. Meltzer,et al.  Epidemiology of autism spectrum disorders in adults in the community in England. , 2011, Archives of general psychiatry.

[97]  C. Gillberg,et al.  Autism spectrum and attention – deficit disorders in girls. Some neuropsychological aspects , 2000, European Child & Adolescent Psychiatry.

[98]  C. Vaidya,et al.  Controlling attention to gaze and arrows in childhood: an fMRI study of typical development and Autism Spectrum Disorders. , 2011, Developmental science.

[99]  Cameron S. Carter,et al.  Cognitive control in autism spectrum disorders , 2008, International Journal of Developmental Neuroscience.

[100]  James D. A. Parker,et al.  The Revised Conners' Parent Rating Scale (CPRS-R): Factor Structure, Reliability, and Criterion Validity , 1998, Journal of abnormal child psychology.

[101]  R. Somsen,et al.  The development of attention regulation in the Wisconsin Card Sorting Task. , 2007, Developmental science.

[102]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .