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The Specificity of Inhibitory Impairments in Autism and Their Relation to ADHD-Type Symptoms

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Abstract

Findings on inhibitory control in autism have been inconsistent. This is perhaps a reflection of the different tasks that have been used. Children with autism (CWA) and typically developing controls, matched for verbal and non-verbal mental age, completed three tasks of inhibition, each representing different inhibitory subcomponents: Go/No-Go (delay inhibition), Dog-Pig Stroop (conflict inhibition), and a Flanker task (resistance to distractor inhibition). Behavioural ratings of inattention and hyperactivity/impulsivity were also obtained, as a possible source of heterogeneity in inhibitory ability. CWA were only impaired on the conflict inhibition task, suggesting that inhibitory difficulty is not a core executive deficit in autism. Symptoms of inattention were related to conflict task performance, and thus may be an important predictor of inhibitory heterogeneity.

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References

  • Adams, N. C., & Jarrold, C. (2009). Inhibition and the validity of the Stroop Task for children with autism. Journal of Autism and Developmental Disorders, 39, 1112–1121.

    Article  PubMed  Google Scholar 

  • American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders. Washington, DC: American Psychiatric Association.

    Google Scholar 

  • Ames, C. S., & Jarrold, C. (2007). The problem with using eye-gaze to infer desire: A deficit of cue inference in children with autism spectrum disorder? Journal of Autism and Developmental Disorders, 37, 1761–1775.

    Article  PubMed  Google Scholar 

  • Ames, C. S., & White, S. J. (2010). Brief report: Are ADHD traits dissociable from the autistic profile? Links between cognition and behaviour. Journal of Autism and Developmental Disorders, 41, 357–363.

    Article  Google Scholar 

  • Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6, 115–116.

    Article  PubMed  Google Scholar 

  • Aron, A. R., & Poldrack, R. A. (2005). The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biological Psychiatry, 57, 1285–1292.

    Article  PubMed  Google Scholar 

  • Barkley, R. A. (1997). ADHD and the nature of self-control. New York: Guilford.

    Google Scholar 

  • Biro, S., & Russell, J. (2001). The execution of arbitrary procedures by children with autism. Development and Psychopathology, 13, 97–110.

    Article  PubMed  Google Scholar 

  • Bishop, D. V. M., & Norbury, C. F. (2005). Executive functions in children with communication impairments, in relation to autistic symptomology. Autism, 9, 7–27.

    Article  PubMed  Google Scholar 

  • Bramham, J., Ambery, F., Young, S., Morris, R., Russell, A., Xenitidis, K., et al. (2009). Executive functioning differences between adults with attention deficit hyperactivity disorder and autistic spectrum disorder in initiation, planning and strategy formation. Autism, 13(3), 245–264.

    Article  PubMed  Google Scholar 

  • Brieber, S., Neufang, S., Bruning, N., Kamp-Becker, I., Remschmidt, H., Herpertz-Dahlmann, B., et al. (2007). Structural brain abnormalities in adolescents with autism spectrum disorder and patients with attention deficit/hyperactivity disorder. Journal of Child Psychology and Psychiatry, 48, 1251–1258.

    Article  PubMed  Google Scholar 

  • Butler, K. M., Zacks, R. T., & Henderson, J. M. (1999). Suppression of reflexive saccades in younger and older adults: Age comparisons on an antisaccade task. Memory & Cognition, 27, 584–591.

    Article  Google Scholar 

  • Carlson, S. M., & Moses, L. J. (2001). Individual differences in inhibitory control and children’s theory of mind. Child Development, 72, 1032–1053.

    Article  PubMed  Google Scholar 

  • Carlson, S. M., Moses, L. J., & Breton, C. (2002). How specific is the relation between executive function and theory of mind? Contributions of inhibitory control and working memory. Infant and Child Development, 11, 73–92.

    Article  Google Scholar 

  • Carlson, S. M., Moses, L. J., & Claxton, L. J. (2004). Individual differences in executive function and theory of mind: An investigation of inhibitory control and planning ability. Journal of Experimental Child Psychology, 87, 299–329.

    Article  PubMed  Google Scholar 

  • Castellanos, F. X., & Tannock, R. (2002). Neuroscience of attention-deficit/hyperactivity disorder: The search for endophenotypes. Nature Reviews Neuroscience, 3, 617–628.

    PubMed  Google Scholar 

  • Chhabildas, N., Pennington, B. F., & Willcutt, E. G. (2001). A comparison of the neuropsychological profiles of the DSM-IV subtypes of ADHD. Journal of Abnormal Child Psychology, 29, 529–540.

    Article  PubMed  Google Scholar 

  • Christ, S. E., Holt, D. D., White, D. A., & Green, L. (2007). Inhibitory control in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 37, 1155–1165.

    Article  PubMed  Google Scholar 

  • Collett, B. R., Ohan, J. L., & Myers, K. M. (2003). Ten-year review of rating scales. V: Scales assessing attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 42, 1015–1037.

    Article  PubMed  Google Scholar 

  • Dagenbach, D., & Carr, T. H. (Eds.). (1994). Inhibitory processes in attention, memory and language. San Diego, CA: Academic Press.

    Google Scholar 

  • Davelaar, E. J., & Cooper, R. P. (2010). Modelling the correlation between two putative inhibition tasks: an analytic approach. In R. Camtrabone & S. Ohlsson (Eds.), Proceedings of the 32nd annual meeting of the cognitive science society (pp. 937–942). Portland, OR: Cognitive Science Society.

    Google Scholar 

  • Diamond, A., & Taylor, C. (1996). Development of an aspect of executive control: Development of the abilities to remember what I said and to “Do as I say, not as I do”. Developmental Psychobiology, 29, 315–334.

    Article  PubMed  Google Scholar 

  • Dichter, G. S., & Belger, A. (2007). Social stimuli interfere with cognitive control in autism. Neuroimage, 35(3), 1219–1230.

    Article  PubMed  Google Scholar 

  • Dunn, L. M., Dunn, L. M., Whetton, C., & Burley, J. (1997). British picture vocabulary scale (2nd ed.). Windsor: NFER-Nelson.

    Google Scholar 

  • Earles, J. L., Connor, L. T., Frieske, D., Park, D. C., Smith, A. D., & Zwahr, M. (1997). Age differences in inhibition: possible causes and consequences. Aging, Neuropsychology, and Cognition, 4(1), 45–57.

    Article  Google Scholar 

  • Eriksen, B. A., & Eriksen, C. W. (1974). Effects of noise letters upon the identification of a target letter in a non-search task. Perception & Psychophysics, 16, 143–149.

    Article  Google Scholar 

  • Eskes, G. A., Bryson, S. E., & McCormick, T. A. (1990). Comprehension of concrete and abstract words in autistic children. Journal of Autism and Developmental Disorders, 20, 61–73.

    Article  PubMed  Google Scholar 

  • Friedman, N. P., & Miyake, A. (2004). The relations among inhibition and interference control functions: A latent variable analysis. Journal of Experimental Psychology: General, 133, 101–135.

    Article  Google Scholar 

  • Garavan, H., Hester, R., Murphy, K., Fassbender, C., & Kelly, C. (2006). Individual differences in the functional neuroanatomy of inhibitory control. Brain Research, 1105, 130–142.

    Article  PubMed  Google Scholar 

  • Gerstadt, C., Hong, Y., & Diamond, A. (1994). The relationship between cognition and action: Performance of children 31/2–7 years on a Stroop-like day-night test. Cognition, 53, 129–153.

    Article  PubMed  Google Scholar 

  • Geurts, H., Verté, S., Oosterlaan, J., Roeyers, H., & Sergeant, J. (2004). How specific are executive functioning deficits in attention deficits in attention deficit hyperactivity disorder and autism? Journal of Child Psychology and Psychiatry and Allied Disciplines, 45, 836–845.

    Article  Google Scholar 

  • Gioia, G. A., Isquith, P. K., Kenworthy, L., & Barton, R. M. (2002). Profiles of everyday executive function in acquired and developmental disorders. Child Neuropsychology, 8, 121–137.

    Article  PubMed  Google Scholar 

  • Goldberg, M. C., Mostofsky, S. H., Cutting, L. E., Mahone, E. M., Astor, B. C., Denckla, M. B., et al. (2005). Subtle executive impairment in children with autism and ADHD. Journal of Autism and Developmental Disorders, 35, 279–293.

    Article  PubMed  Google Scholar 

  • Grier, J. B. (1971). Nonparametric indexes for sensitivity and bias: Computing formulas. Psychological Bulletin, 75, 424–429.

    Article  PubMed  Google Scholar 

  • Hala, S., Hug, S., & Henderson, A. (2003). Executive function and false belief understanding in preschool children: Two tasks are harder than one. Journal of Cognition and Development, 4, 275–298.

    Article  Google Scholar 

  • Happé, F., Booth, R., Charlton, R., & Hughes, C. (2006). Executive function deficits in autism spectrum disorders and attention-deficit/hyperactivity disorder: Examining profiles across domains and ages. Brain and Cognition, 61, 26–39.

    Article  Google Scholar 

  • Henderson, H., Schwartz, C., Mundy, P., Burnette, C., Sutton, S., Zahka, N., et al. (2006). Response monitoring, the error-related negativity and differences in social behaviour in autism. Brain and Cognition, 61(1), 96–109.

    Article  PubMed  Google Scholar 

  • Hill, E. L. (2004a). Evaluating the theory of executive dysfunction in autism. Developmental Review, 24(2), 189–233.

    Article  Google Scholar 

  • Hill, E. L. (2004b). Executive dysfunction in autism. Trends in Cognitive Sciences, 8(1), 26–32.

    Article  PubMed  Google Scholar 

  • Howell, D. (2002). Statistical methods for psychology (5th ed.). Belmont, CA: Duxbury Press.

    Google Scholar 

  • Hughes, C., & Russell, J. (1993). Autistic children’s difficulty with mental disengagement from an object: Its implications for theories of autism. Developmental Psychology, 29, 498–510.

    Article  Google Scholar 

  • Jarrold, C., & Brock, J. (2004). To match or not to match? Methodological issues in autism-related research. Journal of Autism and Developmental Disorders, 34, 81–86.

    Article  PubMed  Google Scholar 

  • Joseph, R. M., Tager-Flusberg, H., & Lord, C. (2002). Cognitive profiles and social-communicative functioning in children with autism spectrum disorder. Journal of Child Psychology and Psychiatry, 43, 807–821.

    Article  PubMed  Google Scholar 

  • Leckman, J., Price, R., Walkup, J., Ort, S., Pauls, D., & Cohen, J. (1987). Nongenetic factors in Gilles de la Tourette’s syndrome. Archives of General Psychiatry, 44, 100.

    Article  PubMed  Google Scholar 

  • Lee, D. O., & Ousley, O. (2006). Attention-deficit hyperactivity disorder symptoms in a clinic sample of children and adolescents with pervasive developmental disorders. Journal of Child and Adolescent Psychopharmacology, 16, 737–746.

    Article  PubMed  Google Scholar 

  • Lemon, J. M., Gargaro, B., Enticott, P. G., & Rinehart, N. J. (2011). Brief report: Executive functioning in autism spectrum disorders: A gender comparison of response inhibition. Journal of Autism and Developmental Disorders, 41, 352–356.

    Article  PubMed  Google Scholar 

  • Levin, H. S., Culhane, K. A., Hartmann, J., Evankovich, K., & Mattson, A. J. (1991). Developmental changes in performance on tests of purported frontal lobe functioning. Developmental Neuropsychology, 7, 377–395.

    Article  Google Scholar 

  • Leyfer, O. T., Folstein, S. E., Bacalman, S., Davis, N. O., Dinh, E., Morgan, J., et al. (2006). Comorbid psychiatric disorders in children with autism: interview development and rates of disorders. Journal of Autism and Developmental Disorder, 36, 849–861.

    Article  Google Scholar 

  • Lijffijt, M., Kenemans, J. L., Verbaten, M. N., & van Engeland, H. (2005). A meta-analytic review of stopping performance in attention-deficit/hyperactivity disorder: Deficient inhibitory motor control? Journal of Abnormal Psychology, 114, 216–222.

    Article  PubMed  Google Scholar 

  • Lopez, B. R., Lincoln, A. J., Ozonoff, S., & Lai, Z. (2005). Examining the relationship between executive functions and restricted, repetitive symptoms of autistic disorder. Journal of Autism and Developmental Disorders, 35, 445–460.

    Article  PubMed  Google Scholar 

  • MacLeod, C. M. (1991). Half a century of research on the Stroop effect: An integrative review. Psychological Bulletin, 109, 163–203.

    Article  PubMed  Google Scholar 

  • Manly, T., Robertson, I. H., Anderson, V., & Nimmo-Smith, I. (1999). The Test of Everyday Attention for Children (TEA-Ch). Bury St. Edmunds, UK: Thames Valley Test Company.

    Google Scholar 

  • Mesibov, G. G., Schopler, E., Schaffer, B., & Michal, N. (1989). Use of the Childhood Autism Rating Scale with autistic adolescents and adults. Journal of the American Academy of Child and Adolescent Psychiatry, 28, 538–541.

    Article  PubMed  Google Scholar 

  • Miller, G. A., & Chapman, J. P. (2001). Misunderstanding analysis of covariance. Journal of Abnormal Psychology, 110(1), 40–48.

    Article  PubMed  Google Scholar 

  • Minshew, N. J., Luna, B., & Sweeney, J. A. (1999). Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology, 52(5), 917–922.

    Article  PubMed  Google Scholar 

  • Mitchell, J. P., Macrae, C. N., & Gilchrist, I. D. (2002). Working memory and the suppression of reflexive saccades. Journal of Cognitive Neuroscience, 14, 95–103.

    Article  PubMed  Google Scholar 

  • Nation, K. (2006). Patterns of reading ability in children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 36, 911–919.

    Article  PubMed  Google Scholar 

  • Nigg, J. T. (2000). On inhibition/disinhibition in developmental psychopathology: Views from cognitive and personality psychology and a working inhibition taxonomy. Psychological Bulletin, 126, 220–246.

    Article  PubMed  Google Scholar 

  • Nigg, J. T. (2001). Is ADHD a disinhibitory disorder? Psychological Bulletin, 127, 571–598.

    Article  PubMed  Google Scholar 

  • Norman, D., & Shallice, T. (1986). Attention to action: Willed and automatic control of behavior. In R. Davidson, R. G. Schwartz, & D. Shapiro (Eds.), Consciousness and self-regulation: Advances in research and theory (pp. 1–18). New York: Plenum Press.

    Google Scholar 

  • Noterdaeme, M., Amorosa, H., Mildenberger, K., Sitter, S., & Minow, F. (2001). Evaluation of attention problems in children with autism and children with a specific language disorder. European Child and Adolescent Psychiatry, 10, 58–66.

    Article  PubMed  Google Scholar 

  • Ozonoff, S., & Jensen, J. (1999). Specific executive function profiles in three neurodevelopmental disorders. Journal of Autism and Developmental Disorder, 29, 171–177.

    Article  Google Scholar 

  • Ozonoff, S., & Strayer, D. L. (1997). Inhibitory function in nonretarded children with Autism. Journal of Autism and Developmental Disorders, 27, 59–77.

    Article  PubMed  Google Scholar 

  • Ozonoff, S., Strayer, D., McMahon, W., & Filloux, F. (1994). Executive function abilities in autism: An informational processing approach. Journal of Child Psychology and Psychiatry, 35, 1015–1031.

    Article  PubMed  Google Scholar 

  • Pennington, B. F. (1997). Dimensions of Executive Functions in Normal and Abnormal Development. In N. Krasnegor, G. R. Lyon, & P. S. Goldman-Rakic (Eds.), Prefrontal cortex: Evolution, development, and behavioral neuroscience (pp. 265–281). Baltimore, MD: Brookes.

    Google Scholar 

  • Perlstein, W., Carter, C., Barch, D., & Baird, J. (1998). The stroop task and attention deficits in Schizophrenia: A critical evaluation of card and single-trial Stroop methodologies. Neuropsychology, 12, 414–425.

    Article  PubMed  Google Scholar 

  • Perret, E. (1974). The left frontal lobe in man and the suppression of habitual responses in verbal categorical behavior. Neuropsychologia, 12, 323–330.

    Article  PubMed  Google Scholar 

  • Raven, J. C., Court, J. H., & Raven, J. (1990). Coloured progressive matrices. Oxford: Oxford Psychologists Press.

    Google Scholar 

  • Ridderinkhof, K. R., Band, G. P. H., & Logan, G. D. (1999). A study of adaptive behavior: Effects of age and irrelevant information on the ability to inhibit one’s actions. Acta Psychologica, 101, 315–337.

    Article  Google Scholar 

  • Rommelse, N. N. J., Franke, B., Geurts, H. M., Hartman, C. A., & Buitelaar, J. K. (2010). Shared heritability of attention-deficit/hyperactivity disorder and autism spectrum disorder. European Child and Adolescent Psychiatry, 19(3), 281–295.

    Article  PubMed  Google Scholar 

  • Russell, J. (1997). Autism as an executive disorder. Oxford: Oxford University Press.

    Google Scholar 

  • Russell, J., Hala, S., & Hill, E. (2003). The automated windows task: the performance of preschool children, children with autism, and children with moderate learning difficulties. Cognitive Development, 18(1), 111–137.

    Article  Google Scholar 

  • Russell, J., Jarrold, C., & Hood, B. (1999). Two intact executive capacities in children with autism: Implications for the core executive dysfunctions in the disorder. Journal of Autism and Developmental Disorders, 29, 103–112.

    Article  PubMed  Google Scholar 

  • Russell, J., Mauthner, N., Sharpe, S., & Tidswell, T. (1991). The ‘windows task’ as a measure of strategic deception in preschoolers and autistic subjects. British Journal of Developmental Psychology, 9, 331–349.

    Article  Google Scholar 

  • Semrud-Clikeman, M., Walkowiak, J., Wilkinson, A., & Butcher, B. (2010). Executive functioning in children with Asperger syndrome, ADHD-Combined type, ADHD-Predominately Inattentive type, and Controls. Journal of Autism and Developmental Disorders, 40(8), 1017–1027.

    Article  PubMed  Google Scholar 

  • Simpson, A., & Riggs, K. J. (2005). Inhibitory and working memory demands of the day-night task in children. British Journal of Developmental Psychology, 23, 471–486.

    Article  Google Scholar 

  • Sinzig, J., Morsch, D., Bruning, N., Schmidt, M. H., & Lehmkuhl, G. (2008). Inhibition, flexibility, working memory and planning in autism spectrum disorders with and without comorbid ADHD-symptoms. Child and Adolescent Psychiatry and Mental Health, 2, 4.

    Article  Google Scholar 

  • Sinzig, J., Walter, D., & Doepfner, M. (2009). Attention deficit/hyperactivity disorder in children and adolescents with autism spectrum disorder: Symptom or syndrome? Journal of Attention Disorders, 13, 117–126.

    Article  PubMed  Google Scholar 

  • Stroop, J. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643–662.

    Article  Google Scholar 

  • Stuss, D. T., Toth, J. P., Franchi, D., Alexander, M. P., Tipper, S., & Craik, F. I. M. (1999). Dissociation of attentional processes in patients with focal frontal and posterior lesions. Neuropsychologia, 37, 1005–1027.

    Article  PubMed  Google Scholar 

  • Tipper, S. P. (1985). The negative priming effect: Inhibitory priming by ignored objects. Quarterly Journal of Experimental Psychology, 37A, 571–590.

    Google Scholar 

  • Turner, M. (1997). Towards an executive dysfunction account of repetitive behaviour in autism. In J. Russell (Ed.), Autism as an executive disorder (pp. 57–100). Oxford, NY: Oxford University Press.

    Google Scholar 

  • Vendrell, P., Junque, C., Pujol, J., Jurado, M. A., Molet, J., & Grafman, J. (1995). The role of prefrontal regions in the Stroop task. Neuropsychologia, 33, 341–352.

    Article  PubMed  Google Scholar 

  • Verté, S., Geurts, H. M., Roeyers, H., Oosterlaan, J., & Sergeant, J. A. (2006). The relationship if working memory, inhibition, and response variability in child psychopathology. Journal of Neuroscience Methods, 151, 5–14.

    Article  PubMed  Google Scholar 

  • Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory: a meta-analysis. Cognitive, Affective and Behavioural Neuroscience, 3, 255–274.

    Article  Google Scholar 

  • Welsh, M. C., & Pennington, B. F. (1988). Assessing frontal lobe functioning in children: Views from developmental psychology. Developmental Neuropsychology, 4, 199–230.

    Article  Google Scholar 

  • Willcutt, E. G., Doyle, A. E., Nigg, J. T., Faraone, S. V., & Pennington, B. F. (2005). Validity of the executive function theory of attention-deficit/hyperactivity disorder: A meta-analytic review. Biological Psychiatry, 57, 1336–1346.

    Article  PubMed  Google Scholar 

  • Williams, B. R., Ponesse, J. S., Schachar, R. J., Logan, G. D., & Tannock, R. (1999). Development of inhibitory control across the life span. Developmental Psychology, 35(1), 205–213.

    Article  PubMed  Google Scholar 

  • Wolraich, M. L., Feurer, I., Hannah, J. N., Pinnock, T. Y., & Baumgaertel, A. (1998). Obtaining systematic teacher reports of disruptive behaviour disorders utilizing DSM-IV. Journal of Abnormal Child Psychology, 26, 141–152.

    Article  PubMed  Google Scholar 

  • Yerys, B. E., Wallace, G. L., Sokoloff, J. L., Shook, D. A., James, J. D., & Kenworthy, L. (2009). Attention deficit/hyperactivity disorder symptoms moderate cognition and behavior in children with autism spectrum disorders. Autism Research, 2(6), 322–333.

    PubMed  Google Scholar 

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Acknowledgments

Many thanks to the staff and students of Peterhouse School, Presfield School, Larkfield Primary School, Trinity St. Peters C of E Primary School and Holy Trinity, Southport.

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  1. Charlotte Sanderson

    Present address: Behavioural and Brain Sciences Unit, University College London (UCL) Institute of Child Health, 30 Guilford Street, London, WC1N 1EH, UK

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  1. Department of Psychology, Lancaster University, Lancashire, UK

    Charlotte Sanderson & Melissa L. Allen

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Sanderson, C., Allen, M.L. The Specificity of Inhibitory Impairments in Autism and Their Relation to ADHD-Type Symptoms. J Autism Dev Disord 43, 1065–1079 (2013). https://doi.org/10.1007/s10803-012-1650-5

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