Exploring ‘The autisms’ at a cognitive level
Corresponding Author
Cathriona Cantio
Child and Adolescent Psychiatric Department, Mental Health Services in Southern Denmark, Odense, Denmark
Institute of Clinical Research, University of Southern Denmark, Odense, Denmark
Address for correspondence and reprints: Cathriona Cantio, Child and Adolescent Psychiatric Department, Odense, Sdr. Boulevard 29, 5000 Odense C, Denmark. E-mail: [email protected]Search for more papers by this authorJens Richardt Møllegaard Jepsen
Centre for Neuropsychiatric Schizophrenia Research & Centre for Clinical Intervention and Neuropsychiatric Schizophrenia Research, Copenhagen University Hospital, Psychiatric Hospital Centre, Glostrup, Denmark
Child and Adolescent Mental Health Centre, Mental Health Services Capital Region of Denmark, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorGitte Falcher Madsen
Child and Adolescent Psychiatric Department, Mental Health Services in Southern Denmark, Odense, Denmark
Search for more papers by this authorNiels Bilenberg
Child and Adolescent Psychiatric Department, Mental Health Services in Southern Denmark, Odense, Denmark
Institute of Clinical Research, University of Southern Denmark, Odense, Denmark
Search for more papers by this authorSarah J. White
Institute of Cognitive Neuroscience, University College London, London, UK
Search for more papers by this authorCorresponding Author
Cathriona Cantio
Child and Adolescent Psychiatric Department, Mental Health Services in Southern Denmark, Odense, Denmark
Institute of Clinical Research, University of Southern Denmark, Odense, Denmark
Address for correspondence and reprints: Cathriona Cantio, Child and Adolescent Psychiatric Department, Odense, Sdr. Boulevard 29, 5000 Odense C, Denmark. E-mail: [email protected]Search for more papers by this authorJens Richardt Møllegaard Jepsen
Centre for Neuropsychiatric Schizophrenia Research & Centre for Clinical Intervention and Neuropsychiatric Schizophrenia Research, Copenhagen University Hospital, Psychiatric Hospital Centre, Glostrup, Denmark
Child and Adolescent Mental Health Centre, Mental Health Services Capital Region of Denmark, University of Copenhagen, Copenhagen, Denmark
Search for more papers by this authorGitte Falcher Madsen
Child and Adolescent Psychiatric Department, Mental Health Services in Southern Denmark, Odense, Denmark
Search for more papers by this authorNiels Bilenberg
Child and Adolescent Psychiatric Department, Mental Health Services in Southern Denmark, Odense, Denmark
Institute of Clinical Research, University of Southern Denmark, Odense, Denmark
Search for more papers by this authorSarah J. White
Institute of Cognitive Neuroscience, University College London, London, UK
Search for more papers by this authorAbstract
The autism spectrum is characterized by genetic and behavioral heterogeneity. However, it is still unknown whether there is a universal pattern of cognitive impairment in autism spectrum disorder (ASD) and whether multiple cognitive impairments are needed to explain the full range of behavioral symptoms. This study aimed to determine whether three widely acknowledged cognitive abnormalities (Theory of Mind (ToM) impairment, Executive Function (EF) impairment, and the presence of a Local Processing Bias (LB)) are universal and fractionable in autism, and whether the relationship between cognition and behavior is dependent on the method of behavioral assessment. Thirty-one high-functioning children with ASD and thirty-seven children with neurotypical development (NTD), comparable in age, gender and Intelligence Quotient (IQ), completed several tasks tapping into ToM, EF, and LB, and autistic symptomatology was assessed through parental and teacher questionnaires, parental interview and direct observation. We found that ToM and EF deficits differentiated the groups and some ToM and EF tasks were related to each other. ToM and EF were together able to correctly classify more than three-quarters of the children into cases and controls, despite relating to none of the specific behavioral measures. Only a small subgroup of individuals displayed a LB, which was unrelated to ToM and EF, and did not aid diagnostic classification, most likely contributing to non-diagnostic symptoms in a subgroup. Despite the characteristic heterogeneity of the autism spectrum, it remains a possibility therefore that a single cognitive cause may underlie the range of diagnostic symptoms in all individuals with autism. Autism Res 2016, 9: 1328–1339. © 2016 International Society for Autism Research, Wiley Periodicals, Inc.
References
- Abell, F., Happé, F., & Frith, U. (2000). Do triangles play tricks? Attribution of mental states to animated shapes in normal and abnormal development. Cognitive Development, 15(1), 1–16. doi:10.1016/S0885-2014%2800%2900014-9
- Abrahams, B.S., & Geschwind, D.H. (2008). Advances in autism genetics: on the threshold of a new neurobiology. Nature Reviews Genetics, 9(5), 341–355. doi:10.1038/nrg2346
- Amaral, D.G., Schumann, C.M., & Nordahl, C.W. (2008). Neuroanatomy of autism. Trends in Neurosciences, 31(3), 137–145. doi:10.1016/j.tins.2007.12.005
- Ambery, F.Z., Russell, J., Perry, K., Morris, R., & Murphy, D.G. (2006). Neuropsychological functioning in adults with Asperger syndrome. Autism, 10(6), 551–564. doi:10.1177/1362361306068507
- American Psychiatric Association (2013). Diagnostic and statistical manual of mental disorders (5th ed.).
- Baron-Cohen, S., Leslie, A.M., & Frith, U. (1985). Does the autistic child have a “theory of mind”? Cognition, 21(1), 37–46.
- Berument, S.K., Rutter, M., Lord, C., Pickles, A., & Bailey, A. (1999). Autism screening questionnaire: diagnostic validity. The British Journal of Psychiatry: The Journal of Mental Science, 175, 444–451.
- Betancur, C. (2011). Etiological heterogeneity in autism spectrum disorders: more than 100 genetic and genomic disorders and still counting. Brain Research, 1380, 42–77. doi:10.1016/j.brainres.2010.11.078
- Bishop, D.V., & Norbury, C.F. (2005a). Executive functions in children with communication impairments, in relation to autistic symptomatology. 1: generativity. Autism, 9(1), 7–27. doi:10.1177/1362361305049027
- Bishop, D.V., & Norbury, C.F. (2005b). Executive functions in children with communication impairments, in relation to autistic symptomatology. 2: response inhibition. Autism, 9(1), 29–43. doi:10.1177/1362361305049028
- Brunsdon, V.E., Colvert, E., Ames, C., Garnett, T., Gillan, N., Hallett, V., … Happé, F. (2014). Exploring the cognitive features in children with autism spectrum disorder, their co-twins, and typically developing children within a population-based sample. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 56(8), 893–902. doi:10.1111/jcpp.12362
- Brunsdon, V.E., & Happé, F. (2014). Exploring the 'fractionation' of autism at the cognitive level. Autism, 18(1), 17–30. doi:10.1177/1362361313499456
- Castellanos, F.X., Sonuga-Barke, E.J., Milham, M.P., & Tannock, R. (2006). Characterizing cognition in ADHD: beyond executive dysfunction. Trends in Cognitive Sciences, 10(3), 117–123. doi:10.1016/j.tics.2006.01.011
- Castelli, F., Frith, C., Happé, F., & Frith, U. (2002). Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain, 125(Pt 8), 1839–1849.
- Charman, T., Baird, G., Simonoff, E., Loucas, T., Chandler, S., Meldrum, D., & Pickles, A. (2007). Efficacy of three screening instruments in the identification of autistic-spectrum disorders. The British Journal of Psychiatry: The Journal of Mental Science, 191, 554–559. doi:10.1192/bjp.bp.107.040196
- Constantino, J.N., Davis, S.A., Todd, R.D., Schindler, M.K., Gross, M.M., Brophy, S.L., … Reich, W. (2003). Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433.
- Corbett, B.A., Constantine, L.J., Hendren, R., Rocke, D., & Ozonoff, S. (2009). Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development. Psychiatry Research, 166(2-3), 210–222. doi:10.1016/j.psychres.2008.02.005
- Frith, U. (1989). Autism: explaining the enigma. Cambridge, Massachusettes: Blackwell.
- Frith, U. (2012). Why we need cognitive explanations of autism. Quarterly Journal of Experimental Psychology, 65(11), 2073–2092. doi:10.1080/17470218.2012.697178
- Geschwind, D.H. (2009). Advances in autism. Annual Review of Medicine, 60, 367–380. doi:10.1146/annurev.med.60.053107.121225
- Geschwind, D.H., & Levitt, P. (2007). Autism spectrum disorders: developmental disconnection syndromes. Current Opinion in Neurobiology, 17(1), 103–111. doi:10.1016/j.conb.2007.01.009
- Gliga, T., Jones, E.J., Bedford, R., Charman, T., & Johnson, M.H. (2014). From early markers to neuro-developmental mechanisms of autism. Developmental Review, 34(3), 189–207. doi:10.1016/j.dr.2014.05.003
- Goldani, A.A., Downs, S.R., Widjaja, F., Lawton, B., & Hendren, R.L. (2014). Biomarkers in autism. Frontiers in Psychiatry, 5, 100. doi:10.3389/fpsyt.2014.00100
- Goldberg, M.C., Mostofsky, S.H., Cutting, L.E., Mahone, E.M., Astor, B.C., Denckla, M.B., & Landa, R.J. (2005). Subtle executive impairment in children with autism and children with ADHD. Journal of Autism and Developmental Disorders, 35(3), 279–293.
- Happé, F., & Frith, U. (2006). The weak coherence account: detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 5–25. doi:10.1007/s10803-005-0039-0
- Happé, F., & Ronald, A. (2008). The 'fractionable autism triad': a review of evidence from behavioural, genetic, cognitive and neural research. Neuropsychology Review, 18(4), 287–304. doi:10.1007/s11065-008-9076-8
- Happé, F., Ronald, A., & Plomin, R. (2006). Time to give up on a single explanation for autism. Nature Neuroscience, 9(10), 1218–1220. doi:10.1038/nn1770
- Hill, E.L. (2004). Executive dysfunction in autism. Trends in Cognitive Sciences, 8(1), 26–32.
- Hooper, H.E. (1983). The Hooper visual organisation test manual. Los Angeles, CA: Western Psychological Services.
- Jolliffe, T., & Baron-Cohen, S. (2001). A test of central coherence theory: can adults with high-functioning autism or Asperger syndrome integrate fragments of an object? Cognitive Neuropsychiatry, 6(3), 193–216. doi:10.1080/13546800042000124
- Joseph, R.M., & Tager-Flusberg, H. (2004). The relationship of theory of mind and executive functions to symptom type and severity in children with autism. Development and Psychopathology, 16(1), 137–155.
- Kaland, N., Callesen, K., Moller-Nielsen, A., Mortensen, E.L., & Smith, L. (2008). Performance of children and adolescents with Asperger syndrome or high-functioning autism on advanced theory of mind tasks. Journal of Autism and Developmental Disorders, 38(6), 1112–1123. doi:10.1007/s10803-007-0496-8
- Kenworthy, L., Yerys, B.E., Anthony, L.G., & Wallace, G.L. (2008). Understanding executive control in autism spectrum disorders in the lab and in the real world. Neuropsychology Review, 18(4), 320–338. doi:10.1007/s11065-008-9077-7
- Lai, M.C., Lombardo, M.V., & Baron-Cohen, S. (2013). Autism. Lancet, 383(9920), 896–910. doi:10.1016/S0140-6736(13)61539-1
- Lai, M.C., Lombardo, M.V., Ruigrok, A.N., Chakrabarti, B., Wheelwright, S.J., Auyeung, B., … Baron-Cohen, S. (2012). Cognition in males and females with autism: similarities and differences. PLoS One, 7(10), e47198. doi:10.1371/journal.pone.0047198
- Lam, Y.G. (2013). Re-examining the cognitive phenotype in autism: a study with young Chinese children. Research in Developmental Disabilities, 34(12), 4591–4598. doi:10.1016/j.ridd.2013.09.039
- Lawson, R.P., Rees, G., & Friston, K.J. (2014). An aberrant precision account of autism. Frontiers in Human Neuroscience, 8, 302. doi:10.3389/fnhum.2014.00302
- Lord, C., Risi, S., Lambrecht, L., Cook, E.H. Jr., Leventhal, B.L., DiLavore, P.C., … Rutter, M. (2000). The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.
- Lord, C., Rutter, M., & Le Couteur, A. (1994). Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24(5), 659–685.
- Morton, J. (2008). Understanding developmental disorders: a causal modelling approach. Oxford, UK: Wiley-Blackwell.
- Munson, J., Faja, S., Meltzoff, A., Abbott, R., & Dawson, G. (2008). Neurocognitive predictors of social and communicative developmental trajectories in preschoolers with autism spectrum disorders. Journal of the International Neuropsychological Society: JINS, 14(6), 956–966. doi:10.1017/S1355617708081393
- O'Roak, B.J., Vives, L., Fu, W., Egertson, J.D., Stanaway, I.B., Phelps, I.G., … Shendure, J. (2012). Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science, 338(6114), 1619–1622. doi:10.1126/science.1227764
- Ozonoff, S., Pennington, B.F., & Rogers, S.J. (1991). Executive function deficits in high-functioning autistic individuals: relationship to theory of mind. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 32(7), 1081–1105.
- Pellicano, E. (2007). Links between theory of mind and executive function in young children with autism: clues to developmental primacy. Developmental Psychology, 43(4), 974–990. doi:10.1037/0012-1649.43.4.974
- Pellicano, E. (2010). Individual differences in executive function and central coherence predict developmental changes in theory of mind in autism. Developmental Psychology, 46(2), 530–544. doi:10.1037/a0018287
- Pellicano, E., & Burr, D. (2012). When the world becomes 'too real': a Bayesian explanation of autistic perception. Trends in Cognitive Sciences, 16(10), 504–510. doi:10.1016/j.tics.2012.08.009
- Pellicano, E., Maybery, M., Durkin, K., & Maley, A. (2006). Multiple cognitive capabilities/deficits in children with an autism spectrum disorder: “weak” central coherence and its relationship to theory of mind and executive control. Development and Psychopathology, 18( 1), 77−98. doi:10.1017/s0954579406060056
- Rajendran, G., & Mitchell, P. (2007). Cognitive theories of autism. Developmental Review, 27(2), 224–260.
- Ronald, A., Happé, F., Price, T.S., Baron-Cohen, S., & Plomin, R. (2006). Phenotypic and genetic overlap between autistic traits at the extremes of the general population. Journal of the American Academy of Child and Adolescent Psychiatry, 45(10), 1206–1214. doi:10.1097/01.chi.0000230165.54117.41
- Russo, N., Flanagan, T., Iarocci, G., Berringer, D., Zelazo, P.D., & Burack, J.A. (2007). Deconstructing executive deficits among persons with autism: implications for cognitive neuroscience. Brain and Cognition, 65(1), 77–86. doi:10.1016/j.bandc.2006.04.007
- Rutter, M. (2000). Genetic studies of autism: from the 1970s into the millennium. Journal of Abnormal Child Psychology, 28(1), 3–14.
- Salter, G., Seigal, A., Claxton, M., Lawrence, K., & Skuse, D. (2008). Can autistic children read the mind of an animated triangle? Autism, 12(4), 349–371. doi:10.1177/1362361308091654
- Schuwerk, T., Vuori, M., & Sodian, B. (2015). Implicit and explicit theory of mind reasoning in autism spectrum disorders: the impact of experience. Autism, 19(4), 459–468. doi:10.1177/1362361314526004
- Senju, A. (2012). Spontaneous theory of mind and its absence in autism spectrum disorders. Neuroscientist, 18(2), 108–113. doi:10.1177/1073858410397208
- Senju, A., Southgate, V., White, S., & Frith, U. (2009). Mindblind eyes: an absence of spontaneous theory of mind in Asperger syndrome. Science, 325(5942), 883–885. doi:10.1126/science.1176170
- Sodian, B., & Thoermer, C. (2008). Precursors to a theory of mind in infancy: perspectives for research on autism. Quarterly Journal of Experimental Psychology, 61(1), 27–39. doi:10.1080/17470210701508681
- Spek, A.A., Scholte, E.M., & Van Berckelaer-Onnes, I.A. (2010). Theory of mind in adults with HFA and Asperger syndrome. Journal of Autism and Developmental Disorders, 40(3), 280–289. doi:10.1007/s10803-009-0860-y
- Spreen, O., & Benton, L.A. (1969). Embedded figures test. University of Victoria, Victoria, BC: Neuropsychological Laboratory.
- Towgood, K.J., Meuwese, J.D., Gilbert, S.J., Turner, M.S., & Burgess, P.W. (2009). Advantages of the multiple case series approach to the study of cognitive deficits in autism spectrum disorder. Neuropsychologia, 47(13), 2981–2988. doi:10.1016/j.neuropsychologia.2009.06.028
- Turner, M.A. (1999). Generating novel ideas: fluency performance in high-functioning and learning disabled individuals with autism. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 40(2), 189–201.
- Velloso Rde, L., Duarte, C.P., & Schwartzman, J.S. (2013). Evaluation of the theory of mind in autism spectrum disorders with the Strange Stories test. Arquivos de Neuro-Psiquiatria, 71(11), 871–876. doi:10.1590/0004-282X20130171
- White, S. (2013). The Triple I Hypothesis: taking another('s) perspective on executive dysfunction in autism. Journal of Autism and Developmental Disorders, 43(1), 114–121. doi:10.1007/s10803-012-1550-8
- White, S., Hill, E., Happé, F., & Frith, U. (2009). Revisiting the strange stories: revealing mentalizing impairments in autism. Child Development, 80(4), 1097–1117. doi:10.1111/j.1467-8624.2009.01319.x
- White, S., Milne, E., Rosen, S., Hansen, P., Swettenham, J., Frith, U., & Ramus, F. (2006). The role of sensorimotor impairments in dyslexia: a multiple case study of dyslexic children. Developmental Science, 9(3), 237–255; discussion 265-239. doi:10.1111/j.1467-7687.2006.00483.x
- Williams, D., & Jarrold, C. (2013). Assessing planning and set-shifting abilities in autism: are experimenter-administered and computerised versions of tasks equivalent? Autism research: official journal of the International Society for Autism Research, 6(6), 461–467. doi:10.1002/aur.1311
- Zelazo, P.D., Jacques, S., Burack, J.A., Frye, D. (2002). The Relation between theory of mind and rule use: evidence from persons with autism-spectrum disorders. Infant and Child Development, 11, 171–195. doi:10.1002/icd.304
- Zoghbi, H.Y. (2003). Postnatal neurodevelopmental disorders: meeting at the synapse? Science, 302(5646), 826–830. doi:10.1126/science.1089071