Abstract
Impaired executive functioning (EF) has been proposed to underlie symptoms of autism spectrum disorders (ASD). However, insight in the EF profile of ASD individuals is hampered due to task impurity and inconsistent findings. To elucidate these inconsistencies, we investigated the influence of task and sample characteristics on EF in ASD, with an extended test battery designed to reduce task impurity. Additionally, we studied the relation between EF and ASD symptoms. EF (inhibition, cognitive flexibility, generativity, working memory and planning) was measured in open-ended versus structured assessment situations, while controlling for possible confounding EF and non-EF variables. The performance of 50 individuals with ASD was compared with that of 50 age, gender and IQ matched typically developing (TD) individuals. The effects of group (ASD versus TD), age (children versus adolescents) and gender were examined, as well as the correlation between age, IQ, ASD symptoms and EF. Individuals with ASD showed impairments in all EF domains, but deficits were more pronounced in open-ended compared to structured settings. Group differences did not depend on gender and only occasionally on participants’ age. This suggests that inconsistencies between studies largely result from differences in task characteristics and less from differences in the investigated sample features. However, age and IQ strongly correlated with EF, indicating that group differences in these factors should be controlled for when studying EF. Finally, EF correlated with both social and non-social ASD symptoms, but further research is needed to clarify the nature of this relationship.
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Notes
Miyake and Friedman [8] suggested that inhibition is a common component in all EF tasks. Therefore, if one EF measure correlated with an inhibition variable (and group differences were found on both measures), we included the inhibition variable as a covariate in the group analyses of that EF measure, but not vice versa.
Since ADHD is the psychiatric disorder that most often co-occurs with ASD and is the co-occurring disorder that is most linked with EF, we focused on the possible influence of this disorder. The ASD sample excluding individuals with a co-occurring ADHD diagnosis was still matched with the TD sample for age (p = 0.96), PIQ (p = 0.76), TIQ (p = 0.16) and gender-ratio (p = 0.62), but not for VIQ (p = 0.02), as was the case for the full ASD sample (n = 50).
No correlations were found with laboratory main EF variables (that measure a different EF domain), suggesting that there are no confounding EF measures that should be controlled for (see Table 2 in Online Resource 1).
Although we did demonstrate that significant group differences on the main EF measures remained after excluding the individuals with ASD and co-occurring ADHD.
References
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, Arlington
Happé F, Ronald A (2008) The fractionable autism triad: a review of evidence from behavioural, genetic, cognitive and neural research. Neuropsychol Rev 18:287–304
Hill EL (2004) Evaluating the theory of executive dysfunction in autism. Dev Rev 24:189–233
Russell J (1997) Autism as an executive disorder. Oxford University Press, New York
Jurado MB, Rosselli M (2007) The elusive nature of executive functions: a review of our current understanding. Neuropsychol Rev 17:213–233
Goldstein S, Naglieri JA, Princiotta D, Otero TM (2014) Introduction: a history of executive functioning as a theoretical and clinical construct. In: Goldstein S, Naglieri JA (eds) Handbook of executive functioning. Springer, New York, pp 1–12
Denckla MB (1996) A theory and model of executive function: a neuropsychological perspective. In: Lyon GR, Krasnegor NA (eds) Attention, memory, and executive function. Paul H Brookes, Baltimore, pp 263–277
Miyake A, Friedman NP (2012) The nature and organization of individual differences in executive functions: four general conclusions. Curr Dir Psychol Sci 21:8–14
Pennington BF, Ozonoff S (1996) Executive functions and developmental psychopathology. J Child Psychol Psychiatry 37:51–87
Kenworthy L, Yerys BE, Anthony LG, Wallace GL (2008) Understanding executive control in autism spectrum disorders in the lab and in the real world. Neuropsychol Rev 18:320–338
Russo N, Flanagan T, Iarocci G, Berringerb D, Zelazod PD, Burack JA (2007) Deconstructing executive deficits among persons with autism: implications for cognitive neuroscience. Brain Cogn 65:77–86
Geurts HM, de Vries M, van den Bergh SFWM (2014) Executive functioning theory and autism. In: Goldstein S, Naglieri JA (eds) Handbook of executive functioning. Springer, New York, pp 121–141
Gioia GA, Isquith PK, Kenworthy L, Barton RM (2002) Profiles of everyday executive function in acquired and development disorders. Child Neuropsychol 8:121–137
White SJ (2013) The triple I hypothesis: taking another(‘s) perspective on executive dysfunction in autism. J Autism Dev Disord 43:114–121
White SJ, Burgess PW, Hill EL (2009) Impairments on open-ended executive function tests in autism. Autism Res 2:138–147
Arffa S (2007) The relationship of intelligence to executive function and non-executive function measures in a sample of average, above average, and gifted youth. Arch Clin Neuropsychol 22:969–978
Friedman NP, Miyake A, Corley RP, Young SE, DeFries JC, Hewitt JK (2006) Not all executive functions are related to intelligence. Psychol Sci 17:172–179
Best JR, Miller PH (2010) A developmental perspective on executive function. Child Dev 81:1641–1660
Best JR, Miller PH, Jones LL (2009) Executive functions after age 5: changes and correlates. Dev Rev 29:180–200
Mottron L (2004) Matching strategies in cognitive research with individuals with high-functioning autism: current practices, instrument biases, and recommendations. J Autism Dev Disord 34:19–27
Shaked M, Yirmiya N (2004) Matching procedures in autism research: evidence from meta-analytic studies. J Autism Dev Disord 34:35–40
Kirkovski M, Enticott PG, Fitzgerald PB (2013) A review of the role of female gender in autism spectrum disorders. J Autism Dev Disord 43:2584–2603
D’Cruz AM, Ragozzino ME, Mosconi MW et al (2013) Reduced behavioural flexibility in autism spectrum disorders. Neuropsychology 27:152–160
Lopez BR, Lincoln AJ, Ozonoff S, Lai Z (2005) Examining the relationship between executive functions and restricted, repetitive symptoms of autistic disorders. J Autism Dev Disord 35:445–460
Mosconi MW, Kay M, D’Cruz AM et al (2009) Impaired inhibitory control is associated with higher-order repetitive behaviors in autism spectrum disorders. Psychol Med 39:1559–1566
Reed P, Watts H, Truzoli R (2013) Flexibility in young people with autism spectrum disorders on a card sort task. Autism 17:162–171
Yerys BE, Wallace GL, Harrison B, Celano MJ, Giedd JN, Kenworthy LE (2009) Set-shifting in children with autism spectrum disorders: reversal shifting deficits on the intradimensional/extradimensional shift test correlate with repetitive behaviors. Autism 13:523–538
Turner M (1997) Towards an executive dysfunction account of repetitive behaviour in autism. In: Russell J (ed) Autism as an executive disorder. Oxford University Press, New York, pp 57–100
American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th edn text rev. American Psychiatric Association, Washington, DC
Skuse D, Warrington R, Bishop D, Chowdhury U, Lau J, Mandy W, Place M (2004) The developmental, dimensional and diagnostic interview (3di): a novel computerized assessment for autism spectrum disorders. J Am Acad Child Adolesc Psychiatry 43:548–558
Roeyers H, Thys M, Druart C, De Schryver M, Schittekatte M (2011) SRS: screeningslijst voor autismespectrumstoornissen, handleiding. Hogrefe Uitgevers, Amsterdam
Bodfish JW, Symons FJ, Parker DE, Lewis MH (2000) Varieties of repetitive behavior in autism. J Autism Dev Disord 30:237–243
Kort W, Schittekatte M, Dekker PH, Verhaeghe P, Compaan EL, Bosmans M, Vermeir G (2005) WISC-III-NL Wechsler intelligence scale for children-III: handleiding en verantwoording. Harcourt Assessment, London
Wechsler D (2005) WAIS-III-NL Wechsler adult intelligence test—III: afname en scoringshandleiding. Swets Test Publishers, Lisse
Sattler JM, Saklofske DH (2001) Interpreting the WISC-III. In: Sattler JM (ed) Assessment of children: cognitive applications, 4th edn. Jerome M Sattler, San Diego
Christ SE, Kester LE, Bodner KE, Miles JM (2011) Evidence for selective inhibitory impairment in individuals with autism spectrum disorder. Neuropsychology 25:690–701
Van Eylen L, Boets B, Steyaert J, Evers K, Wagemans J, Noens I (2011) Cognitive flexibility in autism spectrum disorder: explaining the inconsistencies? Res Autism Spectr Disord 5:1390–1401
Rubia K, Smith A, Taylor E (2007) Performance of children with attention deficit hyperactivity disorder (ADHD) on a test battery of impulsiveness. Child Neuropsychol 13:276–304
Bishop DVM, Norbury CF (2005) Executive functions in children with communication impairments, in relation to autistic symptomatology. Autism 9:7–25
Turner MA (1999) Generating novel ideas: fluency in high-functioning and learning disabled individuals with autism. J Child Psychol Psychiatry 40:189–201
Delis D, Kaplan E, Kramer J, Dutch adaptation, Noens I, van Berckelaer-Onnes I (2007) Design fluency test. Pearson, Amsterdam
Cognition Cambridge (1996) Cambridge neuropsychological test automated battery. Cambridge Cognition Limited, Cambridge
Wechsler D, Naglieri JA (2008) Wechsler non verbal-NL. Pearson Assessment and Information, Amsterdam
Delis D, Kaplan E, Kramer J, Dutch adaptation, Noens I, van Berckelaer-Onnes I (2007) Tower test. Pearson, Amsterdam
Smidts DP, Huizinga M (2009) BRIEF: Vragenlijst executieve functies voor 5- tot 18-jarigen. Hogrefe Uitgevers, Amsterdam
World Health Organization (1993) The ICD-10 classification of mental and behavioral disorders: diagnostic criteria for research. WHO, Geneva
Lord C, Rutter M, LeCouteur A (1994) Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 24:659–685
Constantino JN, Gruber CP (2005) Social responsiveness scale. Western Psychological Services, Los Angeles
Frazier TW, Youngstrom EA, Speer L, Embacher R, Law P, Constantino J, Findling RL, Hardan AY, Eng C (2012) Validation of proposed DSM-5 criteria for autism spectrum disorder. J Am Acad Child Adolesc Psychiatry 51:28–40
De la Marche W, Noens I, Boets B, Kuppens S, Steyaert J (in press) The underlying symptom structure of autism spectrum disorders: a factor analytic approach using the developmental, dimensional and diagnostic interview. Res Autism Spectr Disord. doi:10.1016/j.rasd.2014.11.002
Burnham KP, Anderson DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale
Geurts HM, van den Bergh SFWM, Ruzanno L (2014) Prepotent response inhibition and interference control in autism spectrum disorders: two meta-analyses. Autism Res 7:407–420
Schmitz N, Rubia K, Daly E, Smith A, Williams S, Murphy DG (2006) Neural correlates of executive function in autistic spectrum disorders. Biol Psychiatry 59:7–16
Geurts HM, Corbett B, Solomon M (2009) The paradox of cognitive flexibility in autism. Trends Cogn Sci 13:74–82
Leung RC, Zakzanis KK (2014) Brief report: cognitive flexibility in autism spectrum disorders: a quantitative review. J Autism Dev Disord 44:2628–2645
Dichter GS, Lam KS, Turner-Brown LM, Holtzclaw TN, Bodfish JW (2009) Generativity abilities predict communication deficits but not repetitive behaviors in autism spectrum disorders. J Autism Dev Disord 39:1298–1304
Low J, Goddard E, Melser J (2009) Generativity and imagination in autism spectrum disorder: evidence from individuals differences in children’s impossible entity drawings. Br J Dev Psychol 27:425–444
Lopez BR, Lincoln AJ, Ozonoff S, Lai Z (2005) Examining the relationship between executive functions and restricted, repetitive symptoms of autistic disorder. J Autism Dev Disord 35:445–460
Barendse EM, Hendriks MPH, Jansen JFA, Backes WH, Hofman PAM, Thoonen G, Kessels RPC, Aldenkamp AP (2013) Working memory deficits in high-functioning adolescents with autism spectrum disorders: neuropsychological and neuroimaging correlates. J Neurodev Disord 5:14–24
Gomot M, Wicker B (2012) A challenging, unpredictable world for people with autism spectrum disorder. Int J Psychophysiol 83:240–247
Van de Cruys S, Evers K, Van der Hallen R, Van Eylen L, Boets B, de-Wit L, Wagemans J (2014) Precise minds in uncertain worlds: predictive coding in autism. Psychol Rev 121:649–675
Dennis M, Francis DJ, Cirino PT, Schachar R, Barnes MA, Fletcher JM (2009) Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. J Int Neuropsychol Soc 15:331–343
Jarrold C, Brock J (2004) To match or not to match: methodological issues in autism-related research. J Autism Dev Disord 34:81–86
Lemon JM, Gargaro B, Enticott PG, Rinehart NJ (2011) Brief report: executive functioning in autism spectrum disorders: a gender comparison of response inhibition. J Autism Dev Disord 41:352–356
Lai MC, Lombardo MV, Ruigrok ANV, Chakrabarti B, Wheelwright SJ, Auyeung B et al (2012) Cognition in males and females with autism: similarities and differences. PLoS One 7:e47198
Dichter GS, Lam KSL, Turner-Brown LM, Holtzclaw TN, Bodfish JW (2009) Generativity abilities predict communication deficits but not repetitive behaviors in autism spectrum disorders. J Autism Dev Disord 39:1298–1304
Gilotty L, Kenworthy L, Sirian L, Black DO, Wagner AE (2002) Adaptive skills and executive function in autism spectrum disorder. Child Neurol 8:241–248
Kenworthy L, Black DO, Harrison B, della Rosa A, Wallace GL (2009) Are executive control functions related to autism symptoms in high-functioning children? Child Neurol 15:425–440
McEvoy RE, Rogers SJ, Pennington BF (1993) Executive function and social communication deficits in young autistic children. J Child Psychol Psychiatry 34:563–578
Brunsdon VEA, Happé F (2014) Exploring the ‘fractionation’ of autism at the cognitive level. Autism 18:17–30
Hill EL, Frith U (2003) Understanding autism: insights from mind and brain. Philos Trans R Soc Lond Series B 358:281–289
Johnson MH (2012) Executive function and developmental disorders: the flip side of the coin. Trends Cogn Sci 16:454–457
Dawson G, Meltzoff AN, Osterling J, Rinaldi J (1998) Neuropsychological correlates of early symptoms of autism. Child Dev 69:1276–1285
Dawson G, Munson J, Estes A et al (2002) Neurocognitive function and joint attention ability in young children with autism spectrum disorder versus developmental delay. Child Dev 73:345–358
Geurts HM, Vissers ME (2011) Eldery with autism: executive functions and memory. J Autism Dev Disord 42:665–675
Griffith EM, Pennington BF, Wehner EA, Rogers SJ (1999) Executive functions in young children with autism. Child Dev 70:817–832
Pellicano E (2007) Links between theory of mind and executive function in young children with autism: clues to developmental primacy. Dev Psychol 43:974–990
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. Dev Psychopathol 18:77–98
Smithson PE, Kenworthy L, Wills MC, Jarrett M, Atmore K, Yerys BE (2013) Real world executive control impairments in preschoolers with autism spectrum disorders. J Autism Dev Disord 43:1967–1975
McLean R, Harrison AJ, Zimak E, Joseph RM, Morrow EM (2014) Executive function in probands with autism with average IQ and their unaffected first-degree relatives. J Am Acad Child Adolesc Psychiatry 53:1001–1009
Yerys BE, Hepburn SL, Pennington BF, Rogers SJ (2007) Executive function in preschoolers with autism: evidence consistent with a secondary deficit. J Autism Dev Disord 37:1068–1079
Espy KA, Bull R, Kaiser H, Martin J, Banet M (2008) Methodological and conceptual issues in understanding the development of executive control in the preschool period. In: Anderson V, Jacobs R, Anderson PJ (eds) Executive functions and the frontal lobes: a lifespan perspective. Taylor & Francis Group, New York, pp 105–122
Wardill T, Anderson V (2008) Assessment of executive functioning in older adults. In: Anderson V, Jacobs R, Anderson PJ (eds) Executive functions and the frontal lobes: a lifespan perspective. Taylor & Francis Group, New York, pp 155–178
Towgood KJ, Meuwese JD, Gilbert SJ, Turner MS, Burgess PW (2009) Avantages of the multiple case series approach to the study of cognitive deficits in autism spectrum disorder. Neuropsychologia 47:2981–2988
Acknowledgments
L. Van Eylen is a doctoral and B. Boets a post-doctoral research fellow of the Research Foundation Flanders (FWO). Additionally, the research was funded by a fellowship from the Marguerite-Marie Delacroix to L. Van Eylen and a grant from the Research Council of KU Leuven (IDO/08/013). We thank all participants, and all master students as well as B. Machilsen, A. Verhappen and V. Stevens for assistance in data collection and scoring.
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Ethical Standards
The study protocol was approved by the Medical Ethical Committee of the University Hospitals Leuven and the Ethical Committee of the Faculty of Psychology and Educational Sciences of the KU Leuven and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.
Informed consent
Informed consent was obtained from the participants’ parents and from participants aged 16 years or older. The study protocol was approved by the Medical Ethical Committee of the University Hospitals Leuven and the Ethical Committee of the Faculty of Psychology and Educational Sciences of the KU Leuven.
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Van Eylen, L., Boets, B., Steyaert, J. et al. Executive functioning in autism spectrum disorders: influence of task and sample characteristics and relation to symptom severity. Eur Child Adolesc Psychiatry 24, 1399–1417 (2015). https://doi.org/10.1007/s00787-015-0689-1
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DOI: https://doi.org/10.1007/s00787-015-0689-1