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Article history:
Accepted 24 June 2009
Available online 22 July 2009
Keywords:
Autism
Asperger syndrome
Autistic spectrum disorder
Executive functions
Development
Children
Mental exibility
Planning
Inhibition
Generativity
a b s t r a c t
Executive dysfunction is a characteristic impairment of individuals with Autism Spectrum Disorders
(ASD). However whether such decits are related to autism per se, or to associated intellectual disability
is unclear. This paper examines executive functions in a group of children with ASD (N = 54, all IQP70) in
relation to a typically developing control group individually matched on the basis of age, gender, IQ and
vocabulary. Signicant impairments in the inhibition of prepotent responses (Stroop, Junior Hayling Test)
and planning (Tower of London) were reported for children with ASD, with preserved performance for
mental exibility (Wisconsin Card Sorting Task) and generativity (Verbal Fluency). Atypical age-related
patterns of performance were reported on tasks tapping response inhibition and self-monitoring for children with ASD compared to controls. The disparity between these and previous research ndings are discussed. A multidimensional notion of executive functions is proposed, with difculties in planning, the
inhibition of prepotent responses and self-monitoring reecting characteristic features of ASD that are
independent of IQ and verbal ability, and relatively stable across the childhood years.
2009 Elsevier Inc. All rights reserved.
1. Introduction
The concept of executive function refers to the higher order
control processes necessary to guide behaviour in a constantly
changing environment (Jurado & Rosselli, 2007). The concept includes abilities such as planning, working memory, mental exibility, response initiation, response inhibition, impulse control and
monitoring of action (Roberts, Robbins, & Weiskrantz, 1998; Stuss
& Knight, 2002). Behavioural and neuropsychological studies originally linked executive functions to the frontal lobes, in particular
the pre-frontal cortex (Baddeley & Wilson, 1988; Stuss & Benson,
1986). However, more recent neuroimaging studies have shown
that executive functions are associated with different regions of
the frontal lobes, with links between frontal and posterior areas,
as well as subcortical and thalamic pathways (Monchi, Petrides,
Strafella, Worsley, & Doyon, 2006; Stuss & Alexander, 2000; Stuss
et al., 2002).
Executive dysfunction has been linked to a number of developmental disorders, including Autism Spectrum Disorder (ASD) (see
Russell, 1997). Behavioural similarities between patients with
frontal lobe lesions and individuals with ASD led to the notion that
some of the everyday social and non-social behaviours seen in
individuals with ASD may reect specic executive dysfunction
(Ozonoff, Pennington, & Rogers, 1991). The behaviours proposed
* Corresponding author.
E-mail address: sally.robinson@kcl.ac.uk (S. Robinson).
0278-2626/$ - see front matter 2009 Elsevier Inc. All rights reserved.
doi:10. 1016/j.bandc.2009.06.007
363
364
Table 1
Participant characteristics: means (standard deviations).
Age (months)
FSIQ
BPVS (ss)
Male:female
ASD
(N = 54)
Means (SD)
TD
(N = 54)
Means (SD)
150.46 (33.55)
103.53 (10.54)
99.70 (18.80)
42:12
144.96 (28.03)
104.80 (9.07)
100.94 (17.51)
42:12
.92
.67
.36
.36
.51
.72
365
1600 ms, during which a xation cross was presented in the middle of the screen. There were eight practice trials, followed by 48
experimental trials with 50% congruence. Performance was scored
for the difference in RT between congruent and incongruent trials,
correct incongruent responses and correct incongruent RTs. The
computerised single trial version was administered as, in addition
to a potential reduction in social task demands, this task has been
reported to be more sensitive to inhibition difculties than standard card versions (Perlstein, Carter, Barch, & Baird, 1998).
3. Results
Table 2
Executive Function test performance.
ASD
TD
Means (SD)
Means (SD)
ANOVA
TD
99.04 (18.18)
98.93 (11.48)
102.30 (12.16)
7.53
29.26
5.30
<.01*
<.001*
.02
.001
.15
.14
.47
.28
.32
.16
.36
.06
.24
<.01*
.68
104.26 (16.95)
108.11 (21.92)
107.56 (17.71)
116.24 (20.81)
1.01
3.91
.31
.05
.19
.25
.16
.07
.38
.31
<.01*
.02
Stroop
Incongruent trials
Incongruent RT
RT difference
22.04 (4.09)
1.21 (.38)
.16 (.19)
23.61 (.83)
1.06 (.28)
.11 (.14)
7.67
5.53
2.38
<.01*
.02
.13
.28
.40
.05
.04
<.01*
.71
.44
.28
.02
.001*
.04
.89
9.13 (1.10)
1.02 (.80)
5.41 (5.50)
3.13 (2.00)
.63 (1.55)
3.41 (1.91)
50.00
9.50 (.82)
.80 (.54)
3.41 (3.50)
2.33 (1.51)
.15 (.63)
2.94 (2.46)
70.37
3.94
2.68
5.07
5.56
4.50
1.19
4.68
.05
.11
.03
.02
.04
.28
.03
.39
.35
.13
.15
.15
.09
<.01*
<.01*
.36
.28
.27
.54
.26
.24
.13
.08
.19
-.03
.06
.08
.37
.58
.17
.86
Verbal Fluency
Total
Perseverations
48.33 (16.29)
1.31 (2.02)
49.81 (10.68)
.52 (.82)
.32
7.21
.57
<.01*
.54
.03
<0.001*
.86
.51
.27
<.001*
.04
ToL
Move score
Rule violations
Time violations
88.74 (20.74)
81.76 (20.30)
95.22 (19.02)
WCST
Total errors
Perseverative errors
366
4. Discussion
The current study aimed to address previous methodological limitations to investigate the nature of executive functions in children
with ASD compared to stringently matched TD peers. To exclude
the possible impact of intellectual disability on executive dysfunction, only children with IQs in the normal range were included.
On the WCST, performance did not differ signicantly between
ASD and TD groups; however, children with ASD tended to make
more perseverative responses. This was consistent with their performance on the VF paradigm, where despite generating a normal
number of items they produced signicantly more perseverative
responses than controls. Children with ASD were also signicantly
poorer than controls at inhibiting incongruent items on the Stroop
and consistently poorer on the inhibition section of the Junior Hayling. Impaired performance was also reported on the ToL, with a
signicant increase in moves and rule violations for children with
ASD compared to controls. Thus, compared to TD peers, children
with ASD exhibited a specic pattern of performance across a
range of executive measures. How do these research ndings compare with or add to previous research in this area?
Preserved performance on the WCST is consistent with previous
studies that have reported normal mental exibility for children
with ASD of average intelligence (Ozonoff, 1995; Rumsey, 1985)
or who were matched to controls on the basis of verbal functioning
(Liss et al., 2001). Nevertheless, children with ASD did tend to generate more perseverative errors than controls. This suggests that
although children with ASD were able to shift sets as accurately
as controls, their ability to self-monitor performance by utilising
feedback to inhibit prepotent responding was poorer.
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368
Broki, K. C., & Bohlin, G. (2004). Executive functions in children aged 613: A
dimensional and developmental study. Developmental Neuropsychology, 26,
571593.
Burgess, P. W., & Shallice, T. (1997). The Hayling and Brixton tests. Bury, St. Edmonds:
Thames Valley Test Company.
Cambridge Cognition (1996). Cambridge Neuropsychological Test Automated Battery.
Chandler, S., Charman, T., Bairs, G., Siminoff, E., Loucas, T., Meldrum, D., et al. (2007).
Validation of the Social Communication Questionnaire in a population cohort of
children with Autism Spectrum Disorder. Journal of the American Academy of
Child and Adolescent Psychiatry, 46, 13241332.
Culbertson, W. C., & Zillmer, E. A. (2005). Tower of LondonDX (2nd ed.). Florida:
Psychological Assessment Resources.
Dunn, L. M., Dunn, L. M., Whetton, C., & Burley, J. (1997). British picture vocabulary
scale (2nd ed.). NFER-Nelson.
Frith, U. (1989). Autism: Explaining the enigma. Oxford: Blackwell.
Frith, U. (2003). Autism: Explaining the enigma (2nd ed.). Oxford: Blackwell.
Geurts, H. M., Verte, S., Oosterlann, J., Roeyers, H., & Sergeant, J. A. (2004). How
specic are executive functioning decits in attention decit hyperactivity
disorder and autism? Journal of Child Psychology and Psychiatry Allied Disciplines,
45, 836854.
Happ, F. (1994). Wechsler IQ prole and theory of mind in autism: Research note.
Journal of Child Psychology and Psychiatry and Allied Disciplines, 35, 1461
1467.
Happ, F., Booth, R., Charlton, R., & Hughes, C. (2006). Executive function
decits in autism spectrum disorders and attention-decit/hyperactivity
disorder: Examining proles across domains and ages. Brain and Cognition,
61, 2539.
Heaton, R. K. (2003). WCST-64: Computerised Version 2 Research Edition. Florida:
Psychological Assessment Resources.
Hill, E. L. (2004). Evaluating the theory of executive dysfunction in autism.
Developmental Review, 24, 189233.
Hill, E. L., & Bird, C. M. (2006). Executive processes in Asperger syndrome: Patterns
of performance in multiple case series. Neuropsychologia, 44, 28222835.
Hill, E., & Russell, J. (2002). Action memory and self monitoring in children with
autism: Self versus other. Infant and Child Development, 11(2), 159170.
Hughes, C. (1996). Brief report: Planning problems in autism at the level of motor
control. Journal of Autism and Developmental Disorders, 26, 99107.
Hughes, C., & Russell, J. (1993). Autistic childrens difculty with mental
disengagement from an object Its implications for theories of autism.
Developmental Psychology, 29(3), 498510.
Hughes, C., Russell, J., & Robbins, T. W. (1994). Evidence for executive dysfunction in
children with autism. Psychological Medicine, 32, 209220.
Huizinga, M., Dolan, C. V., & van der Molen, Maurits W. (2006). Age-related change
in executive function: Developmental trends and a latent variable analysis.
Neuropsychologia, 44, 20172036.
Jurado, M. B., & Rosselli, M. (2007). The elusive nature of executive functions: A
review of our current understanding. Neuropsychological Review, 17, 213233.
Lee, L.-C., David, A. B., Rusyniak, J., Landa, R., & Newschaffer, C. J. (2007).
Performance of the Social Communication Questionnaire in children receiving
preschool special educational services. Research in Autism Spectrum Disorders, 1,
126138.
Liss, M., Harel, B., Fein, D., Allen, D., Dunn, M., Feinstein, C., et al. (2001). Predictors
and correlates of adaptive functioning in children with developmental
disorders. Journal of Autism and Developmental Disorders, 32, 219230.
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, 659685.
Mari, M., Castiello, U., Marks, D., Marraffa, C., & Prior, M. (2003). The reach-to-grasp
movement in children with autism spectrum disorder. Philosophical
Transactions of the Royal Society of London Series B Biological Science,
358(1430), 393403.
Milner, B. (1965). Visually-guided maze learning in man: Effects of bilateral
hippocampal, bilateral frontal, and unilateral cerebral lesions. Neuropsychologia,
3, 317338.
Minshew, N. J., Goldstein, G., Muenz, L. R., & Payton, J. (1992). Neuropsychological
functioning in nonmentally retarded autistic individuals. Journal of Clinical and
Experimental Neuropsychology, 14, 749761.
Monchi, O., Petrides, M., Strafella, A. P., Worsley, K. J., & Doyon, J. (2006). Functional
role of the basal ganglia in the planning and execution of actions. Annals of
Neurology, 59, 257264.
Ozonoff, S. (1995). Reliability and validity of the Wisconsin Card Sorting Test in
studies of autism. Neuropsychology, 9, 491500.
Ozonoff, S., Cook, I., Coon, H., Dawson, G., Joseph, R. M., Kiln, A., et al. (2004).
Performance on Cambridge neuropsychological Test Automated Battery
subtests sensitive to frontal lobe function in people with autistic disorder:
Evidence from the Collaborative Programs of Excellence in Autism Network.
Journal of Autism and Developmental Disorders, 34, 139150.
Ozonoff, S., & Jensen, J. (1999). Brief report: Specic executive function proles in
three neurodevelopmental disorders. Journal of Autism and Developmental
Disorders, 29, 171177.
Ozonoff, S., & McEvoy, R. E. (1994). A longitudinal study of executive function and
theory of mind development in autism. Development and Psychopathology, 6,
415431.
Ozonoff, S., Pennington, B. F., & Rogers, S. J. (1991). Executive function decits in
high-functioning autistic individuals: Relationship to theory of mind. Journal of
Child Psychology and Psychiatry, 32, 10811105.
Ozonoff, S., & Strayer, D. L. (1997). Further evidence of intact working memory in
autism. Journal of Autism and Developmental Disorders, 31, 257263.
Ozonoff, S., Strayer, D. L., McMahon, W. M., & Filloux, F. (1994). Inhibitory decits in
Tourettes syndrome: A function of comorbidity and symptom severity. Journal
of Clinical Psychiatry, 39, 11091118.
Perlstein, W., Carter, C., Barch, D., & Baird, J. (1998). The stroop task and attention
decits in Schizophrenia: A critical evaluation of card and single-trial stroop
methodologies. Neuropsychology, 12, 414425.
Prior, M., & Hoffman, W. (1990). Brief report: Neuropsychological testing of autistic
children through an exploration with frontal lobe tests. Journal of Autism and
Developmental Disorders, 20, 581590.
Psychological Corporation (1999). Wechsler abbreviated scale of intelligence. San
Anotnia, TX: Psychological Corporation.
Rajendran, G., & Mitchell, P. (2007). Cognitive theories of autism. Developmental
Review, 27, 224260.
Roberts, A. C., Robbins, T. W., & Weiskrantz, L. (1998). The prefrontal cortex. Executive
and cognitive functions. Oxford: Oxford University Press.
Rumsey, J. M. (1985). Conceptual problem-solving in highly verbal, nonretarded
autistic men. Journal of Autism and Developmental Disorders, 15, 2336.
Rumsey, J. M., & Hamburger, S. D. (1988). Neuropsychological ndings in highfunctioning autistic men with infantile autism, residual state. Journal of Clinical
and Experimental Neuropsychology, 10, 201221.
Russell, J. (1997). How executive disorders can bring about adequate theory of
mind. In J. Russell (Ed.), Autism as an executive disorder (pp. 256304). Oxford:
Oxford University Press.
Russell, J., Hala, S., & Hill, E. (2003). The automated windows task: The performance
of preschool children, children with autism, and children with moderate
learning difculties. Cognitive Development, 18(1), 111137.
Russell, J., & Hill, E. L. (2001). Action-monitoring and intention reporting in children
with autism. Journal of Child Psychology and Psychiatry, 42, 317328.
Russell, J., & Jarrold, C. (1998). Errorcorrection problems in autism evidence for a
monitoring impairment? Journal of Autism and Developmental Disorders, 28(3),
177188.
Russell, J., & Jarrold, C. (1999). Memory for actions in children with autism: Self
versus other. Cognitive Neuropsychiatry, 4, 303331.
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, 103112.
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, 331349.
Rutter, M., Bailey, A., & Lord, C. (2003). Social Communication Questionnaire (SCQ).
Test Agency.
Schmitz, N., Rubia, K., Daly, E., Smith, A., Williams, S., & Murphy, D. G. M. (2005).
Neural correlates of executive function in autistic spectrum disorders. Biological
Psychiatry, 59(1), 716.
Scott, F., & Baron-Cohen, S. (1996). Imagining real and unreal things: Evidence of a
dissociation in autism. Journal of Cognitive Neuroscience, 8, 371382.
Shallice, T., Marzocchi, G. M., Coser, S., Savio, M. D., Meuter, F. R., & Rumiati, R. I.
(2002). Executive function prole of children with Attention Decit
Hyperactivity Disorder. Developmental Neuropsychology, 21, 4371.
Stroop, J. R. (1935). Studies of interference in serial verbal reactions. Journal of
experimental Psychology, 18, 643662.
Stuss, D. T., & Alexander, M. P. (2000). Executive functions and the frontal lobes: A
conceptual view. Psychological Research, 63, 289298.
Stuss, D. T., Alexander, M. P., Floden, D., Binns, M. A., Levine, B., McIntosh, A. R., et al.
(2002). Fractionation and localization of distinct frontal lobe processes:
Evidence from focal lesions in humans. In D. T. Stuss & R. T. Knight (Eds.),
Principles of frontal lobe function (pp. 392407). New York: Oxford University
Press.
Stuss, D. T., & Benson, D. F. (1986). The frontal lobes. New York: Raven.
Stuss, D. T., & Knight, R. T. (2002). Principles of frontal lobe function. Oxford: Oxford
University Press.
Turner, M. (1997). Towards an executive dysfunction account of repetitive
behaviour in autism. In J. Russell (Ed.), Autism as an executive disorder
(pp. 57100). Oxford: Oxford University Press.
Turner, M. (1999). Generating novel ideas: Fluency performance in highfunctioning and learning disabled individuals with autism. Journal of Child
Psychology and Psychiatry, 40, 189201.
Welsh, M. C., Pennington, B. F., & Grossier, D. B. (1991). A normative developmental
study of executive function: A window on prefrontal function in children.
Developmental Neuropsychology, 7, 131149.
Williams, B. R., Ponese, J. S., Schachar, R. J., Logan, G. D., & Tannock, R. (1999).
Development of inhibitory control across the life span. Developmental
Psychology, 35, 205213.