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J Autism Dev Disord (2013) 43:10651079

DOI 10.1007/s10803-012-1650-5

ORIGINAL PAPER

The Specificity of Inhibitory Impairments in Autism


and Their Relation to ADHD-Type Symptoms
Charlotte Sanderson Melissa L. Allen

Published online: 9 October 2012


Springer Science+Business Media, LLC 2012

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 nonverbal 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.
Keywords Autism  Inhibition  ADHD 
Executive function

Introduction
A dominant cognitive theory of autism links the social and
non-social features of the disorder to deficits in executive

C. Sanderson  M. L. Allen
Department of Psychology, Lancaster University,
Lancashire, UK
Present Address:
C. Sanderson (&)
Behavioural and Brain Sciences Unit, University College
London (UCL) Institute of Child Health, 30 Guilford Street,
London WC1N 1EH, UK
e-mail: charlotte.sanderson107@gmail.com;
charlotte.sanderson.10@ucl.live.ac.uk

function (EF) (Hill 2004a; Russell 1997). This umbrella


term refers to a range of higher-order cognitive abilities
that together permit an individual to plan and carry out
non-automatic, flexible and goal-directed actions (Welsh
and Pennington 1988). However, executive impairments
have been linked to various developmental disorders,
including attention-deficit/hyperactivity disorder (ADHD)
(Ozonoff and Jensen 1999) and Tourette syndrome
(Leckman et al. 1987). It is thus difficult for an executive
account, in its simplest form, to explain the differential
clinical outcomes in each disorder (Pennington 1997).
Some have argued that autism may thus be distinguishable by a unique executive profile or pattern of strength and
weakness across various subcomponents of EF (e.g. working
memory, planning, inhibitory control) (Pennington 1997;
Happe et al. 2006; Hill 2004a). A specific suggestion is that
inhibitory control may be intact in children with autism
(CWA), which would in particular help to discriminate the
disorder from ADHDwhere inhibition is often considered
a core cognitive deficit (e.g. Happe et al. 2006; Sinzig et al.
2008; Bramham et al. 2009; Lijffijt et al. 2005). However,
the evidence for intact inhibitory control in autism remains
equivocal (Christ et al. 2007; Adams and Jarrold 2009; Hill
2004a, b). Though many studies have failed to identify any
deficit relative to controls, a notable number have reported
impairments in CWA on both verbal and non-verbal inhibition tasks (see Table 1).
Inhibitory Control
Inhibitory control is defined as the ability to suppress
information or a response that may interfere with the
attainment of a cognitive or behavioural goal (Nigg 2000;
Dagenbach and Carr 1994). However, like EF, it is arguably not a unitary construct (e.g. Friedman and Miyake

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Autism
Autism

HFA/AS

HFA
Autism
Autism
HFA
Autism/PDD-NOS

Autism
Autism

Study 2

Lemon et al. (2011)

Minshew et al. (1999)

Noterdaeme et al. (2001)

Ozonoff and Jensen (1999)

Ozonoff and Strayer (1997)

Ozonoff et al. (1994)

Russell et al. (1991)

Russell et al. (1999)

HFA

Study 1

Hughes and Russell (1993)

Henderson et al. (2006)

HFA

Happe et al. (2006)


AS

HFA
HFA

Geurts et al. (2004)

Autism

Eskes et al. (1990)

Goldberg et al. (2005)

Autism/AS/PDD

Christ et al. (2007)

TD/MLD

Down Syndrome

TD

Tourette syndrome

TD

TD

TD

TD

TD

MLD/TD

MLD

TD

TD

TD

TD

TD

TD/ASD siblings

TD

TD/MLD

Autism
HFA

Biro and Russell (2001)

Bishop and Norbury (2005)

TD/MLD

Autism/AS/PDD-NOS

Ames and Jarrold (2007)

TD

Comparisons

Autism

ASD

Sample characteristics

Adams and Jarrold (2009)

Study

VMA

Word Reading (BAS)

CA/Gender/VIQ/PIQ/FSIQ

CA/Gender/VIQ/PIQ/FSIQ

CA (FIQ used as Covariate).

CA/PIQ

CA/IQ (Ammons)

CA/FIQ

VMA

VMA

CA/MA

CA/IQ (FSIQ, PIQ, VIQ)

CA

CA

Reading Speed

Statistically controlled for IQ (WASI) & CA

NVMA

VMA

VMA/NVMA (BPVS/RCPM)

NVMA (RCPM)/Word Reading (BAS)

Matching criteria

Yes

Flanker Task

No

Day/Night Stroop

No

Yes

Yes
Windows task

No
Prepotent response set

No
Neutral response set

Go/No-Go

Stop-task

No

No

Go/No-Go
Colour-word Stroop

Yes

Directional conflict task

Yes

No

Male Participants
Anti-Saccade Task

Yes

Female Participants

Stop-task

Yes
Knob

Yes

No

Detour Reaching Task


Switch

Windows Task

Flanker

No

Circle Drawing Task


Go/No-Go

Yes
Yes

Change Task

No
No

Opposite Worlds

Colour-word Stroop

No

No

Colour-word Stroop

No

Colour-word Stroop

Yes
Yes

Yes

Yes

Go/No-Go

Opposite-Worlds
Walk-Dont Walk

Detour Reaching Task

Dog-Pig Stroop (Card-version)

No
No

Colour-word Stroop

ASD impaired?

Chimeric Animal Stroop

Inhibitory control task

Table 1 Summary of previous findings on inhibitory ability in children with autism and typically developing (TD) and/or moderate learning difficulty (MD) controls

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J Autism Dev Disord (2013) 43:10651079

N.B. In some studies listed, additional clinical groups and/or other executive tasks (not detailed here) were included. FSIQ Full-scale IQ, VIQ verbal IQ, PIQ performance IQ, VMA verbal
mental age, NVMA non-verbal mental age, CA chronological age, WASI Wechsler Abbreviated Scale of Intelligence, BPVS British Picture Vocabulary Scale, RCPM Ravens coloured
progressive matrices, BAS British Ability Scales

No
Go/No-Go
CA/IQ corrected z-scores
HFA/AS
Sinzig et al. (2008)

TD

No

Yes
Automated Windows Task

Classic (colour-word) Stroop


CA/FIQ

VMA (BPVS)
TD/MLD
Autism

AS

Russell et al. (2003)

Semrud-Clikeman et al. (2010)

Comparisons
ASD

Matching criteria

Inhibitory control task


Sample characteristics
Study

Table 1 continued

TD

ASD impaired?

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2004), and there may be fundamental distinctions between


different tasks in terms of the cognitive processes they
draw upon. It may thus be that some types of inhibition
task are more problematic for CWA than others, which
could fuel inconsistency between studies. In this study,
three types of inhibitory paradigm that have been used are
considered, which we refer to as delay, conflict and resistance to distractor inhibition.
Delay paradigms require children to delay, temper, or
altogether suppress an impulsive response when a task calls
for it (Carlson and Moses 2001, p. 103). Examples
include the Go/No-Go task (e.g. Christ et al. 2007; Happe
et al. 2006; Noterdaeme et al. 2001; Ozonoff et al. 1994;
and Sinzig et al. 2008), the stop-Signal task (Ozonoff and
Strayer 1997; Lemon et al. 2011) and the TEA-Ch WalkDont Walk subtest (Manly et al. 1999). In the widely used
Go/No-Go task, participants are typically presented with a
sequence of visual stimuli (e.g. shapes or letters), and they
must make a speeded motor response to the majority of
stimuli (Go) but withhold responding to one or more
pre-specified shapes/letters. These No-Go stimuli appear
only on a minority (e.g. 25 %) of trials, thus generating a
prepotent response tendency. Inhibitory performance is
gauged by the number of false positive responses made.
The core cognitive process in these tasks is the active
suppression of a habitual response, and thus they are often
construed as simple tests of the supervisory attentional
system (SAS) (Norman and Shallice 1986). Indeed, performance declines with concurrent cognitive load (e.g.
Mitchell et al. 2002) and with age (e.g. Butler et al. 1999)
indicating a limited-capacity executive process. Neuroimaging points towards widespread activation across the
frontal cortex with delay inhibition, particularly in right
inferior (ventrolateral) regions (Aron and Poldrack 2005),
and patients with right inferior frontal damage show disrupted performance (Aron et al. 2003).
Conflict inhibition paradigms share functional similarities with delay tasks, in that they too test individuals
ability to hold in mind task rules/goals and actively suppress prepotent responses (Carlson and Moses 2001).
However, importantly, conflict tasks also require participants to replace that suppressed response with an opposing
onewhich may explain why the two task-types load onto
distinct factors in factor analysis (Carlson and Moses
2001). The classic conflict task is the colour-word Stroop
task (Stroop 1935). In this, participants are shown colourwords printed in different coloured ink (e.g. BLUE printed
in red ink) and are asked to name the ink-colour instead of
the written word. Yet, although widely used, it is thought
that this task may systematically overestimate inhibitory
abilities in ASD populations (Adams and Jarrold 2009).
This is because as the to-be-inhibited information is the
semantic meaning of written words (MacLeod 1991)and

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Table 2 Participant background/matching measures


Autism group (N = 31)

TD group (N = 28)

SD

F value

p value

Effect-size (g2p)

SD

32.60

5.97

15.66

1.12

218.22***

\0.001

0.793

164.03

24.80

106.71

16.24

117.56***

\0.001

0.673

BPVS age (months; max. 160)

91.87

20.36

93.79

12.38

0.186

0.668

0.003

Ravens CPM score (max. 36)

28.10a

4.98

29.46a

3.89

1.362

0.248

0.023

Inattentiveness (VADTRS total score)

14.29

4.89

2.86

3.62

102.463*** \0.001

0.643

Hyperactivity/Impulsivity (VADTRS total score)

11.26

5.92

2.29

3.91

46.123*** \0.001

0.447

CARS autism rating


CA (months)

* p \ 0.05; ** p \ 0.01, *** p \ 0.001


a

Ravens CPM score of 2830 is equivalent to a standardised score (UK) of 9.510 years (Raven et al. 1990)

CWA appear to access the semantic meaning of written


words less automatically (Nation 2006).
Other conflict inhibition tasks avoid this confound
however, and are thus more suitable for ASD samplesfor
instance, the Windows (Russell et al. 1991), detour
reaching (Russell et al. 1999), TEA-Ch Opposite World
(Manly, et al. 1999), Day/Night (Gerstadt et al. 1994) and
Dog/Pig Stroop (Ames and Jarrold 2007) tasks. Like the
colour-word Stroop, each of these requires the suppression
of a prepotent response and the replacement of that
response with a conflicting and less salient one. This
additional process undoubtedly augments both working
memory and conflict resolution demands, which may
explain why conflict tasks better predict working memory
(and Theory of Mind) ability than delay tasks (Carlson and
Moses 2001; Carlson et al. 2002, 2004; Hala et al. 2003).
Nonetheless, the executive processes involved are still
thought to be largely frontal lobe mediated, with lateral
prefrontal lesions again known to be detrimental to task
accuracy (Vendrell et al. 1995; Perret 1974).
Resistance to distractor paradigms require participants to
select targets presented alongside irrelevant distractors, or
more broadly, resist interference from information in the
external environment that is irrelevant to the task (Friedman and Miyake 2004, p. 104). One such task is the computerised Eriksen flanker task (Eriksen and Eriksen 1974).
Here, participants identify a target (e.g. letter/shape/arrow)
that is presented either on its own, or flanked by responseincompatible stimuli. Performance is thought to be associated with the ability to actively suppress distracting information (e.g. Tipper 1985) and/or capacities for focussed and
selective attention. These tasks arguably therefore involve
earlier (i.e. perceptual) stages of information processing and
preattentive sensory gating. But again, aging (Earles et al.
1997) and frontal lesions (Stuss et al. 1999) are both detrimental to performance, indicating the recruitment of
domain-general executive processes. Neuroimaging studies
suggest particularly important roles for the dorsolateral PFC,
ventrolateral PFC and ACC (Wager and Smith 2003).

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Inhibitory Control in Autism


Existing research indicates that some inhibition task-types
might be more problematic for CWA than others (Christ
et al. 2007). For delay inhibition, the majority of evidence
has come from the Go/No-Go task, and these have typically
found no evidence of impairment. Indeed, the one study
that did report impaired Go/No-Go performance (Ozonoff
et al. 1994) has since been contested due to a set-shifting
confound. Corroborating findings from the Go/No-Go,
Ozonoff and Strayer (1997) found equivalent error-rates
and stop-signal reaction times (SSRTs) in CWA and TD
controls on the Stop-task. Although another study (Lemon
et al. 2011) did find significantly slower SSRTs in CWA
(females only), mean full-scale IQ was considerably lower
than that of the controls, probably only failing to reach
significance due to low power. Yerys et al. (2009) found no
evidence of impairment amongst CWA on the TEA-Ch
Walk-Dont Walk task. Together these indicate that simple
delay tasks of behavioural inhibition are not problematic
for CWA.
Regarding conflict inhibition, the most dominant task in
ASD research has been the classic colour-word Stroopand
these typically suggest no evidence of impairment (e.g.
Ozonoff and Jensen 1999). However, due to the earlier
discussed confound, findings using this particular paradigm
should be interpreted with caution in CWA. This is particularly true given the less favourable picture painted by other
conflict paradigms. Russell and colleagues (1991; Hughes
and Russell 1993) reported that CWA persistently failed on
both the Windows and Detour reaching tasks, making more
errors than TD/MLD children of matched verbal mental age.
Similarly, CWA have been shown to make more inhibitory
errors than controls on the Opposite World task (Bishop and
Norbury 2005) and the Dog/Pig Stroop task (Ames and
Jarrold 2007). Russell et al. (1999) found no evidence of
impairment on the Day/Night task, despite structural similarities to the Dog/Pig Stroopbut this study notably only
matched groups on non-verbal mental age (Jarrold and

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Brock 2004). This can leave CWA at a disadvantage, as


verbal ability is often poorer than non-verbal ability in this
population (Joseph et al. 2002).
Finally, findings on resistance to distractor inhibition have
been both scarce and inconsistent. Whereas one study
reported clear inhibitory impairments in CWA (Christ et al.
2007), two others found no such evidence (Dichter and
Belger 2007; Henderson et al. 2006). This again may relate to
a non-inhibitory confound. The flanker task in Christ et al.
required children to maintain online numerous arbitrary
response mappings, which arguably augments working
memory demands compared to the simpler designs used
elsewhere (i.e. arrows flanker tasks). Nonetheless, it is
notable that both Dichter and Belger (2007) and Henderson
et al. (2006) used adult samples. It is therefore conceivable
that delays in resistance to distraction development are
observable amongst CWA, but that typical functioning is
reached by adulthood. No study has implemented a simple,
arrows flanker task with a child ASD sample to address this
possibility.
Overall, existing research suggests that conflict tasks of
inhibition may be most problematic for CWA, perhaps
owing to greater working memory and conflict demands
although evidence on resistance to distractor evidence is
limited and difficult to decipher. However, without
administering all three paradigm types to the same sample
of CWA, it is hard to rule out the possibility that disparate
findings are cohort, rather than task related (Christ et al.
2007)especially given the known heterogeneity in the
autism population. Therefore the first aim of this study was
to administer three different tasks to CWA and a control
group matched for verbal and non-verbal mental age: one
delay, one conflict, and one resistance to distractor. These
tasks, respectively, were a Go/No-Go task, the Dog/Pig
Stroop task and an arrows Flanker task. These are all well
established in the inhibitory literature, have been applied
successfully in ASD research and avoid various known
confounds. We expected that impairment was most likely
to emerge on the Dog-Pig Stroop (conflict) task.
ASD, Inhibitory Control and the Role of ADHD-Type
Symptoms
A further aim of our investigation was to address a potentially important source of heterogeneity in inhibitory ability
in this population. At least 30 % of CWA meet diagnostic
criteria for ADHD, and many more show elevated symptoms
of inattention and hyperactivity (Leyfer et al. 2006; see also
Sinzig et al. 2009). Associations between autism and
attentional disorders have been suggested at a genetic (e.g.
Rommelse et al. 2010), functional (e.g. Brieber et al. 2007)
and behavioural level (Sinzig et al. 2008). This overlap is of
particular relevance to studies of inhibition in autism

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because inhibitory control is often considered the core deficit in ADHD, with children with the disorder almost
invariably exhibiting broad-ranging inhibitory impairments
(Barkley 1997; Nigg 2001; Aron and Poldrack 2005; Willcutt et al. 2005). Given symptomatic overlaps, it may be that
covarying ADHD-type symptoms are more important predictors of inhibitory ability in CWA than core autistic
symptoms themselves. Indeed, ADHD-type symptoms may
be a significant driver of group differences (Castellanos and
Tannock 2002).
In high-functioning groups, the presence and severity of
both inattentive and hyperactive traits have already been
shown to predict performance on a Go/No-Go task (Sinzig
et al. 2008) and change task (a conflict variant of the
Stop-task) (Verte et al. 2006). Notably, in both studies this
was despite overall group differences between CWA and
TD controls failing to reach significance. Bishop and
Norbury (2005) also found symptoms of inattention and
hyperactivity/impulsivity to be moderately predictive of
inhibitory impairment on the Opposite World and Walk/
Dont Walk tasks in CWA (high-functioning), pragmatic
language impairment (PLI) and specific language impairment (SLI). It appears therefore that ADHD symptompresence may be an important predictor of individual differences in inhibitory ability amongst CWA.
Thus, for each child taking part, an objective measure of
inattention and hyperactivity/impulsivity was obtained to
gauge the importance of ADHD-type symptoms in any
observed group differences. The Vanderbilt ADHD Diagnostic Teacher Rating Scale (VADTRS; Wolraich et al.
1998) was used as it provides separate estimates for
symptoms of inattention and hyperactivity/impulsivity
based upon DSM-IV (American Psychiatric Association
[APA] 1994) criteria. Given that associations between both
inattention (e.g. Bishop and Norbury 2005) and overactivity (e.g. Ames and White 2010; Verte et al. 2006) and
inhibitory performance in CWA have been reported across
various inhibition tasks, we expected that both ADHDsymptom types might predict inhibitory deficits, and no
task specific predictions were made.
Together, the two overarching predictions of this
research have various implications for our understanding of
inhibition in autism. First, uneven patterns of performance
across different tasks would help to explain a record of
inconsistency in the field. Impairment on the Dog/Pig
Stroop only would suggest that inhibitory control is not a
core or pervasive deficit in CWA, but also that generalist
claims of intact inhibition are misguided. Crucially, this
notion would help to differentiate the executive profile of
autism from that of other developmental disorders with
known executive dysfunction (particularly ADHD). Second, if symptoms of inattention and/or hyperactivity help
predict which children demonstrate inhibitory difficulties,

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it would highlight the importance of considering overlapping symptoms between developmental disorders.

Method
Participants
Written informed consent was obtained from a parent/
guardian of all children taking part. Children also provided
verbal consent prior to commencing sessions.

J Autism Dev Disord (2013) 43:10651079

Procedure and Task Design(s)


Participants were tested individually in a well-lit, quiet, and
distraction-free room. Each completed the three inhibitory
control tasks (Go/No-Go; Dog-Pig Stroop; Flanker) and
two standardised measures (RCPM; BPVS) in counterbalanced order. Sessions lasted 4060 min. Inhibition tasks
were written in Psyscript, and run on a computer using an
OS X 10.6 operating system.
Go/No-Go Task

ASD Group

Task Design

All CWA who participated were enrolled in a specialist


school for autism and had formal diagnoses of an ASD made
by a qualified clinical or educational psychologist using
DSM criteria (e.g. ADOS/ADI). A teacher/teaching assistant completed the Childhood Autism Rating Scale (CARS)
to confirm that clear ASD symptomatology was still present.
The CARS was selected as it provides a cut-off for symptom
severity. Thirty-one participants (5 female, 26 male) with
CARS scores of \27 points (Mesibov et al. 1989) and who
completed all tasks successfully were included in the final
sample (Mean Age = 163 months, SD = 22.8 months).

On each trial, a shape (O, D, h, or e) appeared centrally


on the computer screen. Children were instructed to
respond to three of the shapes by pressing a large external
star button (i.e. Go stimuli), but to resist responding
to a fourth shape (i.e. the No-Go stimulus). The shape
designated as the No-Go stimulus was counterbalanced
between participants. To generate a prepotent response,
75 % of trials were Go trials requiring a button press,
and 25 % of trials were No-Go trials where the response
should be withheld.
The maximum inter-stimulus interval (ISI) was
2,500 ms. At the start of each trial, a fixation-cross
appeared at the centre of the screen for 200 ms. The
stimulus then appeared for 200 ms. After stimulus offset,
participants had a further 1,000 ms to respond before the
trial automatically terminated. There was then a 1,100 ms
pause before the next trial commenced. An error tone
(bleep) was played immediately if the child made an
omission error (i.e. failed to respond on a Go trial), or a
false positive (i.e. pressed the star button on a No-Go
trial). A positive feedback-noise (ping) was played for
correct responses.

Control Group
Twenty-eight typically developing (TD) children, aged
611 years, were recruited from three local primary
schools. No child had any clinical diagnosis or was on the
school register for special educational needs. On the
CARS, all TD children scored between 15 (the minimum
score) and 19 points. Thus, all twenty-eight children (17
female, 11 male) were included in the final sample (Mean
Age = 106 months, SD = 16.2 months).
ASD and TD groups were matched on estimated verbal
and non-verbal mental age (MA), according to performance on the BPVS (Dunn et al. 1997) and the Ravens
Coloured Progressive Matrices (Ravens CPM) (Raven
et al. 1990). For all children, a teacher completed the first
19-items of the 35-item Vanderbilt AD/HD Diagnostic
Teacher Rating Scale (VADTRS). The VADTRS assesses
symptoms of attention-deficit/hyperactivity disorder based
upon DSM-IV (1994) criteria, with 19-items rated on a
four-point frequency scale (0 = Never; 1 = Occasionally;
2 = Often; 3 = Very Often). A child is indicated as above
the DSM-IV threshold for AD/HD Inattentive-Type if they
receive a rating of 2 or 3 on six or more from Items 19.
AD/HD-Hyperactive/Impulsive Type is indicated by six or
more ratings of 2 or 3 on Items 1019. AD/HD Combined
type is indicated by six or more ratings of 2 or 3 on both
dimensions. For normative data, see Wolraich et al. (1998).

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Procedure
A warm-up session was initially conducted to familiarize
participants with the stimuli. Training was terminated only
when the child could correctly identify the required
response for each shape (i.e. Go vs. No-Go). Children then
completed a short practice block of eight trials containing
all four stimuli presented in a fixed but superficially random order. 144 experimental trials then followed, split into
three 48-trial blocks separated by short breaks. Stimulus
presentation was randomised throughout each half block.
Four measures of task performance were obtained: False
positive rate (No-Go trials on which the button was
pressed); hit rate (Go trials on which the child responded); hit trial reaction time (RT); and task sensitivity. The
latter differentiates participants who make fewer false

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positives despite a good hit rate (good sensitivity) from


those who make fewer false positives but fewer hits as well
(poor sensitivity) (see Grier 1971).
Dog-Pig Stroop Task
Task Design
Stimuli were two simple line drawings of a dog and a pig,
which were presented centrally on a computer screen. Two
experimental conditions, each containing 32 trials were
administered. In the control (baseline) condition, children
were instructed to say dog when they see the dog image
and pig when they see a pig, as quickly and accurately as
possible. In the Stroop (i.e. inhibition) condition, children
were instructed to say dog to pig images, and pig to
dog-images.
Childrens responses were recorded online during the
task and audiotaped for subsequent checking. If a child
made a mistake on a trial but then corrected him/herself,
the initial response was recorded. To estimate response
latency on each trial, the experimenter pressed a large
external button in time with the childs initial response.
Although this measure of reaction time is relatively crude,
many of the children would not have been testable with
throat microphones that measure voice-onset due to interference from task irrelevant movements and vocalisations.
Notably, any additional error introduced via the reactiontime estimate was constant across groups.
On each trial, the stimulus remained centrally on-screen
until a response had been registered. After 3,000 ms had
elapsed without a response, the trial automatically terminated and the message Too Slow was presented for
500 ms. Stimulus presentation was followed by a 2,000 ms
pause before the next trial commenced. The maximum ISI
was 5,500 ms.
Procedure
All children completed the control condition first to obtain
baseline picture naming speed and accuracy, followed by
Stroop training slides. After completing four Stroop practice trials successfully, children commenced the 32-trial
Stroop condition block.
Flanker Task
Task Design
Children were presented with two large arrow-shaped
buttonsone pointing left and one pointing right. There
were three conditions in this task. In all conditions, children were asked to press the button pointing the same way

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as a white target arrow that would appear (centrally) onscreen. On baseline trials, the target arrow was presented
alone. On congruent trials, the target arrow was flanked by
four red distractor arrows (two either side) pointing the
same way as the target (e.g.
). On incongruent trials,
the target arrow was flanked by distractor arrows facing in
the opposite direction to the target (e.g.
).
The maximum ISI was 2,900 ms. On each trial, a fixation cross appeared centrally on-screen for 200 ms. This
was replaced by the stimulus (neutral, congruent or
incongruent), which remained on-screen until a buttonpress was registered. If no response had been registered
after 1,200 ms, the trial automatically terminated and a
Too-Slow message was briefly displayed accompanied
by an error tone (bleep). The error-tone also sounded if
the participant responded incorrectly. A positive feedbacknoise was played (ping) for correct responses. There was
a 1,100 ms pause (inter-trial interval) between trials.
Procedure
Familiarisation trials were followed by three blocks of 30
trials, each separated by a short break (90 trials in total).
Each block contained ten baseline, ten congruent and ten
distractor trials, which were distributed randomly. Errorrates and mean RTs were recorded for all trials.
Planned Comparisons
A MANOVA with group as the between-group factor was
used to assess group differences in chronological age (CA),
BPVS, Ravens CPM, CARS and VADTRS scores. Difference in gender-distribution between groups was estimated using a Chi-square test. Regarding task
performance, a series of Pearson correlations were implemented between the three inhibitory measures (all participants included). To permit these correlations, single-figure
estimates of inhibitory performance had to be calculated
for the Dog-Pig Stroop and Flanker task by subtracting
participants baseline RT and error-rates from their Stroop/
incongruent trial RT and error-rates. False positive rate was
used to represent inhibitory performance on the Go/No-Go.
Between task correlations (N = 59) could detect large
effect sizes (r = 0.5) at a = 0.05 (2-tailed) at 99 % power,
and medium effect sizes (r = 0.3) at approximately 66 %
power. Simple bivariate correlations were also performed
to highlight any associations between CA, MA (BPVS/
RCPM) and CARS rating and inhibitory outcome measures
(see Table 3). As these were carried out separately for each
group (N = *30), we only had sufficient power (80 %) to
detect large effect sizes (r = 0.5) at a = 0.05 (2-tailed).
Although CA was not matched between groups, CA was
not used as a covariate for group comparisons of inhibitory

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Table 3 Pearson (r) correlations between CA, BPVS, Ravens CPM


and CARS (ASD only) and inhibitory performance
CA

BPVS

Ravens

Inhibitory RT

-0.174

-0.072

0.019

Inhibitory error

-0.311

0.039

0.010

Inhibitory errors

-0.139

-0.179

-0.136

Inhibitory RT

-0.095

-0.334

-0.405*

-0.031

-0.033

-0.083

TD group (N = 28)
Flanker

Dog Pig Stroop

Go/No-Go
False positives
CA

BPVS

Ravens

CARS

Autism group (N = 31)


Flanker
Inhibitory RT

-0.429*

-0.394*

0.042

0.012

Inhibitory error

-0.096

-0.175

-0.435*

0.012

Dog Pig Stroop


Inhibitory errors
Inhibitory RT

0.037

-0.374*

-0.299

0.156

-0.482**

-0.127

-0.207

-0.357

0.060

-0.161

-0.456**

Go/No-Go
False positives

0.315

* p \ 0.05; ** p \ 0.01 (2-tailed)

performance. This is because covariates have been ill


advised for the control of non-trivial groups differences
(Miller and Chapman 2001), as it can cause observed
means to be adjusted for spurious reasons (Jarrold and
Brock 2004). Pearsons correlations were used, however, to
estimate any influence CA may have had on inhibitory
performance and possible implications for group differences. However, again, there was only sufficient power to
detect large (i.e. r = 0.5) effect sizes at a = 0.05.
Group differences in Go/No-Go task performance were
assessed via a one-way MANOVA. Group was the
between-participants factor, and false alarms, hits, A (task
sensitivity), Go-trial RT and No-Go-trial RT were the
dependent variables. The main measure of inhibition was
false alarm rate. Group differences in Dog-Pig Stroop task
performance were investigated using a 2 9 2 mixed MANOVA. Trial-type was the within-participants factor, group
was the between-participants factor, and error-rate and RT
were the dependent variables. Errors were classified as any
trial on which the child either said the wrong animal name
(i.e. Incorrect Response Errors) or failed to make a
response before the trial terminated (i.e. Too Slow Errors).
Group differences on the Flanker task were assessed using
a 3 9 2 mixed MANOVA, with trial-type as a withinparticipants factor, group as a between-participants factor,
and error-rate and RT as the dependent variables. Post hoc

123

pair-wise comparisons (using Bonferroni correction) clarified group differences across conditions (no-distractor,
congruent, incongruent).
Associations between inhibitory performance and
ADHD-like symptoms were assessed in the ASD group
only as TD children scored very low (mostly zero) on both
dimensions. For this, subgroups of high and low scoring
CWA were identified for both inattentiveness and hyperactivity/impulsivity scales. High Scorers were children
scoring six or more ratings of 2 (often) or 3 (very often) on
relevant items. This is cut-off flags children who may meet
the diagnostic criteria for ADHD-Inattentive type (n = 9),
or ADHD-Hyperactive/Impulsive type (n = 7) (APA
1994). Low scorers received no more than one rating of
2 (often) or 3 (very often) on items for ADHD-Inattentive
type (n = 11) and ADHD-Hyperactive/Impulsive type
(n = 12). Performance of high/low scoring groups was
compared via one-way multiple ANOVAs with the key
inhibitory performance measures as dependent variables.
This subgroup approach was used to maintain the threshold-based scoring method on which the VADTRS was
validated.
For all comparisons, an alpha level of 0.05 was used and
exact p values and effect sizes are provided where appropriate to make results as transparent and easily comparable
to previous findings as possible. Although a number of
statistical tests were performed, Howell (2002) argues that
correction for multiple comparisons is not warranted where
a priori predictions are made. However, we caution readers
to interpret non-corrected results conservatively, particularly where strong a priori predictions were not made (e.g.
ADHD-symptom effects).

Results
As shown in Table 2, CARS ratings were higher amongst
CWA than TD controls, as were VADTRS inattention and
hyperactivity scores. VADTRS inattention ratings and
CARS-rating were positively correlated in CWA,
r(29) = 0.384, p = 0.033 (2-tailed). The two groups were
satisfactorily matched on BPVS and Ravens score.
Although the ASD group was significantly older than the
TD group, Pearsons correlations indicated few associations
between CA and inhibitory performance: in the ASD group
only, higher CA was predictive of faster inhibitory RTs on
the flanker task (p = 0.016) and the Dog-Pig Stroop
(p = 0.007). In terms of MA, higher RCPM scores were
predictive of better inhibitory performance (faster RT)
amongst TD children in the Dog-Pig Stroop (p = 0.033).
Amongst CWA, higher Ravens scores predicted more
inhibitory errors on the Flanker task (p = 0.014) and more
false-positives (p = 0.010) on the Go/No-Go. Higher BPVS

J Autism Dev Disord (2013) 43:10651079

1073

Table 4 Pearson correlations (N) between inhibitory performance on the three inhibitory control tasks

Go/No Go (false alarms)

Flanker (errors)

Dog-Pig Stroop (errors)

Flanker (RT)

Dog-Pig Stroop (RT)

0.193 (59)

-0.030 (58)

-0.075 (59)

0.169 (58)

0.248 (58)

0.043 (59)

0.032 (58)

0.152 (58)

0.262 (58)

Flanker (errors)
Dog-Pig Stroop (errors)
Flanker (RT)

0.149 (58)

* p \ 0.05; ** p \ 0.01 (2-tailed)

Table 5 Group effects (ASD/TD) for Go/No-Go task measures

False alarms (/36 No-Go trials)


Hits(/108 Go-trials)
Task sensitivity (A0 ) (0.5 = random;
1.0 = perfect sensitivity)

F value

p value

Effect-size (g2p)

6.35
2.00

6.830
4.629

0.011*
0.036*

0.107
0.075

0.061

6.275

0.015*

0.099

ASD group (N = 31)

TD group (N = 28)

SD

SD

17.74
104.4

8.05
4.43

22.71
106.3

0.623

0.118

0.561

Go-trial RT (ms)

0.422 s

0.112 s

0.410 s

0.064 s

0.262

0.611

0.005

No-Go-trial RT (ms)

0.341 s

0.081 s

0.343 s

0.043 s

0.004

0.950

0.000

scores were associated with slower inhibitory RTs on the


Flanker Task, and more inhibitory errors on the Dog-Pig
Stroop. Notably, there were no significant correlations
between inhibitory performance on any task and CARS
score (all r \ 0.357, p [ 0.05).
Inhibitory Control Measures
There were no significant correlations between any of the
main inhibitory measures between tasks, although the
association between inhibitory error-rates on the Flanker
and Dog-Pig Stroop tasks did approach significance,
r(56) = 0.248, p = 0.061 (2-tailed) (see Table 4).
On the Go/No-Go task, CWA made significantly fewer
false positives than TD children (p = 0.01) (see Table 5).
Logistic regression showed that false alarm rate still helped
to differentiate between CWA and TD participants after the
higher hit-rate in the ASD group has been taken into
account (v2(1, N = 59) = 5.078, p = 0.024). CWA also
showed better task sensitivity (A0 ) than TD children
(p \ 0.05). Together these indicate better overall accuracy
on the task, rather than just a tendency to press the button
less across the board.
On the Dog-Pig Stroop Task, there was a significant
within-participants effect of trial-type on error-rate,
F(1,56) = 58.970, p \ 0.001, g2p = 0.513, and on RT,
F(1,56) = 147.544, p \ 0.001, g2p = 0.725, with children
making more errors and responding slower on Stroop trials
than on baseline trials. This indicates that Stroop trials did
impose additional inhibitory demands.

There was a marginally significant effect of group upon


error-rate, F(1,56) = 3.264, p = 0.076, g2p = 0.055, with
CWA making more total errors (M = 3.3; SE = 0.445)
than TD children (M = 2.1; SE = 0.461) across both
baseline and Stroop trials. The main effect of group upon
RT was also significant, F(1,56) = 4.576, p = 0.037,
g2p = 0.076, with CWA tending to respond significantly
slower (M = 0.881 s; SE = 0.036) than TD children
(M = 0.772; SE = 0.037).
Figure 1 illustrates a significant trial-type h group
interaction for error-rate, F(1,56) = 7.425, p = 0.009,
g2p = 0.117. Post hoc exploration indicated that this was
due to CWA making more errors on Stroop trials than controls, t(59) = 2.277, p = 0.027, despite an equivalent errorrate on baseline trials t(59) = -0.287, p = 0.775. However,
there was no significant trial-type h group interaction for RT
on this task, F(1,56) = 0.396, p = 0.532, g2p = 0.007.
For the Flanker Task, the main effect of trial-type was
significant for both error-rate, F(1.60,116) = 41.763,
p \ 0.001, g2p = 0.419, and RT, F(1.54,116) = 218.595,
p \ 0.001, g2p = 0.790. Post hoc exploration showed that
this was because children made significantly more errors on
incongruent distractor trials (M = 4.44, SD = 2.334) than
on baseline (M = 2.00, SD = 2.147) or congruent distractor
trials (M = 1.90, SD = 2.147) (both, p \ 0.001). Children
also responded significantly slower on incongruent distractor trials (M = 0.675 s, SD = 0.128 s) than on both baseline (M = 0.560 s, SD = 0.111 s) and congruent distractor
trials (M = 0.584 s, SD = 0.117 s) (both, p \ 0.001).
Children were still significantly slower on congruent than

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J Autism Dev Disord (2013) 43:10651079

Fig. 1 Mean and SE of a error


rate and b reaction time on the
Dog-Pig Stroop task

Symptoms of Inattention and Hyperactivity/Impulsivity


There were no significant differences between the high and
low hyperactivity/impulsivity subgroups of CWA on any
inhibitory measure (all p [ 0.3). The high inattention subgroup did, however, show significantly poorer inhibitory
performance on the Dog-Pig Stroop task than the low inattention subgroup, F(1,18) = 4.273, p = 0.05, g2p = 0.192
(see Fig. 3). No differences between inattention subgroups
were observed on the Go/No-Go and Flanker (all p [ 0.1).
Two further one-way ANOVAs were performed to
gauge whether overall group-differences in Dog-Pig Stroop
error-rate were driven by poor performance in the highinattention ASD subgroup. These demonstrated that the
high inattention CWA made significantly more inhibitory
errors than a random subgroup of TD children (N = 10),
Fig. 2 Mean and SE of a error
rate and b reaction time on the
Flanker task for no distractor,
congruent and incongruent
distractor trials

123

Number of Inhibition Errors


(Dog-Pig Stroop)

baseline trials though (p \ 0.001), suggesting that even nonconflicting peripheral stimuli cause some interference.
There was no main effect of group on error-rate,
F(1,57) = 0.780, p = 0.381, g2p = 0.014, but there was a
significant group effect on RT, F(1,57) = 5.316,
p = 0.018, g2p = 0.085, with CWA tending to respond
significantly faster (M = 0.575; SE = 0.020) than TD
children (M = 0.642; SE = 0.021). However, the trial-type
h group interaction was insignificant for error-rate,
F(1.605, 114) = 0.882, p = 0.417, g2p = 0.015, and RT,
F(1.534,114) = 0.049, p = 0.914, g2p = 0.001, implying
no inhibitory advantage in CWA (see Fig. 2).

7
6
5
4
3
2
1
0
High

Low

Symptoms of Inattention
Fig. 3 Mean and SE of error rate for the high and low inattention
subgroups of CWA on the Dog-Pig Stroop

F(1,17) = 6.322, p = 0.022, g2p = 0.659, but that the low


inattentive subgroup did not, F(1,17) = 0.383, p = 0.543,
g2p = 0.091.

Discussion
Overall, the present research suggests that children do not
perform equivalently on different tasks of inhibitory control, and that some tasks may be more likely to reveal
impairments in CWA than others. It is possible to make this
statement with confidence because this study administered
multiple measures of inhibitory control to the same cohort of

J Autism Dev Disord (2013) 43:10651079

children (Christ et al. 2007). Impairments in inhibitory


control were seen on the Dog/Pig Stroop task, but not on two
other tasks thought to tap into inhibitory function. We
propose that this selective impairment might relate to disparities in the cognitive and executive demands imposed by
the tasks. In particular, conflict tasks of inhibition might be
more problematic for CWA because of the considerable (and
simultaneous) working memory demands they exert.
On the Go/No-Go task, our measure of delay inhibition,
CWA actually demonstrated better inhibitory performance
than TD controls. They made fewer false positives and
showed better task sensitivity, which indicates a genuine
inhibitory advantage (i.e. CWA did not just response less
across both Go and No-Go stimuli, which would more
indicate sustained attentional difficulties). Although
intact inhibitory performance amongst CWA has been
documented on numerous occasions on this task (e.g.
Christ et al. 2007; Geurts et al. 2004; Noterdaeme et al.
2001; Sinzig et al. 2008), superior performance has not. It
is thus conceivable the CA difference between the two
groups was influential. Although no significant correlation
between inhibitory performance and CA was observed in
either group on this task, voluntary inhibitory functions are
known to develop and improve throughout childhood
(Diamond and Taylor 1996; Levin et al. 1991) and into
adolescence (Ridderinkhof et al. 1999).
For this reason, the observed superiority of CWA on our
Go/No-Go task should be interpreted with some caution.
However, this result is still relatively strong evidence that
autism is not associated with Go/No-Go task impairments,
adding to a growing body of research from tasks tapping
simple delayed response inhibition like the Go/No-Go task,
Stop-task (Ozonoff and Strayer 1997) and TEA-Ch WalkDont Walk task (Yerys et al. 2009; although see Bishop
and Norbury 2005). Particularly notable here is that these
children showed spared performance on the Go/No-Go
despite showing an inhibitory deficit on another taskthe
Dog/Pig Stroop (Gerstadt et al. 1994). This is a powerful
indication that something about the tasks themselves is
driving differential inhibitory performance.
The Dog-Pig Stroop task has been used once previously
to measure inhibitory capacities in CWA (Ames and Jarrold
2007), and similar inhibitory impairments were observed.
However, the single-trial computerised version used here is
arguably more sensitive to group-based differences in performance, providing separate trial-by-trial measures of
accuracy and response time (Perlstein et al. 1998). These
results corroborate a number of previous studies that have
observed difficulties amongst CWA on other tasks of conflict inhibition, including the Windows (Hughes and Russell
1993; Russell et al. 2003), detour reaching (Biro and Russell
2001), and the TEA-Ch Opposite Worlds tasks (Bishop and
Norbury 2005, although see Geurts et al. 2004).

1075

The CWAs performance on the conflict inhibition task


suggests that inhibition is not completely spared in autism
(cf. Pennington 1997). However, it is perhaps more interesting to ask why CWA might have more difficulty with this
paradigm compared to others. One argument is that these
tasks impose considerable working memory as well as
inhibitory demandsby necessitating the suppression of an
inappropriate (yet prepotent) response, whilst also simultaneously activating and implementing a conflicting and novel
response (Carlson and Moses 2001; Carlson et al. 2002).
This additional requirement is absent in the Go/No-Go task
and Flanker task, in which children need only suppress either
a prepotent response or distracting information. Supporting
this conjecture, Carlson et al. demonstrated that performance on conflict inhibition tasks was significantly correlated with working memory abilities in young TD children,
but performance on delay inhibition tasks was not. Thus it
may be this simultaneous strain on two core executive
components that it problematic for CWA.
Our measure of resistance to distractor inhibition, the
arrows Flanker task, measured participants ability to
suppress interference from distracting information in the
external environment that is irrelevant to the task at hand.
Both CWA and TD children had difficulty suppressing
irrelevant distractors. Further, although incongruent distractors were most problematic, children in both groups
experienced some interference even from non-conflicting
distractors, illustrating the sensitivity of the task to lowlevel attentional processes. However, CWA showed no
greater inhibitory difficulty than controls, corroborating
two previous studies that administered a similar arrows
Flanker task to adults with autism (Henderson et al. 2006;
Dichter and Belger 2007). The results do conflict with
another study, however, that reported clearly impaired
performance amongst CWA using a slightly different
Flanker task (Christ et al. 2007)which may point towards
subtle non-inhibitory differences between the two taskversions (see Friedman and Miyake 2004). For instance, in
Christ et al., children had to hold in mind four different
arbitrary response mappings throughout the task, whereas
an arrows paradigm only requires participants to hold in
mind two logical stimulusresponse mappings. Thus, it
may be that elevated working memory demands make
Christ et al.s task more problematic for CWA, as opposed
to the central inhibitory components. Given this, we would
argue that our task is the purer measure. However, before
generalising to claims of intact resistance to distractor
inhibition, it is important to undertake further research with
different task variants.
The lack of any strong correlation between tasks and the
disparate group-differences across paradigms arguably
point towards separate inhibitory functions that are in turn
differentially affected in autism. However, it is critical to

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1076

recognise other factors may have influenced task performance differences. One possibility is that the strength or
potency of the to be inhibited information or impulse
varies between tasks. That is, the Dog-Pig Stroop may
simply be more sensitive to group differences because of
its inhibitory difficulty, and performance on the three tasks
may not correlate well simply because the prepotentresponse strengths are not equivalent. Indeed, through
computational modelling using various task parameters,
Davelaar and Cooper (2010) showed that the strongest (and
in fact only) mediator of correlation between two inhibitory
tasks (a Stop-task and a Stroop task) was the prepotent
response potency channel. Although more extensive computational modelling using a numerous delay, resistance to
distractor and conflict tasks would be required to
strengthen this argument, it is important to remember that
shared/non-shared executive processes are not the only
possible mediators of group differences and between-task
correlations. Regardless of the interpretation of group differences, however, the current findings are still a relatively
strong indication that inhibitory function is not a core
deficit in ASD (e.g. Yerys et al. 2009, although see
Simpson and Riggs 2005). This message is particularly
clear if one considers that children with AD/HD almost
invariably show inhibitory impairments irrespective of the
task choice (e.g. Happe et al. 2006).
Our second objective was to consider the role of symptoms of inattention and/or hyperactivity/impulsivity in predicting inhibitory impairments in CWA. As expected, these
symptoms were far more common in CWA than TD children
(see Lee and Ousley 2006)with approximately one-third
of CWA scoring above the clinical cut-off for AD/HDinattentive type, and one quarter above cut-off for hyperactive/impulsive type on the VADTRS. This corroborates a
recent large-scale study that estimated that 31 % of individuals with autism meet diagnostic criteria for AD/HD
(Leyfer et al. 2006). In contrast, no TD child came close to
either cut-off and the majority scored extremely low on both
scales.
We found no link between symptoms of hyperactivity/
impulsivity and inhibitory performance in CWA (unlikely
due to low power because the observed effect sizes were
relatively small). This is perhaps somewhat surprising
given that correlations between inhibitory performance on
various different tasks and these symptoms in CWA have
been reported (e.g. Ames and White 2010; Bishop and
Norbury 2005; Sinzig et al. 2008; Verte et al. 2006). One
plausible explanation is that VADTRS is a less sensitive
measure of hyperactive/impulsive symptoms as those used
in previous studies, because although based upon DSM-IV
criteria, the VADTRS is a relatively new scale backed by
relatively limited validity and normative data. However, a
review of the psychometric properties of various ADHD

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J Autism Dev Disord (2013) 43:10651079

rating scales, Collett et al. (2003) did conclude that the


VADTRS is psychometrically strong despite its relative
youth (p. 1027). Therefore, it seems unlikely that insensitivity of the VADTRS is responsible for the null hyperactivity/impulsivity findings.
In contrast, CWA who scored over the diagnostic cut-off
for AD/HD inattentive-type made more inhibitory errors on
the Dog/Pig Stroop than those with low inattentiveness
ratings. Furthermore, whereas the high-inattention subgroup of CWA performed more poorly on the task than a
randomly selected TD subgroup, the low-inattention subgroup of CWA did not. One possible implication here is
that the ASD group impairment on the Dog/Pig Stroop may
have been driven primarily by the poor performance of this
highly inattentive subgroup of CWA.
Although this finding corroborates others studies linking
symptoms of inattention to inhibitory control in autism
(Bishop and Norbury 2005; Chhabildas et al. 2001), why
would attentional-deficits in CWA predict inhibitory
impairments on some, but not all, tasks of inhibitory control? One possibility, again, is the fact that conflict tasks
draw heavily (and simultaneously) upon both inhibitory
control abilities and working memory (Carlson and Moses
2001; Carlson et al. 2002): the two domains of executive
function that have most consistently been shown to be
impaired in attentional disorders (Castellanos and Tannock
2002; Gioia et al. 2002; Semrud-Clikeman et al. 2010).
Indeed, in a meta-analysis of 83 studies, Willcutt et al.
(2005) reported that the most robust and consistent executive impairments amongst children with ADHD are
response inhibition and working memory (verbal and spatial), as well as vigilance and planning. The Dog/Pig Stroop
task may thus be particularly sensitive to attentional
impairments because it draws upon not one, but two, of the
key areas of executive dysfunction associated with attentional difficulties. That is, in these children, the need to
actively maintain rule-bound processes may divert (limited) attentional resources away from the inhibitory element of the task, leading to poorer inhibitory performance.
Explicit measures of working memory capacity would be
needed to explore this hypothesis further.
Again, the fact that inattention only predicted poorer
performance on the Dog-Pig Stroop is particularly poignant
if we consider that inhibitory impairments in AD/HD
populations are far less dependent on the task measurement
used (Barkley 1997). Indeed, the specificity of inhibitory
difficulties in these CWA compared to AD/HD groups
shows some support for executive accounts of autism,
because it suggests that different profiles of executive
ability may indeed be observable in different disorders
(Pennington 1997). It is perhaps rather unrealistic to expect
disorders to be characterised by impaired subcomponents
of EF alongside completely spared ones, as subcomponents

J Autism Dev Disord (2013) 43:10651079

are inherently intertwined (Welsh and Pennington 1988).


The results we obtained here, however, support the notion
that disorders differ in terms of where their core or most
pervasive executive difficulties lie.
Although speculative, our findings also point to a more
fundamental issue. When differences are found between
individuals with autism and control groups, there is often
an assumption that they relate to the core symptoms of the
autistic disorder. For instance, authors readily link
observed impairments in inhibitory function to restricted or
repetitive behaviours (e.g. Turner 1997; Lopez et al. 2005).
However, it might be that group differences are more
closely associated with a covariate of the disorder or
underlying endophenotypes (e.g. symptoms of inattention),
rather than core autistic symptoms themselves. It is thus
important that studies of autism take into account symptoms of ADHD in their sample (and vice versa for ADHDrelated studies)particularly when investigating impairments, like executive dysfunction, that have been implicated in both disorders.
Several methodological limitations of the study should be
noted. First, whilst ASD and TD groups were matched for
non-verbal and verbal mental age, they were not matched for
chronological age. Although a CA difference is expected
when comparing TD and ASD groups, future studies would
benefit from ensuring sufficient age overlap between comparison groups. This would permit the use of CA as a
covariate and additional CA-matched subgroup analyses
(Jarrold and Brock 2004). Correlational analyses indicated
that between-group differences were if anything more conservative as a result of the CA disparity, as older CWA
showed faster inhibitory reaction times on the Flanker and
Stroop task than younger CWA. The fact that this relationship was observed in the ASD group only may have reflected
the wide age range of the group. We also note that we only
had sufficient power (80 %) to identify relatively large effect
sizes. Secondly, it is notable that the two groups had nonequivalent gender distributions. Although we confirmed no
sex-related differences in inhibitory performance in either
group on any task, gender differences have been observed in
brain activation on inhibition tasks (Garavan et al. 2006). It
should be stressed, however, that studies have typically
found no evidence of sex differences in behavioural performance on inhibition tasks including the Stop task
(Williams et al. 1999), the Go/No-Go (Garavan et al. 2006)
and the Stroop task (MacLeod 1991). Finally, although all
children in the ASD group had received a formal diagnosis of
an ASD using DSM criteria and their current symptoms were
clearly suggested by the CARS, confirmation of current
symptomology using the ADOS-G/ADI-R would have permitted more detailed analysis of the autistic symptom-profile
of the ASD group, and would describe current symptomology according to DSM-IV most appropriately.

1077
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.
Conflict of interest
of interest.

The authors declare that they have no conflict

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, 11121121.
American Psychiatric Association. (1994). Diagnostic and statistical
manual of mental disorders. Washington, DC: American
Psychiatric Association.
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, 17611775.
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, 357363.
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, 115116.
Aron, A. R., & Poldrack, R. A. (2005). The cognitive neuroscience of
response inhibition: relevance for genetic research in attentiondeficit/hyperactivity disorder. Biological Psychiatry, 57, 1285
1292.
Barkley, R. A. (1997). ADHD and the nature of self-control. New
York: Guilford.
Biro, S., & Russell, J. (2001). The execution of arbitrary procedures
by children with autism. Development and Psychopathology, 13,
97110.
Bishop, D. V. M., & Norbury, C. F. (2005). Executive functions in
children with communication impairments, in relation to autistic
symptomology. Autism, 9, 727.
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), 245264.
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, 12511258.
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, 584591.
Carlson, S. M., & Moses, L. J. (2001). Individual differences in
inhibitory control and childrens theory of mind. Child Development, 72, 10321053.
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, 7392.
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, 299329.

123

1078
Castellanos, F. X., & Tannock, R. (2002). Neuroscience of attentiondeficit/hyperactivity disorder: The search for endophenotypes.
Nature Reviews Neuroscience, 3, 617628.
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,
529540.
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, 11551165.
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, 10151037.
Dagenbach, D., & Carr, T. H. (Eds.). (1994). Inhibitory processes in
attention, memory and language. San Diego, CA: Academic
Press.
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. 937942).
Portland, OR: Cognitive Science Society.
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, 315334.
Dichter, G. S., & Belger, A. (2007). Social stimuli interfere with
cognitive control in autism. Neuroimage, 35(3), 12191230.
Dunn, L. M., Dunn, L. M., Whetton, C., & Burley, J. (1997). British
picture vocabulary scale (2nd ed.). Windsor: NFER-Nelson.
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), 4557.
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, 143149.
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, 6173.
Friedman, N. P., & Miyake, A. (2004). The relations among inhibition
and interference control functions: A latent variable analysis.
Journal of Experimental Psychology: General, 133, 101135.
Garavan, H., Hester, R., Murphy, K., Fassbender, C., & Kelly, C.
(2006). Individual differences in the functional neuroanatomy of
inhibitory control. Brain Research, 1105, 130142.
Gerstadt, C., Hong, Y., & Diamond, A. (1994). The relationship
between cognition and action: Performance of children
31/27 years on a Stroop-like day-night test. Cognition, 53,
129153.
Geurts, H., Verte, 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, 836845.
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, 121137.
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, 279293.
Grier, J. B. (1971). Nonparametric indexes for sensitivity and bias:
Computing formulas. Psychological Bulletin, 75, 424429.
Hala, S., Hug, S., & Henderson, A. (2003). Executive function and
false belief understanding in preschool children: Two tasks are

123

J Autism Dev Disord (2013) 43:10651079


harder than one. Journal of Cognition and Development, 4,
275298.
Happe, F., Booth, R., Charlton, R., & Hughes, C. (2006). Executive
function deficits in autism spectrum disorders and attentiondeficit/hyperactivity disorder: Examining profiles across
domains and ages. Brain and Cognition, 61, 2639.
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), 96109.
Hill, E. L. (2004a). Evaluating the theory of executive dysfunction in
autism. Developmental Review, 24(2), 189233.
Hill, E. L. (2004b). Executive dysfunction in autism. Trends in
Cognitive Sciences, 8(1), 2632.
Howell, D. (2002). Statistical methods for psychology (5th ed.).
Belmont, CA: Duxbury Press.
Hughes, C., & Russell, J. (1993). Autistic childrens difficulty with
mental disengagement from an object: Its implications for
theories of autism. Developmental Psychology, 29, 498510.
Jarrold, C., & Brock, J. (2004). To match or not to match?
Methodological issues in autism-related research. Journal of
Autism and Developmental Disorders, 34, 8186.
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, 807821.
Leckman, J., Price, R., Walkup, J., Ort, S., Pauls, D., & Cohen, J.
(1987). Nongenetic factors in Gilles de la Tourettes syndrome.
Archives of General Psychiatry, 44, 100.
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, 737746.
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, 352356.
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, 377395.
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,
849861.
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, 216222.
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, 445460.
MacLeod, C. M. (1991). Half a century of research on the Stroop
effect: An integrative review. Psychological Bulletin, 109,
163203.
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.
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, 538541.
Miller, G. A., & Chapman, J. P. (2001). Misunderstanding analysis of
covariance. Journal of Abnormal Psychology, 110(1), 4048.

J Autism Dev Disord (2013) 43:10651079


Minshew, N. J., Luna, B., & Sweeney, J. A. (1999). Oculomotor
evidence for neocortical systems but not cerebellar dysfunction
in autism. Neurology, 52(5), 917922.
Mitchell, J. P., Macrae, C. N., & Gilchrist, I. D. (2002). Working
memory and the suppression of reflexive saccades. Journal of
Cognitive Neuroscience, 14, 95103.
Nation, K. (2006). Patterns of reading ability in children with autism
spectrum disorder. Journal of Autism and Developmental
Disorders, 36, 911919.
Nigg, J. T. (2000). On inhibition/disinhibition in developmental
psychopathology: Views from cognitive and personality psychology and a working inhibition taxonomy. Psychological
Bulletin, 126, 220246.
Nigg, J. T. (2001). Is ADHD a disinhibitory disorder? Psychological
Bulletin, 127, 571598.
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. 118). New York: Plenum
Press.
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, 5866.
Ozonoff, S., & Jensen, J. (1999). Specific executive function profiles
in three neurodevelopmental disorders. Journal of Autism and
Developmental Disorder, 29, 171177.
Ozonoff, S., & Strayer, D. L. (1997). Inhibitory function in
nonretarded children with Autism. Journal of Autism and
Developmental Disorders, 27, 5977.
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, 10151031.
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.
265281). Baltimore, MD: Brookes.
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, 414425.
Perret, E. (1974). The left frontal lobe in man and the suppression of
habitual responses in verbal categorical behavior. Neuropsychologia, 12, 323330.
Raven, J. C., Court, J. H., & Raven, J. (1990). Coloured progressive
matrices. Oxford: Oxford Psychologists Press.
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 ones actions. Acta Psychologica, 101,
315337.
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), 281295.
Russell, J. (1997). Autism as an executive disorder. 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 difficulties. Cognitive Development, 18(1), 111137.
Russell, J., Jarrold, C., & Hood, B. (1999). Two intact executive
capacities in children with autism: Implications for the core

1079
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.
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), 10171027.
Simpson, A., & Riggs, K. J. (2005). Inhibitory and working memory
demands of the day-night task in children. British Journal of
Developmental Psychology, 23, 471486.
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 ADHDsymptoms. Child and Adolescent Psychiatry and Mental Health,
2, 4.
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, 117126.
Stroop, J. (1935). Studies of interference in serial verbal reactions.
Journal of Experimental Psychology, 18, 643662.
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, 10051027.
Tipper, S. P. (1985). The negative priming effect: Inhibitory priming
by ignored objects. Quarterly Journal of Experimental Psychology, 37A, 571590.
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, NY: Oxford University
Press.
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, 341352.
Verte, 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, 514.
Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of
working memory: a meta-analysis. Cognitive, Affective and
Behavioural Neuroscience, 3, 255274.
Welsh, M. C., & Pennington, B. F. (1988). Assessing frontal lobe
functioning in children: Views from developmental psychology.
Developmental Neuropsychology, 4, 199230.
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, 13361346.
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), 205213.
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, 141152.
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), 322333.

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