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DOI 10.1007/s10803-012-1650-5
ORIGINAL PAPER
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
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Autism
Autism
HFA/AS
HFA
Autism
Autism
HFA
Autism/PDD-NOS
Autism
Autism
Study 2
HFA
Study 1
HFA
HFA
HFA
Autism
Autism/AS/PDD
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
TD/MLD
Autism/AS/PDD-NOS
TD
Comparisons
Autism
ASD
Sample characteristics
Study
VMA
CA/Gender/VIQ/PIQ/FSIQ
CA/Gender/VIQ/PIQ/FSIQ
CA/PIQ
CA/IQ (Ammons)
CA/FIQ
VMA
VMA
CA/MA
CA
CA
Reading Speed
NVMA
VMA
VMA/NVMA (BPVS/RCPM)
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
Yes
No
Male Participants
Anti-Saccade Task
Yes
Female Participants
Stop-task
Yes
Knob
Yes
No
Windows Task
Flanker
No
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
No
No
Colour-word Stroop
ASD impaired?
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
VMA (BPVS)
TD/MLD
Autism
AS
Comparisons
ASD
Matching criteria
Table 1 continued
TD
ASD impaired?
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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
91.87
20.36
93.79
12.38
0.186
0.668
0.003
28.10a
4.98
29.46a
3.89
1.362
0.248
0.023
14.29
4.89
2.86
3.62
102.463*** \0.001
0.643
11.26
5.92
2.29
3.91
46.123*** \0.001
0.447
Ravens CPM score of 2830 is equivalent to a standardised score (UK) of 9.510 years (Raven et al. 1990)
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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.
ASD Group
Task Design
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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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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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
Go/No-Go
False positives
CA
BPVS
Ravens
CARS
-0.429*
-0.394*
0.042
0.012
Inhibitory error
-0.096
-0.175
-0.435*
0.012
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
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
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Table 4 Pearson correlations (N) between inhibitory performance on the three inhibitory control tasks
Flanker (errors)
Flanker (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)
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
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
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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
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
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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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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.
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