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On: 24 December 2014, At: 11:17
Publisher: Routledge
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a b
To cite this article: Joseph H. R. Maes , Paul A. T. M. Eling , Elke Wezenberg , Constance Th. W. M. Vissers & Cees C.
Kan (2011) Attentional set shifting in autism spectrum disorder: Differentiating between the role of perseveration,
learned irrelevance, and novelty processing, Journal of Clinical and Experimental Neuropsychology, 33:2, 210-217,
DOI: 10.1080/13803395.2010.501327
To link to this article: http://dx.doi.org/10.1080/13803395.2010.501327
NCEN
Autism spectrum disorders (ASD) are associated with impaired attentional set shifting, which may reflect
enhanced perseverative responding, enhanced learned irrelevance, and/or reduced novelty processing. We assessed
the contribution of these potential error sources in ASD adults. A total of 17 ASD and 19 matched comparison
individuals first solved a discrimination learning task. Thereafter, the participants faced three types of attentional
shift, specifically designed to isolate the effect of the three possible error sources. ASD participants made more
errors than comparison individuals in a shift implying a choice between a novel relevant stimulus attribute and a
familiar attribute that was previously relevant but now irrelevant. However, they made fewer errors in a shift
involving a choice between a novel irrelevant attribute and a familiar, previously irrelevant but now relevant
attribute. The results in combination suggest that the performance difference, at least in the present shift task, is
caused by reduced novelty processing in ASD participants.
Keywords: Autism spectrum disorder; Attentional set shifting; Learned irrelevance; Perseveration; Novelty processing.
Autism spectrum disorders (ASD) are pervasive developmental disorders, characterized by aberrant social
interaction and communication, repetitive behaviors,
and insistence on sameness (e.g., Frith & Happ, 2005).
It has been proposed that the core deficit involves cognitive dysfunctions, especially those related to frontallobe-mediated executive functions. Recognizing that the
concept of executive function is an umbrella term, Hill
(2004a, 2004b), in evaluating the theory of executive dysfunction in autism, focused on studies on planning, mental flexibility, and inhibition. It was concluded that
deficits in planning and mental flexibility have been
demonstrated, but that the issue is still far from resolved.
A specific problem appears to be that impaired performance on tests for executive functioning may be caused by
other cognitive deficits. Another review of studies using
a wide variety of executive-functioning tests indicated
Since January 2010 C. Th. W. M. Vissers has been at Centre of Excellence for Neuropsychiatry, Vincent van Gogh Institute for
Psychiatry, Venray, The Netherlands. We thank Leontine Kock and Hanneke Bertens for their help in collecting the data.
Address correspondence to J. H. R. Maes, Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour,
Centre for Cognition, P.O. Box 9104, 6500 HE Nijmegen, The Netherlands (E-mail: r.maes@donders.ru.nl).
2010 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business
http://www.psypress.com/jcen
DOI: 10.1080/13803395.2010.501327
restarting and general task performance can be examined separately, Poljac et al. (2010) observed a switching
deficit for children with dyslexia, but not for children
with ASD. Taken together, the evidence for a deficit in
cognitive flexibility is equivocal, and there is a great need
for tasks enabling a more fine-grained decomposition of
processes involved in switching.
The aim of the present experiment was to further
unravel in ASD impaired cognitive flexibility or attentional set shifting, using a novel shift-learning task. A
majority of studies using standard shifting tasks, such as
the WCST, found that ASD participants have more difficulty finding the new rule than do matched comparison
groups (see Geurts et al., 2009, for a review). A common
interpretation of this difficulty is that it reflects perseverative responding: the inability to disengage attention
from, or inhibit responding to, the previously relevant
stimulus attribute that has become irrelevant. However,
continued choice of the wrong attribute after a shift may
just as well be caused by an impaired ability to redirect
ones attention to a previously irrelevant (but currently
relevant) stimulus dimension, a tendency reflecting a
process termed learned irrelevance (Mackintosh, 1975).
In fact, the results of two of our previous studies suggest
that, at least in healthy participants, learned irrelevance
plays a more dominant role than perseveration (Maes,
Damen, & Eling, 2004; Maes, Vich, & Eling, 2006). In
these studies, different types of shift were created in different groups of participants using a two-choice discrimination learning task with multidimensional stimuli.
These shifts enabled the assessment of the separate contribution of perseveration and learned irrelevance. Specifically, in a perseveration (P) group, the previously
relevant stimulus attribute became irrelevant, whereas a
novel stimulus attribute was introduced as now-relevant
attribute. The learned irrelevance mechanism could not
play a role, because the previous irrelevant attribute was
no longer present. Instead, in a learned irrelevance
(LI) group, the previous irrelevant stimulus attribute
became relevant, whereas a novel stimulus attribute
became the irrelevant attribute. Because the former relevant attribute was no longer present, perseverative
responding was impossible. Finally, in a standard shift
group, the previous relevant attribute became irrelevant,
and vice versa, which allowed (at least in principle) both
perseveration and learned irrelevance to affect responding (P+LI shift group). The number of incorrect
choices in the latter group did not differ significantly
from that in the LI group, both of which displayed
more errors than the P group. These results are indicative of learned irrelevance, rather than perseveration,
being the determinant of postshift errors in a standard
shift condition.
To the best of our knowledge, data on learned irrelevance in autism are scarce, and the available data are inconclusive. Two studies that used an attentional-set-shifting
procedure that enabled separating perseveration and
learned irrelevance provided mixed results. Wong,
Maybery, Bishop, Maley, and Hallmayer (2006) examined
set shifting in parents and siblings of ASD individuals
and found that fathers from ASD individuals displayed
211
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MAES ET AL.
METHOD
TABLE 1
Overview of assumptions and corresponding hypotheses
about number of errors in the different types of shift
Assumption concerning
affected process in ASD
Participants
The participants consisted of 23 ASD and 20 healthy
comparison (COMP) individuals. A total of 6 ASD participants and 1 COMP participant were unable to solve
the preshift training phase of the discrimination learning
task within 80 trials. The data from these participants
were excluded from further analysis, because a meaningful interpretation of the shift data is only possible for
participants that were able to solve the initial, preshift
task. The diagnoses of the participants in the ASD group
had been made clinically, according to the DSMIV
(Diagnostic and Statistical Manual of Mental Disorders
Fourth Edition; American Psychiatric Association, 1994),
at the Department of Psychiatry of the Radboud University Nijmegen Medical Centre, The Netherlands, by
means of a thorough psychiatric examination, including
a collateral diagnostic developmental interview (in most
cases with the parents). A Dutch version of the Autism
Spectrum Quotient (AQ; Baron-Cohen, Wheelwright,
Skinner, Martin, & Clubley, 2001; see below) was always
administered during the diagnostic procedure. The ASD
group consisted of 7 individuals with Aspergers disorder,
5 with PDD-NOS (pervasive developmental disorder
not otherwise specified), and 5 with autistic disorder (the
subtypes were determined on the basis of the DSMIV
criteria and psychiatric examination). All ASD participants lived in the Nijmegen region, whereas the matched
COMP participants were selected across The Netherlands,
partly among visitors of the Radboud University
Nijmegen Medical Centre. After being informed about
the basic testing procedures, all individuals agreed to
take part in the study and received a small financial
reward for their participation. The participants were
individually tested in a quiet room, either in the psychiatric
outpatient department or in the home environment.
Demographic and clinical data for each group are shown
in Table 2 (see below for more information on the
neuropsychological test performance).
Hypotheses
Increased perseverative
tendencies
Decreased or increased
learned irrelevance
TABLE 2
Demographic and clinical data
COMP (n = 19: 15M/4F)
Age
Education level
AQtot*
Raven
NLV
WCST N categories
WCST % P errors
SD
Minmax
38.4
3.1
11.7
11.0
89.4
4.8
11.7
14.8
0.9
5.4
1.4
8.0
1.9
5.9
2258
24
021
712
66100
06
424
SD
Minmax
45.2
2.9
34.3
11.0
90.2
4.9
11.4
13.1
1.1
8.7
1.2
7.8
1.8
7.6
2166
14
2047
912
8098
16
527
Note. ASD = autism spectrum disorder individuals. COMP = comparison participants. M = male; F = female. AQ = Autism Spectrum
Quotient. NLV = Dutch version of the National Adult Reading Test. WCST = Wisconsin Card Sorting Test; N categories = number of
finished categories; %P = percentage of perseverative errors. In the ASD group, n = 9 for the Raven and NLV scores. Education
level: 1 = primary school; 4 = university. This scale (14) corresponds to approximately 9, 11, 15, and 18 years of education, respectively.
*p < .001.
213
Next, two practice trials were presented. A picture consisting of a black square (left) and an open circle (right)
on Trial 1 and a picture of a black square (right) and an
open triangle (left) on Trial 2 were presented. After the
participant had made a response to each of these trials
and had received feedback about the correctness of the
responses, the following text appeared:
Now the real experiment will start. Please try to find the
rules as quickly as possible. The rules will be as simple as
in the example. Keep in mind that the rules will change
during the test.
The following stages (Stages 16) were presented sequentially without interruption. Stages 1 and 2 were presented to
Shift 1
Shift 2
Shift 3
Stage 3: Pre-shift
Stage 4: P-shift
Stage 6: P+LI-shift
Rel: Shape
Irrel.: Quantity
Rel: Colour
Irrel.: Shape
Stage 5: LI-shift
Rel: Shape
Irrel.: Quantity
Rel: Quantity
Irrel.: Shape
Figure 1. Example of stimuli presented during Phases 36. Within each phase, stimuli varied in two of three stimulus attributes (color,
shape, or quantity), with one attribute being relevant for solving the task (Rel.) and the other one being irrelevant (Irrel.). The correct
(to-be-chosen) stimulus of each pair is indicated by a plus sign. Spatial location (left or right) of the correct stimulus was counterbalanced within each phase. The nature of relevant and irrelevant attributes and the order of the different types of shift (P, LI, and P+LI)
were counterbalanced using different task versions. To view a color version of this figure, please see the online issue of the Journal.
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MAES ET AL.
25
COMP
ASD
20
15
10
5
0
Pre
P-Shift
LI-Shift
P+LI-Shift
215
in more detail. The aim of the current study was performed in this framework. Specifically, we used a paradigm that allowed us to differentiate between various
factors that may prevent patients with autism to flexibly
shift attentional set: perseveration, learned irrelevance,
and reduced novelty processing.
Relative to their preshift performance, the COMP
group had more difficulty solving the LI shift than the P
shift, whereas the reverse held for the participants in the
ASD group. Both COMP and ASD groups made more
errors during the combined, P+LI, shift than during the
preshift phase. The collective results can be most parsimoniously explained by assuming that, given a choice
between a relatively novel stimulus attribute and a familiar attribute, the ASD participants (regardless of specific
subclass) were more inclined to choose the familiar
attribute than the COMP participants (see first assumption
and corresponding hypotheses in Table 1). This tendency
is favorable for performing the LI shift, in which the
familiar attribute is task relevant, but hinders adequate
performance of the P shift, in which the more familiar
attribute is irrelevant.
The number of errors during the P+LI shift was correlated with the number of LI-shift, but not P-shift, errors,
suggesting that the main process involved in the P+LI
shift was learned irrelevance, a conclusion that is consistent with our previous studies using between- and withinsubject versions of our discrimination learning task
(Maes et al., 2004; Maes et al., 2009; Maes et al., 2006).
Accordingly, the absence of a group difference in errors
during the P+LI shift (also relative to preshift responding: both groups showing more P+LI-shift than preshift
errors) suggests the absence of a difference in learned
irrelevance. Therefore, the group difference regarding
performance during the LI shift can be explained by
assuming a reduced novelty processing in the ASD
group. This same tendency to avoid novel attributes
hampers the ASD participants in the P shift, which suffices
to explain the group difference in P-shift performance.
Therefore, the data also do not demand the presumption
of a between-group difference in perseveration.
The percentage of WCST perseveration errors was
significantly (but relatively weakly) correlated with the
P-shift errors during the DLT, suggesting at least one
common underlying process. According to our interpretation of the joint data described above, this process
might be linked to novelty processing. At the same time,
there was no significant correlation between WCST perseveration and P+LI-shift performance. At first sight,
this is surprising, because the WCST shifts are conceptually identical to the P+LI shift in the discrimination
learning task: Both types of shift imply that a previously
relevant stimulus attribute becomes relevant, and vice
versa. However, given the correlation differences, some
feature of the WCST shifts must make these shifts more
similar to the P than to the P+LI shift in the DLT. Possibly, this is related to the fact that the WCST implies the
presence of 64 different stimuli (target cards), which are
unique with respect to attribute exemplars (but not with
respect to stimulus attributes). Instead, in the P+LI shift
the stimuli remained identical to those presented during
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MAES ET AL.
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