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Attentional set shifting in autism spectrumdisorder: Differentiating between the role ofperseveration, learned irrelevance, and noveltyprocessingJoseph H. R. Maes a , Paul A. T. M. Eling a , Elke Wezenberg b , Constance Th. W. M.Vissers a b & Cees C. Kan ba Donders Institute for Brain, Cognition and Behaviour , Radboud UniversityNijmegen , Nijmegen, The Netherlandsb Department of Psychiatry , Radboud University Nijmegen Medical Centre ,Nijmegen, The NetherlandsPublished online: 05 Aug 2010.

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

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http://www.psypress.com/jcen DOI: 10.1080/13803395.2010.501327

JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY2011, 33 (2), 210217

NCEN Attentional set shifting in autism spectrum disorder: Differentiating between the role of perseveration,

learned irrelevance, and novelty processingAttentional Set Shifting In Asd Joseph H. R. Maes,1 Paul A. T. M. Eling,1 Elke Wezenberg,2

Constance Th. W. M. Vissers,1,2 and Cees C. Kan2

1Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands2Department of Psychiatry, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

Autism spectrum disorders (ASD) are associated with impaired attentional set shifting, which may reflectenhanced perseverative responding, enhanced learned irrelevance, and/or reduced novelty processing. We assessedthe contribution of these potential error sources in ASD adults. A total of 17 ASD and 19 matched comparisonindividuals first solved a discrimination learning task. Thereafter, the participants faced three types of attentionalshift, specifically designed to isolate the effect of the three possible error sources. ASD participants made moreerrors than comparison individuals in a shift implying a choice between a novel relevant stimulus attribute and afamiliar attribute that was previously relevant but now irrelevant. However, they made fewer errors in a shiftinvolving a choice between a novel irrelevant attribute and a familiar, previously irrelevant but now relevantattribute. The results in combination suggest that the performance difference, at least in the present shift task, iscaused 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 devel-opmental disorders, characterized by aberrant socialinteraction and communication, repetitive behaviors,and insistence on sameness (e.g., Frith & Happ, 2005).It has been proposed that the core deficit involves cogni-tive dysfunctions, especially those related to frontal-lobe-mediated executive functions. Recognizing that theconcept of executive function is an umbrella term, Hill(2004a, 2004b), in evaluating the theory of executive dys-function in autism, focused on studies on planning, men-tal flexibility, and inhibition. It was concluded thatdeficits in planning and mental flexibility have beendemonstrated, but that the issue is still far from resolved.A specific problem appears to be that impaired perform-ance on tests for executive functioning may be caused byother cognitive deficits. Another review of studies usinga wide variety of executive-functioning tests indicated

that the perseverative response style in adults withautism, observed in several studies, does not appear tobe related to underlying difficulties in response inhibi-tion, nor can it be attributed to problems in workingmemory (Russo et al., 2007). Yet another recent reviewspecifically focused on cognitive flexibility, taking vari-ous testsfor example, the Wisconsin Card Sorting Test(WCST, Heaton, Chelune, Talley, Kay, & Curtiss, 1993)and the Cambridge Neuropsychological Test AutomatedBattery (CANTAB)and experimental procedures intoaccount and also looking at various subgroups (Geurts,Corbett, & Solomon, 2009). It appeared that no consist-ent evidence for cognitive flexibility deficits in autismcan be found. The authors argued that, to advance thefield, experimental measures must evolve to reflect mech-anistic models of flexibility deficits. Finally, using a task-switching paradigm, with which effects of switching and

Since January 2010 C. Th. W. M. Vissers has been at Centre of Excellence for Neuropsychiatry, Vincent van Gogh Institute forPsychiatry, 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).

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ATTENTIONAL SET SHIFTING IN ASD 211

restarting and general task performance can be exam-ined separately, Poljac et al. (2010) observed a switchingdeficit for children with dyslexia, but not for childrenwith ASD. Taken together, the evidence for a deficit incognitive flexibility is equivocal, and there is a great needfor tasks enabling a more fine-grained decomposition ofprocesses involved in switching.

The aim of the present experiment was to furtherunravel in ASD impaired cognitive flexibility or atten-tional set shifting, using a novel shift-learning task. Amajority of studies using standard shifting tasks, such asthe WCST, found that ASD participants have more dif-ficulty finding the new rule than do matched comparisongroups (see Geurts et al., 2009, for a review). A commoninterpretation of this difficulty is that it reflects persever-ative responding: the inability to disengage attentionfrom, or inhibit responding to, the previously relevantstimulus attribute that has become irrelevant. However,continued choice of the wrong attribute after a shift mayjust as well be caused by an impaired ability to redirectones attention to a previously irrelevant (but currentlyrelevant) stimulus dimension, a tendency reflecting aprocess termed learned irrelevance (Mackintosh, 1975).In fact, the results of two of our previous studies suggestthat, at least in healthy participants, learned irrelevanceplays a more dominant role than perseveration (Maes,Damen, & Eling, 2004; Maes, Vich, & Eling, 2006). Inthese studies, different types of shift were created in dif-ferent groups of participants using a two-choice discrim-ination learning task with multidimensional stimuli.These shifts enabled the assessment of the separate con-tribution of perseveration and learned irrelevance. Spe-cifically, in a perseveration (P) group, the previouslyrelevant stimulus attribute became irrelevant, whereas anovel stimulus attribute was introduced as now-relevantattribute. The learned irrelevance mechanism could notplay a role, because the previous irrelevant attribute wasno longer present. Instead, in a learned irrelevance(LI) group, the previous irrelevant stimulus attributebecame relevant, whereas a novel stimulus attributebecame the irrelevant attribute. Because the former rel-evant attribute was no longer present, perseverativeresponding was impossible. Finally, in a standard shiftgroup, the previous relevant attribute became irrelevant,and vice versa, which allowed (at least in principle) bothperseveration and learned irrelevance to affect respond-ing (P+LI shift group). The number of incorrectchoices in the latter group did not differ significantlyfrom that in the LI group, both of which displayedmore errors than the P group. These results are indica-tive of learned irrelevance, rather than perseveration,being the determinant of postshift errors in a standardshift condition.

To the best of our knowledge, data on learned irrele-vance in autism are scarce, and the available data are incon-clusive. Two studies that used an attentional-set-shiftingprocedure that enabled separating perseveration andlearned irrelevance provided mixed results. Wong,Maybery, Bishop, Maley, and Hallmayer (2006) examinedset shifting in parents and siblings of ASD individualsand found that fathers from ASD individuals displayed

more learned irrelevance errors, but not perseverationerrors, than did fathers from control persons. Turner(1997) reported that, relative to control individuals,learning-disabled ASD participants displayed impairedperformance on a perseveration shift, but not a learnedirrelevance shift, whereas high-functioning ASD indi-viduals did not differ from controls on either type ofshift.

Still another attentional process potentially involvedin attentional set shifting is the processing of novel stimuli.For example, some shift conditions, such as those cre-ated in the P and LI conditions outlined above, imply achoice between a stimulus that was also present in a pre-vious phasethat is, a familiar stimulusand a novelstimulus. The number of errors displayed in each ofthese conditions may be related to the responsivity thatthe participant displays to novel stimuli in general. Spe-cifically, in a P condition, a tendency to not pay muchattention to novel stimuli works against switching to thecurrent relevant stimulus (which is a novel stimulus). Incontrast, in a LI condition, such a tendency works infavor of selecting the postshift relevant dimension, whichwas previously irrelevant, but familiar.

Notably, children with ASD have been shown to dis-play a reduced responsivity to novel stimulifor example,as measured by electrophysiological responses (e.g.,Courchesne, Lincoln, Kilman, & Galambos, 1985;Goodwin et al., 2006; Orekhova et al., 2009; Van Engeland,Roelofs, Verbaten, & Slangen, 1991). This, in turn, mayalso be related to low novelty seeking, a personality traitassociated with autism (e.g., Anckarster et al., 2006).Therefore, it is conceivable that the pattern of respondingin attentional-set-shifting tasks is profoundly affected bya novelty-processing deficit.

In the (very) large majority of prior studies, the cognitiveprocesses related to perseveration, learned irrelevance,and impaired novelty processing are either intermixed ornot examined in a counterbalanced manner with respectto the order in which they are assessed. The presentstudy aims at improving this examination, by assessingin a balanced design the relative contribution of perse-veration, learned irrelevance, and novelty processing tothe performance of ASD participants in attentional setshifting. To this end, we used an adapted version of atask described in Maes and Eling (2009), in which ASDparticipants and healthy comparison participants firstlearned a discrimination task, followed by P, LI, andP+LI shifts (order randomly determined). A number ofhypotheses can be formulated, based on differentassumptions regarding the main cognitive deficit under-lying set-shifting performance in ASD (see Table 1 for anoverview). If impaired novelty processing is the domi-nant process affecting performance in this task, we mustexpect more errors in the P shift for the ASD participantsthan for the comparison group. As outlined above,reduced responding to novelty implies sticking to thenow irrelevant, but familiar, stimulus attribute. At thesame time, we must then also expect fewer errors in theLI shift for the ASD than for the comparison groupbecause a reduced responsivity to the novel stimulusattribute implies attention for the now relevant and

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familiar attribute. The P+LI condition does not imply anovel stimulus attribute. Hence, in this case we mayexpect no group performance difference. Instead, if ASDparticipants mainly differ from the comparison groupin the strength of perseverative tendencies, we mayexpect the former participants to make more errors inthe P shift than the latter, with no difference in LI-shiftperformance. Moreover, at least in healthy partici-pants, learned irrelevance, rather than perseveration, isthe dominant process affecting performance in thecombined P+LI shift. If this also holds for ASD partic-ipants, we must then expect no difference betweengroups with respect to this type of shift. Finally, if themajor difference between the participant groups con-cerns the learned irrelevance process, given the lack ofconclusive data on this issue we may expect eitherfewer or more errors in the LI and the P+LI shift con-ditions in the ASD than in the comparison partici-pants, whereas there will be no difference in the Pcondition.

METHOD

Participants

The participants consisted of 23 ASD and 20 healthycomparison (COMP) individuals. A total of 6 ASD par-ticipants and 1 COMP participant were unable to solvethe preshift training phase of the discrimination learningtask within 80 trials. The data from these participantswere excluded from further analysis, because a meaning-ful interpretation of the shift data is only possible forparticipants that were able to solve the initial, preshifttask. The diagnoses of the participants in the ASD grouphad been made clinically, according to the DSMIV(Diagnostic and Statistical Manual of Mental DisordersFourth Edition; American Psychiatric Association, 1994),at the Department of Psychiatry of the Radboud Univer-sity Nijmegen Medical Centre, The Netherlands, bymeans of a thorough psychiatric examination, includinga collateral diagnostic developmental interview (in mostcases with the parents). A Dutch version of the AutismSpectrum Quotient (AQ; Baron-Cohen, Wheelwright,Skinner, Martin, & Clubley, 2001; see below) was alwaysadministered during the diagnostic procedure. The ASDgroup consisted of 7 individuals with Aspergers disorder,5 with PDD-NOS (pervasive developmental disordernot otherwise specified), and 5 with autistic disorder (thesubtypes were determined on the basis of the DSMIVcriteria and psychiatric examination). All ASD partici-pants lived in the Nijmegen region, whereas the matchedCOMP participants were selected across The Netherlands,partly among visitors of the Radboud UniversityNijmegen Medical Centre. After being informed aboutthe basic testing procedures, all individuals agreed totake part in the study and received a small financialreward for their participation. The participants wereindividually tested in a quiet room, either in the psychiatricoutpatient department or in the home environment.Demographic and clinical data for each group are shownin Table 2 (see below for more information on theneuropsychological test performance).

TABLE 1 Overview of assumptions and corresponding hypotheses

about number of errors in the different types of shift

Assumption concerning affected process in ASD Hypotheses

Impaired novelty processing P shift: ASD > COMPLI shift: ASD < COMPP+LI shift: ASD = COMP

Increased perseverative tendencies

P shift: ASD > COMPLI shift: ASD = COMPP+LI shift: ASD = COMP

Decreased or increased learned irrelevance

P shift: ASD = COMPLI shift: ASD > or or 7.10, ps < .01.

The percentage of perseveration errors made duringthe WCST was significantly and positively correlatedwith the number of P-shift errors during the DLT, = .34,p < .05, but not significantly correlated with the numberof LI-shift or P+LI-shift errors, = .05 and = .19,respectively. The number of P+LI-shift errors was posi-tively correlated with the number of LI-shift errors, = .35,p < .05, but not with the number of P-shift errors, = .10.

DISCUSSION

For some time now, studies have attempted to demon-strate that a deficit in executive functioning is a core fea-ture of autism. Various reviews have shown that resultsare inconclusive (Geurts et al., 2009; Hill, 2004a, 2004b;Russo et al., 2007). While there may be a problem in setshifting, the underlying mechanisms are not clear, andGeurts et al. (2009) have suggested that other paradigmsneed to be developed in order to analyze these problems

in more detail. The aim of the current study was per-formed in this framework. Specifically, we used a para-digm that allowed us to differentiate between variousfactors that may prevent patients with autism to flexiblyshift attentional set: perseveration, learned irrelevance,and reduced novelty processing.

Relative to their preshift performance, the COMPgroup had more difficulty solving the LI shift than the Pshift, whereas the reverse held for the participants in theASD group. Both COMP and ASD groups made moreerrors during the combined, P+LI, shift than during thepreshift phase. The collective results can be most parsi-moniously explained by assuming that, given a choicebetween a relatively novel stimulus attribute and a famil-iar attribute, the ASD participants (regardless of specificsubclass) were more inclined to choose the familiarattribute than the COMP participants (see first assumptionand corresponding hypotheses in Table 1). This tendencyis favorable for performing the LI shift, in which thefamiliar attribute is task relevant, but hinders adequateperformance of the P shift, in which the more familiarattribute is irrelevant.

The number of errors during the P+LI shift was corre-lated with the number of LI-shift, but not P-shift, errors,suggesting that the main process involved in the P+LIshift was learned irrelevance, a conclusion that is consist-ent with our previous studies using between- and within-subject 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 errorsduring the P+LI shift (also relative to preshift respond-ing: both groups showing more P+LI-shift than preshifterrors) suggests the absence of a difference in learnedirrelevance. Therefore, the group difference regardingperformance during the LI shift can be explained byassuming a reduced novelty processing in the ASDgroup. This same tendency to avoid novel attributeshampers the ASD participants in the P shift, which sufficesto explain the group difference in P-shift performance.Therefore, the data also do not demand the presumptionof a between-group difference in perseveration.

The percentage of WCST perseveration errors wassignificantly (but relatively weakly) correlated with theP-shift errors during the DLT, suggesting at least onecommon underlying process. According to our interpre-tation of the joint data described above, this processmight be linked to novelty processing. At the same time,there was no significant correlation between WCST per-severation and P+LI-shift performance. At first sight,this is surprising, because the WCST shifts are conceptu-ally identical to the P+LI shift in the discriminationlearning task: Both types of shift imply that a previouslyrelevant stimulus attribute becomes relevant, and viceversa. However, given the correlation differences, somefeature of the WCST shifts must make these shifts moresimilar to the P than to the P+LI shift in the DLT. Possi-bly, this is related to the fact that the WCST implies thepresence of 64 different stimuli (target cards), which areunique with respect to attribute exemplars (but not withrespect to stimulus attributes). Instead, in the P+LI shiftthe stimuli remained identical to those presented during

Figure 2. Groups mean number of errors (+ SEM) during thepreshift phase and during each of the three types of shift intro-duced after this phase. ASD = autism spectrum disorder indi-viduals. COMP = comparison participants. P = perseveration;LI = learned irrelevance. Note that, relative to the preshiftphase of the task, the ASD participants made significantly moreerrors during the P shift, but not during the LI shift. Instead,again relative to the preshift phase, the comparison participantsmade significantly more errors during the LI shift, but notduring the P shift. Both groups displayed more errors duringthe P+LI shift than during the preshift phase.

Pre P-Shift LI-Shift P+LI-Shift0

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the immediately preceding phase. These differencesimply a larger novelty of the stimuli in the WCST thanin the P+LI shift, but both these tasks still imply astronger stimulus familiarity than the P shift, in which acomplete stimulus attribute, not present in the immedi-ately preceding phase, was suddenly introduced. On thisaccount, the P-shift condition is more sensitive for differ-entiating between ASD and COMP participants than isboth the WCST perseveration measure and the P+LI shiftin the DLT task, which accords with the empirical results.

The majority of studies using the WCST foundimpaired performance in ASD individuals relative tomatched comparison participants (Geurts et al., 2009).The fact that we did not find a difference using this taskmay be due to specific characteristics of our ASD sample.Our sample consisted of ASD adults with normal (ver-bal) intelligence, and at least some studies suggest that,compared to matched controls, this population does notshow impaired WCST performance (e.g., Hill & Bird,2006; Liss et al., 2001; but see, e.g., Ambery, Russell,Perry, Morris, & Murphy, 2006; Lopez, Lincoln,Ozonoff, & Lai, 2005). Moreover, the use of a computer-ized test version (as in our study) may have decreasedfurther the chance of finding differences on a number ofWCST performance measures (e.g., Ozonoff, 1995;Pascualvaca, Fantie, Papageorgiou, & Mirsky, 1998).However, our results suggest that differences might evenbe found in this type of subgroup when using tasks ena-bling a more fine-grained analysis of cognitive compo-nent processes. Conversely, our results also suggest thatin previous studies that did find WCST performance dif-ferences, these differences might reflect cognitive proc-esses other than those typically assumed to be involved(such as perseveration).

So far, we have explained the data in terms of differ-ences in novelty processing, claiming that ASD partici-pants tend to avoid novelty or show reduced noveltyprocessing. However, we cannot exclude the possibilitythat the difference between participant groups involves adifference in preference for familiarity. Both enhancednovelty avoidance and enhanced familiarity preferencewould result in more errors in the perseveration shiftcondition and fewer errors in the learned irrelevanceshift condition. Possibly, responses to novelty and famil-iarity reflect two separate processes, an assumption forwhich there is some support based on neurophysiologi-cal studies (e.g., Xiang & Brown, 1998). Moreover, Gus-tafsson and Paplinski (2004) used an artificial neuralnetwork approach to investigate different theories on thedevelopment of autism. Specifically, using simulationswithin a self-organizing network, they examined to whatextent attention-shift impairments, novelty avoidance,and/or familiarity preference can best model impair-ments in the categorization of two-dimensional stimulithat are characteristic of autism. The authors concludedthat familiarity preference could best account for thedevelopment of abnormal networks, showing autistic-like learning characteristics. However, clearly muchmore experimental and clinical work is required to assesswhich of the two possibilities, novelty avoidance orfamiliarity preference, is the more important one.

Irrespective of these speculations, the present resultssuggest that reduced novelty processing or enhancedfamiliarity preference (a phenomenon implying learningabout stimuli), rather than the more commonly sug-gested attentional-shifting impairment or perseverative-responding mechanisms, may profoundly affect the per-formance of ASD participants in tasks aimed at measur-ing attentional set shifting. More generally, the presentresults underscore the necessity to carefully examinecomponent processes underlying task performance inexecutive function tasks and to develop tasks that can beused for this purpose. Failure to do so may seriouslyundermine the validity of claims about the presenceor absence of impaired cognitive processes in patientpopulations that are made on the basis of test results.

Original manuscript received 19 February 2010Revised manuscript accepted 7 June 2010

First published online 5 August 2010

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