Oct 28, 2003 - receptive vocabulary and verbal mental age (Dunn & Dunn, 1981). .... were a winter jacket (wear, outside) and a teddy bear (play, inside).
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Executive Function Deficits in Children with
Autism
Ellen Bialystok , Simon B. Sherry, Stuart Shanker and
Judith Codd
Keywords: Executive functioning, Autism , Inhibition , Dimensional change card sort task Abstract.
A group of 8-year- old children with autism was compared to a group of tYPically-
develoPing 4-year- olds (approximately matched for verbal mental age)
and to a group of tyPically-develoPing 8-year- olds (matched for chronological age) on a computerized version of the dimensional change card sort task. This task requires children to classif a set of stimuli first by one dimension (pre- switch phase) and then to reclassif the same stimuli by another contrasting dimension (post-switch phase). There were four conditions that difred in the nature of the
demands required by the post-switch phase. Children with autism were both quantitatively and qualitatively difrent from the other children in the post- switch phase. They obtained the lowest scores across the four conditions and were the only group to experience difculty in the simplest condition in which only a single perceptual feature was used to sort the stimuli. Nonetheless, the children with autism solved the rule used to sort the stimuli and the processing
most difcult condition based on a conceptual
classifcation better than the tyPically- develoPing
year- olds, once vocabulary level was controlled. The results are discussed in terms of the role of inhibition in the executive
fUnctioning of children with autism.
For children with autism ,
cognitive deficits are only one aspect of a complex set of symptoms , including ritualism , behavioural rigidity, perseveration , social difficulties narrow focus , impulsivity, and communication impairments (American Psychiatric Association , 1994). The cause of the cognitive deficits in particular is a matter of controversy. Planning and regulation (e. , Adrien et al. , 1995; Hughes , 1996), metarepresentation (e. , Baron- Cohen , 1994; Baron- Cohen , Leslie , & Frith , 1985), inhibitory control and selective attention (e. , Hughes & Russell , 1993; Ozonoff & Strayer 1997), working memory (e. , Boucher , 1981; Boucher & Lewis , 1989), and weak central coherence (e. , Frith , 1989; Frith & Happe , 1994), have all been considered as the locus of the cognitive deficit implicated in the pathogenesis of autism.
Although children with autism present a common, identifiable symptom profie (American Psychiatric Association, 1994), the course , severity, aetiology, and expression of autism is heterogeneous (e. , Pelios & Lund , 2001).
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Two primary hypotheses have been proposed for the cognitive deficits of autism:
the theory of mind (TOM) or " mindblindness " hypothesis , and the executive dysfunction hypothesis. According to the TOM hypothesis , autism is caused by impair-
ments in intuiting and representing mental states on both an intrapersonal and an interpersonal level (Baron- Cohen , 1989 , 1995; Perner , Frith , Leslie , & Leekam 1989). Advocates of this view contend that TOM deficits render the mutual understandings , shared feelings , surmised intentions , and jointly held beliefs characteristic of everyday social relationships and interactions inaccessible to children with autism (Baron- Cohen , 1989). This hypothesis was proposed by Baron- Cohen , Leslie , and
Frith (1985) when they discovered that many children with autism had diffculty in passing the Sally- Anne false belief task (Wimmer & Perner , 1983), a classic measure of TOM. Since then , extensive evidence has accumulated supporting this interpretation (Grant, Grayson , & Boucher , 2001; Happe , 1995; Or & Yirmiya , 1993; Yirmiya Erel , Shaked , & Solomonica- Levi , 1998). There is a substantial literature supporting this view , but several issues challenge the TOM hypothesis. Foremost among these are concerns about reliability and validity. Regarding reliability, not all children with autism are characterized by TOM deficits. For performance on first- order TOM tasks , Dahlgren and Trilingsgaard (1996) report a
10% failure rate among 20 children with autism (age range = 6. 3 to
Prior , Dahlstrom , and Squires (1990) report a 40% failure rate among 20 individuals with autism (age range = 5. 0 to 25. 0); and , Reed and Peterson (1990) report an 85% failure rate among 13 participants (age range = 4. 3 to 29.1). Therefore , some children with autism maintain at least some TOM abilities , undermining its causal role in the disorder. Regarding validity, children with autism demonstrate proficiencies in daily living that would presumably be impossible with their alleged subnormal TOM abilities (Frith , Happe , & Siddons , 1994; Happe , 1994). Some researchers (e. , Happe , 1995; Hobson , 1991) contend that the poor performance of these chil15. 5);
dren on TOM tasks is (in
part) an artefact of the structure of those tasks that chal-
lenges other difficulties that children with autism experience. Even children who pass these tasks may do so by using compensatory strategies that enable them to mimic appropriate responses without fully appreciating the mental states of others (Frith Morton , & Leslie , 1991; Happe , 1993 , 1995). The relation between TOM and autism may be mediated by language ability. A study by Peterson and Siegal (1995) revealed that 17 of 26 patients with prelingual deafness (age range = 8 to 23), all with normal intelligence , failed a simple TOM task. Using more precise linguistic measures , de Viliers (1999) has identified the syntactic ability to use that- complement clauses as the single best predictor of performance in TOM tasks. She speculates that this linguistic achievement might be one factor in the failure of children with autism to solve these tasks. Children with autism frequently
suffer from poorly developed
language competence , and several studies have
demonstrated a positive relation between verbal mental age and performance on TOM tasks (Eisenmajer & Prior , 1991; Leekam & Perner , 1991).
An alternative to the TOM hypothesis is that executive dysfunction is the primary explanation for the cognitive deficits typical of autism (Bryson , Landry, &
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EXECUTIVE FUNCTION IN AUTISM
Wainwright, 1997; Pennington & Ozonoff, 1996). ' Beginning with the seminal investigation of Hermelin and O' Connor (1970) and subsequently replicated in numerous studies , it has been shown that individuals with autism consistently perseverate on a well- known measure of executive dysfunction: the Wisconsin Card- Sorting Task (WCST) (Bennetto , Pennington , & Rogers , 1996; Ozonoff, 1995; Ozonoff & McEvoy, 1994; Ozonoff et al. , 1991; Prior & Hoffman , 1990; Rumsey, 1985; Rumsey & Hamburger , 1988; Shu , Lung, Tien , & Chen , 2001; Szatmari , Tuff, Finlayson Bartolucci , 1990). Zelazo Jacques , Burack , and Frye (2002) extended these results by
showing that severely impaired children with autism perseverated on the dimensional change card sort task , similar to the WCST , but that there was no relation between their performance on the card sort task and TOM tasks. Perseveration on these tasks is regarded as a failure to inhibit a well- rehearsed , prepotent response and a tendency " to persist with a specific strategy, despite corrective feedback" (Ozonoff 1995; Shu et al. , 2001 , p. 170). Executive dysfunction comprises impairments in goal- directed , future- oriented
mental operations that are mediated by the frontal lobes and involve planning, attention , inhibition , cognitive flexibility, working memory, and organized searching (McEvoy, Rogers , & Pennington , 1993; Ozonoff, 1995; Pennington et al. , 1997). Using criteria such as these , Ozonoff andJensen (1999) point out that the majority of studies on children with autism have uncovered evidence of executive dysfunction. battery of tasks administered to children with autism , attention-
In a wide- ranging
deficit/hyperactivity disorder (ADHD), dyslexia , and mild mental retardation Ozonoff et al. (1991) found that only the executive dysfunction measures (i. , the WCST and the Tower of Hanoi) discriminated among groups. Although first- order TOM tasks correctly classified 65% of the 23 children with autism (age range = 8. 0), executive dysfunction measures correctly classified 80% of the children with autism.
to 20.
Recent research has examined the cognitive architecture underlying the executive dysfunction hypothesis in an effort to determine the exact nature of the impairment. Some studies (e. , Noterdaeme , Amorosa , Mildenberger , Sitter , & Minow 2001; Ozonoff & Jensen ,
are related to
1999) have considered how various executive components
different developmental disorders (e.
, autism vs. attention-
deficit/hyperactivity disorder), while others have investigated how the cognitive processes encompassed by the executive dysfunction hypothesis relate to autism. For example , Russell and his colleagues have shown that children with autism struggle with (1) disengaging attention from a focal object (Hughes & Russell , 1993), (2) attentional set- shifting and planning (Hughes , Russell , & Robbins , 1994), (3) choosing between equally weighted alternatives (Russell , Jarrold , & Henry, 1996), (4) encod-
'Unlike Ozonoff , Pennington , and Rogers (1991) or Pennington et al. (1997), we do not consider executive dysfunction to be the primary cause of autism. We do , however , believe executive dysfunction to be an important aspect of autism , functioning as a contributing factor but not as a causal agent. Thus , like Liss et al. (2001), we maintain that " although impaired executive dysfunction is a commonly associated feature of autism... (it) is unlikely to cause (autism)" (p. 261).
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ELLEN BIALYSTOK, ET. AL.
ing rules in a verbal form (Russell Jarrold , & Hood , 1999), and (5) following arbitrary procedures (Biro & Russell , 2001).
Problem solving inevitably requires an intentional focus on some parts of a problem display, some aspects of an associated mental representation , or some portion of
a knowledge base. Identifying the details relevant to a problem entails excluding
irrelevant ones that may appear
to be connected but are actually misleading.
Attention to these irrelevant cues must be inhibited. As Chao and Knight (1997 67) point out: " One of the main functions of the attentional system is to enable cognitive processing to focus on stimulus attributes and ignore or inhibit irrelevant aspects. " The ability to control attention and inhibition in this matter develops significantly in the first five years (Diamond , 2002; Diamond & Taylor , 1996; Gerstad Hong, & Diamond , 1994) and has been credited for a variety of important changes in problem solving (Dagenbach & Carr , 1994; Dempster , 1992; Harnishfeger & Bjorklund , 1993). The dimensional change card sort task , developed by Zelazo and his colleagues (e. , Zelazo & Frye , 1997) and administered to children with autism (Zelazo et al. 2002) provides a means of examining the development of these processes. Children are required to sort a set of cards by one dimension and then to re- sort the same cards by a competing dimension. Thus , the feature that is attended to in the first stage must be ignored in the second. This is difficult for typically- developing children and they are not successful until they are about 5-years old. The error is to continue to sort the cards according to the pre- switch rule.
We explored the problem in more detail by creating a computerized version of the dimensional change card sort task consisting of four conditions , called (1) the colour game , (2) the colour- shape game , (3) the colour- object game , and (4) the function- location game (Bialystok & Martin , in press). The intention was to vary the atten-
tion and inhibition demands of each condition to isolate their role in solving the task. All four conditions required the cards to be reclassified in the post- switch phase , but all four presented different representational (and , therefore , inhibition) problems. One of the conditions , the colour game, was based on a single perceptual feature; two conditions , colour- shape and colour- object, were based on two perceptual features and the fourth condition , function- location , was based on a conceptual feature of the depicted objects. The task difficulty is in re- assigning the stimuli to a new perceptual (or conceptual) category when there is interference from the previously relevant category that needs to be ignored (Bialystok & Martin , in press). The task involves two kinds of inhibition , and the results point out the difference between them. The first response inhibition is the suppression of a practised response between a stimulus and response that needs to be overridden. In a study or association by Jacques , Zelazo , Kirkham , and Semcesen (1999), children observed as a puppet performed the classification and the child simply decided if the puppet sorted correctly or not. This procedure eliminated the need for children to carry out the motor response and therefore eliminated the need to inhibit this response in the post- switch phase. Nonetheless , performance in this modified task was no better than that on the standard version and they concluded that inhibition was not a factor in solving the
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EXECUTIVE FUNCTION IN AUTISM
problem. Similarly, Perner (2001) demonstrated that a control condition that requires reversing the destination of the card following the switch , even in the absence of con-
flicting information from the targets , does not improve children s performance. This is the kind of inhibition required in the colour game. The second conceptual inhibition, is the suppression of attention to a salient but
competing mental representation. This is the inhibition central to the other three conditions- attention has to be shifted from one stimulus feature (e. , colour) to another (e. , shape), even though the initial feature (colour) remains present and salient. The function- location condition is more difficult than the other two because the classifications are not based directly on perceptual features-children need to
identify the objects and then classify them to one of the two categories (Bialystok & Martin , in press). At the same time , the classification itself is difficult, and children make many errors in both the pre- switch and post- switch phases. This condition therefore , requires higher levels of representation ability than the other three to identify, classify, and then re- classify the stimuli. The interpretation that conceptual inhibition is responsible for problem difficulty is supported by research that has assisted children s focus on the relevant dimension in the post- switch
phase. This can be achieved by removing one of the stimulus fea-
tures during the post- switch phase (Bialystok & Martin , in press; Zelazo & Frye , 1997; Zelazo & Jacques ,
1996), questioning children about the feature to which they are
Redbond , Houston- Price , & Cook , 2000), or requiring children to label the relevant dimension on each sorting trial (Kirkham , Cruess , & Diamond , in attending (Towse ,
press). These methods all significantly improve performance and point to the role conceptual inhibition as the primary difficulty in the task. In sum , the dimensional change card sort task includes at least three kinds of processing demands: response inhibition , conceptual inhibition , and representational complexity. The potential to isolate these three processes makes the task a promising test of the kind of executive process that might be impaired in children with autism. If children with autism have a specific impairment in the ability to inhibit attention to prepotent responses (response inhibition) or to competing mental representations (conceptual inhibition), then they wil find the task difficult. Comparing their performance to the different conditions of this problem and to the performance of chil-
dren who are comparable in verbal mental age and chronological
age wil help to
identify one of the core cognitive deficits in autism. The hypothesis was that children with autism would be delayed in their ability to solve the problems requiring conceptual inhibition and that increasing demands on representational complexity would disproportionately disrupt their performance relative to the typically- developing children. In contrast , we expected no relative deficit in their performance on the colour game that depends primarily on response inhibition.
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Method Participants This study compared a group of children with autism and two groups of typically-
developing children on their ability to solve the four conditions of the dimension change card sort task. The first group included 15 children (14 boys and 1 girl; mean age = 8;4 years) who had received a diagnosis of Autistic Disorder (American Psychiatric Association , 1994). The cognitively- matched control group included 184year- olds (9 boys and 9 girls; mean age = 4;7 years) and the age- matched control group included 11 8-year- olds (5 boys and 6 girls; mean age = 8;0 years). Parents , educators , and clinicians verified diagnoses for children with Autistic Disorder and relevant records were consulted whenever possible. Participants were recruited through announcements to service organizations , day care centers , public schools , and special programs in major urban centres. Participants ' socio- economic status ranged from middle class to upper-middle class. All participants had received
their diagnosis of Autistic Disorder from qualified medical experts according to DSM- IV (American Psychiatric Association , 1994) diagnostic criteria. Participants were free from psychoactive medication and no participants were diagnosed with co-
morbid mental disorders.
Instruments Forward Digit Span. The forward digit span was used to assess verbal short- term memory capacity (WISC- R; Weschler , 1974). A sequence ofrandom digits was read twice , and the child was asked to repeat this sequence to the experimenter. The test began with a sequence of three digits , and the number of digits increased by one after
each correct trial. If an error occurred, a second sequence was given at the same length. Testing ended when two consecutive errors were made at the same length. The number of digits in the last correct sequence is the forward digit span score. One child with autism was unable to perform the forward digit span. Ravens Coloured Progressive Matrices (sets A , AB , B). The Coloured Progressive Matrices (Raven , Court , & Raven , 1986) was employed to assess visual- spatial abilities (i. , abilities to arrange spatial perceptions into semantically related wholes) and
to assess comparison- making skils. The task is comprised of 36 pictures (organized as 3 sets of 12 items), each of which has a portion missing. Children must select which of six possible segments correctly completes the picture. The score is the total number of items out of 36 that the child completes correctly. One child with autism was unable to complete the task. Peabody Picture Vocabulary- Revised (PPVT- R). This task was used to assess
receptive vocabulary and verbal mental age (Dunn & Dunn , 1981). The child is asked to select one picture from a set of four that ilustrates the word spoken by the exper-
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imenter. Items become more difficult as testing progresses. Testing continues until the participant makes six mistakes in eight consecutive responses. Raw scores are converted to standard scores by means of normalized tables. Computerized Dimensional Change Card Sort Task. This task included four con-
ditions (games) that were presented to the children on an IBM Thinkpad. A black cover was placed over the keyboard exposing only three keys: the " , the " , and the spacebar. The " W" and " P" keys were selected for their symmetry to the screen and were covered with keycaps clearly marked " X" and " , respectively. The spacebar was covered with a blank white keycap. An animated character appeared on the screen before each new game and each switch phase in order to explain the rules of each game to the child. For each game , the stimulus to be classified appeared in the centre of the screen and children were given instructions about which key to
press. For three of the games , small target stimuli also appeared near the bottom of the screen directly aligned with one of the response keys. This configuration is ilustrated in Figure 1 for each of the four conditions. The child was allowed three practice trials with feedback. If the child was incorrect on one of the practice trials , the rules of the game repeated automatically. This continued until the child was able to perform the three practice trials accurately. The experimenter remained with the child and repeated instructions if the child did not fully understand the task.
a. Colour Task
b. Shape- Colour Task
OR8
c. Colour- Object Task
FIGURE 1: Sample of stimuli for four conditions.
d. Function- Location Task
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a. Colour Game
The children were told to watch for either a blue square or a red square. In the first set of rules , they were told to press the button with the X on it when the red square appeared , and to press the button with the 0 on it when the blue square appeared. There were 10 items in this set , including equal numbers of red and blue squares presented in a random order. Following this , they were told that the rules had now switched and they were to press the X if the blue square appeared , and the 0 if the red square appeared. Again , there were 10 trials , and the squares were presented in a random order. The order of these rules was counterbalanced across all children.
b. Colour- Shape Game This condition , consisting of red and blue circles and squares , was presented as the colour game or the shape game in counterbalanced order. If the colour game was first , the child was told to put all the blue pictures in the box with the blue picture on , and all the red pictures in the box with the red picture on it. Two boxes appeared at the bottom of the screen with the appropriate picture on the box, and the image to be sorted appeared in the middle of the screen. If the boxes had a red square and a blue circle on them , then the pictures to be sorted were red circles and blue squares. The child pressed the button closest to the box that the picture was to be placed in.
The picture visually dropped into the appropriate box. When the first part of the game was completed , the animated figure appeared again and explained the post-
switch rules. In this example , the new game was the shape game, and children were told to place the squares in the box with the square on it , and the circles into the box with the circle on it. Again , there were 10 trials in each of the two games , consisting of five circles and five squares presented in a random order. The programme randomized whether the sorting stimuli were blue circles and red squares or red circles and blue squares.
c. Colour-Picture Game
This task was identical to the previous condition except that the stimuli were red or blue rabbits or flowers.
d. Function-Location Game Unlike the previous three conditions , the sorting dimensions in this game were not perceptual features but functional properties of the stimuli. In the first part of the
"We did not expect any difference between these two conditions but wanted to vary the kind of stimuli that was used.
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EXECUTIVE FUNCTION IN AUTISM
game , the children had to sort the pictures based on whether they would play with the item or wear the item. All 10 pictures clearly belonged to one category or the other (these were: a bicycle , a skateboard , a pail and shovel , a skipping rope , a kite a pair of slippers ,
a nightgown , a bib , ballet slippers , and baby pyjamas). The post-
switch rules required the child to sort the
pictures based on whether these items
belonged inside or outside the house. The target stimuli on the sorting compartments were a winter jacket (wear , outside) and a teddy bear (play, inside). There were items in each of the two games and the order (function and location) was counterbalnaced across subjects. The task demands change across these conditions. The colour game requires response inhibition to resist placing the card in the previously correct manner but no conceptual inhibition because there is only one possible dimension to which to attend , namely colour. Representing this rule is also straightforward. The colourshape and colour object games require response inhibition because , like the colour game , each card must be placed in the box opposite to that used in the pre- switch phase. Additionally, however , these conditions require conceptual inhibition because the dimension that previously defined the correct placement is stil present but is now misleading. The representation demands require the ability to represent two perceptual dimensions. The function- location game has the same demands for response inhibition and conceptual inhibition as do the two previous games , but the representational demands are more difficult because the classification needed is based on functional properties that must be conceptualized from the pictures rather simple perceptual attributes.
The conditions were presented in the fixed order described above but items were randomized within the games. The order of games (e. , colour versus shape) within conditions was counterbalanced. The scores were the number of correct classifications out of 10 in each of the pre- switch and post- switch phases of each game.
Procedures The children were tested individually during two separate sessions that lasted roughly 25 to 35 minutes. Testing sessions were self- paced; breaks were permitted to ensure attention and co- operation. During Session 1 ,
participants received the for-
ward digit span , the Ravens Matrices and the PPVT- R. During Session 2 , participants completed the computerized dimensional change card sort task.
Results Children s scores on the background cognitive measures are reported in Table A one-way ANOVA for digit span scores indicated that the difference between the groups was not significant F(2 42) = 2.
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ELLEN BIALYSTOK, ET. AL.
Table 1: Mean scores and stadard deviatons on cognitive taks by group
Group Digit Span PPVT Autism year- olds year- olds
2 (1.5) 9 (1.6) 5.4 (0.
43. 7
Raw PPVT Standard 50. 8
Ravens
67.4 (14.
117.0 (17.8)
18. 21 (7. 7) 12. 7 (5.
95. 3
105.1 (15.1)
23.1 (5.
(18.4)
(11.0)
(13.4)
PPVT raw scores and standard scores are presented in Table 1. PPVT raw scores reflect absolute performance levels. Although PPVT standard scores (i. , the normalized calculation of PPVT raw scores in terms of the child' s age) are generally
more meaningful because they allow children to be compared across ages , they are not utilized in this study (but are reported in the table) because a standardized conversion according to chronological age is inappropriate for children with autism. Predictably, a one- way ANOVA for group on these standard scores indicated a significant difference 42) = 73. 0001 , and Duncan contrasts revealed that the 4- year- olds and 8 year olds levels were not significantly different from each other but the children with autism scored significantly lower than the other two groups. This is the expected finding, because the purpose of the standard scores is to adjust the raw scores according to age of typically- developing children , making them all
equivalent irrespective of age. A one- way ANOVA on PPVT raw scores was used to determine the relative proficiency of the autistic and typically- developing groups without considering age dif43) = 35. 0001 , and Duncan contrasts revealed three distinct levels. Therefore , the receptive vocabulary of the children with autism is more impoverished than that of typically developing 4-
ferences. This analysis showed an effect of group,
year- olds in absolute (raw) terms. A one-way ANOVA for the total score on the Ravens Matrices revealed an effect 0004 , caused by the difference between the 8-year, 42) = 9.45 of group, olds who scored the highest and the 4- year- olds who scored the lowest. These scores are reported in Table 1. The children with autism performed the same as typicallydeveloping children on the Ravens Progessive Matices , a test of nonverbal intelligence , but were significantly lower than the two control groups in a test of receptive vocabulary knowledge (PPVT).
Results for the card sort task are analysed in two ways. The traditional procedure is to determine a criterion level of performance and classify children as either passing or failing the post- switch phase (Zelazo & Frye , 1997). The present analyses use both the conventional pass- fail categories and a more detailed three- way classification that includes a category for guessing. Second , to obtain a more graded understanding of the results , analysis of variance and covariance was used to determine the effect of group and task differences on performance.
Children were classified into one of three categories based on their score in the post- switch phase of each condition. Children who correctly sorted between 7 and 10 4Another control group consisting of 5-year- olds , not reported in this paper , scored exactly the same as the children with autism on the Ravens Matrices but was even higher than the 4-year- olds included here on the PPVT. Therefore , the 4- year- olds were considered to be a more appropriate control group.
~. 037- 056
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-( .
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EXECUTIVE FUNCTION IN AUTISM items in the post- switch
phase of a particular game were classified as " Correct" responders for that game; children who sorted between 4 and 6 items correctly were called " Chance " responders; and those who correctly classified only 0 to 3 items in were designated as " Perseverators " for that game. This adaptation of the usual binary classification is more precise because it enables a distinction to be made between children who fail because they perseverate and those who fail because the post- switch
they respond at chance. The combination of these two non- correct the usual pass- fail
categories yields
distinction. The number of children in each category for each of
the games is reported in Table 2. The chi- square analyses , conducted for both the two- way and three-way classifi-
cation of responders , indicate the extent to which the distribution across the categories is the same for the three groups. The results are indicated in the table beside the distribution for each condition. Chance responding was rare , and the consistency of the analysis for both the two- and three- category classification suggests that guessing was not a problem , or at least , not a problem specific to only one of the groups. The only distribution to differ from chance is the colour condition in which the children with autism were disproportionately weak. For the other three conditions , the proportion of children passing and failing was the same. The result does not change if the chi- square analysis compares only the children with autism and the 4-year- olds for their likelihood of passing and failing in each condition. Again , the distribution is 01. Therefore , the responses of different only for the colour game , X' (1)= 6. the children with autism are qualitatively different from those in the other two groups for the colour condition but the same as the other children for the other three. Although children passed the other three games in equivalent proportions , their relative success on these games may stil be different. Therefore , analysis of variance was used to provide more detail about children s performance. The mean scores out of 10 for the pre- and post- switch phases of each condition are displayed in Figures 2 and 3 respectively. A 3- way ANOVA for group (3), condition (4), and phase (2) Table 2: Distrbution
of responses by group on the computeried dimensional change card sort tak
Game
Group
Correct (Pass)
Autism years years Colour- Autism years Shape years Colour- Autism years Object years Function- Autism Location years years
Colour
Fail
Chance
Perseverator
Pass- Fail df= 2 12.
4.42
2 3- Category df= 4
002
14.4
5.47
006
~.
p~
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ELLEN BIALYSTOK, ET. AL.
F(2 41) = 18.10 0001 , MSE = 11.39 , condition 0003 , MSE = 5. , and phase F(1 41) = 78.12 0001 , MSE= 12. 27. The group effect was that all three groups were significantly different from each other , with the highest scores obtained by the 8- year- olds and the lowest by the chil-
indicated main effects of group,
F(3
123)
dren with autism. The condition effect indicated that the colour condition was easier than the other three , which did not differ from each other. The phase effect reflected the higher performance on the pre- switch problems.
The children with autism obtained lower scores than the other children in all four conditions. However , the children with autism also had lower receptive vocabulary scores than the other children , and this disadvantage in verbal skil may have been partly responsible for their performance. Therefore , scores were re- examined using
EJ 8 years
4 years
Autism
Colour
Colour- Shape Colour - Obj
ect
FunctionLocation
FIGURE 2. Means scores in pre- switch phase by condition and group.
8 years
4 years Au ti sm
Colour
Colour
Colour
FunctionLocation
FIGURE 3. Means scores in post- switch phase by condition and group.
~.
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EXECUTIVE FUNCTION IN AUTISM
ANCOVA analysis with PPVT Stanine scores as the covariate to establish performance levels that might be obtained assuming relative equivalence of vocabulary lev-
els. The least squares means generated from this analysis for each group and condition are presented in Table 3. Note that these means do not correspond to those plotted in Figures 2 and 3 because they have been adjusted for vocabulary ability. Because the executive processing demands of each condition were different , sep-
arate analyses were conducted for each to focus on group differences in performance of these specific problems when vocabulary knowledge has been controlled. Consequently, there were four two-way ANCOVA (PPVT covariate) analyses for phase (pre- and post- switch) and group. For the colour game , there was an effect of , 39) = 6. 003 , MSE = 4. , in which all three groups were differgroup, ent from each other , the 8- year- olds achieving the highest and the children with autism receiving the lowest scores. The colour- shape game also revealed an effect of 39) = 3. , MSE = 7.88 , this time indicating that both the 8- yeargroup, olds and 4- year- olds (not differing from each other) performed better than the children with autism. The colour- object game produced only a main effect of phase 39) = 13.14 0008 , MSE = 10.17 , in which pre- switch scores were consistently higher than post- switch for all the children. Finally, the function- location condition , MSE = 7.96 , and phase F(1 39) revealed an effect of group, F(2 39) = 4. = 7.27 01. The 4-year- olds obtained the lowest scores with no difference between the 8- year- olds and children with autism. Pre- switch trials were reliably better than post- switch trials for all the children.
Discussion A group of 8- year- old children with autism was compared to a group of typicallydeveloping 4-year- olds who were expected to match for mental age and to a group of typically- developing 8- year- olds who were matched for chronological age on a
computerized version of the dimensional change card sort task. All the children performed similarly on a digit span test, a rough guide to verbal short- term memory capacity. The children with autism were not significantly different from either the 4year- olds or the 8- year- olds on the Ravens Progressive Matrices , although these two groups were different from each other. Scores for receptive vocabulary, however indicated an important disparity between the groups. This is an unfortunate outcome but it may be unavoidable. The standardized receptive vocabulary scores for the
Table 3: Least squares means (PPVT Covarate) and stadard errors on the computeried dimensional change card sort tak by group Colour
Group Autism years years
Pre
Post
9 (. 71) 8.4 (. 52) 6 (.49)
7.1 (.85)
5 (1.2) 5 (. 82)
ColourPre Post
ect ColourPre Post
2 (. 87) 8 (. 63) 9.1 (. 60)
6 (.63) 9.4 (.46) 8 (.44)
2 (1.7) 5.4 (1.2) 7.4 (1.2)
2 (1.7) 7 (1.3) 5.4 (1.2)
F unction- Location Pre Post 8.4 (. 75) 6 (. 55) 7 (.52)
5 (1. 7)
3 (1.2) 2 (1.2)
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year- old children with autism was lower than that for typically- developing 4- yearolds , but matching to a control group younger than 4-years old would not have been reasonable for the other tasks. A group of 3- year- olds , for example , may have provided a better match in receptive vocabulary for the children with autism ,
but they would not have provided a match on the Ravens Progressive Matrices and their performance on the experimental sorting task would likely have been unreliable , if they could do it at all. Our solution , therefore , was to use analysis of covariance to statis-
tically control for initial differences in levels of vocabulary knowledge. The data were examined by means of chi- square analysis , ANOVA , and ANCOVA to investigate different aspects of the results. First, the chi square analyses compared the proportion of children who passed or failed each of the conditions across groups. This proportion was only different for the colour game , where a significantly larger group of children with autism failed the post- switch phase. This pat-
tern indicates a qualitative difference in the way in which children in these three groups solve this problem. Importantly, the chi- square analysis of the three-way classification indicated that very few of the children were chance responders , although the majority of guessers were children with autism. Second , the ANOVA analysis showed that the scores of the children with autism were lower than those of all the other children across all the conditions. The main effect of group also indicated the superiority of the 8- year- olds for all the conditions. This was a difficult task , especially for the children with autism. Finally, the ANCOVA provides more detailed understanding by comparing the performance of each group on each condition controlling for initial differences in
vocabulary knowledge. These results showed that the children with autism performed lower than the other children in both the colour game and the colour- shape game , but were not lower on the other two games. In fact , these children were better than the 4- year- olds in the function- location condition. Once corrections for vocabulary knowledge have been made , the children with autism were only slightly disadvantaged on these semantically complex conditions based on more sophisticated representations. Therefore, initial deficits in language proficiency account for some but not all of the diffculty that children with autism experience on this task. Evidence that children with autism score poorly relative to typically- developing children on a cognitive task is not surprising; it is more important to identify the specific deficit responsible for that poor performance. Consider the three processes involved in solving this task: representation , response inhibition , and conceptual inhibition. The 4-year- olds experienced difficulties with representation and were particularly challenged by the function- location game; the children with autism experienced difficulties with response inhibition even though the colour game was easy for the other children; and all the children , including the 8-year- olds , found the conceptual inhibition demands to be challenging, as even this oldest group did not achieve ceiling performance on the most difficult condition. Three aspects of this pattern are striking. First , children with autism are distin-
guished by their difficulty in inhibiting a familiar or learned response association to a single perceptual cue as in the colour game. This finding is congruent with a grow-
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ing body of research (e. , Bryson , Landry, & Wainwright , 1997) implicating executive function deficits , especially inhibitory control (e. , Hughes & Russell , 1993), in the pathogenesis of autism. Second , when initial vocabulary levels were controlled children with autism performed as well as typically- developing 8-year- olds and significantly better than typically- developing 4- year- olds on a problem that was based on a complex conceptual classification. Hence , the ability of children with autism to represent conceptual information ,
once vocabulary had been adjusted ,
was not
impaired. This optimistic interpretation is confirmed by their performance on the Raven s Matrices. Together , these results locate the source of difficulty for the children with autism in the need for inhibition , particularly for response inhibition. Finally, the surprising finding that typically- developing 8- year- olds continue to perseverate on the dimensional change card sort task , especially in its more complex
development of inhibitory executive processes is more protracted than previously believed (e. , Zelazo , Frye , & Rapus
representational forms , suggests that the
1996). In the executive dysfunction perspective on autism , inhibitory control is a primary source of cognitive impairment (e. , Hughes & Russell , 1993). Our results corroborate this view but point to a particular deficit in response inhibition that is not evident in the other typically- developing children. Children with autism also have less control over conceptual inhibition than do typically- developing children , but
only when the conceptual basis for the classification is easy (colour- shape game). As that conceptual basis becomes slightly richer , requiring more detailed mental repre-
sentations , the children with autism do just as well as the other children if language proficiency is taken into account (colour- object game) and better than 4-year- olds if the classification is based on functional categories instead of perceptual ones (function- location game). Future efforts aimed at specifying the exact inhibitory executive
children with autism may want to distinguish between response inhibition and conceptual inhibition so as to enable precise conclusions. The results point to an executive deficit in children with autism in which they have difficulty in disengaging from a simple ongoing cognitive routine and making an adjustment in that routine. Children with autism are compromised both in the extent to which inhibition processes are functional and in the nature of inhibition processes that are impaired. These children not only experienced deficits in performance on all tasks requiring conceptual inhibition , but also experienced deficits in a condition requiring response inhibition. These inhibition processes are central to the executive system that is responsible for planful and controlled problem solving. Such executive function deficits may contribute to social communication impairments in children with autism. Unable to flexibly and efficiently disengage and coordinate attention , the rapid shifts and constant changes that typify social communication confuse children with autism (e. , Courchesne et al. , 1999; McEvoy processes impaired in
et al. ,
1993).
Autism is a complex disorder influencing many domains , including social difficulties , behavioural rigidity, and communication impairments. Although our results address one notable aspect (i. , inhibition of attention) of one important component
),
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ELLEN BIALYSTOK, ET. AL. (i. , cognitive deficits) of the symptomatology of children with autism , they do not explain the potentially simultaneous involvement of other impairments in different domains. It may be that cognitive deficits (such as inhibition of attention) underlie social difficulties (such as mindblindness) or that social difficulties encourage cognitive deficits or that cognitive deficits and social difficulties emerge in a complex dialectical transaction (Fine , Lumsden , & Blair , 2001). Clearly, no single factor or unitary theory is likely to adequately explain the severity and complexity of autism.
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Address ftr Correspondence:
Ellen Bialystok Department of Psychology York University 4700 Keele Street Toronto,
Ontario, M3J
Canada Email: ellenbr:yorku.
Authors ' Note: This research was supported by a grant (A2559) awarded to the first author from the Natural Sciences and Engineering Research Council of Canada (NSERC).
