Article review
Psychology & Neuroscience

Performance of Children/Adolescents With Autism Spectrum Disorders in Executive Function: Study of Case Series Fernanda Rasch Czermainski, Cleonice Alves Bosa, Camila Schorr Mina, Maíra Ainhoren Meimes, Monica Carolina Miranda, Daniela Carim, and Jerusa Fumagalli de Salles Online First Publication, August 24, 2015. http://dx.doi.org/10.1037/h0101279

CITATION Czermainski, F. R., Bosa, C. A., Mina, C. S., Meimes, M. A., Miranda, M. C., Carim, D., & de Salles, J. F. (2015, August 24). Performance of Children/Adolescents With Autism Spectrum Disorders in Executive Function: Study of Case Series. Psychology & Neuroscience. Advance online publication. http://dx.doi.org/10.1037/h0101279

Performance of Children/Adolescents With Autism Spectrum Disorders in Executive Function: Study of Case Series

Fernanda Rasch Czermainski, Cleonice Alves Bosa, Camila Schorr Mina,

and Maíra Ainhoren Meimes Universidade Federal do Rio Grande do Sul

Monica Carolina Miranda Universidade Federal de São Paulo

Daniela Carim Santa Casa de Misericórdia do Rio de Janeiro

Jerusa Fumagalli de Salles Universidade Federal do Rio Grande do Sul

Autism spectrum disorder (ASD) is a developmental condition characterized by various cognitive and behavioral symptoms that may be associated, among other factors, with executive dysfunction. However, the relationship between these aspects still needs to be understood in more detail. The present study investigated associations and dissociations in the performance of 11 children/adolescents who were diagnosed with ASD without mental retardation, aged 10 –15 years, in tasks that assessed executive function and working memory. Formal and functional assessment instruments and a questionnaire on developmental history and health-related aspects were used. Performance in tasks that were used for the objective assessment of executive function ranged from preserved to impaired, making the identification of specific performance profiles difficult. In con- trast, functional assessment indicated the presence of important executive dysfunctions in 9 of the 11 cases. The present study stresses the importance of neuropsychological assessment using formal and functional (environmental) tools and mixed-model ap- proaches (cases and groups) to provide a further understanding of executive dysfunc- tion in ASD.

Keywords: autism spectrum disorder, executive function, working memory, neuropsychology, neuropsychological assessment

Autism spectrum disorder (ASD) is a condi- tion that affects children’s overall development and is characterized by the presence of qualita-

tive impairments in social interaction, commu- nication, and behavior (American Psychiatric Association, 2013). Difficulties that involve re- ciprocal interaction, such as establishing eye contact, engaging in collective activities (espe- cially social initiatives), modulation and varia- tion in the expression of love/affection, and stereotyped and rigid behaviors, are usually present in individuals with ASD, and social isolation is common (Wing, Gould, & Gillberg, 2011). However, ASD is a clinically heteroge- neous disorder that has important differences in the manifestation and intensity of symptoms (Towgood, Meuwese, Gilbert, Turner, & Bur- gess, 2009).

The characterization and understanding of the diversity of ASD are based on different theoretical contributions (Bosa & Callias,

Fernanda Rasch Czermainski, Cleonice Alves Bosa, Camila Schorr Mina, and Maíra Ainhoren Meimes, Depart- ment of Developmental Psychology and Personality, Uni- versidade Federal do Rio Grande do Sul; Monica Carolina Miranda, Department of Psychobiology, Universidade Fed- eral de São Paulo; Daniela Carim, Department of Psychia- try, Santa Casa de Misericórdia do Rio de Janeiro; Jerusa Fumagalli de Salles, Department of Developmental Psy- chology and Personality, Universidade Federal do Rio Grande do Sul.

Correspondence concerning this article should be ad- dressed to Fernanda Rasch Czermainski, Gaston Englert, 785/491, CEP: 91360-210, Porto Alegre-RS, Brazil. E-mail: [email protected]

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Psychology & Neuroscience © 2015 American Psychological Association 2015, Vol. 8, No. 3, 000 1983-3288/15/$12.00 http://dx.doi.org/10.1037/h0101279

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2000). A neuropsychological approach was used in the present study because many studies have reported associations between ASD symp- toms and deficits in executive function (EF; Chan et al., 2009; Czermainski, Riesgo, Guimarães, Bosa, & Salles, 2014; Landa & Goldberg, 2005; Robinson, Goddard, Dritschel, Wisley, & Howlin, 2009).

EF comprises several cognitive and behav- ioral processes, including reasoning, problem- solving, anticipation, planning, organization, sequencing, resistance to interference, cognitive flexibility, monitoring, and the ability to deal with new situations (Chan, Shum, Toulopoulou, & Chen, 2008; Jurado & Rosselli, 2007; Rob- inson et al., 2009). An appropriate and adaptive behavior in response to a changing environment results from integrated actions of these compo- nents (Gazzaniga, Ivry, & Mangun, 2006; Ham- dan & Pereira, 2009; Lezak, Howieson, & Lor- ing, 2004). Executive dysfunction may involve important functional impairment that causes significant problems that are related to social adaptation, the organization of daily activities, and emotional control of the individual (Mal- loy-Diniz, de Paula, Loschiavo-Alvares, Fuen- tes, & Leite, 2010).

Recent studies on EF in children and adoles- cents with ASD compared with individuals with typical development found evidence of de- creases in performance in tasks that involve inhibition, planning, verbal fluency, cognitive flexibility, and working memory (i.e., a con- struct that is closely related to EF) in individ- uals who were diagnosed with ASD (Chan et al., 2009; Czermainski et al., 2014; Geurts, Verté, Oosterlaan, Roeyers, & Sergeant, 2004; Kilinçaslan, Motavalli Mukaddes, Sözen Küçükyazici, & Gürvit, 2010; Landa & Goldberg, 2005; Robinson et al., 2009; Van Eylen et al., 2011). However, it is important to note that no consensus has been reached in the literature regarding which executive com- ponents are impaired and which are preserved in ASD. This inconsistency can be partly related to the different methods and tests that are used (Czermainski, Bosa, & Salles, 2013).

Moreover, most studies on EF in ASD in- volve comparisons because clinical and control groups use objective (formal) testing to assess EF. In addition, children and adolescents with ASD may not present impairments in perfor- mance in structured tests of EF despite having

serious difficulties with EF in everyday situa- tions (Chan et al., 2009). This discrepancy be- tween test performance and real-life situations may be related to the characteristics of the gen- erally structured tests, which may mask the real difficulties that are faced by people with ASD (Kristensen, 2006). Therefore, the use of more functional tools that are sensitive to dysfunc- tions that are related to solving daily problems is necessary and desirable because cognitive abilities and personal and social behavior are regulated by EF (Ardila, 2008; Corso, Sperb, Jou, & Salles, 2013).

Most studies in this field have used group- study designs, which usually mask the expected heterogeneity of neuropsychological perfor- mance in individuals with ASD (Czermainski et al., 2014; Towgood et al., 2009). A case series approach should be used to identify these dif- ferences (Schwartz & Dell, 2010). The present study assessed associations and dissociations in EF performance, including working memory, in a case series of children and adolescents who were diagnosed with ASD without mental re- tardation. In addition to a battery of objective assessments (formal), an environmental (func- tional) tool was used to assess EF, the Behavior Rating Inventory of Executive Function (BRIEF; Carim, Miranda, & Bueno, 2012; Gioia, Isquith, Guy, & Kenworthy, 2000), as a complementary measure. In view of the chal- lenges in assessing EF in a natural environment, the BRIEF has strong reliability and appropriate psychometric properties (Carim et al., 2012).

Method

Design

The present study used a case series ap- proach, a method that seeks to understand asso- ciations and dissociations between individuals with a given clinical condition (Schwartz & Dell, 2010). According to Schwartz and Dell (2010), case series complement other methods and involve “systematic assessment of a sample of related patients, with the goal of understand- ing how and why they differ from one another.” Therefore, each participant’s performance in EF and working memory tasks was individually assessed.

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Participants

Eleven children/adolescents (two girls and nine boys) with ASD (six with Asperger syn- drome and five with autism disorder) partici- pated in the study. They were aged 10 –15 years and were students from the fourth to seventh grade of elementary school. The inclusion cri- teria were the following: literate, aged between 10 and 15 years, IQ within the normal range (validated by Raven’s Colored Progressive Ma- trices–Special Scale; Angelini, Alves, Custódio, Duarte, & Duarte, 1999; Raven, Raven, & Court, 1988), and not diagnosed with other psy- chiatric or neurological disorders (data reported by parents or guardians). In addition, the par- ticipants should not have physical or sensory disorders, such as visual or hearing impairment (reported by parents/guardians).

All of the children and adolescents had a confirmed medical diagnosis of ASD according to the criteria of the Diagnostic and Statistical Manual of Mental Disorders, 4th edition, text revision (DSM–IV–TR; American Psychiatric Association, 2002). The participants were se- lected by convenience, and part of the sample was obtained from the database of a program for individuals with ASD, attached to a general hospital. The other participants of the sample were suggested by professionals.

On the basis of the analysis of data from the questionnaire on developmental history and

health-related aspects, of the 11 cases, only 4 were diagnosed early (age 5 years or younger; Cases 1, 2, 6, and 8). With regard to qualitative impairments in ASD, the most common prob- lems (according to parents) were verbal com- munication and understanding of school tasks (communication domain); interaction with classmates and tendency toward isolation (in- teraction domain); and repetitive and inade- quate behaviors, agitation, and aggression (be- havioral domain). Four cases were taking medications: two for anxiety control (Cases 2 and 9) and two for attention deficits (Cases 3 and 11). Table 1 shows the characterization of the cases by sex, age, diagnosis, schooling, and IQ (Raven’s Colored Progressive Matrices– Special Scale).

Instruments

Instrument for assessing developmental history and health-related aspects. This questionnaire was answered by the parents or guardians of the participants. It included ques- tions that were related to the ASD diagnosis (repetitive/restricted interests and behaviors, communication, and social interaction) on the basis of DSM–IV–TR criteria (American Psy- chiatric Association, 2002).

Raven’s Colored Progressive Matrices– Special Scale. This tool was used to measure intelligence (Angelini et al., 1999; Raven et al.,

Table 1 Characterization of Cases With ASD (N ? 11) With Regard to Sex, Age, Diagnosis, Age at Diagnosis, Psychological or Psychiatric Treatment, Use of Medications, School Type, Years of Schooling, and IQ (Raven’s Colored Progressive Matrices—Special Scale)

Case Sex Age

(years) Diagnosis Age at

diagnosis

Psychological or psychiatric

treatment Use of

medications School

type Years of schooling

Raven (?)a

1 F 15 Autism 2 ? ? PR; R 6 27 2 M 14 Autism 3 Y Y PU; R 4 28 3 M 10 Autism 9 Y Y PU; R 3 34 4 M 10 Asperger 10 Y ? PR; R 4 35 5 M 10 Asperger 10 ? ? PR; R 4 29 6 M 11 Autism 5 ? ? PR; R 3 30 7 M 13 Asperger 8 Y ? PR; R 5 28 8 F 10 Asperger 4 Y ? PR; R 3 36 9 M 13 Asperger 6 Y Y PU; I 6 31

10 M 10 Autism 8 ? ? PU; R 3 23 11 M 13 Asperger 10 Y Y PU; I 5 31

Note. F ? female; I ? inclusion; M ? male; PR ? private; PU ? public; R ? regular; Y? yes. a Raven sum of performance scores was adopted because some cases were older than the age established in the Brazilian version of this instrument.

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1988). It consisted of a copy book with 36 figures to be completed. Analyses of the results were performed by summing the scores because some participants were older than the age that was established in Brazilian standards. The par- ticipants with scores that indicated mental re- tardation were excluded from the study.

Stroop test. The Stroop test (Golden, 1978) is a general measure of cognitive flexibility, inhi- bition, and attentional control through the desig- nation of words and colors. It assesses a child’s ability to switch types of responses according to stimuli and inhibit an habitual response with an unusual response. Inhibitory control involves the ability to inhibit irrelevant or learned stimuli or responses in favor of more adaptive responses (Barkley, 2001).

Trail Making Test. The Trail Making Test (TMT; Capovilla, Assef, & Cozza, 2007) is composed of two parts: A and B. Part A eval- uates visual search speed as a control for the interpretation of performance in Part B. Part B involves measures of divided attention, speed of information processing, cognitive flexibility, and alternation (Ashendorf et al., 2008). The task-alternation paradigm (task-switching) in- volves the ability to flexibly switch from one activity to another, which, in addition to cogni- tive flexibility, requires working memory and inhibition to inhibit the behavior of merely fol- lowing the sequence of number or sequence of letters. The extra time that is needed to com- plete Part B compared with Part A reflects the cost of switching from numbers to letters and vice versa (cost-switching). Slower perfor- mance in Part B compared with Part A is con- sidered an indication of impairment in EF (Ash- endorf et al., 2008; Davidson, Amso, Anderson, & Diamond, 2006; Van Der Elst, Van Boxtel, Van Breukelen, & Jolles, 2006).

Rey’s Complex Figure. Rey’s Complex Figure (RCF; Oliveira & Rigoni, 2010 ) is an instrument composed of two figures (A and B) and evaluates visual perception that is involved in the organization of elements that form a whole, planning and the development of strate- gies to perform a task, and the ability of visual memorization and constructive praxis. Planning consists of a complex and dynamic operation in which a sequence of planned actions needs to be constantly monitored, reevaluated, and updated (Jurado & Rosselli, 2007). In the present study, only Figure A from RCF was used. The partic-

ipants were asked to reproduce the figure by copying and 3 min after exposure to the stimu- lus (immediate memory).

Digit span (backward). Four sequences of two to five digits were presented, which had to be repeated by the participant in reverse order, with two trials for each sequence. The maxi- mum score was 28 points.

Pseudowords repetition (span). Sequences of pseudowords (one to four stimuli) were pre- sented and had to be repeated in the same order by the child shortly thereafter. The maximum score was 20 points.

Visuospatial working memory. The ex- aminer indicated progressive sequences of stim- uli (i.e., squares that were randomly arranged on a blank sheet), ranging from two to five, and the child was asked to repeat them, indicating the stimuli on the page, in reverse order (back- ward), immediately after the model was pre- sented by the examiner. The maximum score was 28 points.

Phonemic verbal fluency. The child was asked to evoke words that begin with the letter M for 1 min. Words that were repeated or derived from the same root word were not con- sidered. The score was the number of words that were correctly evoked.

Semantic verbal fluency. The child was asked to evoke names of animals for 1 min. Repeated animals were not considered. The score was the number of words that were cor- rectly evoked. Verbal fluency involves the abil- ity to produce a series of behaviors within a specific framework of rules and has been related to the ability to generate new ideas and behav- iors in a spontaneous manner (Strauss, Sher- man, & Spreen, 2006; Tombaugh, Kozak, & Rees, 1999).

Auditory go/no go. In this task, zero to nine digits were presented to subjects at a rate of one item per second. The subject had to respond “yes” each time he or she listened to one digit, except for the digit 8, for which he or she should remain silent. The score was calculated as the difference between the errors and omissions and maximum number of correct responses (60 points). Tasks 6 –11 were removed from the Child Brief Neuropsychological Assessment Battery (NEUPSILIN-INF; Salles et al., 2011, 2015). The scores of the clinical cases were compared with the means of the normative group of the instrument, and performance was

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considered deficient for scores ?1.5 SD for the number of correct responses (Schoenberg et al., 2006). The comparison table that was used de- pended on whether the subject attended a public or private school.

BRIEF. This instrument assessed EF using 86 items that reflect aspects of the daily life of children and adolescents aged 5–18 years (Ca- rim et al., 2012; Gioia et al., 2000). The parent rating version was used in this study. The par- ents were instructed to select one of the words on a scale (never, sometimes, often) to indicate how often the child/adolescent exhibited the problem behavior. The BRIEF took approxi- mately 10 –15 min to complete. The results of the scale provide a global measure of EF and two indices: Behavior Regulation and Metacog- nition. The Behavior Regulation index included three domains: inhibition, flexibility, and emo- tional control. The Metacognition index in- cluded five domains: initiative, operational memory, planning/organization, organization of materials, and monitoring. The scores are ex- pressed as standard scores and percentile ranks. The values were converted into T scores, thus allowing comparisons of the results of the child with those of the normative group. Because the tool is currently being adjusted to Brazilian standards, comparisons of means were made with data from the normative sample (Carim et al., 2012). Performance was considered poor for scores ?1.5 SD for the number of responses (Schoenberg et al., 2006). The cutoff point of z ? 1.5 or ?1.5 is representative of an index of a deficit in neuropsychological practice (Fon- seca, Salles, & Parente, 2009; Strauss et al., 2006).

Procedures

The study was approved by the Ethics Com- mittee of the Instituto de Psicologia da Univer- sidade Federal do Rio Grande do Sul (UFRGS; no. 2011031). A pilot study was previously conducted with children with typical and atyp- ical development. Participation by the children/ adolescents was voluntary, and consent was given by their parents or guardians, who signed a free informed consent form. The parents/ guardians were contacted by telephone and in- vited to participate in the study. The objectives and procedures of the study were explained and

subsequently discussed in the evaluation meet- ing.

The children/adolescents were individually assessed at the Instituto de Psicologia, UFRGS, or in educational or care institutions that were attended by them. This evaluation was per- formed in a single session that lasted approxi- mately 1 h. While the participants were evalu- ated, their parents or guardians completed the questionnaire on sociodemographic and devel- opmental history and the BRIEF with the help of a research assistant (psychology student). The families of the participants received a syn- thesis of the neuropsychological evaluation.

The evaluations of intelligence, EF, and working memory followed a fixed order of ap- plication for all of the participants. The tools were applied in the following order: Raven’s Colored Progressive Matrices–Special Scale, TMT, Stroop test, RCF (Figure A, copy), pho- nemic verbal fluency, semantic verbal fluency, RCF (Figure A, memory), digit span backward, pseudowords repetition, visuospatial working memory, and auditory go/no go.

Data Analysis

For the objective evaluation, comparisons were made between the raw scores of the clinical cases and performance (means and SD) of the Brazilian normative samples of the NEUPSILIN- INF (Salles et al., 2011). Likewise, for the func- tional assessment of EF, the scores of the clin- ical cases and means (SD) of the Brazilian nor- mative sample of the BRIEF were also compared (Carim et al., 2012; Gioia et al., 2000).

For the analysis of the scores on Raven’s Colored Progressive Matrices–Special Scale (Angelini et al., 1999; Raven et al., 1988) and the RCF (Oliveira & Rigoni, 2010), the stan- dards that were provided by the manuals of these instruments were used as performance parameters. For the analysis of scores on the Stroop test (Golden, 1978) and TMT (Capovilla et al., 2007), the performance of each case was compared with the performance (mean and SD) of a control sample with typical development (n ? 19), the characterization of which is avail- able in Czermainski et al. (2014). An attempt was made to integrate the results of the objec- tive and functional evaluations with the data that were provided by the parents/guardians us-

5EXECUTIVE FUNCTION IN AUTISM SPECTRUM DISORDER

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ing a questionnaire on developmental history and health-related aspects.

Results

The formal neuropsychological evaluation of EF consisted of tests that assessed the following subcomponents: planning, inhibitory control, cognitive flexibility, and verbal fluency. The evaluation also included tests for assessing working memory. Table 2 shows the perfor- mance of each case, presented as raw scores on the Stroop test, TMT, and RCF (Figure A). Table 3 presents the raw scores of each clinical case compared with the respective normative means (SD) by age and type of school (private and public) on the subtests of the NEUPSILIN- INF (Salles et al., 2015). School type (public or private), one of the variables that can be inves- tigated in addition to years of schooling, is associated with socioeconomic status and ped- agogical issues, environmental factors that are related to neurodevelopment (Corso, Sperb, & Salles, 2013). The socioeconomic and cultural levels of private school attendees tend to be higher than those of public school students (Ma- tute Villaseñor, Sanz Martín, Gumá Díaz, Ros- selli, & Ardila, 2009). This variable is widely used in research with Brazilian children because there are qualitative differences between the

educational systems that can influence chil- dren’s performance on cognitive tasks.

In the Stroop test, the performance of eight cases indicated difficulties associated with re- sponse inhibition, represented as an interference score ?0 (Cases 1–5 and 9 –11). Cases 7 and 8 presented scores closer to 0 (.8 and .7), and Case 6 did not complete the task. Compared with the results of the clinical cases, a group of children/adolescents (n ? 19) of the same age range with typical development had an average interference score of .7 (SD ? 3.8) on this test (Czermainski et al., 2014). In the TMT, all of the assessed individuals required at least twice as much time to complete Part B compared with Part A. Five cases took approximately twice as much time (Cases 1, 2, 7, 8, and 11), and six cases needed even more time to complete Part B (Cases 3– 6, 9, and 10). A control group of the same age range with typical development (n ? 19) required an average of twice as much time to complete Part B (117.9 s, SD ? 46.3 s) compared with Part A (52.4 s, SD ? 16.4 s; Czermainski et al., 2014). With regard to errors, seven cases made more errors in Part B than in Part A (Cases 1, 3, 4, 6, 8, 10, and 11), and four cases made no errors in any part of the test (Cases 2, 5, 7, and 9). The latter, although slower, accurately performed the task.

Table 2 Performance of Each Clinical Case With ASD (N ? 11), Presented as Raw Scores or Percentiles in the Stroop Test, TMT, and RCF (Figure A)

Instrument 1 2 3 4 5 6 7 8 9 10 11

Stroop test Words 35 58 50 45 84 60 102 65 51 53 50 Colors 40 50 33 39 61 a 69 34 49 35 34 Color-word 33 32 24 27 41 a 42 23 33 16 26 Interference 14.3 5.1 4.1 6.1 5.7 a .8 .7 8.0 5.0 5.7

TMT Trail A (time) 58 52 66 44 36 96 57 48 65 113 63 Trail A (error) 0 0 0 0 0 0 0 0 0 2 0 Trail B (time) 94 120 337 117 162 228 102 107 178 278 146 Trail B (error) 7 0 2 7 0 11 0 10 0 12 5

RCF (Figure A) Percentile copy ?10 ?10 ?10 70 ?10 ?10 ?10 ?10 ?10 ?10 ?10 Time/copy (min) 7 7 2 3 5 3 8 6 4 2 2 Percentile memory ?10 ?10 ?10 ?10 ?10 ?10 ?10 ?10 ?10 ?10 ?10 Time memory (min) 5 6 2 1 3 1 3 1 1 1 1

Note. TNT ? Trail Making Test; RCF ? Rey’s Complex Figure. a Noncompleted tasks.

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In the reproduction of Figure A from the RCF by copying, 10 cases obtained a percentile score ?10, with the exception of Case 4, who obtained a percentile score of 70 (according to the instructions of the manual). Concerning the repro- duction of memory, all of the cases obtained a percentile score ?10 for performance on the test. According to the instructions of the test (Oliveira & Rigoni, 2010), a percentile score ?10 indicates significant impairment in the abilities of visual perception, constructive praxis, planning, and working memory, expressed as distortions in the shape and location of the figure and the omission

of elements of the figure. Considering the overall deficits in performance on the RCF in the assessed cases (except for Case 4, memory reproduction), a qualitative analysis of the data was performed using the following domains: reproduction strat- egy, planning, constructive praxis, visual percep- tion, and visuospatial working memory. Identify- ing a standard strategy for reproduction was not possible. There was a predominance of attention to detail instead of the whole, disproportionality, designs with stereotypical traits (exaggerated pro- duction lines and repetitive design features), and the occurrence of perseveration in the drawings,

Table 3 Performance of Each Clinical Case With ASD (N ? 11), Presented as Raw Scores and Normative Means (SD) by Age and Type of School (Public and Private) in the Subtests of the Child Brief Neuropsychological Assessment Battery

NEUPSILIN-INF

Clinical Case

1b 2c 3c 4b 5b 6b 7b 8b 9c 10c 11c

Working memory Digit span (backward)

Score 16 24 17 15 28 a 28 18 21 10 7 Mean 22.08 20.34 18.83 20.70 20.70 a 22.08 20.70 20.34 18.83 20.34 SD 4.09 3.89 3.26 3.46 3.46 a 4.09 3.46 3.89 3.26 3.89 ?1.5 SD 15.95 14.51 13.94 15.51 15.51 a 15.95 15.51 14.51 13.94 14.51

Pseudowords repetition

Score 4 4 11 12 14 12 17 12 20 14 …

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