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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-
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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 9 Mean 15.00 14.55 13.33 13.73 13.73 15.04 15.00 13.73 14.55 13.33 14.55 SD 3.04 2.98 3.10 3.08 3.08 2.97 3.04 3.08 2.98 3.10 2.98 �1.5 SD 10.44 10.08 8.68 9.11 9.11 10.59 10.44 9.11 10.08 8.68 10.08
Visuospatial working memory
Score 7 5 19 23 28 a 18 20 28 4 10 Mean 24.85 24.44 22.83 24.70 24.70 a 24.85 24.70 24.44 22.83 24.44 SD 3.33 3.69 4.56 3.30 3.30 a 3.33 3.30 3.69 4.56 3.69 �1.5 SD 19.86 18.91 15.99 19.75 19.75 a 19.86 19.75 18.91 15.99 18.91
Verbal fluency Phonological
Score 3 7 5 8 9 a 12 6 3 6 5 Mean 10.77 9.94 7.87 8.43 8.43 a 10.77 8.43 9.94 7.87 9.94 SD 3.12 3.68 3.01 3.36 3.36 a 3.12 3.36 3.68 3.01 3.68 �1.5 DP 6.09 4.42 3.36 3.39 3.39 a 6.09 3.39 4.42 3.36 4.42
Semantic Score 11 7 5 16 11 19 19 14 14 14 11 Mean 18.73 16.97 14.70 16.63 16.63 17.28 18.73 16.63 16.97 14.70 16.97 SD 4.73 5.13 3.90 5.11 5.11 4.30 4.73 5.11 5.13 3.90 5.13 �1.5 SD 11.64 9.28 8.85 8.97 8.97 10.83 11.64 8.97 9.28 8.85 9.28
Auditory go/no go (total) Score 57 45 a 58 60 a 52 59 52 47 a
Mean 58.54 58.28 a 55.67 55.67 a 58.54 55.67 58.28 55.55 a
SD 1.67 1.48 a 5.93 5.93 a 1.67 5.93 1.48 3.32 a
�1.5 SD 56.04 56.06 a 46.78 46.78 a 56.04 46.78 56.06 50.57 a
a Noncompleted tasks. b Standards for private school. c Standards for public school.
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suggesting possible difficulties in inhibitory con- trol and cognitive inflexibility.
Working memory was assessed using the digit span (backward), pseudowords repetition, and visuospatial working memory subtests of the NEUPSILIN-INF (Salles et al., 2011). In the digit span (backward) subtest, only two partic- ipants reached the maximum score (28 points; Cases 5 and 7). Cases 2 and 9 obtained 24 and 21 points, respectively, performance that is con- sidered above the mean of the normative group. More than half of the clinical cases obtained performance below the mean of the normative group (Cases 1, 3, 4, 8, 10, and 11), and only three of these participants had performance � �1.5 SD from the normative sample mean (Cases 4, 10, and 11), suggestive of a deficit. Case 6 failed to complete the task.
In pseudowords repetition, only one partici- pant obtained the maximum score in the task (20 points; Case 9). Three other participants reached performance above the normative mean (Cases 5 and 10, with 14 points each, and Case 7, with 17 points). The other cases obtained performance below the normative range (Cases 1– 4, 6, 8, and 11), and two cases obtained scores �1.5 SD (Cases 1 and 2), suggestive of a deficit. In the visuospatial working memory subtest, two participants reached the maximum score (28 points; Cases 5 and 9). The other participants obtained performance below the normative mean (Cases 1– 4, 7, 8, 10, and 11), and five of these cases had scores � �1.5 SD from the normative sample mean (Cases 1, 2, 7, 10, and 11), suggestive of a deficit. Case 6 failed to complete the task.
In the phonological verbal fluency task, only one participant had a score above the normative mean (Case 7 evoked 12 words). The other cases had scores below the normative mean (Cases 1–5 and 8 –11); of these, two cases ob- tained scores � �1.5 SD from the mean (Cases 1 and 9), suggestive of a deficit. Despite under- standing the task, Case 6 has been unable to complete the task. In the semantic verbal flu- ency task, the participants were asked to evoke the names of animals. Only two of the cases had performance above the normative mean (Cases 6 and 7 evoked 19 words each). The other cases had scores below the mean (Cases 1–5 and 8 –11), and three of them had performance � �1.5 SD (Cases 1–3), suggestive of a deficit.
In the auditory go/no go subtest of the NEUPSILIN-INF (Salles et al., 2011), only one case obtained the maximum score (Case 5). Two other cases obtained scores above the nor- mative mean (Cases 4 and 8, with 58 and 59 points, respectively). The other cases obtained scores below the normative mean (Cases 1, 2, 7, 9, and 10); of these, three cases obtained scores � �1.5 SD (Cases 2, 7, and 9), sugges- tive of a deficit. Cases 3, 6, and 11 did not complete the task.
Predominantly lower overall performance in all of the tasks was identified in only two cases (Cases 1 and 3). They showed performance that was suggestive of impairment in inhibition (Stroop test), cognitive flexibility (TMT), and planning (RCF). In the NEUPSILIN-INF sub- tests, Case 1 had lower performance in two working memory tasks (pseudowords repetition and visuospatial working memory) and the ver- bal fluency tasks. Case 3 presented performance deficits in only the semantic verbal fluency task. In the other NEUPSILIN-INF tasks, the perfor- mance of both cases was below the normative sample mean. The attention deficits of Case 3 may be related to the lower overall performance that was presented by this case (information provided by the parents).
Another subgroup of cases also had perfor- mance that was indicative of important deficits in several tasks (Cases 2, 9, 10, and 11). How- ever, these cases also showed preserved perfor- mance in other tasks, presenting heterogeneous profiles of cognitive performance. Case 2 showed deficits in six tasks (Stroop test, RCF, pseudowords repetition, visuospatial working memory, semantic verbal fluency, and auditory go/no go). Case 9 showed deficits in four tasks (Stroop test, TMT, phonological verbal fluency, and auditory go/no go). Case 10 showed deficits in five tasks (Stroop test, TMT, RCF, visuospa- tial working memory, and auditory go/no go). Case 11 showed deficits in five tasks (Stroop test, RCF, digit span, pseudowords repetition, and visuospatial working memory).
Interestingly, Case 6 did not complete five tasks (Stroop test, digit span, visuospatial work- ing memory, phonological verbal fluency, and auditory go/no go), which differed from the other cases. This case also presented impaired performance in the tasks that were completed, except for the semantic verbal fluency task, in
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which performance was above the normative sample mean.
Cases 4, 5, 7, and 8 appeared to have gener- ally preserved neuropsychological performance. Case 4 presented deficits only in three tasks (Stroop test, RCF-memory, and digit span). Case 5 presented deficits in only two tasks (Stroop test and RCF). Case 7 presented deficits in three tasks (RCF, auditory go/no go, and visuospatial working memory). Case 8 pre- sented low performance in only one task (RCF).
The results of the functional measure of EF using the BRIEF, parent rating version (Carim et al., 2012; Gioia et al., 2000), are described in Table 4, which presents the raw scores for each participant in the two BRIEF indices and re- spective domains compared with the mean (SD) of the Brazilian normative sample of the instru- ment, which is composed of 155 subjects of the same age group as the clinical cases (Carim et al., 2012).
The Behavior Regulation index includes three domains: inhibition, flexibility, and emo- tional control. In the inhibition domain, only two cases had scores lower than the mean of the normative group (Cases 1 and 7). The other cases were above the mean, and seven cases had scores �1.5 SD for this domain (Cases 2, 4, 6, and 8 –11), suggestive of a deficit. In the flexi- bility domain, only one case (Case 7) had a score that was below the normative sample mean. The other cases had scores above the mean, and four cases had scores �1.5 SD
(Cases 2, 8, 10, and 11), suggestive of a deficit. In the emotional control domain, three cases were below the mean (Cases 1, 5, and 7), and all of the other cases obtained scores above the mean, with Cases 3 and 9 obtaining scores �1.5 SD, suggestive of a deficit. These results indi- cate that eight cases obtained scores that indi- cated EF impairment in the Behavior Regula- tion index.
The Metacognition index includes five do- mains: initiative, operational memory, plan- ning/organization, organization of material, and monitoring. In the initiative domain, only two cases had scores below the normative sample mean (Cases 1 and 7). The other cases had scores �1.5 SD from the mean, suggestive of a deficit. The same results were observed in the operational memory domain, except for Case 3, who had a score above the mean but did not reach 1.5 SD above the mean. In the organiza- tion and planning domain, only one case had a score below the mean (Case 7). The other cases had scores �1.5 SD from the mean (suggestive of a deficit), except for Case 1, which had a score only above the mean, but did not reach 1.5 SD above the mean. In the material organization domain, five cases had scores below the mean (Cases 1, 2, 3, 7, and 9). The other cases were above the mean, and Cases 4, 8, 10, and 11 had scores �1.5 SD from the mean, suggestive of a deficit. In the monitoring domain, two cases had scores below the mean (Cases 5 and 7). The other cases had scores �1.5 SD from the mean
Table 4 Comparison of Individual Raw Scores of the Clinical Cases With ASD (N � 11) in the BRIEF–Parent Rating Version and the Mean (SD) of the Brazilian Normative Sample of the Instrument
BRIEF
Clinical case (n � 11) Normative group
(n � 155)
1 2 3 4 5 6 7 8 9 10 11 M (SD) �1.5 SD
Inhibition 10 20 18 22 16 22 13 21 26 28 24 14.0 (3.0) 18.5 Flexibility 16 19 16 14 14 16 8 17 16 18 20 12.0 (2.8) 16.2 Emotional control 12 20 24 22 13 18 11 20 25 21 16 15.6 (4.6) 22.5 Behavior regulation 38 59 58 58 43 56 32 58 67 67 60 41.6 (9.1) 55.3
Initiative 11 24 19 20 18 16 10 19 19 22 18 11.8 (2.6) 15.7 Operational memory 11 27 18 27 23 25 13 22 21 24 25 14.2 (3.6) 19.6 Organization and planning 17 26 28 31 28 34 12 30 26 33 23 16.0 (3.6) 21.4 Material organization 6 8 6 18 13 14 6 17 10 18 18 10.7 (3.4) 15.8 Monitoring 19 15 17 19 11 23 11 21 17 18 20 12.1 (2.7) 16.2
Metacognition 64 100 88 115 93 112 52 109 93 115 104 65.0 (12.7) 84.1 Overall executive functioning 102 159 146 173 136 168 84 167 160 182 164 106.7 (19.5) 136.0
Note. BRIEF � Behavior Rating Inventory of Executive Function.
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(suggestive of a deficit), except for Case 2. These results indicate that nine cases had scores that indicated impairment in the Metacognition index. The values of the Global Executive index indicated that 9 (Cases 2– 6 and 8 –11) of 11 cases had scores that indicated EF impairment.
Discussion
The analysis of the results demonstrated the heterogeneous nature of sample performance in the formal tasks of EF and working memory assessment, revealing the presence of associa- tions and dissociations (some performance was impaired, and other performance was pre- served) that varied according to the tasks. We were not able to identify a characteristic profile of preserved and impaired cases but rather im- portant performance variability. These results are consistent with previous findings, showing similar performance variability in individuals with ASD in EF tasks (Chan et al., 2009; Czermainski et al., 2014; Manjiviona & Prior, 1999; Robinson et al., 2009; Towgood et al., 2009).
On the basis of this performance variability, four subgroups were identified: (a) predomi- nantly lower overall performance (Cases 1 and 3), (b) deficits in many neuropsychological tasks (Cases 2, 9, 10, and 11), (c) neuropsycho- logical performance that was fairly preserved with deficits in a few tasks (Cases 4, 5, 7, and 8), and (d) a case that did not complete the assessment battery (Case 6). Of the six cases that showed the poorest neuropsychological performance (Cases 1–3 and 9 –11), four were taking medications: two for anxiety control (Cases 2 and 9) and two for attention deficits (Cases 3 and 11). Therefore, the most impaired neuropsychological profile appeared to be con- sistent with the behavioral profile, justifying drug prescription.
In Case 1, a profile of simple performance dissociation was observed. This case presented a series of neuropsychological deficits in formal neuropsychological tasks. However, no other evident difficulties were found in the functional assessment (BRIEF), revealing poor consis- tency between the results of the formal assess- ment and parental perception of their child’s difficulties. Interestingly, this case was the one with the earliest diagnoses (at 2 years of age), suggesting a greater severity of ASD compared
with the other cases. However, this case re- ceived no psychological or psychiatric treat- ment and thus was not prescribed any medica- tions. This case also attended few years of school (the child was removed from school by the parents), which may indicate parental disin- vestment, a lack of understanding of the child’s condition, and/or difficulties adapting the child to the school environment. With regard to pa- rental perception on the child’s characteristics, some studies have shown that this perception may be more related to the impact of the child’s condition on the family and thus psychosocial factors that are associated with family dynamics than related to actual symptoms that are mani- fested by the child (Zablotsky, Bramlett, & Blumberg, 2015). Therefore, Case 1 had impor- tant difficulties that involved EF, despite not being under psychological or psychiatric treat- ment, and did not attend school (parent’s deci- sion).
Case 3 and Cases 2, 9, 10, and 11 (second subgroup identified above) showed greater con- sistency between the formal and functional as- sessments (which indicated important impair- ments), showing consistency between the profile observed in the tests and parental per- ception of the development of their children.
Cases 5 and 7 (third subgroup identified above) presented preserved profiles in both the formal and functional assessments. In addition to Cases 4 and 8, the four cases in this subgroup were diagnosed with Asperger syndrome. Al- though the DSM–5 (American Psychiatric As- sociation, 2013) no longer includes this diag- nostic category, the behavioral phenotype of these individuals is more preserved in the cur- rent autistic spectrum (McPartland, Reichow, & Volkmar, 2012). Moreover, Cases 4 and 5 were diagnosed with ASD/late Asperger syndrome at 10 years of age. This late diagnosis may be due to the milder expression of cognitive and be- havioral symptoms, which prevented the early identification of this disorder. Three of these cases were undergoing psychological or psychi- atric treatment (Cases 4, 7, and 8), and this can also be associated with more preserved perfor- mance in neuropsychological assessments. However, despite their few neuropsychological deficits in formal tests (e.g., Case 8 showed a deficit in only one neuropsychological task), the performance of Cases 4 and 8 in the functional assessment (BRIEF) suggested executive dys-
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function. This discrepancy can be associated with greater parental involvement in their chil- dren’s development, although the history and performance of these subjects indicated the oc- currence of milder cognitive and behavioral symptoms compared with the other cases in this study.
Case 6 also showed impaired performance in the completed tasks but failed to complete five tasks and showed normal performance on the verbal fluency task with semantic criteria. One possible explanation for such discrepancy is that, according to the parents’ report, this case presented restricted and repetitive interests, characterized by, among other aspects, a predi- lection for animal names, which likely facili- tated the case’s performance. The case was un- dergoing no psychological or psychiatric treatment and consequently did not take any medications. This case illustrates the impor- tance of clinical assessment and the collection of information by the families of individuals with ASD to complement neuropsychological evaluations.
Of note, only two cases (Cases 7 and 8) showed satisfactory performance in the Stroop test. The performance of Case 7 in this measure was consistent with the results that were ob- tained in the inhibition and flexibility domains of the functional assessment (BRIEF), which were considered preserved. Nevertheless, no consistency was found between these measures for Case 8, in which this case obtained satisfac- tory performance in the Stroop test, and scores that indicated deficits in the inhibition and flex- ibility domains of the functional assessment.
Despite the variability of performance of the cases in most of the objective measures, the RCF scores were very similar (except for Case 4 in memory reproduction). A qualitative as- sessment of the RCF scores revealed perfor- mance that was lower than expected and not related to mental deficits in any of the 11 cases. Although identifying a pattern of strategies of reproduction of the figure that was common to all of the cases was not possible, the profiles of the cases appeared to indicate impairment in EF (planning and working memory), constructive praxis, visual perception, and of the ability of central coherence (Happé & Frith, 1996; Hill & Frith, 2003). Difficulties in planning were re- flected by failures in the process of sequencing and distribution of the elements of the repro-
duced figure. Thus, there was a tendency to start the test by copying a secondary element (e.g., a circle) and not the element that underpins the figure as a whole (e.g., rectangle), resulting in disorganized reproduction. Individuals with ASD appear to show an atypical pattern of visual processing, in which details are perceived rather than the figure as a whole (gestalt). This is the opposite of the typical pattern of visual processing (Schlooz et al., 2006). However, Chan et al. (2009) did not find any differences in RCF performance between an ASD sample and controls.
The majority of the assessed cases showed difficulty in tasks that involved inhibition, flex- ibility, planning, and working memory, which was consistent with other recent studies (Hill & Bird, 2006; Kenworthy, Yerys, Anthony, & Wallace, 2008; Lopez, Lincoln, Ozonoff, & Lai, 2005; Ozonoff et al., 2004). Three extensive reviews indicated the presence of deficits in these components of EF in individuals with ASD (Hill, 2004; Pennington & Ozonoff, 1996; Sergeant, Geurts, & Oosterlaan, 2002). Pen- nington and Ozonoff (1996) reported that, among several measures of EF, cognitive in- flexibility and poor planning were more fre- quent in ASD compared with other EF measures in other developmental disorders (attention- deficit/hyperactivity disorder [ADHD], conduct disorder, and Tourette’s syndrome). Sergeant et al. (2002) and Hill (2004) reported similar find- ings. However, in Hill’s review, the results also suggested deficits in inhibition and generativity in ASD individuals. A recent review of studies that evaluated only children with ASD (Czermainski et al., 2013) found that inhibition, planning, flexibility, generativity, and working memory were the main EF components that are impaired in ASD. According to the literature, such deficits can be associated with common features of ASD. High levels of impulsivity, the need for sameness, a strong liking for repetitive behaviors, difficulties in initiating new nonrou- tine actions, difficulty in switching between tasks, a lack of self-regulation and self- monitoring, and inflexibility in thought and ac- tions are some of these features (Robinson et al., 2009; Wing et al., 2011).
In contrast to the formal neuropsychological evaluation, the assessment of EF using a func- tional measure (BRIEF; Carim et al., 2012; Gioia et al., 2000) demonstrated that most of the
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cases had significant dysfunction in their daily lives, as reported by their parents. According to the Global Executive index, the scores that were obtained by 9 of the 11 cases indicated overall impairment in EF, consisting of the Behavior Regulation and Metacognition indices. The dis- crepant results that were found for the formal and functional assessments reinforce the need to observe executive functioning using multiple sources. Gioia et al. (2000) explained that the formal assessment of EF is usually conducted in a quiet room with one highly supportive exam- iner who prompts performance. In general, in this structured arrangement, the examiner pro- vides the plan, organizes the activities, and pres- ents one task at a time, supporting executive control. In this context, children with ASD re- spond well to highly structured settings and explicit rules; therefore, they often perform bet- ter on structured (formal) measures than on executive control-related tasks in more natural settings (Kenworthy et al., 2008). In fact, the present results showed that the subjects tended to have more evident executive dysfunction in the functional measure (BRIEF) than in the formal tasks when a complex mixed pattern (some components impaired and others spared) of deficits in EF was observed.
Nevertheless, Kenworthy et al. (2008) em- phasized the fact that there are few studies on formal and functional assessments of EF with ASD individuals. Consistent with our study, investigations that used the BRIEF reported higher executive-control deficits in ASD com- pared with normative data, typical controls, and children with ADHD (Gioia, Isquith, Kenwor- thy, & Barton, 2002; Kenworthy et al., 2005; Winsler, Abar, Feder, Schunn, & Rubio, 2007). Children with ASD appear to have unique def- icits in flexibility based on a comparison of BRIEF profiles across groups of children with different developmental and acquired disorders (Gioia et al., 2002). These results show that the complementary use of some functional mea- sures that provide normative data can contribute to a greater understanding of “real-life” execu- tive-control difficulties in individuals with ASD.
Final Considerations
The present study assessed the performance of 11 children and adolescents who were diag-
nosed with ASD without mental retardation on tasks that assessed EF and working memory. The neuropsychological assessment battery consisted of formal measures and one functional measure of EF, as well as a questionnaire on developmental history and health-related as- pects. The results of the formal neuropsycho- logical evaluation indicated heterogeneity in the profiles of the assessed cases. The cases pre- sented a complex pattern of strengths and weak- nesses of EF in the tasks. Four subgroups were identified: (a) predominantly lower overall per- formance (Cases 1 and 3), (b) deficits in various neuropsychological functions but some of them with preserved performance (Cases 2 and 9 –11), (c) relatively preserved neuropsycholog- ical skills with deficits in a few tasks (Cases 4, 5, 7, and 8), and (d) one case who did not complete the assessment battery (Case 6).
The functional neuropsychological assess- ment indicated the presence of significant exec- utive dysfunctions in most of the cases. How- ever, this variability can be partially attributable to a methodological artifact because no behav- ioral measure of ASD symptoms or overall measure of intellectual level was used (i.e., only nonverbal IQ tests were used). This method- ological decision was made to avoid stress and fatigue bias in performance in the EF tasks.
The difficulty in identifying deficits of EF using only formal tests is an issue that was highlighted in this study. Children and adoles- cents with ASD may not have impaired perfor- mance in structured EF tests, although they face serious difficulties in their daily executive func- tioning when assessed by functional measures. The present study addressed this issue by em- phasizing the importance of using multiple measures (objective, functional, and clinical) in the neuropsychological assessment of ASD. These measures should be used in conjunction to prevent the collection of incomplete or in- consistent data regarding executive dysfunction in ASD.
Another aspect that deserves attention con- cerns the method adopted. Individuals with ASD may differ significantly in the manifesta- tion and intensity of cognitive and behavioral impairments, which can be better identified and analyzed using a case series design. Case series studies are recommended in investigations of performance profiles and specificities associ- ated with certain clinical conditions (Caramazza
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& Coltheart, 2006). However, because of the complexity and heterogeneity of ASD, a com- bination of methods provides more consistent data regarding the presence of executive dys- function in ASD (Czermainski et al., 2014). Group studies may not be sensitive to heteroge- neity of the sample. For example, Czermainski et al. (2014) studied the same sample but used a group design, concluding that the ASD group had lower performance than the control group in all of the tasks. Most of the reported differences were statistically significant. Therefore, case se- ries studies and studies that use group designs may have conflicting results, which leads us to consider the use of mixed methods as more appropriate in investigations of EF in ASD. Studies with larger samples are also needed because individuals with ASD without mental retardation constitute a very small portion of the autism spectrum, which is still poorly under- stood with regard to EF impairment.
Consistent with the conclusions of Manjivi- ona and Prior (1999), the neuropsychological profile that was found in the present study sup- ports the view that autism is a spectrum condi- tion, ranging from preserved to highly impaired skills in EF. Such a profile has implications for the ordinary life of children and their families because the child’s behavior may be very dis- ruptive and increase social withdrawal. How- ever, further studies are clearly needed. In con- clusion, the results of the present study corroborate the view that ASD is a spectrum condition, characterized by a complex pattern of strengths and weaknesses concerning EF. Fur- ther research is needed to improve ASD diag- nostic evaluation and treatment.
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Received December 22, 2014 Revision received June 25, 2015
Accepted July 13, 2015 �
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