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Gender Difference in The Association Between Executive Function and Autistic Traits in Typically Developing Children
Gender Difference in The Association Between Executive Function and Autistic Traits in Typically Developing Children
https://doi.org/10.1007/s10803-018-3813-5
ORIGINAL PAPER
Abstract
Autistic traits and executive function (EF) were assessed in 413 typically developing children aged 6–9 years. The children
were divided into the high- autistic-trait (HAT) and low-autistic-trait (LAT) groups based on their total autistic traits. Results
suggested that there were gender differences in specific autistic traits in children with LAT. There were gender-specific
associations between EF and autistic traits in children with HAT: the set shifting of EF predicted difficulties in social aware-
ness in boys; whereas all the EF components predicted difficulties in social communication and social cognition in girls.
These findings may have implications for developing customized interventions that are targeted at specific autistic deficits
in males and females.
Introduction symptoms. For instance, it was found that females with ASD
exhibit fewer restricted and repetitive behaviors but greater
Autism spectrum disorder (ASD) is a neurodevelopmental communication deficits than males with ASD (Frazier et al.
disorder characterized by impaired social communication 2014; Jamison et al. 2017; Rynkiewicz et al. 2016; Wang
and interaction, as well as restricted and repetitive pattern of et al. 2017). Although many studies have reported higher
behaviors (American Psychiatric Association 2013). One of total autistic traits in typically developing (TD) males than
the important features of ASD is the skewness in gender dis- females (Ruzich et al. 2015), few studies have compared the
tribution that ASD is more prevent in males than in females autistic phenotypes between genders in the general popu-
(Baxter et al. 2015; Christensen et al. 2016; Schaafsma and lations. In one previous study, researchers found that TD
Pfaff 2014). Recent examinations of autistic traits in general boys exhibited more restricted and repetitive behaviors and
population have shown a similar pattern of gender difference social interaction than girls (Hsiao et al. 2013). However,
in high autistic traits (Posserud et al. 2006; Sun et al. 2014). another study found no significant difference in autistic traits
Moreover, numerous studies have suggested that females between TD boys and girls (Solomon et al. 2012). Despite
with ASD are different from males with regard to behavioral being a topic of great interest, gender differences in autistic
traits in general populations and the underlying mechanisms
Electronic supplementary material The online version of this remains unclear (Lai et al. 2015).
article (https://doi.org/10.1007/s10803-018-3813-5) contains It has been proposed that cognitive impairments, espe-
supplementary material, which is available to authorized users. cially the executive function (EF), have distinct interactions
with various autistic behavioral symptoms (Happé et al. 2006;
* Zengjian Wang
wangzj27@mail.sysu.edu.cn Happé and Ronald 2008; Hill 2004). Therefore, an important
consideration in understanding gender differences in autistic
* Jin Jing
jingjin@mail.sysu.edu.cn behaviors is the role of EF. EF refers to a set of purposeful
higher-order neuropsychological domains, including planning,
1
Faculty of Maternal and Child Health, School of Public working memory, inhibition, mental flexibility, as well as the
Health, Sun Yat-sen University, 74 Zhong‑shan Road 2, control and shifting of attention (Johnson 2012). EF impair-
Guangzhou 510080, China
ments are commonly reported in ASD. A recent meta-analysis
2
School of Public Health, Peking University Health Science showed the occurrence of executive dysfunction in ASD such
Center, Beijing 100191, China
13
Vol.:(0123456789)
Journal of Autism and Developmental Disorders
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Journal of Autism and Developmental Disorders
in a quiet room without distractions. In addition to testing after 2–9 consecutive correct responses. SE was cal-
the children, SRS was also completed by parents within culated as proposed by Cianchetti et al. (2005): score of
15–20 min under the supervision of investigators. Any ques- SE = CC*6 + [128 − (the number of cards that had been
tion or confusion from parents was clarified to ensure that used)]. This method of scoring takes efficiency in achieving
they understood all of the items. The completed question- CC into account by rewarding unused cards which helps
naires were checked for quality control. to detect differences in task performance (Cianchetti et al.
2005). CC indicates the ability of set shifting, FMS reflects
Measures difficulties in sustained attention, NPE may simply reflect
the efficiency of discovering rules and the SE indicates the
Autistic Traits cognitive flexibility (Landry and Al-Taie 2016).
The WCST is a quintessential and widely used executive We divided all the participants into HAT and LAT groups
functioning test. We used the computerized version of 128- according to the SRS cut-off of 56.5. Gender differences in
cards WCST to examine executive function (EF), because it age, FSIQ and autistic traits were examined in the whole
helps to reduce confounding influences on task performance sample, as well as in the HAT group and LAT group respec-
of examiners (Shan et al. 2008; South et al. 2007). Partici- tively. Two-sample t-tests were used to investigate the gen-
pants were asked to sort cards in accordance with one of der differences in age and FSIQ. Analysis of covariance
the three rules (color, shape and number) via mouse click- (ANCOVA) was used to examine gender differences in
ing. The card sorting rules were not revealed to the exami- autistic traits after controlling for age and FSIQ. A false
nees, but must be inferred from the feedback provided by discovery rate (FDR) of 0.05 was used to correct for multi-
the computer. Computer screen displayed ‘√’ for a correct ple comparisons of autistic traits (total autistic traits, social
card sorted and ‘×’ for an incorrect card sorted. After 10 awareness, social cognition, social communication, social
consecutive correct responses, card sorting rules changed motivation and autistic mannerisms) for the whole sample,
without announcement. This task procedure continued until the HAT group and the LAT group (Benjamini and Hoch-
participants completed six sorting categories (color, shape, berg 1995, 2000).
number, color, shape, number) or when all 128 cards were Pearson correlation analysis was conducted to explore
sorted. the correlations between EF and autistic traits in HAT
Four WCST indices were used for analysis: number of boys, HAT girls, LAT boys and LAT girls separately. Fur-
completed categories (CC), failure to maintain set (FMS), thermore, linear regression models were used to explore
non-preservative errors (NPE) and shifting efficiency the contributions of EF in predicting autistic traits in boys
(SE). CC was the number of sets of 10 consecutive cor- and girls with HAT respectively, with age and FSIQ as
rect responses. NPE comprised all errors except persevera- covariates. For all the Pearson correlation and linear
tive errors. FMS was the number of incorrect responses regression analyses, FDR corrections were applied within
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Journal of Autism and Developmental Disorders
each domain (total autistic traits, social awareness, social Gender Differences in Associations Between Autistic
cognition, social communication, social motivation and Traits and EF
autistic mannerisms) to maintain a Type 1 error rate at
0.05 (Benjamini and Hochberg 1995, 2000). The results Table 2 shows the correlation patterns between SRS and
of linear regression models were reported with unstand- WCST variables at two levels of SRS total score (HAT and
ardized regression coefficients (β), 95% confidence inter- LAT) from boys and girls. For the boys with HAT, there was
(val (CI) )and the proportions of variance explained a significant negative correlation between CC and the Social
R2(adjusted) . Analyses were performed using SAS version Awareness scores (r = − 0.309, P = 0.036). For the girls with
HAT, CC-Social Cognition scores (r = − 0.456, P = 0.012)
9.2 (SAS Institute, Cary, NC, USA). For all the analyses
and SE-Social Cognition scores (r = − 0.539, P = 0.004)
involving multiple comparisons, results were reported
were negatively correlated; while the NPE-Social Cogni-
after correction using FDR procedure.
tion scores was positively correlated (r = 0.423, P = 0.015).
As for the boys with LAT and the girls with LAT, there was
no significant correlation between SRS and WCST variables
(all Ps > 0.05).
Results We further performed force-entry linear regression mod-
els of each SRS score in the boys and girls with HAT. Each
Sample Characteristics and Gender Difference EF component was used as a predictor, and age and FSIQ
in Autistic Trait were covariates (Table 3). The proportions of variance
( )
explained R2(adjusted) by the models are shown in Fig. 2. The
A total of 413 children (239 boys and 174 girls) were
included in the data analysis. Table 1 shows the charac- results indicated that for the boys with HAT, CC signifi-
teristics of the sample. There was no significant difference cantly predicted Social Awareness scores (β = − 0.45,
in age (t(1,411) = 0.45, P = 0.655) and FSIQ (t(1,411) = 1.93, P = 0.039) and CC together with age and FSIQ explained
P = 0.055) between boys and girls. The ANCOVA analysis (11.0% of the variances in Social Awareness scores
showed that boys scored significantly higher than girls on
)
R2(adjusted) = 0.110 .
Social Awareness (F(1,411) = 7.01, P = 0.024, η2 = 0.02) and
Autism Mannerisms (F(1,411) = 16.92, P < 0.001, η2 = 0.04) In girls with HAT, CC, NPE, SE and FMS were signifi-
after controlling for age and FSIQ. cantly associated with SRS scores. CC, NPE and SE signifi-
We also divided the participants into the HAT group cantly predicted variance of scores on SRS total scale (CC:
and LAT group using a cut-off value of 56.5 for SRS. Two- β = − 3.25, P = 0.011; R2(adjusted) = 0.274; NPE: β = 0.22,
sample t-test analysis showed that there were no signifi- P = 0.011; R2(adjusted) = 0.269; SE: β = − 0.28, P = 0.002;
cant gender differences in age (t (1,103) = 1.67, P = 0.098;
R2(adjusted) = 0.382) and Social Communication (CC:
t (1,306) = 0.34, P = 0.734) and FSIQ (t (1,103) = 0.48,
P = 0.635; t(1,306) = 1.36, P = 0.176) in the HAT group and β = − 1.70, P = 0.010; R2(adjusted) = 0.294; NPE: β = 0.12,
LAT group, respectively. In the children with HAT, the
P = 0.007; R2(adjusted) = 0.325; SE: β = − 0.13, P = 0.007;
ANCOVA analysis showed that there were no significant
gender differences in all SRS variables (all Ps > 0.05). R2(adjusted) = 0.330). CC, NPE, SE and FMS significantly pre-
However, in children with LAT, boys scored significantly dicted variance of Social Cognition scores (CC: β = − 0.81,
higher on Autism Mannerisms (F(1,306) = 12.00, P = 0.006, P = 0.012; R2(adjusted) = 0.239; NPE: β = 0.05, P = 0.044;
η2 = 0.038), but scored significantly lower on Social Cog-
nition (F(1,306) = 8.56, P = 0.012, η2 = 0.027) compared to R2(adjusted) = 0.220; SE: β = − 0.07, P = 0.012; R2(adjusted) = 0.324;
girls. FMS: β = 0.74, P = 0.004; R2(adjusted) = 0.145).
Additionally, we compared age, FSIQ and SRS scores
between HAT and LAT groups within each gender. Two-
sample t-test analysis showed that boys and girls with
HAT had significantly lower FSIQ than boys and girls with Discussion
LAT (boys: t(1,237) = 4.25, P < 0.001; girls: t(1,172) = 3.52,
P < 0.001). The ANCOVA analysis showed that boys with This study explored the gender difference in the associations
HAT had significantly higher scores on SRS total scale and between executive function (EF) and autistic traits in a large
all subscales than boys with LAT (all Ps < 0.001). Similar sample of typically developing children. We found that: (1)
results were obtained for girls with HAT compared to girls there were gender differences in autistic traits in children
with LAT (all Ps < 0.001). with LAT; (2) the association patterns of EF and autistic
13
Table 1 Differences of SRS and WCST scores between boys and girls (mean ± SD)
Measures All children Children with HAT Children with LAT Difference between Difference between
HAT and LAT boys HAT and LAT Girls
Boys (n = 239) Girls (n = 174) Pa Boys (n = 70) Girls (n = 35) Pa Boys (n = 169) Girls (n = 139) Pa Pa Pa
Journal of Autism and Developmental Disorders
Ageb 7.61 ± 0.96 7.65 ± 0.95 0.655 7.56 ± 0.96 7.89 ± 0.93 0.098 7.63 ± 0.96 7.59 ± 0.95 0.734 0.608 0.102
FSIQb 107.40 ± 13.27 109.93 ± 13.01 0.055 101.93 ± 13.5 103.23 ± 12.54 0.635 109.67 ± 12.53 111.62 ± 12.61 0.176 < 0.001 < 0.001
SRS
TS 48.95 ± 16.03 45.80 ± 14.82 0.163 68.87 ± 10.28 67.14 ± 10.57 0.555 40.70 ± 9.32 40.42 ± 10.16 0.942 < 0.001 < 0.001
SA 8.43 ± 2.33 7.75 ± 2.40 0.024 9.89 ± 2.26 9.20 ± 2.27 0.516 7.83 ± 2.09 7.39 ± 2.29 0.149 < 0.001 < 0.001
SCog 10.71 ± 3.74 11.09 ± 3.66 0.156 14.36 ± 2.39 14.94 ± 2.51 0.555 9.20 ± 3.11 10.12 ± 3.25 0.012 < 0.001 < 0.001
SCom 14.49 ± 6.66 13.16 ± 6.15 0.163 22.14 ± 4.83 21.80 ± 5.61 0.888 11.31 ± 4.32 10.98 ± 3.99 0.796 < 0.001 < 0.001
SM 8.70 ± 3.65 8.71 ± 3.35 0.575 12.23 ± 3.46 12.43 ± 3.4 0.932 7.24 ± 2.58 7.77 ± 2.61 0.080 < 0.001 < 0.001
AM 6.63 ± 3.71 5.09 ± 3.18 < 0.001 10.26 ± 3.74 8.77 ± 3.65 0.324 5.13 ± 2.44 4.17 ± 2.26 0.006 < 0.001 < 0.001
WCST
CC 4.30 ± 1.70 4.78 ± 1.50 4.13 ± 1.73 4.54 ± 1.77 4.37 ± 1.68 4.84 ± 1.43
FMS 2.15 ± 1.52 1.82 ± 1.54 2.07 ± 1.64 1.54 ± 1.46 2.19 ± 1.47 1.88 ± 1.56
NPE 41.23 ± 21.55 37.51 ± 22.72 41.34 ± 21.55 41.06 ± 28.06 41.19 ± 21.61 36.61 ± 21.19
SE 33.44 ± 20.99 40.45 ± 22.83 33.10 ± 22.99 39.57 ± 24.56 33.58 ± 20.17 40.67 ± 22.46
SRS Social Responsiveness Scale, WCST Wisconsin Card Sorting Test, TS total score, SA social awareness, SCog social cognition, SCom social communication, SM social motivation, AM autis-
tic mannerism, CC categories completed, FMS failure to maintain set, NPE non-perseverative errors, SE shifting efficiency
a
Adjusted for age and IQ, and after false-discovery-rate correction for multiple comparisons of SRS scores
b
Comparison using Two-sample t test
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Journal of Autism and Developmental Disorders
Table 2 Pearson correlation coefficients of SRS and EF from different SRS levels of boys and girls
EF SRS SRS
TS SA SCog SCom SM AM TS SA SCog SCom SM AM
EF executive function, SRS Social Responsiveness Scale, TS total score, SA social awareness, SCog social cognition, SCom social communica-
tion, SM social motivation, AM autistic mannerism, CC categories completed, FMS failure to maintain set, NPE non-perseverative errors, SE
shifting efficiency, HAT high-autistic-trait, LAT low-autistic-trait
*P < 0.05 after false-discovery-rate correction within each SRS score
traits were different in boys and girls with HAT; (3) for the Valla and colleagues (Valla et al. 2010, 2013) found that
boys with HAT, CC predicted the individual differences of attention to detail was positively related to face recogni-
difficulties in social awareness; (4) for the girls with HAT, tion and facial emotion reading ability in general males but
the CC, NPE, FMS and SE predicted variances of difficulties not in females, thus may lead to better social interaction in
in social cognition and social communication; (5) there were males than females. We observed no difference in autistic
no significant associations between EF and autistic traits in traits between boys and girls with HAT. Inconsistent to this
boys and girls with LAT. finding, Dworzynski et al. (2012) found that compared to
In the present study, all the participants were from main- boys with high autistic traits (measured with The Childhood
stream schools. Compared to the girls with LAT, boys with Autism Spectrum Test), girls with high autistic traits had
LAT scored significantly higher on Autistic Mannerisms and more communication difficulties. Baron-Cohen and col-
lower on Social Cognition, although there were no signifi- leagues (2014) investigated gender difference in total autistic
cant differences in autistic traits between boys and girls with traits using the largest sample size to date, 811 adults (454
HAT. These findings indicate that boys with LAT have more females) with autism and 3,906 age-matched typical controls
repetitive/restricted behaviors, while girls with LAT have (2,562 females). They found that the gender differences in
more difficulties in social interaction. In line with our find- total autistic traits were smaller in the autism group than in
ing, previous researches consistently reported more repeti- the control group (indicated by the significant ordinal inter-
tive/restricted behaviors in boys than girls from general child action between gender and diagnosis) (Baron-Cohen et al.
population (Hsiao et al. 2013; Nowack et al. 2015). Similar 2014). This finding may suggest that increased statistical
to the findings of Hsiao et al (2013) in which TD boys and power is required to detect gender differences in samples
girls scored 6.20 and 5.08 points, respectively, on SRS sub- with ASD or high autistic traits. Further studies with larger
scale measuring repetitive/restricted behaviors, boys and and gender-balanced sample sizes are warranted to clarify
girls with LAT scored 6.63 and 5.13 points, respectively, in the phenotypic gender difference in children with high level
our study. This result suggests that the SRS measurements of of autistic traits.
autistic traits obtained from different studies are similar. The We further investigated the relationship between EF
differences in restricted/repetitive behaviors between boys and autistic traits in boys and girls with LAT and HAT
and girls with LAT may be due to the normative sex differ- separately. We found gender-specific associations between
ence in dimorphic brain structure (Lai et al. 2012; Supekar EF and autistic traits in children with HAT, although we
and Menon 2015). For example, gray matter morphometry observed no significant associations between EF and autis-
in the right putamen was different between TD boys and tic traits in boys and girls with LAT. Regression analysis
girls and was related with repetitive/restricted behaviors revealed that in boys with HAT, CC could explain the 11.0%
measured with ADI-R (Supekar and Menon 2015). Fewer of the individual differences in Social Awareness. For girls
difficulties in social interaction in boys with LAT may link with HAT, the CC, NPE, SE and FMS predicted variances
to their preferences for attention to detail (Nebot 1988). of autistic traits related to Social Cognition (23.9%, 22.0%,
13
Table 3 Multiple regression analysis of executive functions predicting autistic traits in HAT boys and girls a
EF SRS
Journal of Autism and Developmental Disorders
TS SA SCog SCom SM AM
b b b b b
β (95% CI) P β (95% CI) P β (95% CI) P β (95% CI) P β (95% CI) P β (95% CI) Pb
EF executive function, SRS Social Responsiveness Scale, TS total score, SA social awareness, SCog social cognition, SCom social communication, SM social motivation, AM autistic mannerism,
CC categories completed, FMS failure to maintain set, NPE non-perseverative errors, SE, shifting efficiency, HAT, high-autistic-trait
a
Adjusted for age and IQ
b
After false-discovery-rate correction within each SRS score
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Journal of Autism and Developmental Disorders
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Journal of Autism and Developmental Disorders
relation to specific autistic traits in children with HAT may Acknowledgments Jin Jing was supported by National Natural Science
be relevant for developing gender-specific interventions for Foundation of China (Grant No. 81573169). Zengjian Wang was sup-
ported by Guangdong medical science and technology research fund
autistic deficits. EF components, such as flexibility and mon- Project (A2018190) and the PhD Start-up Fund of Natural Science
itoring are thought to facilitate the ability to engage in social Foundation of Guangdong Province (2018A030310336). We thank
interactions (van Lier and Deater-Deckard 2016). Interven- all the participating children and their families. We acknowledge the
tions that target EF components, such as flexibility, insist- relevant staffs and students for their contributions to data collection.
ence to sameness and planning, have been shown to reduce
Author Contributions MD, LL and JL contributed to the data collec-
social impairment (total SRS scores) in children with ASD tion. MD designed the current study, performed the statistical anal-
(Kenworthy et al. 2014). Our study showed that shifting can ysis and drafted the manuscript. ZW guided the statistical analysis
negatively predict difficulties in perceiving social cues and and revised the manuscript. JJ supervised the analysis and revised the
social communication in boys with HAT; while in girls with manuscript. All authors read and approved the final manuscript.
HAT, all EF components were linked to the ability to process
social cues and social communication. This indicates that Compliance with Ethical Standards
boys with difficulties in perceiving social cues and social
Conflict of interest The authors declare no conflicts of interest in this
communication might benefit from interventions designed work.
to improve EF in terms of shifting, whereas girls with dif-
ficulties in processing social cues and social communication
might benefit from interventions designed to improve EF
References
in general. Further studies are warranted to test the clinical
implication of these findings. American Psychiatric Association. (2013). Diagnostic and Statistical
Our study has the following limitations. First, we did Manual of Mental Disorders (DSM-5). Philadelphia: American
not clinically preclude the possibility of children with HAT Psychiatric Pub.
Baron-Cohen, S., Cassidy, S., Auyeung, B., Allison, C., Achoukhi, M.,
being diagnosed with ASD. However, this limitation could
Robertson, S. al (2014). Attenuation of Typical Sex Differences
not have had a significant impact on the current findings in 800 Adults with Autism vs. 3,900 Controls. PLoS ONE, 9,
given that the autistic traits appear to distribute continuously e102251. https://doi.org/10.1371/journal.pone.0102251.
and share a common pathogenesis throughout the continuum Baxter, A. J., Brugha, T. S., Erskine, H. E., Scheurer, R. W., Vos, T., &
Scott, J. G. (2015). The epidemiology and global burden of autism
(Constantino and Charman 2016; Robinson et al. 2011). Fur-
spectrum disorders. Psychological Medicine, 45, 601–613. https
ther studies involving participants across the whole autistic ://doi.org/10.1017/S003329171400172X.
traits continuum are warranted to test whether the gender- Benjamini, Y., & Hochberg, Y. (1995). Controlling the False Discovery
differential relationships persist in clinical samples. Second, Rate: A Practical and Powerful Approach to Multiple Testing.,
57, 289–300.
the SRS specifically target autistic traits involving reciprocal
Benjamini, Y., & Hochberg, Y. (2000). On the adaptive control of the
social behaviors. Given that autistic traits are supposed to be false discovery rate in multiple testing with independent statistics.
fractionable (Brunsdon and Happe 2014), the associations Journal of Educational and Behavioral Statistics, 25, 60–83.
we found may not generalize to other domains of autistic Brunsdon, V. E., & Happe, F. (2014). Exploring the ‘fractionation’
of autism at the cognitive level. Autism, 18, 17–30. https://doi.
traits, such as restricted/repetitive behaviors and interests.
org/10.1177/1362361313499456.
Finally, due to the cross-sectional nature of this study design, Cen, C., Liang, Y., Chen, Q., Chen, K., Deng, H., Chen, B. al (2017).
we could not speculate the causality in the relationships Investigating the validation of the Chinese Mandarin version of
we have observed. Longitudinal studies are necessary to the Social Responsiveness Scale in a Mainland China child pop-
ulation. BMC Psychiatry, 17, 51. https://doi.org/10.1186/s1288
advance our understanding of the relationship between EF
8-016-1185-y.
and autistic traits. Chen, H., Keith, T. Z., Weiss, L., Zhu, J., & Li, Y. (2010). Testing
To conclude, our study demonstrated that in TD children for multigroup invariance of second-order WISC-IV structure
with LAT, boys had more repetitive/restricted behaviors but across China, Hong Kong, Macau, and Taiwan. Personality and
Individual Differences, 49, 677–682. https://doi.org/10.1016/j.
fewer difficulties in social interaction than girls. Specific EF
paid.2010.06.004.
components had gender-differential relationships to the sub- Christensen, D. L., Baio, J., Van Naarden, B. K., Bilder, D., Charles,
domains of autistic traits in TD children with HAT. In the J., Constantino JNet al (2016). Prevalence and characteristics of
boys with HAT, the categories completed of EF predicted autism spectrum disorder among children aged 8 tears–autism
and developmental disabilities monitoring network, 11 sites,
autistic-like difficulties in social awareness. For the girls
United States, 2012. MMWR Surveill Summ, 65, 1–23. https://
with HAT, the categories completed, the non-perseverative doi.org/10.15585/mmwr.ss6503a1.
errors, the failure to maintain set and the shifting efficiency Cianchetti, C., Corona, S., Foscoliano, M., Scalas, F., & Sannio-Fan-
predicted autistic-like difficulties in social cognition and cello, G. (2005). Modified Wisconsin card sorting test: proposal of
a supplementary scoring method. Archives of Clinical Neuropsy-
communication. Our findings may have implications for
chology, 20, 555–558. https://doi.org/10.1016/j.acn.2004.12.002.
developing gender-specific interventions related to specific Constantino, J. N., & Charman, T. (2016). Diagnosis of autism spec-
autistic deficits. trum disorder: Reconciling the syndrome, its diverse origins,
13
Journal of Autism and Developmental Disorders
and variation in expression. The Lancet Neurology, 15, 279– Kenworthy, L., Anthony, L. G., Naiman, D. Q., Cannon, L., Wills, M.
291. https://doi.org/10.1016/S1474-4422(15)00151-9. C., Luong-Tran Cet al (2014). Randomized controlled effective-
Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., & ness trial of executive function intervention for children on the
Gross, M. M., Brophy S. L., et al. (2003). Validation of a brief autism spectrum. Journal of Child Psychology and Psychiatry,
quantitative measure of autistic traits: Comparison of the social 55, 374–383. https://doi.org/10.1111/jcpp.12161.
responsiveness scale with the autism diagnostic interview- Kenworthy, L., Black, D. O., Harrison, B., Della, R. A., & Wallace,
revised. J Autism Dev Disord, 33, 427–433. doi. G. L. (2009). Are executive control functions related to autism
Constantino, J. N., & Gruber, C. P. (2012). Social Responsiveness symptoms in high-functioning children? Child Neuropsychology,
Scale (SRS). Torrance: Western Psychological Services. 15, 425–440. https://doi.org/10.1080/09297040802646983.
Deaner, R. O., Shepherd, S. V., & Platt, M. L. (2007). Familiarity Lai, M. C., Baroncohen, S., & Buxbaum, J. D. (2015). Understanding
accentuates gaze cuing in women but not men. Biology Letters, autism in the light of sex/gender. Molecular Autismdoi. https://
3, 64–67. doi.org/10.1186/s13229-015-0021-4.
Demetriou, E. A., Lampit, A., Quintana, D. S., Naismith, S. L., Song, Lai, M. C., Lombardo, M. V., Ruigrok, A. N., Chakrabarti, B., Auye-
Y., Pye JEet al (2017). Autism spectrum disorders: A meta- ung, B., Szatmari Pet al (2017). Quantifying and exploring cam-
analysis of executive function. Mol Psychiatrydoi. https://doi. ouflaging in men and women with autism. Autism, 21, 690–702.
org/10.1038/mp.2017.75. https://doi.org/10.1177/1362361316671012.
Dworzynski, K., Ronald, A., Bolton, P., & Happe, F. (2012). How Lai, M. C., Lombardo, M. V., Ruigrok, A. N., Chakrabarti, B., Wheel-
different are girls and boys above and below the diagnostic wright, S. J., Auyeung Bet al (2012). Cognition in males and
threshold for autism spectrum disorders? J Am Acad Child females with autism: Similarities and differences. PLoS One, 7,
Adolesc Psychiatry, 51, 788–797. https: //doi.org/10.1016/j. e47198. https://doi.org/10.1371/journal.pone.0047198.
jaac.2012.05.018. Landry, O., & Al-Taie, S. (2016). A meta-analysis of the Wisconsin
Ferraro, F. R., Hansen, R., & Deling, L. (2016). Executive Function card sort task in autism. Journal of Autism and Developmen-
Index (EFI) performance in nonclinical individuals with high lev- tal Disorders, 46, 1220–1235. https://doi.org/10.1007/s1080
els of autistic traits. Applied Neuropsychology: Adult. https://doi. 3-015-2659-3.
org/10.1080/23279095.2016.1263199. Lehnhardt, F. G., Falter, C. M., Gawronski, A., Pfeiffer, K., Tep-
Frazier, T. W., Georgiades, S., Bishop, S. L., & Hardan, A. Y. (2014). est, R., Franklin Jet al (2016). Sex-related cognitive profile in
Behavioral and cognitive characteristics of females and males with autism spectrum disorders diagnosed late in life: Implications for
autism in the Simons Simplex Collection. Journal of the American the female autistic phenotype. Journal of Autism and Develop-
Academy of Child and Adolescent Psychiatry, 53, 329–340. https mental Disorders, 46, 139–154. https://doi.org/10.1007/s1080
://doi.org/10.1016/j.jaac.2013.12.004. 3-015-2558-7.
Frischen, A., Bayliss, A. P., & Tipper, S. P. (2007). Gaze cueing of Leung, R. C., Vogan, V. M., Powell, T. L., Anagnostou, E., & Taylor,
attention: Visual attention, social cognition, and individual dif- M. J. (2016). The role of executive functions in social impair-
ferences. Psychological Bulletin, 133, 694–724. https://doi. ment in autism Spectrum Disorder. Child Neuropsychology, 22,
org/10.1037/0033-2909.133.4.694. 336–344. https://doi.org/10.1080/09297049.2015.1005066.
Gokcen, S., Bora, E., Erermis, S., Kesikci, H., & Aydin, C. (2009). Lukito, S., Jones, C. R. G., Pickles, A., Baird, G., Happé, F., Char-
Theory of mind and verbal working memory deficits in parents man Tet al. (2017). Specificity of executive function and theory
of autistic children. Psychiatry Research, 166, 46–53. https://doi. of mind performance in relation to attention-deficit/hyperactivity
org/10.1016/j.psychres.2007.11.016. symptoms in autism spectrum disorders. Molecular Autism, https
Happé, F., & Ronald, A. (2008). The ‘Fractionable Autism Triad’: ://doi.org/10.1186/s13229-017-0177-1.
A review of evidence from behavioural, genetic, cognitive and Lundstrom, S., Chang, Z., Kerekes, N., Gumpert, C. H., Rastam, M.,
neural research. Neuropsychology Review, 18, 287–304. https:// Gillberg, C. al (2011). Autisticlike traits and their association with
doi.org/10.1007/s11065-008-9076-8. mental health problems in two nationwide twin cohorts of children
Happé, F., Ronald, A., & Plomin, R. (2006). Time to give up on a single and adults. Psychological Medicine, 41, 2423–2433. doi.
explanation for autism. Nature Neuroscience, 9, 1218–1220. https Miranda, A., Berenguer, C., Roselló, B., Baixauli, I., & Colomer, C.
://doi.org/10.1038/nn1770. (2017). Social cognition in children with high-functioning autism
Hill, E. L. (2004). Executive dysfunction in autism. Trends in Cognitive spectrum disorder and attention-deficit/hyperactivity disorder.
Sciences, 8, 26–32. Associations with executive functions. Frontiers in Psychology,
Houcan, Z. (2009). The revision of WISC-IV Chinese version. Psycho- https://doi.org/10.3389/fpsyg.2017.01035.
logical Science, 32, 1177–1179. Moriguchi, Y. (2014). The early development of executive function
Hsiao, M., Tseng, W., Huang, H., & Gau, S. S. (2013). Effects of autis- and its relation to social interaction: A brief review. Frontiers in
tic traits on social and school adjustment in children and adoles- Psychology, https://doi.org/10.3389/fpsyg.2014.00388.
cents: The moderating roles of age and gender. Research in Devel- Nebot, T. K. (1988). Sex differences among children on embedded
opmental Disabilities, 34, 254–265. https://doi.org/10.1016/j. tasks. Perceptual and Motor Skills, 67, 972–974. https ://doi.
ridd.2012.08.001. org/10.2466/pms.1988.67.3.972.
Jamison, R., Bishop, S. L., Huerta, M., & Halladay, A. K. (2017). Nowack, N., Wittsiepe, J., Kasper-Sonnenberg, M., Wilhelm, M., &
The clinician perspective on sex differences in autism spectrum Schölmerich, A. (2015). Influence of low-level prenatal exposure
disorders. Autism, 21, 772–784. https://doi.org/10.1177/13623 to PCDD/Fs and PCBs on empathizing, systemizing and autistic
61316681481. traits: Results from the duisburg birth cohort study. PLoS ONE,
Johnson, M. H. (2012). Executive function and developmental disor- 10, e129906. https://doi.org/10.1371/journal.pone.0129906.
ders: The flip side of the coin. Trends in Cognitive Sciences, 16, Posserud, M. B., Lundervold, A. J., & Gillberg, C. (2006). Autistic
454–457. https://doi.org/10.1016/j.tics.2012.07.001. features in a total population of 7-9-year-old children assessed by
Jones, C. R. G., Simonoff, E., Baird, G., Pickles, A., Marsden, A. J. the ASSQ (Autism Spectrum Screening Questionnaire). Journal
S., Tregay, J., et al. (2018). The association between theory of of Child Psychology and Psychiatry, 47, 167–175.
mind, executive function, and the symptoms of autism spectrum Robinson, E. B., Koenen, K. C., McCormick, M. C., Munir, K., Hal-
disorder. Autism Research, 11(1), 95–109. https: //doi.org/10.1002/ lett, V., Happe, F. al (2011). Evidence that autistic traits show the
aur.1873. same etiology in the general population and at the quantitative
13
Journal of Autism and Developmental Disorders
extremes (5%, 2.5%, and 1%). Archives of General Psychiatry, 68, Sun, X., Allison, C., Auyeung, B., Matthews, F. E., Sharp, S. J., Baron-
1113–1121. https://doi.org/10.1001/archgenpsychiatry.2011.119. Cohen Set al (2014). The Mandarin Childhood Autism Spectrum
Ruzich, E., Allison, C., Smith, P., Watson, P., Auyeung, B., Ring Het Test (CAST): Sex differences. Journal of Autism and Develop-
al (2015). Measuring autistic traits in the general population: A mental Disorders, 44, 2137–2146. https://doi.org/10.1007/s1080
systematic review of the Autism-Spectrum Quotient (AQ) in a 3-014-2088-8.
nonclinical population sample of 6,900 typical adult males and Supekar, K., & Menon, V. (2015). Sex differences in structural organi-
females. Molecular Autism, 6, 2. zation of motor systems and their dissociable links with repetitive/
Rynkiewicz, A., Schuller, B., Marchi, E., Piana, S., Camurri, A., restricted behaviors in children with autism. Molecular Autism.
Lassalle Aet al (2016). An investigation of the ‘female camou- https://doi.org/10.1186/s13229-015-0042-z.
flage effect’ in autism using a computerized ADOS-2 and a test Torske, T., Nærland, T., Øie, M. G., Stenberg, N., & Andreassen, O.
of sex/gender differences. Molecular Autism, 7, 10. https://doi. A. (2018). Metacognitive aspects of executive function are highly
org/10.1186/s13229-016-0073-0. associated with social functioning on parent-rated measures in
Saito, A., Stickley, A., Haraguchi, H., Takahashi, H., Ishitobi, M., & children with autism spectrum disorder. Frontiers in Behavioral
Kamio, Y. (2017). Association between autistic traits in preschool Neuroscience. https://doi.org/10.3389/fnbeh.2017.00258.
children and later emotional/behavioral outcomes. Journal of Valla, J. M., Ganzel, B. L., Yoder, K. J., Chen, G. M., Lyman, L. T.,
Autism and Developmental Disorders. https://doi.org/10.1007/ Sidari APet al (2010). More than maths and mindreading: Sex dif-
s10803-017-3245-7. ferences in empathizing/systemizing covariance. Autism Research,
Schaafsma, S. M., & Pfaff, D. W. (2014). Etiologies underlying sex dif- 3, 174–184. https://doi.org/10.1002/aur.143.
ferences in autism spectrum disorders. Frontiers in Neuroendocri- Valla, J. M., Maendel, J. W., Ganzel, B. L., Barsky, A. R., & Belmonte,
nology, 35, 255–271. https: //doi.org/10.1016/j.yfrne. 2014.03.006. M. K. (2013). Autistic trait interactions underlie sex-dependent
Shan, I. K., Chen, Y. S., Lee, Y. C., & Su, T. P. (2008). Adult norma- facial recognition abilities in the normal population. Frontiers
tive data of the Wisconsin Card Sorting Test in Taiwan. Journal in Psychology, 4, 286. https://doi.org/10.3389/fpsyg.2013.00286.
of the Chinese Medical Association, 71, 517–522. https://doi. van Lier, P. A. C., & Deater-Deckard, K. (2016). Children’s elementary
org/10.1016/S1726-4901(08)70160-6. school social experience and executive functions development:
Singer, T., & Lamm, C. (2009). The social neuroscience of empathy. Introduction to a special section. Journal of Abnormal Child Psy-
Annals of the New York. Academy of Sciences, 1156, 81–96. https chology, 44, 1–6. https://doi.org/10.1007/s10802-015-0113-9.
://doi.org/10.1111/j.1749-6632.2009.04418.x. Wang, S., Deng, H., You, C., Chen, K., Li, J., Tang, C. al (2017). Sex
Solomon, M., Miller, M., Taylor, S. L., Hinshaw, S. P., & Carter, C. differences in diagnosis and clinical phenotypes of Chinese chil-
S. (2012). Autism Symptoms and Internalizing Psychopathol- dren with autism spectrum disorder. Neuroscience Bulletin, 33,
ogy in Girls and Boys with Autism Spectrum Disorders. Journal 153–160. https://doi.org/10.1007/s12264-017-0102-9.
of Autism and Developmental Disorders, 42, 48–59. https://doi. White, E. I., Wallace, G. L., Bascom, J., Armour, A. C., Register-
org/10.1007/s10803-011-1215-z. Brown, K., Popal, H. Set al (2017). Sex differences in parent-
South, M., Ozonoff, S., & McMahon, W. M. (2007). The relationship reported executive functioning and adaptive behavior in children
between executive functioning, central coherence, and repetitive and young adults with autism spectrum disorder. Autism Research,
behaviors in the high-functioning autism spectrum. Autism, 11, 10, 1653–1662. https://doi.org/10.1002/aur.1811.
437–451. https://doi.org/10.1177/1362361307079606.
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