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Journal of Autism and Developmental Disorders

https://doi.org/10.1007/s10803-018-3813-5

ORIGINAL PAPER

Gender Difference in the Association Between Executive Function


and Autistic Traits in Typically Developing Children
Meixia Dai1 · Lizi Lin1,2 · Jingjing Liang1 · Zengjian Wang1 · Jin Jing1

© Springer Science+Business Media, LLC, part of Springer Nature 2018

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.

Keywords  Gender difference · Autistic trait · Executive functions · Children

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/s1080​3-018-3813-5) 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

as conception formation and cognitive flexibility (Demetriou Method


et al. 2017). Another meta-analysis found that ASD is asso-
ciated with impaired performances on measures of the Wis- Participants
consin Card Sort Test, including the categories completed,
the failure-to-maintain-set and the non-perseverative errors We recruited typically developing children from primary
(Landry and Al-Taie 2016). EF impairments have been linked schools in Guangzhou. The inclusion criteria included: (1)
to autistic behavioral symptoms both in the areas of social aged 6–9 years old; (2) Full-Scale IQ > 70; (3) with normal
communication and restricted and repetitive behaviors pattern naked vision or corrected-vision; (4) without color blind-
(Jones et al. 2018; Kenworthy et al. 2009; Leung et al. 2016; ness and color amblyopia; (5) free from physical disabilities,
Torske et al. 2018). medical illness, and developmental or behavioral disorders
In recent years, increasing evidences have suggested that EF based on parent-report (e.g., ASD, attention deficit hyperac-
may have a different impact on autistic traits between males tivity disorder, developmental delay and depression). A total
and females (Lai et al. 2017; Lehnhardt et al. 2016; White et al. of 451 children were recruited. Thirty-eight children were
2017). For example, Lehnhardt et al. (2016) found that females excluded due to missing data, of whom 22 did not complete
with ASD have better EF than males with ASD using a late- Social Responsiveness Scale (SRS) and 16 did not complete
diagnosed sample. They suggested that EF may enable females the Wisconsin Card Sorting Test (WCST). A sample of 413
with ASD to camouflaging their deficits in social communica- participants (91.6%) was included in the final analysis. The
tions hence lead to missing early diagnosis. Lai et al. (2017) flow chart of the present study is shown in Fig. 1.
defined camouflaging in autism as the discrepancy between
the individual’s external behavioral symptoms in social-inter- Procedure
personal contexts and self-reported dispositional traits. They
found that better camouflaging was associated with EF only The study was approved by the Ethical Committee of the
in females with ASD. These studies suggested that the impact School of Public Health, Sun Yat-sen University. All the
of EF on the manifestation of autism may vary with gender, children and their parents voluntarily participated in this
pointing to the need to explore the gender-specific role of EF study with informed consents. The tests were performed at
in autistic traits. the Research Center for Child and Adolescent Psychologi-
Autistic traits, which are defined as behaviors associated cal and Behavioral Development, Sun Yat-sen University.
with ASD, are known to be distributed continuously across the Each child was tested individually by qualified technicians
general and clinical populations and share a common etiology
(Constantino and Charman 2016; Robinson et al. 2011). EF
deficits were also found in TD individuals with high autis-
tic traits (Ferraro et al. 2016; Gokcen et al. 2009). In light of
these findings, research on autistic traits in the general popu-
lation could be beneficial in understanding ASD as a clinical
disorder.
The aim of the current study was to investigate the associa-
tions between EF and autistic traits in boys and girls using
a school-based sample of children. The autistic traits were
measured using the Social Responsiveness Scale (SRS; scores
of total scale and the subscales including Social Awareness,
Social Cognition, Social Communication, Social Motivation
and Autistic Mannerisms), and EF was assessed with the Wis-
consin Card Sort Test, which is regarded as the quintessential
executive functioning task that is sensitive for the measure-
ment of control and shifting attention, and mental flexibility.
We hypothesized that the manifestation of EF may be different
in boys and girls with high autistic traits.

Fig. 1  The flow chart of the study

13
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).

Autistic traits were assessed using the Chinese version of Intelligence


SRS (Cen et al. 2017). The SRS is a 65-item questionnaire
designed to measure autistic symptomatology (mainly Intelligence was measured using the Wechsler Intelligence
involving reciprocal social behavior) with five specific Scale for Children-Fourth Edition Chinese version (WISC-
symptom domains: Social Awareness, Social Cognition, IV) (Houcan 2009). WISC-IV is an individually adminis-
Social Communication, Social Motivation and Autistic tered and norm-referenced instrument, which consists of 10
Mannerisms (Constantino and Gruber 2012). The SRS has core and four supplemental subtests. The WISC-IV gener-
good internal consistency, high test–retest reliability and ates a full-scale Intelligence Quotient (FSIQ), representing
good discriminative validity (Cen et al. 2017; Constantino overall cognitive ability. In addition, four other composite
et al. 2003). The SRS is rated on 4-point Likert scales (0–3) quotients can be derived: the Verbal Comprehension Index
for each item, with the total raw score ranging from 0 to (VCI), the Perceptual Reasoning Index (PRI), the Work-
195. A higher total score indicates greater levels of autistic ing memory Index (WMI) and the Processing Speed Index
traits. A total raw score of ≥ 56.5 is recommended as a cut- (PSI). The norm mean values of FSIQ and the four com-
off for screening ASD in general population in mainland posite quotients are 100, and the standard deviations are 15.
China (Cen et al. 2017). Accordingly, we classified children The norm of WISC-IV has been established in China. The
who met cut-off score for SRS as having high-autistic-trait validity and reliability of the WISC-IV have been examined
(HAT), and the rest as having low-autistic-trait (LAT). and shown to be satisfactory (Chen et al. 2010).

Executive Function Statistical Analysis

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

13
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

13
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

HAT boys (n = 70) HAT girls (n = 35)


 CC − 0.290 − 0.309* − 0.166 − 0.270 − 0.107 − 0.057 − 0.237 − 0.072 − 0.456* − 0.255 0.161 − 0.085
 FMS − 0.022 − 0.017 − 0.003 − 0.027 0.048 − 0.0571 0.334 0.232 0.265 0.354 − 0.048 0.140
 NPE 0.131 0.163 0.140 0.151 − 0.079 0.051 0.185 0.084 0.423* 0.230 − 0.171 − 0.003
 SE − 0.091 − 0.179 − 0.043 − 0.097 − 0.052 0.059 − 0.373 − 0.213 − 0.539* − 0.339 0.117 − 0.163
LAT boys (n = 169) LAT girls (n = 139)
 CC 0.011 0.013 − 0.046 0.050 − 0.001 − 0.000 0.028 0.052 0.053 0.018 − 0.060 0.035
 FMS − 0.012 0.125 − 0.003 0.063 − 0.141 − 0.112 0.056 0.017 0.016 0.079 0.020 0.051
 NPE 0.045 − 0.049 0.072 − 0.004 0.078 0.048 0.049 − 0.029 0.036 0.030 0.142 − 0.018
 SE − 0.075 − 0.051 − 0.111 − 0.037 − 0.007 − 0.029 − 0.092 0.039 − 0.080 − 0.092 − 0.159 0.009

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

HAT boys (n = 70)


 CC − 1.73 (− 3.27, − 0.20) 0.068 − 0.45 (− 0.78, − 0.11) 0.039 − 0.24 (− 0.59, 0.10) 0.350 − 0.74 (− 1.47, − 0.01) 0.188 − 0.21 (− 0.75, 0.34) 0.753 − 0.10 (− 0.69, 0.49) 0.764
 FMS − 0.21 (− 1.74, 1.31) 0.783 − 0.04 (− 0.37, 0.30) 0.837 − 0.07 (− 0.41, 0.27) 0.866 − 0.08 (− 0.81, 0.64) 0.820 0.10 (− 0.42, 0.62) 0.775 − 0.13 (− 0.69, 0.44) 0.764
 NPE 0.05 (− 0.07, 0.17) 0.667 0.02 (− 0.01, 0.04) 0.263 0.02 (− 0.01, 0.04) 0.350 0.03 (− 0.03, 0.09) 0.552 − 0.02 (− 0.06, 0.02) 0.753 0.01 (− 0.04, 0.05) 0.764
 SE − 0.02 (− 0.14, 0.09) 0.783 − 0.02 (− 0.04, 0.01) 0.263 < 0.00 (− 0.03, 0.02) 0.878 − 0.01 (− 0.07, 0.04) 0.786 − 0.01 (− 0.04, 0.03) 0.775 0.01 (− 0.03, 0.06) 0.764
HAT girls (n = 35)
 CC − 3.25 (− 5.50, − 1.01) 0.011 − 0.12 (− 0.66, 0.43) 0.665 − 0.81 (− 1.36, − 0.27) 0.012 − 1.70 (− 2.88, − 0.52) 0.010 − 0.05 (− 0.82, 0.72) 0.911 − 0.58 (− 1.44, 0.29) 0.460
 FMS 2.01 (− 0.89, 4.92) 0.168 0.31 (− 0.32, 0.94) 0.633 0.74 (0.05, 1.42) 0.044 1.03 (− 0.50, 2.55) 0.180 − 0.28 (− 1.18, 0.62) 0.911 0.22 (− 0.83, 1.27) 0.673
 NPE 0.22 (0.06, 0.37) 0.011 0.01 (− 0.02, 0.05) 0.633 0.05 (0.02, 0.09) 0.012 0.12 (0.05, 0.20) 0.007 < 0.01 (− 0.05, 0.05) 0.911 0.03 (− 0.03, 0.09) 0.597
 SE − 0.28 (− 0.42, − 0.13) 0.002 − 0.02 (− 0.06, 0.01) 0.633 − 0.07 (− 0.10, − 0.03) 0.004 − 0.13 (− 0.21, − 0.05) 0.007 − 0.01 (− 0.06, 0.04) 0.911 − 0.05 (− 0.11, 0.01) 0.440

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

13
Journal of Autism and Developmental Disorders

Executive Composite) of a parent-report measurement (the


Behavior Rating Inventory of Executive Function). But in
the present study, we used EF indicators from a behavioral
task. Therefore, the discrepancy of these findings may due
to the difference in the measurements methods used. Torske
et al. (2018) did not focus on the associations between EF
and specific autistic traits in boys and girls. Further inves-
tigations are needed to clarify whether the EF components
(e.g., Shift and Inhibit) assessed with questionnaires will
show gender-specific associations with autistic traits.
Recent research has shown that EF in children may play
a role in the development of social cognition (Morigu-
chi 2014). In our study, the different association patterns
between EF and autistic traits in boys and girls may result
from the gender differences in social cognition skills, such
as perception of gaze direction and empathy. Gaze cuing
effect, the tendency of orienting to other individuals’ gaze
direction, determines the ability of individuals to capture the
information related to the attention and emotional state of
the individuals they interact with (Frischen et al. 2007). Ear-
lier research found weaker gaze cuing effects in TD males
than females (Deaner et al. 2007). Gender difference was
also reported in empathy (the ability to understand a person’s
Fig. 2  Variances of autistic traits predicted by each executive function
index in boys and girls with HAT. Proportions indicate variances pre- metal states and to respond with an appropriate emotion) in
dicted by( each executive
) function indicators with age and FSIQ which TD females had higher empathy than males (Baron-
together R2(adjusted)  . HAT, high-autistic-trait; SRS Social Respon- Cohen et al. 2014). Both gaze cuing effects and empathy
siveness Scale; CC categories completed; FMS failure to maintain were associated with EF. Gaze cuing effect involves a flex-
set; NPE non-perseverative errors; SE shifting efficiency ible shift of attention (Frischen et al. 2007). While empathy
requires simultaneous processing of multiple information
streams, inhibition of one’s own emotional states and shift-
32.4% and 14.5% respectively), while CC, NPE and SE pre- ing flexibly between one’s own and others’ perspectives and
dicted variances in Social Communication(29.4%, 32.5% motional states (Singer and Lamm 2009). Thus we speculate
and 33.0% respectively). In previous studies, researchers that attention shifting is more related to difficulties in per-
reported that there is association between EF and social ceiving social cues and social interaction in boys with HAT,
cognition in samples with and without ASD. For example, which may be due to their weaker gaze cuing effects. We
Jones et al. (2018) found a significant association between speculate that globe EF (all EF components) is more related
cognitive flexibility and social communication symptoms with abilities in processing social information and reciprocal
in adolescents with ASD. Leung et al. (2016) found that the communication in girls with HAT, which may be due to their
behavioral regulation of the executive processes (i.e., inhibi- higher empathy response.
tion, shifting, and emotional control) could predict the total It is noteworthy that in children with LAT, EF showed
autistic traits (SRS total scores) in children with ASD as no significant association with autistic traits. We speculate
well as in TD children. Gokcen et al. (2009) found a signifi- that there may be other more important factors, for example,
cant negative association between cognitive flexibility and Theory of Mind (ToM), that affect autistic traits in this popu-
total autistic traits in adults and adolescents with sub-clinical lation. Previous studies have demonstrated a link between
high autistic traits. Our study extends the findings of these EF and ToM (Lukito et al. 2017; Miranda et al. 2017). For
studies by incorporating the gender factor. We show that instance, Jones et al. (2018) found that EF had no direct
the associations between EF and specific autistic traits are association with autistic behaviors but had an indirect effect
different in boys and girls. Contrary to our findings, Torske through the association with ToM. Further studies are advo-
et al. (2018) found similar patterns of correlation between cated to test the effect of ToM on gender-specific associa-
EF and total autistic traits (SRS total scores) in boys and tions between EF and autistic traits.
girls with ASD. It should be noted that Torske et al. (2018) High autistic traits appear to cause emotional and behav-
assessed EF using the composite indices (i.e., the Behavioral ioral problems (Lundstrom et al. 2011; Saito et al. 2017).
Regulation Index, the Metacognition Index and the Global Our findings that EF components have a gender-dependent

13
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
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