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https://doi.org/10.1007/s10803-020-04461-z
ORIGINAL PAPER
Abstract
Abnormalities in executive function (EF) are clinical markers for autism spectrum disorder (ASD). However, the neural
mechanisms underlying abnormal EF in ASD remain unclear. This meta-analysis investigated the construct, abnormali-
ties, and age-related changes of EF in ASD. Thirty-three fMRI studies of inhibition, updating, and switching in individuals
with high-functioning ASD were included (n = 1114; age range 7–57 years). The results revealed that the EF construct in
ASD could be unitary (i.e., common EF) in children/adolescents, but unitary and diverse (i.e., common EF and inhibition)
in adults. Abnormalities in this EF construct were found across development in individuals with ASD in comparison with
typically developing individuals. Implications and recommendations are discussed for EF theory and for practice in ASD.
Keywords Autism spectrum disorder · Executive function · Unity and diversity · Development · Fronto-parietal areas ·
Meta-analysis
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Journal of Autism and Developmental Disorders
The Construct of EF in ASD meta-analysis, conducted by Philip et al. (2012), has
explored EF abnormalities in those with ASD. Philip et al.
One explanation for the previous inconsistent findings is included 13 EF studies of ASD. Data for between-group
a clear lack of agreement about the EF construct in those effects (ASD vs. TD) on brain activity were selected. The
with ASD (e.g., Baggetta and Alexander 2016; Barkley results showed greater activation in the left middle fron-
2012). The integrative EF model (unity and diversity) tal gyrus in the ASD group, and greater activation in the
decomposes the EF construct into what is common across right middle frontal gyrus, the left inferior parietal lobe,
all EF processes (i.e., common EF) and what is unique to the left insula, the right posterior cingulate gyrus, and the
each specific EF process (Friedman and Miyake 2017). left lentiform nucleus in the TD group. However, Philip
The specific EF processes are correlated, yet separa- et al.’s meta-analysis integrated all EF processes as unitary
ble. They include inhibition (the restriction of prepotent EF and did not seek to ascertain brain activity specific to
actions); updating (constant monitoring and addition or each of the three fundamental EF processes.
deletion of the contents of working memory); and switch-
ing (task or mindset shifting).
Previous neuroimaging studies of ASD have not fully Age‑Related Changes of EF in ASD
considered this EF construct. For example, Hill (2004)
included planning, mental flexibility, and inhibition in Age-related changes are also worthy of consideration when
order to represent EF. Diamond (2013), however, pos- investigating EF in those with ASD. Until recently, the inte-
ited that planning is a higher-level EF process that the grative model of EF has been generally confirmed by behav-
three fundamental EF processes in the integrative model ioral evidence across different age groups (e.g., Duan et al.
work together to build up. Indeed, among the studies that 2010; Ito et al. 2015; Vaughan and Giovanello 2010). How-
have emphasized the fundamental EF processes, most ever, these studies suggest that the pattern of unity and diver-
have focused on only one or two specific processes; few sity in EF may be quite nuanced and that it can vary with
have evaluated EF across all three. For example, O’Hearn development. At younger ages, different EF processes have
et al. (2008) included only inhibition and updating in been reported as indistinguishable, so that EF in this stage
their investigation of EF, whereas Schmitz et al. (2006) has often been interpreted as a unitary construct (Brydges
explored only inhibition and switching in their attempt to et al. 2014; Wiebe et al. 2011). In later development, how-
understand the specific EF processes in ASD. ever, different EF processes, although they share an overlap-
In addition, among the ASD studies that have focused ping variance (i.e., common EF), become more separable
on a specific EF process, findings are conflicting. For inhi- (Huizinga et al. 2006; Lehto et al. 2003; Senn et al. 2004;
bition, some studies have found significantly increased St Clair-Thompson and Gathercole 2006). Such age-related
brain activation in the inferior frontal gyrus in partici- changes in the EF construct have also been reported in a
pants with ASD in comparison with typically develop- neuroimaging meta-analysis (McKenna et al. 2017). This
ing (TD) controls on go/no-go tasks (Kana et al. 2007; evidence from TD samples indicates that the integrative
Schmitz et al. 2006). But Shafritz et al. (2015) recently model of EF seems to bear a developmental feature.
found that the inferior frontal gyrus was deactivated in Based on neuroscientific evidence from the TD popula-
those with ASD performing two versions of a go/no-go tion, cognitive maturation in EF is believed to be subserved
task (emotional and nonemotional). For updating, Luna by changes in brain activation that continue through child-
et al. (2002) reported deactivation in the prefrontal gyrus hood and begin to reach adult levels in mid-adolescence
and the posterior cingulate gyrus in participants with ASD (Christou et al. 2002; Gogtay et al. 2004). One EF study
in comparison with TD controls. Yet Herrington et al. found that children relied more on the prefrontal areas than
(2015) found increased activation in prefrontal areas in did adults, who relied more on the parietal lobe, indicating a
participants with ASD in comparison with TD controls. transition from the prefrontal areas to the parietal lobe with
As for switching, Schmitz et al. (2006) identified increased increasing age (Houdé et al. 2010). In TD samples, children
activation in the parietal lobe in those with ASD during do not seem to share the completely common neural cor-
task shifting. But Shafritz et al. (2008) provided evidence relates of EF with adults.
to support the opposite view—that reduced activation in In ASD, age-related changes have been reported in the
the parietal lobe was responsible for the underlying abnor- cerebral cortex, limbic structures, and cerebellum (Amaral
malities in switching in those with ASD. et al. 2008). From childhood to adolescence, Amaral et al.
Meta-analysis is an effective way to address these (2008) found an apparent increase in brain size in those
inconsistencies across individual studies (Rothman et al. with ASD in comparison with TD participants, especially
2008). Based on our review, only one neuroimaging in the frontal lobe. Nonetheless, the brain of those with ASD
would result in a normal size by adulthood (Redcay and
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Journal of Autism and Developmental Disorders
Courchesne 2005). Such age-related differences in the brain were implemented as follows. First, data from different EF
structure of those with ASD reflect distinct brain circuits tasks were separated into a young group (< 18 years of age),
recruited by children and adults (Russo et al. 2007). fMRI an adult group (> 18 years), and a whole group (including
studies of ASD have revealed a more direct link between the young and the adult groups). Convergence of brain activ-
abnormalities in the frontal lobe and EF (Hill 2004). The ity across all EF tasks was extracted to identify the brain pat-
failure of the frontal lobe to follow a normal maturational tern for common EF in each of the three groups. The brain
pattern is likely to have long-term consequences for EF pattern of each EF process was identified by calculating
abnormalities in those with ASD (Luna et al. 2002; Ohnishi convergence of activation pertaining to inhibition, switch-
et al. 2000). ing, or updating, separately, in each of the three groups.
Given the evidence for possible effects of age on the These analyses should reveal the neural construct of EF in
neural mechanisms of EF in those with ASD, many stud- those with ASD. Neural abnormalities in EF were revealed
ies have tended to combine participants across different age by comparing common EF and each of the three EF pro-
groups into a single sample, which cannot reflect age-related cesses between the ASD sample and the TD sample in each
changes in EF abnormalities (Mosconi et al. 2009; Philip of the three groups, separately. By comparing common EF
et al. 2012; Wallace et al. 2016). Although a few neuroim- and each of the three EF processes between the young and
aging studies have focused mainly on a specific age range, the adult groups, age effects on the EF construct and the EF
findings are mixed. Specifically, EF abnormalities in those abnormalities in those with ASD were further investigated.
with ASD (including abnormalities in inhibition, updating, We decided to use a cut-off point of 18 years for groups
and switching) have been found in both childhood and adult- because both the behavioral and the neuroimaging literature
hood (Chantiluke et al. 2015; Daly et al. 2014; Gooskens suggest that EF processes including inhibition, updating, and
et al. 2019; Takarae et al. 2007; Vogan et al. 2014; Yerys switching across the development of ASD would be mature
et al. 2015). In contrast, some studies have argued that some in mid-adolescence (Chantiluke et al. 2015; Happé and Frith
EF processes such as those assessed in delayed match-to- 2006; van den Bergh et al. 2014; Yerys et al. 2015) or in
sample tasks and tasks with simple rules are intact in early early adulthood (Lever et al. 2015; Rosenthal et al. 2013;
development (Dawson et al. 2002; Liss et al. 2001). Other Solomon et al. 2014).
studies have also found intact aspects of updating in adult-
hood (Edgin and Pennington 2005). Such discrepancies
across studies may be due to the late maturation of brain Methods
areas including the frontal gyrus that support EF during
development (Gogtay et al. 2004). Given this context, these Studies Search and Selection Criteria
mixed findings of age-related EF abnormalities in those with
ASD are difficult to interpret. Studies for this meta-analysis were identified as follows.
First, a computer search of ERIC, MEDLINE, PsycARTI-
CLES, and PsycINFO databases for studies was conducted
Research Aims from the earliest possible start date through February 2019.
Then, unpublished studies were searched through the Dis-
Since the construct of EF in those with ASD has not been sertation and Masters Abstract indexes in ProQuest Disserta-
established and age-related changes have not been clarified, tions and Theses. The search terms for full-text search com-
EF abnormalities associated with age should be further bined with AND operators were (a) “working memory” OR
investigated in those with ASD. The purpose of the present flexib* OR inhibit* OR execut* OR shift* OR switch* OR
meta-analysis is to identify the neural construct of EF and updat* OR refresh* OR atten*; (b) autis* OR Asperger OR
explore the neural mechanisms underlying abnormal EF, “pervasive developmental” OR PDD OR ASD; (c) fMRI OR
including specific EF processes, in individuals with ASD “functional magnetic resonance.” Next, we hand-searched
across different age groups. citations in prior relevant reviews. Finally, we completed
For this meta-analysis of data from neuroimaging stud- forward and backward searches by reviewing the reference
ies, we used coordinate-based activation likelihood estima- lists of the included studies and searching all the studies that
tion (ALE). fMRI studies that assessed brain activity in cited the included studies in order to identify any that might
high-functioning ASD during EF task performance were have been missed in the former search phases.
included. Specific EF processes of interest included inhibi- The initial search revealed 18,633 studies. Titles and
tion, updating, and switching (Friedman and Miyake 2017). abstracts were then reviewed for removing irrelevant stud-
Data from the contrasts focusing on the within-group effects ies. After 547 duplicate studies and 17,470 irrelevant stud-
in the ASD sample and the TD sample and the between- ies were excluded, 616 studies remained; these were further
group effects (ASD vs. TD) were selected. Data analyses reviewed according to the following criteria:
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Common EF
First‑Level Analyses
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Fig. 4 Brain patterns showing convergence of activation for inhibi- Fig. 5 Brain patterns showing differences in convergence for inhibi-
tion within the ASD sample and the TD sample, respectively. a The tion by comparing the ASD sample and the TD sample. a The whole
whole group. b The young group. c The adult group. IFG inferior group. b The young group. c The adult group. IFG inferior frontal
frontal gyrus, ACG anterior cingulate gyrus, SFG superior frontal gyrus, SMA supplementary motor area, ACGanterior cingulate gyrus,
gyrus, MFG middle frontal gyrus MFG middle frontal gyrus, PreCG precentral gyrus
Second‑Level Analyses the TD sample compared with the ASD sample (Table S8;
Fig. 3).
Comparing common EF between the ASD sample (Contrast Within the ASD sample (Contrast 1), comparing common
1) and the TD sample (Contrast 2) in the whole group, a dif- EF between the young and the adult groups, there was no
ference in convergence was found in the left inferior parietal difference in convergence for the young or the adult group
gyrus for the ASD sample compared with the TD sample. compared with each other. Within the TD sample (Contrast
In the young group, no difference in convergence was found 2), comparing common EF between the two age groups,
for the ASD sample. In the adult group, a difference in con- there was no difference in convergence for the young group,
vergence was found in the left inferior parietal gyrus for the whereas there were differences in convergence in the right
ASD sample (Table S7; Fig. 3). sub-lobar matter, the right inferior frontal gyrus, and the
In contrast, comparing common EF between the ASD right medial frontal gyrus for the adult group.
sample (Contrast 1) and the TD sample (Contrast 2) in the
whole group, differences in convergence were found in
the right inferior frontal gyrus, the right anterior cingulate The Three EF Processes
gyrus, the left supplementary motor area, and the right mid-
dle frontal gyrus for the TD sample compared with the ASD First‑Level Analyses for Contrast 1 (the ASD Sample)
sample. In the young group, differences in convergence were
found in the right inferior frontal gyrus and the right anterior The first-level analyses included 10 experiments with inhibi-
cingulate gyrus for the TD sample compared with the ASD tion (141 foci), four experiments with switching (25 foci),
sample. In the adult group, differences in convergence were and five experiments with updating (63 foci; see Table 1).
found in the right inferior frontal gyrus, the right anterior
cingulate gyrus, and the left supplementary motor area for
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Journal of Autism and Developmental Disorders
In the whole group, the ALE results demonstrated con- For Contrast 3 (16 experiments, 65 foci) and Contrast 4
vergence of activation in the bilateral inferior frontal gyri (17 experiments, 143 foci; see Table 1), no convergence of
and the right anterior cingulate gyrus. No convergence of activation was revealed for any of the three EF processes.
activation was found in the young group, but convergence
of activation was found in the bilateral inferior frontal gyri
in the adult group (Table S5; Fig. 4). Second‑Level Analyses
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Journal of Autism and Developmental Disorders
adult group were compared within the ASD sample (Con- Within the ASD sample, we also identified brain patterns
trast 1) or the TD sample (Contrast 2), separately. of activation for both the young group (in the left inferior
frontal gyrus) and the adult group (in the left inferior frontal
Contributions of the Included Studies to Specific gyrus and the left inferior parietal gyrus). In many EF stud-
Brain Regional Effects ies, the prefrontal areas are well known to be primary brain
areas that support general EF processing (inhibition, updat-
Post-hoc analyses were conducted to provide more detailed ing, switching) in both young individuals and adults in TD
information about the revealed brain areas of convergence. samples (Brázdil et al. 2007; Wang et al. 2010). The present
In the Supplemental Material, we present a list of the stud- findings may indicate that the prefrontal areas also play an
ies that contributed to the specific regional effects, and most important role in individuals with ASD across ages. How-
of the results were stable and not likely to be have been ever, we did not find differences in convergence between the
driven by only a small portion of studies. Specifically, for two age groups for the common EF within the ASD sample.
the first-level analyses within the ASD or the TD sample, Therefore, we suggest that the neural correlates for common
half of the studies or more included in a specific analysis EF in those with ASD may be relatively stable from child-
contributed to the effect in each brain area. For example, 10 hood to adulthood.
studies of inhibition were included in the first-level analysis
for revealing convergence of activation in inhibition. The Inhibition
results showed that five of the 10 studies contributed to the
effect in the right inferior frontal gyrus and six of the 10 Within the ASD sample, we identified a brain pattern of
studies contributed to the effect in the left inferior frontal activation for inhibition in the whole group, mainly in the
gyrus. Less convergence was found in the second-level con- bilateral inferior frontal gyri and the right anterior cingulate
trast analyses, where less than half of the included studies gyrus. In TD samples, the right inferior frontal gyrus has
in a specific analysis contributed to the effect in each brain been found critical for inhibitory control across go/no-go
area, especially for the brain areas in the ASD sample when (Chiu and Egner 2015), stop-signal (Aron 2011), Stroop
compared with the TD sample (only one or two studies). (Kim et al. 2011), and antisaccade (Fitzgerald et al. 2008)
tasks. The right anterior cingulate gyrus has been found
to play a central role in several functions associated with
response inhibition, conflict monitoring, and error detection
Discussion (Botvinick et al. 2004). Findings are similar in ASD studies
(Chan et al. 2011; Kana et al. 2007; Vara et al. 2014). Given
The present meta-analysis is the first to comprehensively this evidence, the right inferior frontal gyrus and the right
explore the construct of EF and the first to investigate EF anterior cingulate gyrus could be the key areas for the inhibi-
abnormalities in individuals with high-functioning ASD tory function in individuals with and without ASD.
across ages. This study provides updated information about Further, within the ASD sample, we did not find any con-
the construct EF and abnormalities of EF associated with vergence of activation in the young group, but we identi-
age in those with ASD on a neural level. fied a brain pattern (in the bilateral inferior frontal gyri) in
adults. In TD samples, previous studies have often failed
The EF Construct and Age‑Related Changes in ASD to find an inhibition factor in young individuals (Karr et al.
2018; McKenna et al. 2017; van der Sluis et al. 2007). With
Common EF increasing age, the process of inhibition emerges (Brydges
et al. 2014; Lerner and Lonigan 2014). Combined with this
Within the ASD sample, we identified a brain pattern of evidence, our findings may indicate that the inhibition-spe-
activation for common EF in the whole group, mainly in cific process may not be observable in individuals with ASD
the bilateral inferior frontal gyri, the left precentral gyrus, until adulthood, in line with TD individuals.
the right superior medial frontal gyrus, and the left inferior
parietal gyrus, consistent with previous ASD studies (Lynch Updating and Switching
et al. 2017; Schmitz et al. 2006). These fronto-parietal areas
were found to be commonly activated across EF tasks in the Within the ASD sample, for updating, we found the conver-
TD samples (Church et al. 2017; Nee et al. 2012; Niendam gence of activation only in the left middle occipital gyrus
et al. 2012; Yaple and Arsalidou 2018). Given the present in the young group. The occipital areas are known to be
findings, the fronto-parietal areas may be the core areas that selective for visual-based functions, such as mirror actions
subserve performance during the common EF processing in (Rizzolatti and Craighero 2004), visual imagery processes
both TD and ASD samples. (Jung and Haier 2007), and face processing (Dalton et al.
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Journal of Autism and Developmental Disorders
2005). ASD studies have proposed that activation in the 2009), indicating the use of different cognitive strategies to
occipital areas may reflect a tendency to rely primarily on successfully solve EF tasks. These findings, together with
visual features and visual attention during cognitive tasks ours, indicate that abnormalities in common EF may be
(Koshino et al. 2007; Mottron et al. 2006; Vogan et al. 2014). associated with abnormal attention control in those with
Given this evidence, our findings may imply that young indi- ASD.
viduals with ASD may utilize visuoperceptual strategies to In contrast, compared with the ASD sample, the TD sam-
perform updating tasks. Hence, the activation in the left mid- ple showed differences in convergence for common EF in the
dle occipital gyrus could not be considered specialized for right inferior frontal gyrus, the right middle frontal gyrus,
updating as a brain pattern in young individuals with ASD. the right anterior cingulate gyrus, and the left supplemen-
In addition, we did not find any convergence of activation tary motor area. Activation in these brain areas is essential
for updating or switching across the three groups. That is, we for performance during EF tasks (Bonini et al. 2009; Wang
failed to identify significant brain patterns for updating or et al. 2010), as well as in supporting sensorimotor function
switching. However, this result should be treated with sub- (Mosconi and Sweeney 2015). It has been reported that sen-
stantial caution due to underpowered analyses of restricted sorimotor deficits are the primary features of ASD (Mosconi
data in our meta-analysis (five experiments and 63 foci for and Sweeney 2015). Abnormalities in these areas under-
updating, four experiments and 25 foci for switching). Alter- lying sensorimotor deficits have been associated with EF
natively, these null results could reflect the heterogeneity in abnormalities (Bock and Girgenrath 2006; Perry et al. 2007;
findings across the included studies of ASD, despite con- Sheridan and Hausdorff 2007) and have even accounted for
sistent task paradigms used for examining updating (n-back them in part (Hyder et al. 1997). Since our findings indicate
tasks) and switching (set-switching or rule-switching tasks) that the ASD sample could be less likely to recruit these sen-
in those studies. Future research, possibly with larger sorimotor areas than would the TD sample during EF tasks,
samples, should continue to explore whether the specific we hypothesize that sensorimotor deficits in those with ASD
processes of updating and switching exist in ASD across may affect these brain areas and thus lead to abnormalities
development, as well as whether the updating or switching in EF (Rødgaard et al. 2019).
measures for the TD population apply to ASD in different In our Introduction, we noted a neuroimaging meta-analy-
age groups. sis (Philip et al. 2012) that also recruited data from between-
In sum, our findings demonstrate that for the ASD sam- group effects (ASD vs. TD) to explore EF abnormalities in
ple, there was a brain pattern of activation for common those with ASD. However, those results show some limita-
EF (in the left inferior frontal gyrus) among children and tions, such as the inclusion of inaccurate data in the analyses
adolescents, and there were brain patterns for common EF and the adopting of an inadequate correction (false discovery
(in part of the fronto-parietal areas) and inhibition (in the rate) to threshold the ALE values. By addressing these limi-
bilateral inferior frontal gyri) in adults. These findings are, tations, we have confirmed some of Philips et al.’s (2012)
to some extent, in line with the body of behavioral literature findings and have extended them by revealing a difference in
on EF development suggesting age-related changes in the EF convergence in the left supplementary motor area for the TD
construct in TD samples (Best and Miller 2010; Karr et al. sample in comparison with the ASD sample. This brain area
2018; Lee et al. 2013; Rottschy et al. 2012). We therefore is often revealed in EF processes in TD individuals (Hazel-
suggest a unitary model of EF (common EF) in children and tine et al. 2000; Scherf et al. 2006; Smolker et al. 2015),
adolescents and a unitary yet diverse model of EF in adults especially in the inhibition of motor behavior (Dinomais
(common EF and inhibition) for ASD individuals. et al. 2009). ASD studies have found abnormal activation
in the left supplementary motor area during EF tasks (Ishii-
The EF Abnormalities and Age‑Related Changes Takahashi et al. 2014; Smith et al. 2004). Combining these
in ASD findings, we propose that the left supplementary motor area
plays an important role in EF abnormalities in ASD.
Common EF Regarding age effects, within the ASD sample, we did not
find differences in convergence between the young and the
Based on the whole group, the ASD sample showed a dif- adult groups for common EF. However, across samples, we
ference in convergence in the left inferior parietal gyrus found a difference in convergence for common EF in the TD
for common EF in comparison with the TD sample. The sample as opposed to the ASD sample in the right inferior
parietal lobe has been found important for spatial atten- frontal gyrus across the young and the adult groups. This
tion and spatial coordinate transformations in TD samples may suggest that the abnormal mechanisms underlying com-
(Merriam et al. 2003). Abnormal parietal activation could mon EF in those with ASD are relatively stable across young
occur with the effort to maintain attention during EF tasks and adult groups. These findings are supported by behavioral
in those with ASD (Fatemi et al. 2002; McAlonan et al. evidence that, overall, EF abnormalities are present from
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Journal of Autism and Developmental Disorders
childhood through adulthood (Dawson 2008; Oznoff et al. meta-analysis or the reliability of the updating and switching
2004; Zelazo and Müller 2002). measures for ASD.
In sum, for common EF, our results show that compared
Inhibition with TD controls, individuals with ASD recruited the left
inferior parietal gyrus but were less likely to recruit the sen-
Based on the whole group, we found a difference in conver- sorimotor areas to perform EF tasks. For inhibition, the left
gence in the left inferior frontal gyrus in those with ASD inferior frontal gyrus could be the core abnormality under-
in comparison with the TD sample. This is consistent with mining inhibition abilities in individuals with ASD. In addi-
previous findings demonstrating that abnormalities in the tion, there were no differences in convergence between the
prefrontal areas undermined inhibitory ability in those with ASD sample and the TD sample for updating or switching.
ASD (Dumontheil et al. 2008; Kana et al. 2007; Schmitz Thus, EF abnormalities in those with ASD may manifest
et al. 2006). The abnormal activation could be due to inef- early in common EF, but with increasing age, they may
ficient effort or neuronal network recruitment in ASD (Rubia manifest in common EF as well as inhibition.
et al. 2006). Of note, in the present study, this difference in
convergence in the inferior frontal gyrus resided only in the Limitations
left hemisphere. On the contrary, in TD samples, the inhibi-
tion process was found to be mediated by the predominantly Some limitations to our meta-analysis should be considered.
right prefrontal areas (Rubia et al. 2006). Thus, this finding To investigate the construct of EF in those with ASD, we
may point toward abnormally left lateralization in individu- conducted an extensive ALE meta-analysis that was robust
als with ASD during inhibition (Paus et al. 1999). (McKenna et al. 2017). In the first-level analyses, conver-
It is also likely that this difference in convergence in the gence of activation for common EF and each of the three
left inferior frontal gyrus may reflect language deficits (e.g., specific processes was found in the young group, the adult
phonological deficits, semantics deficits, and communication group, and the whole group separately. Then, in the second-
disorders) in those with ASD (De Fossé et al. 2004; Tager- level analyses, brain areas commonly activated for each spe-
Flusberg and Joseph 2003). Language deficits are salient cific process compared with common EF was examined for
symptoms for explaining restrictive and repetitive behaviors the three groups separately. Since ALE analyses pool data
in individuals with ASD (Solomon et al. 2014). Previous across studies, they are very likely to include the same study
ASD studies have linked language deficits to abnormalities in common EF and specific process maps, which would lead
in the left inferior frontal gyrus (Hodge et al. 2010; Knaus to a bias in significant convergence. We therefore prevented
et al. 2008; Sharda et al. 2016). Within this context, our any individual study included in two first-level maps from
finding may suggest a unitary site in the left inferior frontal being compared in the second-level analyses. For exam-
gyrus that underlies both language and inhibition deficits in ple, to reveal inhibition-specific activation, the ALE map
those with ASD. for inhibition was compared with that for “common EF”
Regarding age effects, within the ASD sample, we found (updating and switching), which was defined as including
a difference in convergence in the left inferior frontal gyrus all EF processes except inhibition. Corresponding analyses
in the adult group compared with the young group, which were also administered for updating and switching. How-
could indicate that adults with ASD were more likely to ever, due to the small number of qualified studies, some of
recruit this brain area to solve inhibition tasks. On the other these analyses could not be conducted, because at least two
hand, comparing ASD and TD samples, we found a differ- studies must be included in each ALE analysis (Eickhoff
ence in convergence in the right inferior frontal gyrus in et al. 2016). Further, the second-level analyses did not yield
TD adults but not in young individuals. These results, taken any process-specific activation. Thus, our findings on the
together, reveal a lack of significant difference in inhibition construct of EF in those with ASD across ages may have
between children/adolescents with and without ASD, but in been underpowered. Future research should consider recruit-
adults, this difference was becoming pronounced. Thus, we ing sufficient data to clarify the construct of EF in those with
suggest that for those with ASD, abnormalities in inhibitory ASD using this approach.
function may not be manifest until adulthood. Second, it is important to acknowledge issues with the sta-
tistical approach used in this study. ALE, as well as many other
Updating and Switching coordinate-based neuroimaging meta-analytic approaches,
examines spatial convergence of brain effects across individual
The ALE results showed no age-related differences for neuroimaging studies in the null space of random spatial con-
updating and switching within the ASD sample or between vergence (Rottschy et al. 2012). This implies that significant
the two samples (ASD vs. TD). As we have discussed ALE effects should be interpreted as reflecting brain areas
above, these results could owe to limited data in the present commonly associated with a cognitive process across studies
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Journal of Autism and Developmental Disorders
but not as increases or decreases in activation. Similarly, the Conclusions and Implications for Future ASD
contrasts between coordinate-based meta-analyses reveal dif- Studies
ferences in convergence of brain activation between groups but
not convergence of activation in differences between groups. With all these limitations in mind, the present meta-anal-
Since image-based meta-analyses and effect-size signed dif- ysis of neuroimaging data does suggest that the EF con-
ferential mapping do not own these limitations (Radua et al. struct for ASD is unitary in the early stage but unitary and
2012; Salimi-Khorshidi et al. 2009), they provide possibilities partially diverse in later development. Even when com-
for researchers to further discuss EF abnormalities (patterns of pared with TD controls, those with ASD show relatively
increases vs. decreases) in ASD. stable EF abnormalities across development. However, the
Third, we originally aimed to study a wide range of ASD, fractionation of EF abnormalities into specific EF pro-
including high-functioning and other types of ASD. However, cesses is partially supported (mainly in inhibition).
the 33 EF studies included in this meta-analysis focused only These findings may have implications for theory and
on high-functioning ASD. Thus, whether our findings would practice. Theoretically, our findings provide some evi-
generalize across the whole spectrum of individuals with ASD dence that the integrative EF model (Friedman and Miyake
(e.g., individuals with “typical” autism—those with learn- 2017) is partially applicable to those with ASD. Specifi-
ing disabilities and developmental language delay) remains cally, the EF construct and EF abnormalities have a uni-
unresolved. tary and diverse nature in those with ASD, showing more
Fourth, we planned to divide the age groups into several unitary early but becoming more separable with age.
age groups, including children (< 12 years old), adolescents Practically, our findings show that in addition to using
(> 12 & < 18 years old), young adults (> 18 & < 45 years old), behavioral measures, evaluations of neural changes in EF-
middle-aged adults (> 45 & < 65 years old), and older adults related brain areas may provide evidence for the effective-
(< 65 years old). However, owing to the small number of neu- ness of EF interventions for individuals with ASD. Our
roscience EF studies conducted in children or adolescents, findings could not allow any conclusions about increased
we combined children and adolescents into a young group. In or decreased activation in brain areas. Thus, future
addition, no study was conducted in older adults. The exist- research could test what activation patterns (increases vs.
ing brain imaging studies are not well suited to address the decreases) represent training-induced changes in ASD.
important question of whether there are differential brain Brain activity changes in these areas could be indices to
effects across children, adolescents, young adults, middle-aged assess improvements in EF abilities and even the magni-
adults, and older adults. More neuroscience studies associated tude of transfer-related effects on clinical symptoms in
with age would allow a closer look at the neural correlates of those with ASD after EF intervention.
EF processes in ASD across development. Moreover, the establishment of the role of EF in those
Finally, behavioral research suggests that the measurement with ASD in our meta-analysis sheds light for interven-
of EF may make it difficult to explain age-related features of tions in this population. We suggest that any interven-
the EF construct. That is, it is widely acknowledged that EF tion directly targeting the improvement of EF abilities
measures suffer from validity issues such that any tasks tap- by using EF tasks for training may need to consider the
ping a specific EF process often measure other EF processes developmental construct of EF in those with ASD. That
as well. Such validity problems in EF measurement are par- is, early EF interventions may need to consider improv-
ticularly salient among young children, possibly because these ing general EF abilities (common EF), and types of EF
EF tasks are often cognitively demanding (e.g., to perform training tasks may not necessarily moderate intervention
a switching task, besides using switching resources, children outcomes. In contrast, for EF interventions in adults with
often actively use more working memory/updating and inhibi- ASD, researchers might consider programs that not only
tion resources to remember/use switching rules than do adults; consist of training different EF processes but also a spe-
Jacob and Parkinson 2015). Our findings of unclear age effects cific EF process (e.g., inhibition) associated with the tar-
on some EF processes in those with ASD should also be inter- geted individual’s EF behavior.
preted with caution with respect to the validity of EF measures With respect to methodology, all 33 studies included
in young children. in this meta-analysis reported results of whole-brain
analyses. Our search for studies excluded 13 studies that
reported significant effects only in ROI analyses. Of these
13 studies, most defined the inferior frontal gyrus and
anterior cingulate gyrus as ROIs. The left supplementary
motor area and the left inferior parietal gyrus revealed in
our present study were discussed less in the studies using
13
Journal of Autism and Developmental Disorders
the ROI analyses. Additional research on brain activity California Department of Developmental Services. (2019). Fact
and functional connectivity should enable more extensive book: Fiscal year 2017–2018, Sixteenth edition. Retrieved
August 30, 2019, from https://www3.dds.ca.gov/FactsStats/
examination of the functional roles of these brain areas in docs/DDS_FactBook_2019.pdf
the neural basis of EF abnormalities in those with ASD. Chan, A. S., Han, Y. M., Leung, W. W. M., Leung, C., Wong, V. C.,
& Cheung, M. C. (2011). Abnormalities in the anterior cingu-
late cortex associated with attentional and inhibitory control
Author Contributions ZZ conceived of the study, participated in the deficits: A neurophysiological study on children with autism
coordination of the study, performed literature search, data extraction, spectrum disorders. Research in Autism Spectrum Disorders,
coding, and statistical analysis, participated in the interpretation of the 5, 254–266.
data, and drafted the manuscript; PP participated in the coordination of Chantiluke, K., Barrett, N., Giampietro, V., Santosh, P., Brammer, M.,
the study, contributed to the interpretation of the data, and helped draft Simmons, A., et al. (2015). Inverse fluoxetine effects on inhibi-
the manuscript; DZ helped draft the manuscript. All authors have read tory brain activation in non-comorbid boys with ADHD and with
and approved the final manuscript. ASD. Psychopharmacology (Berl), 232, 2071–2082.
Chiu, Y. C., & Egner, T. (2015). Inhibition-induced forgetting: When
more control leads to less memory. Psychological Science, 26,
Funding No funding was received for this study. 27–38.
Christou, C., Spanoudis, G., Demetriou, A., & Platsidou, M. (Eds.).
Compliance with Ethical Standards (2002). The development of mental processing: Efficiency, work-
ing memory, and thinking. Boston, MA: Blackwell.
Conflict of interest The authors declare no conflicts of interest. Church, J. A., Bunge, S. A., Petersen, S. E., & Schlaggar, B. L. (2017).
Preparatory engagement of cognitive control networks increases
Ethical Approval All procedures in this meta-analysis were in accord- late in childhood. Cerebral Cortex, 27, 2139–2153.
ance with the ethical standards of the institutional and/or national Craig, F., Margari, F., Legrottaglie, A. R., Palumbi, R., De Giambat-
research committee and with the 1964 Helsinki declaration and its tista, C., & Margari, L. (2016). A review of executive function
later amendments or comparable ethical standards. deficits in autism spectrum disorder and attention-deficit/hyper-
activation disorder. Neuropsychiatric Disease and Treatment, 12,
1191–1202.
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