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Li 2024 Patrones de Activacion Cortex Prefrontal

This study reviews the activation patterns of the prefrontal cortex in children with Autism Spectrum Disorder (ASD) and Attention Deficit Hyperactivity Disorder (ADHD) during executive function tasks using functional Near-infrared Spectroscopy (fNIRS). It finds that both disorders exhibit opposite PFC activation patterns compared to typically developing controls, suggesting distinct neurophysiological profiles. The review includes 11 studies that met strict criteria, highlighting the importance of understanding these patterns for better identification and treatment of ASD and ADHD.
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0% found this document useful (0 votes)
29 views10 pages

Li 2024 Patrones de Activacion Cortex Prefrontal

This study reviews the activation patterns of the prefrontal cortex in children with Autism Spectrum Disorder (ASD) and Attention Deficit Hyperactivity Disorder (ADHD) during executive function tasks using functional Near-infrared Spectroscopy (fNIRS). It finds that both disorders exhibit opposite PFC activation patterns compared to typically developing controls, suggesting distinct neurophysiological profiles. The review includes 11 studies that met strict criteria, highlighting the importance of understanding these patterns for better identification and treatment of ASD and ADHD.
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© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
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Journal of Psychiatric Research 172 (2024) 187–196

Contents lists available at ScienceDirect

Journal of Psychiatric Research


journal homepage: www.elsevier.com/locate/jpsychires

ASD and ADHD: Divergent activating patterns of prefrontal cortex in


executive function tasks?
Yin Li , Shuai Ma , Xin Zhang , Lei Gao *
Department of Maternal, Child & Adolescent Health, School of Public Health, Tianjin Medical University, Tianjin, China

A R T I C L E I N F O A B S T R A C T

Keywords: The functional Near-infrared Spectroscopy (fNIRS) has been more and more widely used to measure the acti­
Prefrontal cortex (PFC) vation state of prefrontal cortex when performing function-related tasks among children with various develop­
Autism spectrum disorder (ASD) mental disorders. Children with autism spectrum disorder (ASD) and attention deficit hyperactivity disorder
Attention deficit hyperactivity disorder
(ADHD) have shown obvious executive function defects. We aimed to summarize the studies with fNIRS, to
(ADHD)
Executive function (EF)
summarize the activation patterns of prefrontal cortex (PFC) of participants with ASD or ADHD in performing
Functional near-infrared Spectroscopy(fNIRS) functional tasks. We selected 630 articles according to PRISMA guidelines, and the eligibility criteria were: 6–16
years old individuals diagnosed with ASD or ADHD by DSM-4 or 5, using fNIRS, having executive function (EF)
task, typical development (TD) control, and between-group comparison of PFC activation. Eleven studies were
finally included in the quantitative analysis, and compared to TD, ASD and ADHD showed the opposite PFC
activation patterns during n-back tasks. We discussed the task-specific PFC activation in young participants with
ASD and ADHD, and provided some new ideas on that issue.

1. Introduction exhibit deficits in various aspects of EFs, which are related to the eti­
ology hypothesis of ASD, such as theory of mind, social cognition, social
Autism Spectrum Disorder (ASD) is a severe neurodevelopmental impairment, restricted and repetitive behavior patterns and broader
disorder characterized by social-communicative atypicality and a influence on quality of life (Leung et al., 2016; Mostert-Kerckhoffs et al.,
restrictive and rigid repertoire of behaviours (American Psychiatric 2015; Pellicano, 2007). Similarly, individuals with ADHD show consis­
Association, 2013). According to the most recent estimates, as many as 1 tent impairments in EFs, with deficits contributing to symptoms such as
in 36 children were diagnosed with ASD in 2020 in the United States hyperactivity, impulsivity, and inattention (Huang-Pollock et al., 2012;
(Maenner et al., 2023), which represents a more than 10-fold increase in Willcutt et al., 2005; Craig et al., 2016; Pennington and Ozonoff, 1996).
prevalence over the past 50 years. ASD is often comorbid with Despite the association between clinical symptoms and EFs impairments
attention-deficit/hyperactivity disorder (ADHD), with rates ranging in both ASD and ADHD, it is still unclear whether these deficits reflect
from 30% to 60% in community samples (Gjevik et al., 2011; Salazar additive comorbidity or distinct impairments in each disorder.
et al., 2015). The co-occurrence of ASD and ADHD raises questions EFs is a series of mental processes that allow individuals to achieve
about whether they are distinct disorders or manifestations of diseases complex goals through flexible information manipulation, which in­
sharing the same pathogenesis (van der Meer et al., 2012). Further, cludes playing with ideas, taking time to think before acting, meeting
several models have been proposed to explain this comorbidity (Rom­ unanticipated challenges, resisting temptations, and staying focused
melse et al., 2011; Sinzig et al., 2008; Tye et al., 2014). For example, the (Diamond, 2013; Rabinovici et al., 2015). Components of EFs have been
additive model suggests that ASD and ADHD have independent but mainly categorized as inhibitory control, cognitive flexibility and
related risk factors, resulting in a combination of two separate condi­ working memory (Diamond, 2013; Lehto et al., 2003; Miyake et al.,
tions (Banaschewski et al., 2007). And some studies have shown that 2000), and commonly used tasks include the Wisconsin Card Sort Test
impairments of executive functions (EFs) may be the common patho­ (WCST), Tower of London, verbal fluency test, Go/no go task, Stroop
genesis of ASD and ADHD (Cremone-Caira et al., 2021; Karalunas et al., task and n-back task, with ASD and ADHD show varying degrees of EFs
2018; Pellicano et al., 2006). For example, individuals with ASD often impairments (Chen et al., 2020; Diamond, 2013; Guiney and Machado,

* Corresponding author.
E-mail address: [email protected] (L. Gao).

https://doi.org/10.1016/j.jpsychires.2024.02.012
Received 29 November 2022; Received in revised form 22 January 2024; Accepted 1 February 2024
Available online 10 February 2024
0022-3956/© 2024 Elsevier Ltd. All rights reserved.
Y. Li et al. Journal of Psychiatric Research 172 (2024) 187–196

2013; Niendam et al., 2012). Functional magnetic resonance imaging near-infrared spectroscopy OR fNIRS OR NIRS). Additional studies were
(fMRI) studies are increasingly used to understand abnormal neural identified by manually scanning the references of included studies and
structure and atypical brain responses underlying EFs dysfunction in recent review articles.
both conditions (May and Kana, 2020; Nugiel et al., 2020; Vaidya et al.,
2020; Zhang et al., 2020). These studies have significantly deepened our 2.3. Study selection
understanding of the neural bases underlying these disorders, especially
the critical role of the prefrontal cortex (PFC) (May and Kana, 2020; Studies were selected if they met the following criteria: (1) applied
Zhang et al., 2021). For example, the autistic individuals exhibited fNIRS, (2) monitored site locates at PFC, (3) included psychiatric pa­
reduced activation in the PFC (specifically BA9 and BA10) when tients diagnosed with ASD or ADHD based on the DSM, ICD, or other
engaging in perception tasks compared to typical controls (Jassim et al., established diagnostic criteria, (4) included psychiatric patients aged
2021). Similarly, individuals with ADHD demonstrated decreased pre­ 6–16 years old, (5) used the executive function tasks, (6) enrolled
frontal cortex activation during both neurological and emotional tasks healthy controls, and (7) reported original data. In addition, a study was
compared to typically developing controls (Mauri et al., 2018). Despite excluded if it (1) was a review paper, protocol, or case study, (2) was not
its widespread use, fMRI has several limitations, particularly in pediatric written in English, (3) was an animal study, (4) patients had the medi­
populations. These include high sensitivity to movement artifacts, cation during the experiment, or (5) patients diagnosed with hyper­
acoustic noise interference, limited ecological validity, and potential tension or other diseases impact on hemodynamic changes. In addition,
adverse effects of ultra-high field MRI in children (Aslin and Mehler, we did not list handedness as an inclusion criterion because we had no
2005; Gossé et al., 2022). In recent years, the utilization of functional hypothesis that handedness would influence the difference in cortical
near-infrared spectroscopy (fNIRS) has gained significant prominence in activation between patients and controls. The full texts of all screened
studying brain activity. Its successful implementation in neuro­ articles were then retrieved for eligibility assessment, based on the same
developmental research stands out as one of the most promising areas set of criteria.
(Lloyd-Fox et al., 2010). fNIRS is a non-invasive optical imaging tech­
nique that measures changes in hemoglobin (Hb) concentrations within 2.4. Data extraction
the brain by means of the characteristic absorption spectra of Hb in the
near-infrared range (Sangani et al., 2015). fNIRS has emerged as a One reviewer (Y L) extracted data from the newly identified studies
promising neuroimaging technique for social neuroscience, primarily according to the selection criteria. In the case of any uncertainty in data
due to its portability, high ecological validity, motion artifact resistance, extraction, L G and X Z were consulted. A spreadsheet was used to
and cost-effectiveness (Gossé et al., 2022). The aforementioned advan­ document all data extracted from the studies. In addition to the first
tages of fNIRS, in comparison to fMRI, render it particularly valuable authors’ names and publication dates of all studies, the following in­
when working with pediatric populations (Cui et al., 2011). Leveraging formation regarding the research design, experimental paradigm, fNIRS
its distinctive strengths, integrating fNIRS with a range of cognitive measurement, data preprocessing, and data analysis was extracted from
assessment tools presents significant benefits in detecting aberrations in each identified article: sample characteristics, task design, signal
neuronal activity within the brains of individuals with ASD and ADHD. acquisition, data preprocessing, data analysis and factors affecting the
Exploring the similarity between ASD and ADHD in EF dysfunction level of oxy-hemoglobin increases. We attempted to contact the study
may provide important insight into the best way to identify and treat the authors, however, we were unable to obtain additional information or a
two most serious developmental disorders in childhood, and potentially response.
reduce their development risk. We aim to comprehensively examine the
most recent fNIRS studies pertaining to EFs impairments in children and 2.5. Data analysis
adolescents with ASD or ADHD, with a specific focus on the activation
patterns in the PFC. We strictly defined the type of cognitive tasks as Data were only extracted from the peak change in oxy-hemoglobin
interference and attention, such as the go/no-go, “joint-attention” after the initiation of the intervention stimulus. In studies where mul­
Stroop and the n-back, as well as the chronological age (less than 18 tiple fNIRS channels were used over an area of interest, a single data
years old) and IQ (more than 70) of the participants, because age and IQ point was selected that represented the area. We chose the most
strongly correlated with EFs. We hypothesis that ASD and ADHD chil­ orthogonal comparison, cooperation and more than one comparison
dren have the same hemodynamic responses during executive function between other conditions. If more than one channel per region was re­
tasks, i.e., generalized hypo-activation in PFC. ported, we selected the most central channel to the reported brain re­
gion. We transformed effect sizes to Hedges’ g, similar to classical
2. Methodology Cohen’s d, which controls potential biases in studies with small sample
sizes (Czeszumski et al., 2022; Yeung and Lin, 2021). We included
2.1. Protocol and registration commonly reported oxy-hemoglobin outcomes among children with
ASD, ADHD, and TD in the quantitative analysis (meta-analysis). We
We conducted this systematic review by the Preferred Report Item calculated the standardized mean difference (SMD) among children with
(PRISMA) guidelines (Stroup et al., 2000) for systematic review and ASD, ADHD, and TD using the Z-score means (or unadjusted means),
meta-analysis. We have registered the research project in Prospero In­ standard deviations (SD), and sample sizes of both groups. If the full text
ternational Center for Prospective Systematic Review (CRD did not contain SD, we calculated SD from standard error or confidence
42022299580). interval (CI). A random-effects meta-analysis was conducted to calculate
pooled changes of relative oxy-hemoglobin of each disorder, given that
2.2. Search strategy heterogeneity among studies (Borenstein et al., 2010). We conducted
subgroup and meta-regression analyses to explore the source of het­
We searched for studies indexed in the online databases PubMed, erogeneity in the type of disease. Two subgroups in each meta-analysis
Embase, Web of Science, and Cochrane Library from January 1st, 2000 assess the effects of tasks on PFC oxy-hemoglobin in all subjects: fNIRS
and November 30th, 2023. The following search terms were used: with ASD or ADHD and fNIRS with TD. We reported the I2 statistic and
(prefrontal lobe OR prefrontal cortex OR PFC) AND (autism OR autism Cochran’s Q to indicate the degree of heterogeneity between studies
spectrum disorder OR pervasive developmental disorder OR attention- (Higgins et al., 2019). Our threshold for statistical significance was p <
deficit/hyperactivity disorder OR attention deficit disorder with hy­ 0.05. All analyses were performed using STATA statistical software
peractivity) AND (teen OR children OR adolescent) AND (functional package, version 15.0 using metan, metainf, and metareg commands.

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2.6. Study quality assessment Xiao et al., 2012; Zhu et al., 2015, 2023). No studies were reported using
an exact duplicate sample from any earlier studies.
Two authors (Y L and S M) assessed the quality of each included
study using a modified version of the Newcastle-Ottawa Scale, which 3.2. Basic characteristics of included studies
appraises sample representativeness and size, participation rate, statis­
tical quality, and ascertainment of diagnosis (Stang, 2010) (see the As shown in Table 1, these 11 studies represent oxy-hemoglobin data
attachment). from 481 participants. Four (36.36%) studies were ASD studies, six
Study quality was assessed in the included studies and the potential (54.55%) studies were ADHD studies, and 1 (9.09%) study was ASD and
total score ranged from 0 to 5 points. Studies were judged to be of low ADHD study. Therefore, we separately extracted ASD patients compared
risk of bias (<3 points), middle risk of bias (=3 points), or high risk of to typically developing children and ADHD patients compared to typi­
bias (>3 points). cally developing children. A total of 93 children with ASD, 146 children
with ADHD, and 242 children with typical development were enrolled in
3. Results these studies. All subjects have an IQ of over 70 (high-functioning
children). The age of participants in the ASD group ranged from 6.5 to
3.1. Study selection 14 years, while those in the TD group ranged from 6 to 14 years.
Similarly, children with ADHD were between 6 and 14 years old,
Fig. 1 illustrates the PRISMA flow diagram of the literature search. compared with those of TD children ranging from 6 to 14 years.
The initial search identified 630 citations, and no gain was identified by Of the 11 studies, 9 were from China, and 2 were from Japan. A total
checking the reference lists of relevant articles. After 383 duplication of 3 studies were published in 2015 and before, 2 used DSM-4 as the
removal, 247 articles needed further screening according to title, ab­ diagnostic criteria, 1 used DSM-5 as the diagnostic criteria, and 8 studies
stract and full text. In addition, 45 full-text studies were assessed as were published after 2015, all using DSM-5 as the diagnostic criteria.
qualified. Finally, 11 articles were included in the qualitative synthesis, The tasks in the above-mentioned 11 studies were all executive func­
and 11 articles were included in the quantitative synthesis (Table 1) (Gu tional tasks: 2 of which were the Stroop color-word task, 3 used the go/
et al., 2017, 2018; Han et al., 2022; Krishnamurthy et al., 2020; Miao no go task, 1 used the Stroop task and go/no go task comprehensively, 1
et al., 2017; Negoro et al., 2010; Uratani et al., 2019; Wu et al., 2023; used the joint/non-joint attentional task, and 4 used the working

Fig. 1. PRISMA Flow Diagram


*ASD, autism spectrum disorders; ADHD, attention-deficit/hyperactivity disorder.

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Table 1
Study characteristics and qualitative analysis.
reference country disease diagnosis tasks patients (N healthy location fNIRS Number of wavelengths inter-
type criteria (M/F), controls (N of fNIRS instrument channels of fNIRS light probe
mean age (M/F), mean (region) intervals
(SD) age (SD)
[range]) [range])

Uratani et al., Japan ASD DSM-5 Stroop 12(12/0), 12(12/0), PFC Hitachi 24 760/840 nm 3.0 cm
2019 color- 9.75(2.26) 9.50(2.20) ETG-4000
word task [7–15] [6–12]
Zhu et al., 2015 China ASD DSM-4 joint/non- 20(16/4), 20(14/6), PFC FOIRE- 22 780/805/830 3.0 cm
joint 8.75(1.34) 8.09(1.27) 3000 nm
attention [6.5–11] [6–10]
Krishnamurthy China ASD DSM-5 n-back 20(20/0), 19(19/0), PFC Hitachi 52 695/830 nm 3.0 cm
et al., 2020 task 10.16(1.04) 10.28(0.67) ETG-4000
[8–12] [8–12]
Xiao et al., 2012 China ASD DSM-5 Stroop 19(19/0), 16(16/0), PFC JH-NIRS- 16 735/805/850 NA
task go/no 10.11(2.08) 9.69(1.74) BR-05 nm
go task [8–14] [8–14]
Han et al., 2022 China ASD DSM-5 n-back 22(19/3), 24(17/7), PFC Hitachi 52 695/830 nm 3.0 cm
task 10.1(1.0) 10.2(0.8) ETG-4000
[8–12] [8–12]
Gu et al., 2017 China ADHD DSM-5 n-back 15(10/5), 16(10/6), right Hitachi 52 695/830 nm 3.0 cm
task 7.6(1.4) 7.3(1.3) dlPFC ETG-4000
[6–9] [6–9]
Gu et al., 2018 China ADHD DSM-5 n-back 25(16/9), 25(16/9), right Hitachi 52 NA 3.0 cm
task 7.5(1.2) 7.4(1.1) dlPFC ETG-4000
[6–9] [6–9]
Miao et al., 2017 China ADHD DSM-5 go/no-go 14(10/4), 15(11/4), PFC Hitachi 52 695/830 nm NA
task 7.71(0.99) 7.67(1.05) ETG-4000
[6–9] [6–9]
Xiao et al., 2012 China ADHD DSM-5 Stroop 16(16/0), 16(16/0), PFC JH-NIRS- 16 735/805/850 NA
task go/no 9.75(1.18) 9.69(1.74) BR-05 nm
go task [8–14] [8–14]
Negoro et al., Japan ADHD DSM-4 Stroop 20(18/2), 20(17/3), PFC Hitachi 24 760/840 nm 3.0 cm
2010 Color- 9.55(1.93) 9.35(2.13) ETG-100
Word Task [6–13] [6–13]
Wu et al., 2023 China ADHD DSM-5 go/no-go 32(28/4), 31(24/7), PFC NirScan- 48 735/808/850 3.0 cm
task 9.53(1.44) 10.10(1.27) 6000 A nm
[8–13] [8–13]
Zhu et al., 2023 China ADHD DSM-5 go/no-go 24(21/3), 28(14/14), PFC Hitachi 52 695/830 nm 3.0 cm
task 7.75(1.36) 8.07(1.61) ETG-4000
[6–12] [6–12]

* PFC, Prefrontal Cortex; dlPFC, Dorsolateral Prefrontal Cortex.

memory task (n-back task). As to the near-infrared spectroscopy functional tasks. We performed a regression analysis using disease type
equipment used in the studies, 7 of which were Hitachi ETG-4000, 1 (ASD VS ADHD), which was not the source of heterogeneity (z = − 1.62,
study was FOIRE-3000, 1 study was JH-NIRS-BR-05, 1 study was Nir­ P = 0.105). A sensitivity analysis was performed as shown in Fig. 3, in
Scan-6000 A, and 1 study was Hitachi ETG-100. All the studies reported the ASD group, results from two studies which used working memory
channel counts ranging from 16 to 52, with a median channel count of task were reversed from those of the other studies. After elimination,
52. Nine studies reported a spacing of 30 mm between sources and de­ results were shown in Fig. 2C, when the random-effects model was
tectors. In 11 studies, the channels covered the prefrontal cortex. included as a whole, the overall effect was significant (mean = − 0.99,
CI: − 1.20 to − 0.78, Z = − 9.209, P < 0.001), and there was relatively
3.3. Meta-analysis low heterogeneity (I2 = 0.0%, P = 0.904). This indicated that the
working memory task might be the source of heterogeneity, which
In the overall meta-analysis, we found that, compared with typically meant that autistic children have task-specific hemodynamic responses.
developing children, children with ASD and ADHD performed functional Further subgroup analysis showed in Fig. 2D that compared with typi­
tasks with different patterns of activation of the prefrontal cortex. As cally developing children, children with ASD showed significantly
shown in Fig. 2A, when the random-effects model was included as a reduced PFC activation and significant effects (Mean = − 1.00, CI: − 1.42
whole, the overall effect was not significant (mean = − 0.55, CI: − 1.13 – to − 0.57, Z = − 4.619, P < 0.001), with relatively low heterogeneity (I2
0.03, Z = − 1.864, P = 0.062), and there was relatively high heteroge­ = 0.0%, P = 0.663). Considering that both eliminated studies (Han et al.,
neity (I2 = 88.4%, P < 0.001). Further subgroup analysis (Fig. 2B) 2022; Krishnamurthy et al., 2020) performed the same task (working
showed that compared with the TD children, children with ASD showed memory task), an inter-group comparison of ASD and ADHD was per­
insignificantly reduced PFC activation and insignificant effects (Mean = formed for this task, and the results are shown in Fig. 2E, the difference
0.11, 95% CI: − 1.25 – 1.47, Z = 0.158, P = 0.874), with relatively high between the two groups was considered to be statistically significant (P
heterogeneity (I2 = 94.1%, P < 0.001). Compared with the TD children, = 0.003). It showed the opposite PFC activation patterns during n-back
children with ADHD showed significantly reduced PFC activation and tasks in children with ASD and ADHD. Finally, we analyzed publication
significant effects (mean = − 0.99, 95% CI: − 1.23 to − 0.75, Z = − 7.967, bias, as shown in Fig. 4 Egger’s test showed that there was no publica­
P < 0.001), with lower heterogeneity (I2 = 0.0%, P = 0.773), and the tion bias in all the studied executive functions (t = 0.81, p = 0.439).
difference between the two groups was not considered to be statistically
significant (P = 0.118). This indicates that the activation of the cerebral
cortex of ADHD patients is generally weakened when performing

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Fig. 2A. Forest plot for overall oxy-hemoglobin levels using fNIRS in each study.

3.4. Study quality assessment specific EFs task is designed to evaluate one or more of these core
components, for example, the Stroop and Go/No-go tasks focus on the
Table 2 reports the results of our study quality assessment. Studies inhibitory control (Chen et al., 2020; Diamond, 2013; Guiney and
included in the review on average scored 4.36 out of 5 and ranged be­ Machado, 2013; Niendam et al., 2012). Although there is currently no
tween 0 and 5. The sample size of 2 studies is less than 30, and that of 9 clear relationship between joint attention tasks and EFs, from the
studies is higher than 30. Six studies indicated the source of samples, and perspective of the category of joint attention (the definition of atten­
there was more than one site, while the other five failed to clarify the tion), the joint attention task is more closely related to the inhibition
source of samples. All studies were diagnosed as DSM-IV or DSM-V by control because the self-management and self-control of EFs enable in­
clinical psychiatric doctors, and all reported basic data information. dividuals to process more and more complex information over extended
periods (Stern and Maeir, 2014). The n-back task is widely utilized as a
4. Discussion versatile paradigm for investigating working memory, offering consid­
erable flexibility that allows researchers to tailor the task parameters to
We conducted a meta-analysis of the literature on the use of task- their preferences or the cognitive capabilities of the participants. These
state fNIRS to detect the activation of the cerebral cortex during EF parameters include the complexity of the stimuli, inter-stimulus in­
tasks of ASD and ADHD, and found that the weakened activation pattern tervals, and the working memory span relative to preceding stimuli.
of the PFC was different in different EF tasks in ASD and ADHD: for However, the n-back paradigm may bring about a problem that if the
ADHD, the PFC activation was weakened in all the EF tasks, and the task employed during testing is too simplistic, such as when there exists
blood flow signal was reduced compared with that of the TD controls, a significant cognitive disparity between the study group (e.g. ASD) and
indicating that ADHD had universal executive function impairments, the TD control group, the task may be excessively easy for accommo­
which was closely related to prefrontal developmental disorders and/or dating the study group’s abilities. Consequently, the TD control group
functional impairment. However, ASD participants showed task-specific may also complete the task with ease, resulting in minimal activation
heterogeneity because different tasks required different EF components. and an apparent discrepancy in activation levels between the study and
As to the ASD group, compared with TD controls, three studies showed control groups. This phenomenon has been reported in the fMRI study of
reduced prefrontal cortex activation compared with TD controls under cognitive function in patients with schizophrenia (Fukumoto-Motoshita
the Go/No-go task, Stroop task, and joint attention tasks, while the other et al., 2009). Therefore, when analyzing the brain activation patterns of
two showed increased prefrontal cortex activation under the N-back ASD subgroups during EFs tasks, it is crucial to consider the impact of
tasks. The presence of heterogeneity in EFs may be attributed to varia­ varying task difficulties on activation differences. Additionally, match­
tions in the structural composition and distinct processes associated with ing the intelligence levels between the research and control groups may
specific EFs (Larson et al., 2020; Zhang et al., 2020). Although there is help mitigate this phenomenon. Our findings demonstrate that among
still debated, the majority of researchers agree upon the three principal the brain activation patterns elicited by EF tasks in the ASD group, tasks
components of EFs: inhibitory control, working memory, and cognitive emphasizing inhibitory control reveal notable deficiencies in PFC acti­
flexibility (Diamond, 2013; Lehto et al., 2003; Miyake et al., 2000). Each vation compared to the TD control group. This is consistent with a

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Y. Li et al. Journal of Psychiatric Research 172 (2024) 187–196

Fig. 2B. Forest plot for overall oxy-hemoglobin levels using fNIRS in subgroup analysis.

Fig. 2C. Forest plot for overall oxy-hemoglobin levels using fNIRS in each study after elimination.

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Y. Li et al. Journal of Psychiatric Research 172 (2024) 187–196

Fig. 2D. Forest plot for overall oxy-hemoglobin levels using fNIRS in subgroup analysis after elimination.

Fig. 2E. Forest plot for overall oxy-hemoglobin levels using fNIRS in subgroup analysis under n-back tasks.

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Y. Li et al. Journal of Psychiatric Research 172 (2024) 187–196

regions in ADHD patients as compared to the TD control group. Addi­


tionally, attention activity was reduced in the right dorsolateral pre­
frontal cortex, posterior basal ganglia, thalamus, and parietal regions.
These findings support Barkley’s hypothesis regarding the EF model of
the PFC (Barkley, 1997a, 1997b). The use of fNIRS to investigate pre­
frontal cortex activation patterns during executive function-related tasks
in ADHD patients can yield similar results as those obtained from fMRI
studies, offering advantages such as low equipment cost, simple opera­
tion, strong device mobility, less restriction on subjects, and good ex­
ercise tolerance. fNIRS is expected to replace fMRI to study the abnormal
activation of the prefrontal cortex in ADHD patients when performing
functional tasks. Nevertheless, it is essential to acknowledge that fNIRS
can only measure superficial cerebral cortex activity at a depth of 2–3
mm, while deeper cortex and subcortical regions remain undetected.
Therefore, it is more appropriate to focus on the prefrontal cortex and
temporal cortex, which are associated with social cognition, language
processing, and executive functions. As such, it is premature to replace
fMRI entirely with fNIRS for studying the executive function of ADHD
Fig. 3. Sensitivity analysis.
patients. Future research should concentrate on examining the sensi­
tivity and specificity of fNIRS and fMRI for a specific EF component.
Interestingly, we observed distinct activation patterns in the right
PFC during the n-back task in the ASD and ADHD groups. Specifically,
during the 1-back task, the ASD group exhibited over-activation,
whereas the ADHD group demonstrated under-activation compared to
the TD control group. This suggests potential differences in working
memory impairment between individuals with ASD and ADHD, which
was consistent with the previous studies. For example, Chantiluke et al.
(2015b) investigated the effects of fluoxetine and placebo on the N-back
task in patients with ASD and ADHD. They found that in the placebo
group, the right dorsolateral prefrontal cortex (DLPFC) of subjects with
ADHD and ASD exhibited under-activation relative to the control group.
However, compared to the TD group, fluoxetine induced contrasting
effects on frontal lobe dysfunctions in both disorders, down-regulating
abnormally increased frontal activation in ASD and up-regulating
abnormally decreased frontal activation in ADHD. Furthermore, Chan­
tiluke et al. (2015a) observed opposite effects of fluoxetine on the
medial prefrontal cortex (mPFC) during reversal learning in ADHD and
Fig. 4. Egger’s publication bias plot. ASD subjects. These studies collectively suggest that EF dysfunction
plays distinct roles in the pathogenesis of ASD and ADHD. The distinct
Japanese study that suggested that the low activation of the right PFC activation patterns observed in n-back tasks may be attributed to
could be regarded as a potential biomarker for identifying ASD children divergent attentional impairments in individuals with ASD and ADHD.
in the Go/No-go task (Ikeda et al., 2018). ASD is characterized by a tendency to focus excessively on details while
In the ADHD group, PFC activation was consistently weaker than neglecting holistic processing, particularly in tasks involving face
that of the TD control group across five studies under the Go/No-go task, recognition (Tian et al., 2023), whereas ADHD is associated with broad
Stroop task, and N-back task. Similar conclusions were reached in and deep attentional impairments (Craig et al., 2016). In the context of
related fMRI studies. For example, Hart et al. (2013) conducted a the 1-back tasks, which primarily assess attentional depth rather than
meta-analysis of 21 inhibitory control studies (287 ADHD patients and breadth, the over-activation of the DLPFC in ASD individuals can be
320 control subjects) and 13 attention function studies (171 ADHD pa­ attributed to their attention-to-detail characteristic. Our findings
tients and 178 control subjects) under fMRI, revealing reduced inhibi­ emphasize the differential role of EF dysfunction in the pathogenesis of
tory activity in multiple regions, including the right lower frontal cortex, ASD and ADHD. Further research on this topic holds significant value.
accessory motor area, anterior cingulate cortex, and striatum-thalamus Firstly, it contributes to a comprehensive understanding of the

Table 2
Study quality assessment.
Reference Representativeness Sample size Non-respondents Validity of diagnosis Quality of statistics Total score Quality score

Mitsuhiro Uratani et al., 2019 0 0 1 1 1 3 middle


Huilin Zhu et al., 2015 0 1 1 1 1 4 high
Karthikeyan Krishnamurthy et al., 2020 1 1 1 1 1 5 high
Ting Xiao et al., 2012 1 1 1 1 1 5 high
Yvonne M. Y. Han et al., 2022 1 1 1 1 1 5 high
Yue Gu et al., 2017 1 1 1 1 1 5 high
Yue Gu et al., 2018 0 1 1 1 1 4 high
Shuo Miao et al., 2017 1 0 1 1 1 4 high
Hideki Negoro et al., 2010 0 1 1 1 1 4 high
Ting Wu et al., 2023 1 1 1 1 1 5 high
Yike Zhu et al., 2023 0 1 1 1 1 4 high

194
Y. Li et al. Journal of Psychiatric Research 172 (2024) 187–196

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CRediT authorship contribution statement Gjevik, E., Eldevik, S., Fjæran-Granum, T., Sponheim, E., 2011. Kiddie-SADS reveals high
rates of DSM-IV disorders in children and adolescents with autism spectrum
Yin Li: Writing – original draft, Methodology, Data curation. Shuai disorders. J. Autism Dev. Disord. 41 (6), 761–769. https://doi.org/10.1007/s10803-
010-1095-7.
Ma: Investigation, Data curation. Xin Zhang: Funding acquisition, Gossé, L.K., Bell, S.W., Hosseini, S.M.H., 2022. Functional near-infrared spectroscopy in
Conceptualization. Lei Gao: Writing – review & editing, Supervision, developmental psychiatry: a review of attention deficit hyperactivity disorder. Eur.
Funding acquisition. Arch. Psychiatr. Clin. Neurosci. 272 (2), 273–290. https://doi.org/10.1007/s00406-
021-01288-2.
Gu, Y., Miao, S., Han, J., Liang, Z., Ouyang, G., Yang, J., Li, X., 2018. Identifying ADHD
children using hemodynamic responses during a working memory task measured by
Declaration of competing interest functional near-infrared spectroscopy. J. Neural. Eng. 15 (3), 035005 https://doi.
org/10.1088/1741-2552/aa9ee9.
The authors declare that the research was conducted in the absence Gu, Y., Miao, S., Han, J., Zeng, K., Ouyang, G., Yang, J., Li, X., 2017. Complexity analysis
of fNIRS signals in ADHD children during working memory task. Sci. Rep. 7 (1), 829.
of any commercial or financial relationships that could be construed as a https://doi.org/10.1038/s41598-017-00965-4.
potential conflict of interest. Guiney, H., Machado, L., 2013. Benefits of regular aerobic exercise for executive
functioning in healthy populations. Psychon. Bull. Rev. 20 (1), 73–86. https://doi.
org/10.3758/s13423-012-0345-4.
Acknowledgements Han, Y.M.Y., Chan, M.C., Chan, M.M.Y., Yeung, M.K., Chan, A.S., 2022. Effects of
working memory load on frontal connectivity in children with autism spectrum
This study has received research grants from National Natural Sci­ disorder: a fNIRS study. Sci. Rep. 12 (1), 1522. https://doi.org/10.1038/s41598-
022-05432-3.
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