Background
Executive functions are a set of cognitive abilities that are needed for regulating behavior, including inhibition, working memory, and planning. The ability to regulate behavior is important, as executive functioning has a substantial impact on short-term and long-term life outcomes such as physical and mental health, performance in school, and socioeconomic status [
1,
2]. Executive functioning is often impaired in psychiatric disorders [
3,
4], including neurodevelopmental disorders, such as autism spectrum disorder (ASD) and attention-deficit/hyperactivity disorder (ADHD) [
5,
6]. So far, little is known about early executive functioning problems in young children with subclinical traits of ASD and ADHD.
Autism spectrum disorder is characterized by deficits in social interaction and communication, and restricted behavior and interests, whereas the main symptoms in ADHD are inattention and hyperactivity/impulsivity [
7]. The prevalence of these disorders among children under 18 years are approximately 1% [
8,
9] and 3–5% [
10,
11], respectively. Children with ASD and ADHD can have lower educational achievements and poorer social outcomes, with problems often extending into adulthood [
12,
13]. Importantly, traits of ASD and ADHD occur along a continuum of severity [
14,
15], ranging from sub-clinical to severely impaired. However, children with lower levels of ASD and ADHD traits, not sufficient for a diagnosis, are also suffering from daily impairments.
Executive functioning deficits associated with both ASD and ADHD are found consistently throughout the literature [
5,
6,
16,
17]. The main domains in children with ASD comprise shifting, planning, and working memory [
5,
6,
16], although broader executive functioning deficits across all domains have been observed as well [
5,
18‐
20]. Conversely, children with ADHD have more pronounced difficulties in executive functioning, in the domains of inhibition, working memory, vigilance, and planning [
5,
17,
18]. These difficulties are not only seen among those with a clinical diagnosis, as few population-based studies suggest that (young) children and adults with subclinical traits of ASD or ADHD also experience problems in executive functioning [
21‐
26]. These findings are important, as children with subclinical traits of disorders often remain undetected by mental health services for various reasons [
27‐
29], including symptoms not being severe enough to warrant help seeking, stigmatization of seeking help for mental problems, and inability to pay. However, sub-clinical symptoms may be associated with other sub-clinical characteristics, such as cognition function, which may result in some impairment [
27,
30,
31]. Indeed, executive functioning has a substantial impact on short-term and long-term life outcomes [
1,
2,
32].
Only a minority of studies in this field has focused on young children with neurodevelopmental traits. Young children with ADHD or at high risk for ADHD appear to be impaired in executive functioning [
33‐
35], while research on young children with ASD is more inconclusive [
36‐
39]. Some studies find no differences in executive functioning between children with and without ASD [
38,
39], whereas others do, but depending on the different age or means of measuring executive functioning [
20,
36,
37]. It has been argued that performance tasks and behavioral ratings should be distinguished from each other, as they may measure different aspects of executive functioning [
40,
41]. Performance tasks are more situational and measure abilities in a specific (test-) environment, whereas behavioral ratings focus on the ability to apply these skills in daily life, perhaps making the latter more generalizable and therefore clinically more relevant.
Furthermore, most of the previous studies employed cross-sectional designs, impeding any conclusions on timing and temporality of associations. In addition, clinical studies often only include children in the clinical range, disregarding the other end of the spectrum. However, population studies include children from the general population, representing the full continuum and allowing for analysis along the entire dimension of executive functioning, ASD and ADHD. Potentially, deficits in executive functioning may be an expression of the latent vulnerability to ASD and ADHD [
42]. A better understanding of neurodevelopmental pathways across early childhood may allow early identification and early intervention for children with traits of these disorders.
The aim of the current study was to investigate the association of executive functioning at age 4 years with ASD and ADHD traits at age 6/7 years. Specifically, we wanted to determine whether executive functioning could be an early indicator of later neurodevelopmental traits, independent of pre-existing traits. For this, we used a behavioral measure of executive functioning assessed in a general population cohort to explore impairment across the continuum of ASD and ADHD. Based on existing research, we expected impaired overall executive functioning to be prospectively associated with greater levels of ASD and ADHD traits. First, we expected that all executive functioning subdomains are associated with ASD traits. Second, we expect that specific executive function subdomains, including difficulties with inhibition, working memory, and planning, are associated with ADHD traits.
Discussion
This study found that impaired executive functioning at the age of 4 years was prospectively associated with ASD and ADHD traits 2–3 years later, independent of multiple confounders and pre-existing psychopathology. Difficulties across executive functioning domains were associated with higher levels of ASD traits, whereas only impaired inhibition, working memory, and planning/organization were associated with more traits of ADHD. Importantly, our findings were consistent across informants: mother-reported ASD traits and clinical ASD diagnoses yielded similar results, as did teacher-reported ADHD traits and ADHD diagnoses based on mother reports. When excluding children with an ASD or ADHD diagnosis from the analysis, we were able to confirm that this association is not fully driven by a subgroup with clinically relevant levels of ASD and ADHD traits, but that, importantly, the associations were also observed in children with sub-clinical levels of these traits. Therefore, our findings provide evidence for a graded association of executive function impairments along the continuum of ASD and ADHD. Due to the nature of our data, we cannot draw any causal conclusions. However, our results implicate future studies to add to our findings, examining the causality of this relationship more in depth.
In line with several previous studies [
5,
19,
20,
25], we found that difficulties in all subdomains of executive functioning were associated with higher levels of ASD traits as well as a greater risk of having an ASD diagnosis. Some studies suggest that deficits primarily in shifting and planning characterize ASD [
5,
6], and that these domains distinguish children with ASD from children with other developmental disorders. Our findings do suggest that shifting may be more predictive for clinical ASD than other executive functioning domains, which might be explained by the high resemblance to the rigid and inflexible behavioral patterns characterizing ASD [
7].
Our study also showed that deficits in overall executive functioning were associated with higher levels of ADHD traits and with a greater likelihood of being diagnosed with ADHD. In line with most previous research, specific domains of executive functioning, inhibition, working memory, and planning/organization, were related to ADHD traits and likewise to ADHD diagnoses [
17,
18]. However, not all studies found planning to be impaired in children with ADHD [
5,
65]. This could be due to the different ways of measuring planning (performance task or behavioral rating). Interestingly, we found that better shifting abilities were related to higher levels of ADHD traits. Perhaps teachers mistook the child’s ability to easily switch between situations for inattention. This association was, however, not significant for ADHD cases in this study, and has not been described previously [
5,
17]. Further exploration and replication of our finding is needed.
The results of the current study support the notion that executive functioning deficits overlap considerably among neurodevelopmental disorders. A general psychopathology factor has indeed been identified by multiple studies [
66,
67], suggesting a substantial phenomenological overlap among (neurodevelopmental) psychopathology. The association of executive functioning with the general psychopathology factor was similar to the relation between executive functioning and separate disorders [
68,
69]. This is supported by several previous studies, which have proposed that problems in executive function constitute an important part of the broader phenotypes of ASD and ADHD [
23,
70,
71]. Furthermore, polygenic risk studies have shown that clinical and subclinical ASD and ADHD share latent genetic vulnerability [
42]. Also, neuroimaging studies observed that frontal areas in the brain are involved in the development of ASD and ADHD symptoms, such as hypoactivation in frontal and parietal regions [
52,
72‐
74], and similar brain areas are implicated in executive functioning [
75]. All this possibly indicates that an underlying factor contributes to executive functioning, ASD, and ADHD.
Despite this evidence for an overlap of executive functioning deficits with ASD and ADHD symptoms, unique variance needs to be considered as well. Reviews on the neurobiology of ASD and ADHD show several differences [
73,
74], such as deficient connectivity between networks in the brain, which shows stronger association with ASD, and deficits in the attentional network, which has stronger associations with ADHD. These specific underlying neural correlates could potentially explain the differing patterns of associations of executive functioning deficits with ASD and ADHD traits that were found in the current and other studies [
5,
16,
17], as well as differences in behavioral expression. Additionally, various unique genetic influences for ASD and ADHD have been found in twin and molecular studies [
76‐
78], which might also explain differences in behavior between these disorders. Reviewing the evidence for unique and overlapping variance among executive dysfunction, ASD, and ADHD, a combination of specific and shared factors is likely to be most accurate: an underlying construct may explain similarities in the areas of executive functioning deficits, ASD, and ADHD, yet each problem domain results from unique genetic, neurobiological and environmental contributing factors, which, in turn, lead to differential behavioral expressions. More research is needed on the similarities and differences among executive functioning and neurodevelopmental problems, and what role executive functioning plays in their etiologies.
Executive dysfunction could be part of the broader phenotype of neurodevelopmental traits, but our findings also suggest other possibilities. The longitudinal design of this study suggests some developmental difference in the trajectory of symptoms: rather than being parallel to ASD and ADHD traits, executive functioning may precede traits of these neurodevelopmental disorders. The associations remained even after adjusting for baseline behavioral problems. It could potentially be that deficits in executive functioning worsen the expression of children’s ASD or ADHD traits and, reversely, perhaps good executive functioning skills can serve as a buffer, tempering the severity of developmental disorders [
79]. However, a more likely explanation is that problems in executive functioning are an expression of the latent genetic vulnerability for ASD and ADHD [
42].
Strengths and limitations
The current study had several strengths. First, we examined the prospective relationship between executive functioning and neurodevelopmental disorders in very young children in a large cohort, enabling us to control for multiple confounding variables, importantly baseline emotional and behavioral problems of the children. Second, we used multiple informants in this study; namely mothers, teachers, and medical records, yielding largely consistent results across these raters. Finally, both clinical diagnoses as well as sub-threshold traits of ASD and ADHD were considered, which addresses the research questions across the neurodevelopmental continuum.
Despite these strengths, multiple limitations need to be mentioned as well. First, the non-response analysis indicated that socially disadvantaged children who are at higher risk of psychiatric problems were more likely to drop out. However, this selective loss to follow-up seems to affect only prevalence estimates, while longitudinal relationships estimated by association analyses remain relatively unchanged [
80]. Second, despite our careful approach to identify those likely to have an ASD or ADHD diagnosis, we potentially missed cases. We also lack the data of diagnosis of ASD, as the children were likely diagnosed within the first 2 or 3 years of life. Third, we measured executive functioning with the BRIEF-P, a questionnaire that was completed mostly by mothers. Despite the marginal but considerable correlation between informants, it is recommended to verify whether the results remain with different informants [
45]. Last, most of our questionnaires were completed by mothers, inducing considerable shared method variance. Nonetheless, to address this, the TRF to assess ADHD traits was administered to teachers and the ASD diagnoses were verified by medical records.
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