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. Author manuscript; available in PMC: 2023 Jul 1.
Published in final edited form as: Autism Res. 2022 Apr 6;15(7):1336–1347. doi: 10.1002/aur.2715

Elevated symptoms of executive dysfunction predict lower adaptive functioning in 3-year-olds with autism spectrum disorder

Kelly Powell 1, Suzanne Macari 1, Emma Brennan-Wydra 1, Hannah Feiner 1, Maurine Butler 1, Diogo Goncalves Fortes 1, Alexandra Boxberger 1, Mariana Torres-Viso 1, Chelsea Morgan 1, Megan Lyons 1, Katarzyna Chawarska 1
PMCID: PMC9253075  NIHMSID: NIHMS1792312  PMID: 35388596

Abstract

Executive functioning (EF) deficits co-occur frequently with autism spectrum disorder (ASD) and have a long-term detrimental impact on quality of life of children and their families. Timely identification of risk for EF vulnerabilities may hasten access to early intervention and alleviate their long-term consequences. This study examines (1) if EF deficits are elevated in toddlers with ASD compared to nonautistic siblings of children with ASD, typically developing (TYP) toddlers, and toddlers with atypical developmental presentation; and (2) if EF deficits have a detrimental effect on adaptive functioning in ASD. Participants were recruited between September 2014 and October 2019 and included 73 toddlers with ASD, 33 nonautistic siblings of children with ASD, 35 toddlers with atypical development, and 28 TYP toddlers matched on chronological age (M = 39.01 months, SD = 3.11). EF deficits were measured using the BRIEF-P; adaptive skills were measured using the VABS-II. Whenever appropriate, analyses were controlled for MSEL verbal and nonverbal developmental quotient, ADOS-2 autism severity scores, and sex. Analyses revealed that toddlers with ASD exhibited elevated BRIEF-P scores across all domains compared to each of the three comparison groups. Higher BRIEF-P scores were associated with lower adaptive social, communication, and daily living skills while controlling for symptom severity, verbal and nonverbal functioning, and sex. In conclusion, marked vulnerabilities in EF are already present in 3-year-old toddlers with ASD and are predictive of the level of adaptive functioning in ASD. EF vulnerabilities in toddlers should be targeted for intervention to improve long-term outcomes in ASD.

Keywords: autism, executive function, sibling, toddlers

Lay Summary

Many children with autism experience vulnerabilities in executive functioning (EF), which may include challenges with inhibition, working memory, cognitive flexibility, and planning. The study shows that these vulnerabilities can already be detected at age three and that their presence is linked with lower social, communication, and daily living skills. Screening children with ASD for EF challenges and helping those who have difficulties may improve their long-term outcomes.

INTRODUCTION

Autism spectrum disorder (ASD) is characterized by atypical patterns of social interaction and communication as well as the presence of repetitive movements, activities, and interests (American Psychiatric Association, 2013). Amongst conditions commonly co-occurring with ASD are impaired executive functioning (EF) skills (Hutchison et al., 2020; Smithson et al., 2013; Vogan et al., 2018). The EF system, whose primary function is to facilitate problem-solving in novel situations (Rabbitt, 1997), comprises a host of basic cognitive processes such as working memory, inhibitory control, set shifting, and planning, all working in concert within an overarching attentional supervisory system (Norman & Shallice, 1986). Impairments in the EF domain are thought to result in difficulties in everyday life such as remembering and following directions, inhibiting inappropriate behavior, keeping belongings organized, or transitioning between tasks (Gioia et al., 2002). In the general population, early EF skills predict later school readiness and teacher-child relationships, cognitive development, academic achievement, attention and impulsivity, and social skills (Carlson & Moses, 2001; Gooch et al., 2016; Henning et al., 2011). EF deficits are common in many neurodevelopmental disorders, including ADHD (Barkley, 1997; Nigg et al., 2002; Willcutt et al., 2005), learning disabilities (Toll et al., 2011), and ASD (Hill, 2004; Kenworthy et al., 2008; O’Hearn et al., 2008).

In children and adolescents with ASD, EF difficulties arise frequently in the domains of inhibition, working memory, cognitive flexibility, and planning. EF difficulties are already present in preschoolers with ASD, with 43%–67% scoring in the clinically relevant range on a scale capturing EF deficits via parent report, the Behavioral Rating Inventory of EF, Preschool Version (BRIEF-P) (McLean et al., 2014; Smithson et al., 2013). However, it is not clear if EF deficits can be detected at earlier ages and whether they are more common or more pronounced in children with ASD than in other clinical or at-risk groups. Finally, frequent focus in the extant literature on more cognitively able children with ASD may limit generalizability of the findings to a broader population of very young children with ASD.

The concept of adaptive skills captures the ability to carry out day-to-day activities necessary to take care of oneself and get along with others, including effective communication skills, social competency, and daily living skills (Sparrow & Cicchetti, 1985). Adaptive behavior reflects what a child accomplishes in an independent manner and within everyday environments (e.g., home, school, and their community), as opposed to what the child has the capability to do according to standardized measures of the child’s IQ or language level. Adaptive skills are typically impaired in children with ASD, as exemplified by marked discrepancies between cognitive and adaptive skill levels (Klin et al., 2007). The gap between cognitive and adaptive skill levels is present already at 3 years of age in children with ASD, as well as in siblings of children with ASD who due to familial risk factors, often exhibit broader autism phenotype (BAP or subclinical autism) features, and the gap tends to widen throughout development into school-age years (Bradshaw et al., 2019; Salomone et al., 2018). Adaptive functioning skills are vital as they relate to key outcomes for adolescents and adults with ASD such as social engagement, employment, and independent living (Anderson et al., 2014; Esbensen et al., 2010; Howlin et al., 2013; Huang et al., 2012; Orsmond et al., 2013). Furthermore, low-adaptive functioning predicts concurrent measures of decreased parent-reported quality of life (Gardiner & Iarocci, 2015) and worse health-related quality of life in children with ASD (Kuhlthau et al., 2010).

Extensive empirical evidence suggests strong links between EF vulnerabilities and lower adaptive functioning in ASD. In school-aged children with ASD, elevated Behavioral Rating Inventory of EF (BRIEF) scores are associated with lower adaptive behavior scores as measured by the Vineland Adaptive Behavior Scales (VABS) and the Behavior Assessment System for Children, Second Edition (BASC-2) when controlling for IQ (Gardiner & Iarocci, 2018; Gilotty et al., 2002; McLean et al., 2014; Pugliese et al., 2016). These relationships suggest that EF vulnerabilities have negative effects on overall functioning in school-aged children with ASD. To the best of our knowledge, however, there is little known about the impact of executive function vulnerabilities on adaptive behavior in toddlers with ASD.

Taken together, there is extensive evidence regarding the presence of EF dysfunction in school age children and adolescents with ASD, and their predictive links with later weaknesses in adaptive functioning. Elevated symptoms of EF impairments are already present in preschool, although it is not clear when they first begin to manifest at clinically relevant levels. The present study examines parent-rated EF skills in a large sample of 3-year-olds with ASD with a wide range of verbal and nonverbal skills. We compare toddlers with ASD with three non-ASD chronological-age matched groups: nonautistic younger siblings of children with ASD, who, due to genetic factors, have elevated likelihood of developing co-occurring conditions, as well as with children without familial risk factors for ASD exhibiting either typical (TYP) or atypical developmental (ATP) characteristics. We hypothesize that toddlers with ASD will exhibit elevated BRIEF-P scores compared to the two comparison groups without history of ASD. Should their BRIEF-P scores be elevated compared to the SIB group, we would conclude that the elevation is specific to those with the fully expressed syndrome as compared to those who share only some of the genetic risk factors. Alternatively, we may find that the ASD and SIB groups have similar level of symptoms, suggesting that the vulnerability extends to a broader spectrum of children carrying genetic risk for ASD. We also hypothesize that as in older children (Gilotty et al., 2002; Yerys et al., 2019), elevated BRIEF-P scores will be associated with lower adaptive functioning, after controlling for the effects of autism symptom severity, verbal and nonverbal DQ, and sex. If the hypotheses are supported, the study would offer clear translational implications highly relevant to the well-being of the children and their families related to screening for and treatment of EF dysfunction symptoms before these symptoms exert lasting impact on long-term outcomes.

METHOD

Participants

All children participated in a study of social–emotional development. The study was approved by the Human Investigation Committee of the Institutional Review Board and parents gave informed consent for their children to participate in the study. Participants (mean age: 39.01 months, SD = 3.11) were 169 chronological age (CA) matched toddlers, including 73 with ASD, 33 younger siblings of children with ASD who themselves did not have ASD (SIB), 35 with developmental delays or other atypical features (e.g., global developmental delays, language delays, subthreshold clinical features; ATP) and 28 typically developing (TYP) children. The ATP and TYP groups had no known history of ASD in the first or second degree relatives. Participants were referred for a differential diagnosis or evaluated due to familial risk for ASD (ASD, ATP, SIB), or were recruited from the feeder studies conducted at the Center or from the community (TYP). All children underwent a comprehensive evaluation including assessment of autism symptoms, developmental skills, and adaptive behaviors. Autism symptom severity was quantified using the Autism Diagnostic Observation Schedule, Second Edition (ADOS-2) (Lord et al., 2012). Verbal and nonverbal development were assessed using the Mullen Scales of Early Learning (MSEL) (Mullen, 1995). MSEL developmental quotient (DQ) scores were derived from age equivalent (AE) scores in Receptive and Expressive Language (verbal) and in Fine Motor and Visual Reception (nonverbal); DQ = (mean of AE scores/CA) × 100. Adaptive functioning was evaluated using the Vineland Adaptive Behavior Scales, Second Edition (VABS-II), a structured parent interview providing standard scores (SS) with a mean of 100 and standard deviation of 15 (Sparrow et al., 2005). In the present paper, we consider three VABS-II domains relevant to the primary aims of the study: Socialization, Communication, and Daily Living Skills.

Diagnostic classification was based on the clinical best estimate diagnosis established by an interdisciplinary clinical team based on all available information. The four groups (ASD, SIB, ATP, TYP) did not differ in CA (F [3, 165] = 1.04, p = 0.378). The proportion of males differed by group, χ2(3) = 10.06, p = 0.008. Specifically, there were significantly more males in the ASD group (80.8%) than in the ATP (54.3%) group (p = 0.008) and SIB (60.6%) group (p = 0.049). Mean scores for the ADOS-2, MSEL, and VABS-II for each group are displayed in Table 1. As expected, children in the ASD group had consistently lower verbal, nonverbal, and adaptive scores than the comparison groups. The SIB group fell in between the ATP and TYP groups in terms of verbal and nonverbal scores and had adaptive skills comparable to that observed in the TYP group.

TABLE 1.

Sample characteristics

Group ASD SIB ATP TYP Contrast
N 73 33 35 28
Male (%) 59 (80.8) 20 (60.6) 19 (54.3) 17 (60.7) ASD > ATP = SIB; ASD = TYP; ATP = SIB = TYP
Race
 White (%) 46 (66.7) 24 (72.7) 25 (71.4) 21 (75.0) ASD = SIB = ATP = TYP
 Non-White (%) 23 (33.3) 9 (27.3) 10 (28.6) 7 (25.0)
Ethnicity
 Hispanic or Latino (%) 17 (25.0) 4 (12.1) 6 (18.2) 8 (29.6) ASD = SIB = ATP = TYP
 Not Hispanic or Latino (%) 51 (75.0) 29 (87.9) 27 (81.8) 19 (70.4)
Highest parental education
 No college degree (%) 15 (21.4) 4 (13.3) 7 (21.9) 3 (11.5) ASD = SIB = ATP = TYP
 College degree or higher (%) 55 (78.6) 26 (86.7) 25 (78.1) 23 (88.5)
Age in months (SD) 39.4 (3.5) 38.7 (3.1) 39.0 (2.9) 38.3 (2.3) ASD = SIB = ATP = TYP
ADOS-2 - SA Severity (SD) 5.63 (2.02) 1.76 (1.39) 2.29 (1.70) — ASD < ATP = SIB
ADOS-2 - RRB Severity (SD) 8.00 (1.75) 4.03 (2.57) 4.32 (2.90) — ASD < ATP = SIB
ADOS-2 - CSS (SD) 6.22 (1.83) 1.61 (1.00) 2.00 (1.41) — ASD < ATP = SIB
MSEL - Verbal DQ (SD) 70.8 (33.6) 103.3 (16.6) 90.0 (25.7) 120.4 (16.3) ASD < ATP = SIB < TYP
MSEL - Nonverbal DQ (SD) 77.8 (26.5) 108.2 (18.5) 93.5 (23.1) 122.7 (17.9) ASD < ATP < SIB = TYP
VABS-II - Communication (SD) 85.7 (16.9) 99.0 (13.5) 90.3 (12.5) 109.0 (12.4) ASD = ATP < SIB = TYP
VABS-II - Daily Living Skills (SD) 83.7 (15.6) 97.5 (11.2) 90.6 (12.2) 99.2 (10.5) ASD < ATP = SIB = TYP
VABS-II – Socialization (SD) 78.1 (12.3) 97.4 (13.1) 89.0 (10.0) 98.7 (11.2) ASD < ATP < SIB = TYP
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Abbreviations: ADOS-2: autism diagnostic observation schedule, second edition; CSS, calibrated severity score; DQ, developmental quotient; MSEL, Mullen scales of early learning; RRB, restricted and repetitive behaviors; SA, social affect; VABS-II, Vineland adaptive behaviors acales, section edition

Sociodemographic characteristics of the sample are presented in Table 1. With respect to race, 68.6% of the sample were White, 9.5% Asian, 7.1% Black, 12.4% multiple races (total Non-White: 29.0%) and 2.4% unspecified race. Chi-squared analysis comparing the proportion of White and Non-White participants revealed no significant differences between the groups, χ2(3) = 0.847, p = 0.838. In addition, 20.7% were Hispanic or Latino, 74.6% were not Hispanic or Latino, and 4.7% did not specify their ethnicity. The groups did not differ in their ethnic composition, χ2(3) = 3.453, p = 0.327. The racial and ethnic composition of our sample is consistent with that of the local region. With respect to parental educational attainment, 76.3% of families reported having a 4-year college degree or higher, with a similar breakdown across all groups, χ2(3) = 2.017, p = 0.569.

Procedure

EF measurement

The study used the BRIEF-P, a 63-item parent report questionnaire designed for children ages 2.5–5 years (Gioia et al., 2003). The BRIEF-P consists of five scales: Inhibit, Emotional Control (EC), Shift, Working Memory (WM), and Plan/Organize (PO), from which index scores are computed for three domains: Inhibitory Self-Control Index (ISCI, comprised of Inhibit and EC scales), Flexibility Index (Fl, comprised of Shift and EC), and Emergent Metacognition Index (EMI, comprised of WM and PO). The BRIEF-P also yields a global score, the Global Executive Composite (GEC). Scores are reported as T-scores, with higher scores indicating areas of greater EF difficulties. T-scores of 65 or greater indicate clinically significant concerns.

Statistical analysis

To analyze the BRIEF-P scores we used a group (4) × sex (2) general linear model with planned contrasts between toddlers with ASD and the three comparison groups: SIB, ATP, and TYP. MSEL verbal and nonverbal DQ (VDQ and NVDQ) were included as covariates. Cohen’s d was used as an index of effect size for the comparisons. To compare the number of children in the ASD group exceeding the cutoffs for clinically significant executive dysfunction to the remaining groups combined (SIB, ATP, and TYP), we calculated proportions as well as odds ratios and corresponding 95% confidence intervals. To evaluate the unique effects of executive dysfunction on VABS-II subscale scores (Communication, Socialization, and Daily Living Skills) in the ASD group, we conducted multiple regression analyses with sex, ADOS-2 calibrated severity score (CSS), and MSEL VDQ and NVDQ included as predictors in the models.

RESULTS

EF scores

Between-group ANOVA on the GEC score indicated a significant main effect of group (F[3, 158] = 7.21, p < 0.001); neither the effects of sex (F[1, 158] = 1.44, p = 0.231) nor group x sex interaction (F[3, 158] = 0.20, p = 0.897) were statistically significant. Planned contrasts revealed that the ASD group had significantly higher BRIEF-P scores compared with the SIB (p < 0.001, d = 1.32), ATP (p < 0.001, d = 0.85), and TYP (p < 0.001, d = 1.34) groups (Figure 1). Contributions of VDQ (p = 0.291) and NDQ (p = 0.264) to the model were not statistically significant.

FIGURE 1.

FIGURE 1

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Raw means for BRIEF-P global executive composite (a) and BRIEF-P subdomains (b) for toddlers with autism spectrum disorder (ASD), siblings of children with ASD (SIB), atypical development (ATP), and typical development (TYP) in the ASD, SIB, ATP, and TYP groups

Subsequent analyses of the subscales of the BRIEF-P indicate that the overall differences between ASD and comparison groups noted on the GEC T-score were driven by multiple indices. For ISCI, there was a significant main effect of group (F[3, 158] = 5.94, p < 0.001) but no significant effects of sex (F[1, 158] = 0.54, p = 0.464) or group x sex interaction (F[3, 158] = 0.25, p = 0.860). Planned comparisons revealed that the ASD group had significantly higher mean ISCI scores than the SIB (p < 0.001, d = 1.13), ATP (p < 0.001, d = 0.80), and TYP (p < 0.001, d = 1.00) groups. Neither VDQ (p = 0.104) nor NVDQ (p = 0.974) contributed significantly to the model. For FI, ANOVA revealed a significant effect of group (F[3, 158] = 4.34, p = 0.006). Neither the effects of sex (F[1, 158] = 0.22, p = 0.637) nor group x sex interaction (F[3, 158] = 0.08, p = 0.971) were significant. Planned contrasts indicated that the ASD group had higher FI scores compared with the SIB (p < 0.001, d = 0.93), ATP (p < 0.001, d = 0.74), and TYP (p < 0.001, d = 0.97) groups. The contributions of VDQ (p = 0.358) and NVDQ (p = 0.739) were negligible. For EMI, there was a significant effect of group (F[3, 158] = 6.34, p < 0.001) but not of sex (F [1, 158] = 2.57, p = 0.111) or group x sex interaction (F[3, 158] = 0.17, p = 0.919). Planned comparisons between groups revealed that the ASD group had significantly higher EMI scores compared with peers in the SIB (p < 0.001, d = 1.30), ATP (p < 0.001, d = 0.73), and TYP (p < 0.001, d = 1.44) groups. The effects of neither VDQ (p = 0.588) nor NVDQ (p = 0.055) were significant in the model. The index (ISCI, FI, and EMI) and overall (GEC) T-scores on the BRIEF-P are presented in Table 2.

TABLE 2.

Raw means and standard deviations (SD) for EF deficits by group. Comparisons to ASD group are shown for SIB, ATP, and TYP groups (t = test statistic for two sample t-test, p = p-value, d = Cohen’s d effect size for difference)

Mean SD t p d
BRIEF-P GEC T-score
 ASD 65.15 15.79 — — —
 SIB 46.03 11.06 7.16 <0.001 1.32
 ATP 52.17 14.27 4.27 <0.001 0.85
 TYP 45.35 11.62 6.89 <0.001 1.34
BRIEF-P ISCI T-score
 ASD 61.27 14.18 — — —
 SIB 46.03 11.59 5.84 <0.001 1.13
 ATP 50.34 12.47 4.07 <0.001 0.80
 TYP 47.64 12.31 4.77 <0.001 1.00
BRIEF-P FI T-score
 ASD 59.25 14.20 — — —
 SIB 46.67 11.90 4.74 <0.001 0.93
 ATP 49.31 11.34 3.92 <0.001 0.74
 TYP 46.35 10.75 4.91 <0.001 0.97
BRIEF-P EMI T-score
 ASD 65.70 16.27 — — —
 SIB 46.97 8.93 7.62 <0.001 1.30
 ATP 54.09 15.13 3.64 <0.001 0.73
 TYP 44.36 9.68 8.08 <0.001 1.44
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EF clinical cutoffs

Based on the GEC T-score, 52.1% (n = 38) of the ASD group met the threshold for clinically significant EF deficits, compared with 20.0% (n = 7) in the ATP group, 6.0% (n = 2) in the SIB group, and 3.6% (n = 1) in the TYP group. The odds ratio of a toddler with ASD crossing clinical threshold on the BRIEF-P GEC index compared to toddlers without the ASD diagnosis (the ATP, SIB, and TYP combined) was 9.34 (95% confidence interval: 4.20 to 20.78, p < 0.001).

Associations between EF and adaptive behavior in the ASD group

Associations between the VABS-II domain scores and the BRIEF-P GEC in the ASD group are presented in Figure 2. See Table S1 for all correlations amongst VABS-II domain scores, BRIEF-P GEC, ADOS-2 CSS, and MSEL VDQ and NVDQ scores in the ASD group. To test for independent contributions of the BRIEF-P GEC scores as well as sex, ADOS-2, and MSEL DQ scores, to the VABS-II socialization, communication, and daily living skills domain scores in the ASD group, we conducted three multiple linear regressions (Table 3). For VABS-II Communication SS, the predictors were collectively significant (F[5, 66] = 34.34, p < 0.001, adjusted R2 = 0.701). Examination of individual predictors indicated significant negative effects of elevated BRIEF-P GEC scores (β= −0.22, t = −3.18, p = 0.002) and lower MSEL VDQ (β= 0.63, t = 4.62, p < 0.001) on adaptive communication skills. Sex was not a significant predictor in the model (β = 0.06, t = 0.94, p = 0.353) nor was MSEL NVDQ (β = 0.17, t = 1.20, p = 0.234) or ADOS-2 CSS (β= 0.02, t = 0.26, p = 0.793). For VABS-II Socialization SS, the predictors had a significant collective effect (F[5, 66] = 23.42, p < 0.001, adjusted R2 = 0.612). Both elevated BRIEF-P GEC scores (β = −0.27, t = −3.47, p = 0.001) and lower MSEL VDQ (β= 0.55, t = 3.55, p = 0.001) contributed to lower adaptive socialization scores. The effect of sex was not significant (β= 0.04, t = 0.58, p = 0.565), nor was MSEL NVDQ (β= 0.10, t = 0.60, p = 0.553) or ADOS-2 CSS (β = −0.14, t = −1.71, p = 0.092). For VABS-II Daily Living Skills SS, the predictors were collectively significant (F[5, 66] = 17.51, p < 0.001, adjusted R2 = 0.538). Elevated BRIEF-P GEC scores (β = −0.31, t = −3.61, p < 0.001), lower MSEL VDQ (β = 0.48, t = 2.84, p = 0.006), and higher ADOS-2 CSS (β = −0.23, t = −2.54, p = 0.014) had a negative impact on daily living skills scores. The effect of sex was not significant (β = 0.11, t = 1.34, p = 0.184), nor was MSEL NVDQ (β= 0.05, t = 0.27, p = 0.792).

FIGURE 2.

FIGURE 2

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Associations between EF deficits (BRIEF-P GEC T score) and three Vineland communication, socialization, and daily living skills domains in toddlers with ASD

TABLE 3.

Multiple regression models for the effects of EF deficits (BRIEF-P GEC T score), sex, verbal and nonverbal ability (MSEL VDQ and NVDQ), and autism severity (ADOS-2 CSS) on VABS-II communication, socialization, and daily living skills domain standard scores in the ASD group

VABS-II communication VABS-II socialization VABS-II daily living skills
F(5,66) 34.34, p < 0.001 23.42, p < 0.001 17.51, p < 0.001
Multiple R2 0.722 0.640 0.570
Adjusted R2 0.701 0.612 0.538
B (SE) β p B (SE) β p B (SE) β p
Female 1.34 (1.43) 0.06 0.353 0.69 (1.19) 0.04 0.565 2.20 (1.64) 0.11 0.184
GEC T score −0.24 (0.07) −0.22 0.002 −0.21 (0.06) −0.27 0.001 −0.31 (0.09) −0.31 0.001
MSEL VDQ −0.32 (0.07) 0.63 <0.001 0.20 (0.06) 0.55 0.001 0.22 (0.08) 0.48 0.006
MSEL NVDQ 0.11 (0.09) 0.17 0.234 0.05 (0.08) 0.10 0.553 0.03 (0.11) 0.05 0.792
ADOS-2 CSS 0.18 (0.67) 0.02 0.793 −0.94 (0.55) −0.14 0.092 −1.93 (0.76) −0.23 0.014
(Intercept) 68.23 (9.12) — <0.001 79.67 (7.57) — <0.001 96.20 (10.44) —
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Note: Bolded values represent p < 0.05

DISCUSSION

By the age of 3 years, children with ASD exhibit marked signs of EF impairments. Effect sizes range from medium for ASD versus atypical development group comparison to very large for ASD versus nonautistic siblings, and versus the TYP control group. Compared to all the control groups combined, toddlers with ASD are over nine times more likely to experience clinically relevant levels of executive dysfunction. The proportion of toddlers crossing the clinical threshold for executive dysfunction is comparable to that observed in preschoolers (McLean et al., 2014; Smithson et al., 2013) and school age children with ASD (McLean et al., 2014) suggesting that the challenges described in older children are already manifesting in early childhood. EF vulnerabilities are present in all three domains: inhibitory self-control, flexibility, and metacognition, and the scores in the three domains were highly intercorrelated, suggesting that in 3-year-olds, EF skills may not yet be fully differentiated and reflect a domain-general vulnerability (Wiebe et al., 2011). While prior work showed elevated EF scores in preschoolers with ASD compared to typical controls or population norms (McLean et al., 2014; Smithson et al., 2013), we demonstrate that toddlers with ASD show elevated symptoms compared to those with other developmental concerns as well.

Interestingly, while siblings of children with ASD share a genetic liability for a range of neurodevelopmental symptoms (Ghirardi et al., 2018; Miller et al., 2019), the siblings did not exhibit elevated executive dysfunction symptoms at age 3. In fact, their performance was closely aligned with TYP children without a genetic liability for autism (McLean et al., 2014). This suggests that, at least in early development, EF impairments are not pronounced in the siblings, and unlike social vulnerabilities and language delays (Marrus et al., 2018), EF dysfunction does not appear to be distributed along the genetic autism liability spectrum.

Elevated executive dysfunction symptoms in the ASD group contributed uniquely to lower adaptive functioning in the areas of communication, socialization, and daily living skills. This relationship was present when the effects of Mullen verbal and nonverbal ability, estimated autism symptom severity, and sex were taken under consideration in our analytic models. These findings extend the literature on EF and adaptive behavior in school-aged children and adolescents with ASD (Bertollo & Yerys, 2019; Gardiner & Iarocci, 2018; Gilotty et al., 2002; Pugliese et al., 2015; Pugliese et al., 2016; Sikora et al., 2012) and show that these domains are interconnected already in early childhood. Given that deficits in adaptive functioning tend to worsen over time for individuals with ASD (Klin et al., 2007; Pugliese et al., 2015; Pugliese et al., 2016; Salomone et al., 2018), our findings underscore the importance of early identification of vulnerabilities in EF and targeting these deficits in treatment. The early interventions may include supporting development of sustaining attention to tasks, inhibiting actions at the appropriate time, remembering directions, planning and organizing approaches to play and problem solving, regulating emotional responses, transitioning between activities, completing activities, amongst others. Early intervention focused on attentional, behavioral, and emotional control has potential to exert a lasting effect on children improving their overall quality of life and that of their families, as many adaptive skills tasks, particularly daily living skills, tend to require adult support to complete if the child does not yet demonstrate independence. While there are several manualized interventions and curricula as well as resources for teaching young children EF skills including Tools of the Mind designed for preschool and kindergarteners (Blair & Raver, 2014; Bodrova & Leong, 2007; Diamond et al., 2007), to the best of our knowledge, very few have been designed specifically for children with ASD (Cannon, 2021; Kenworthy et al., 2014). Presently there are no empirically supported EF curricula specifically designed for toddlers and preschoolers with ASD, which represents a major gap in the intervention field.

Lastly, we found that in toddlers, level of autism symptoms is not associated with severity of executive dysfunction. Similar findings have been reported in school-age children with ASD (Lee et al., 2021). However, in adolescents, links between EF and autism symptom severity have been reported after controlling for sex and IQ (Torske et al., 2017). It is plausible that, similarly as the emotional vulnerability traits and autism severity (Macari et al., 2017; Macari et al., 2018), the two domains are initially distinct and driven by different underlying factors. Over time, however, persistent EF deficits may exacerbate vulnerabilities in social skills and communication, leading to stronger associations later on. Since EF skills continue to develop into early adulthood, if children with ASD demonstrate worse EF skills earlier on, the gap between them and their peers may grow over time (Hill, 2004; Rosenthal et al., 2013). Further, considering EF has a negative impact on social communication and adaptive skills, the negative influence of low EF skills on other domains likely intensifies as children age. Relatedly, EF skills are often viewed as a muscle that requires exercise; without constant challenge and practice, skills may be lost over time (Diamond & Ling, 2016). Therefore, it is imperative that EF skills be continuously practiced, even if improvements are initially observed.

The present study has focused on a parent-report measure of EF dysfunction. Other measures include direct assessment of specific EF functions in experimental and standard assessment settings (Kenworthy et al., 2008; McAuley et al., 2010; McLean et al., 2014). Rating scales are thought by many to be more ecologically valid than lab-based EF tasks (Demetriou et al., 2018; Demetriou et al., 2019; Kenworthy et al., 2008; Snyder et al., 2015). Indeed, there has been a major effort in EF research to increase the relevance of lab-based tests to everyday life situations by adding information from behavioral rating scales (Wilson et al., 1998). Solving EF tasks in a quiet setting, presented one at a time after clear instructions, may not engage the same set of EF skills required in everyday situations (Shallice & Burgess, 1991). Furthermore, unlike questionnaire-based EF, task-based EF performance is inconsistently or modestly related to functional outcomes (Barkley & Fischer, 2011; Barkley & Murphy, 2011; Denckla, 1996) and is related to general cognitive ability in both adults (Barkley & Murphy, 2011) and children (Mahone et al., 2002; McLean et al., 2014) limiting its applicability to young children with ASD with a wide range of developmental skills. Still, considering that the laboratory-based and parent report-measure may provide complementary information regarding specific skills that are affected and contexts in which the deficits become most apparent (McAuley et al., 2010), future research into executive dysfunction in toddlers with ASD should consider a multi-method approach including parent and teacher ratings as well as performance on neuropsychological tasks targeting EF skills.

Clinical significance

Given our evidence of EF vulnerabilities for young children with ASD, these should be considered and promptly targeted with tailored EF interventions. Early detection of EF dysfunction in toddlers and subsequent intervention could considerably attenuate long-term negative effects, including increased severity of EF deficits (Luna et al., 2007; Rosenthal et al., 2013), emotional and regulatory problems (Sikora et al., 2012; Simonoff et al., 2008), and plateaus in adaptive functioning (Bal et al., 2015). For example, toddlers entering preschool or intervention programs could be screened for EF deficits by collecting relatively brief parent-report measures. Preschool and/or clinical teams could then proactively incorporate EF-specific learning targets for children with elevated screener scores. Importantly, given our findings around the relationship between EF deficits and adaptive skills impairment, intervention approaches that more readily address emerging metacognitive skills may be better able to specifically address adaptive living challenges and ameliorate future difficulties. For example, in addition to targeting common EF challenges such as behavioral/emotional regulation and inflexibility that can manifest as oppositional behavior (e.g., via parent management training), deliberately tailoring interventions to include planning and organizing, identification and following of multi-step directions, and other working memory-based tasks, could significantly reduce existing adaptive challenges found in toddlers with ASD and EF vulnerabilities. Furthermore, efforts to extend EF profile-based subtyping to very young children may hold promise for individualizing their treatment targets and tracking treatment responses (Vaidya et al., 2020). Future studies are needed to address these important translational questions.

Limitations and future directions

The present study examines concurrent associations between adaptive skills and vulnerabilities in EF in 3-year-old children with ASD. To fully appreciate predictive links between early EF vulnerabilities and later adaptive outcomes, samples such as ours would need to be followed prospectively into school-age and adolescence. Identification of reliable predictors and understanding of the developmental dynamic between executive dysfunction and social and cognitive vulnerabilities would help inform development of tools for identifying and treating these vulnerabilities in young children. Presently, there are no empirically supported EF interventions for very young children with ASD, despite the growing evidence supporting the need for such interventions. Thus, it is crucial that such interventions be developed, rigorously tested, and then disseminated. Future research should also strive to evaluate causal links by studying effects of early intervention on prevalence and severity of co-occurring conditions linked with EF impairment. In addition, multi-method approaches to the measurement of EF including both parent report and direct assessment should be considered in future studies.

CONCLUSIONS

This study assessed EF deficits in toddlers with and without genetic liability for ASD, offering a nuanced and thorough analysis of the notable weaknesses in very young children with ASD. The study demonstrates pronounced vulnerabilities in EF in 3-year-olds with ASD in Inhibitory Self-Control, Flexibility, and Emergent Metacognition domains. In children with ASD, these deficits do not vary by sex, do not appear to track with severity of autism symptoms or developmental level and they contribute uniquely to lower adaptive functioning skills. The EF vulnerabilities can be rapidly quantified using readily available parent and teacher report measures. Given that evidence-based interventions to target EF vulnerabilities exist for older children (Cannon, 2021; Kenworthy et al., 2014), therapeutic efforts should focus on downward-extending these interventions and employing them in service of development of adaptive skills and independence. Targeted and prompt treatment of EF vulnerabilities has the potential to improve long term outcomes for the child, as well as to support their caregivers and families.

Supplementary Material

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ACKNOWLEDGMENTS

We thank the children and their families for participating in the study. We acknowledge the clinical team of the Yale Social and Affective Neuroscience of Autism Program for their contribution to sample characterization and data collection.

Funding information

The study was supported by the National Institute of Mental Health R01 MH100182 and R01 MH111652 grants awarded to Katarzyna Chawarska. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Footnotes

ETHICS STATEMENT

All research activities described in the article meet ethical guidelines, including the obtaining of informed consent, and the research was approved by Yale University’s Institutional Review Board (IRB #).

CONFLICT OF INTEREST

The authors declare no conflicts of interest.

SUPPORTING INFORMATION

Additional supporting information may be found in the online version of the article at the publisher’s website.

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

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NIHMS1792312-supplement-supinfo.docx (13.5KB, docx)

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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