Memory, attention, and executive function in intellectual and developmental disabilities

Memory, attention, and executive function are core cognitive areas that shape multiple domains throughout the lifespan, including early communication and language development in infancy, academic achievement and social skills in childhood, and employment, interpersonal relationships and quality of life in adulthood. Individuals with intellectual and developmental disabilities (IDDs) often exhibit impairments in these core cognitive areas. Yet, there remain critical gaps in our understanding of how to assess memory, attention, and executive functioning and in understanding how these core cognitive areas develop. This special issue integrates new research articles aimed at addressing these gaps. The ultimate goal of this work is to help researchers and clinicians design more effective interventions, support strategies, and educational approaches to enhance memory, attention, and executive functioning performance and ultimately improve quality of life for individuals with intellectual and developmental disabilities (IDDs).

This special issue contains 11 empirical studies from researchers at NICHD-funded Eunice Kennedy Shriver Intellectual and Developmental Disabilities Research Centers (IDDRCs) across the United States. The articles explore memory, attention, and executive function in very preterm children, Down syndrome and fragile X syndrome, autistic children, non-autistic children at high likelihood of autism, and unaffected siblings of autistic children.

One paper in this issue examined children born very preterm. Lean and colleagues from the Washington University IDDRC examined executive function (EF) and the Preterm Behavioral Phenotype (PBP) in children born very preterm (VPT) with white matter injury (WMI) [1]. The study prospectively compared the developmental outcomes of 123 children born VPT (≤ 30 weeks gestation), some of whom (n = 44) had marked WMI, and 79 full-term control infants at ages 5 and 9–10 years. The VPT infants, and especially those with WMI, demonstrated lower EF abilities at both timepoints compared to the full-term control group. In early childhood (age 5 years), problems in inhibitory control were most prominent, and by age 9–10 years group differences were observed in all EF domains. The VPT infants and those with WMI also had higher informant-reported characteristics consistent with the preterm behavioral phenotype at age 9–10 years. Childhood exposure to social disadvantaged contexts independently contributed to worse EF outcomes. Impairments in EF appeared to partially explain the connection between being born VPT and having WMI and having characteristics consistent with the preterm behavioral phenotype at age 9 to 10 years. Overall, this study built on prior (largely cross-sectional) research to show that disruptions in EF may be a key contributor to the emotional and social challenges that children born VPT, and especially those with VMI, often experience. This work highlights the potential need for targeted EF interventions to support optimal developmental outcomes in these at-risk groups.

Two papers in this issue addressed Down syndrome (DS). Ludwig and colleagues from the Kennedy Krieger Institute IDDRC examined the caregiver-reported relevance of the Behavior Rating Inventory of Executive Function in school-aged youth with DS [2]. They queried caregivers of 281 youth with DS 6–18 years old and found that just under half of caregivers reported that they deemed items not relevant. Additionally, caregivers of youth who were < 12 years old who tended to have lower expressive language skills or lower adaptive function rated items as not relevant to their child more often and provided lower overall measure relevance ratings. This study highlights the importance of examining different aspects of a scale’s content validity for distinct IDD populations during discreet developmental windows.

Sterling and colleagues from the Waisman Center IDDRC examined the relationship between language and executive functions (EF) in adolescents with DS (N = 25) and fragile X syndrome (N = 21) [3]. The two groups were matched on chronological age and had similar nonverbal IQ and vocabulary ability. The experimental tasks were direct measures of performance and designed to overcome challenges with standardized tests and language samples including floor effects, restricted score range, and limited spontaneous language production. The experimental tasks assessed grammatical judgement and sentence imitation (language) and inhibition, shifting, and working memory (EF). The authors found that the experimental tasks had high feasibility (72–91% of participants completed), with older participants especially likely to complete the tasks. The experimental tasks yielded different findings than standardized tests. The Down syndrome and fragile X syndrome groups did not differ in grammar or executive function on the experimental tasks. However, the fragile X group was rated as having more impaired EF on the standardized parent-reported measure. These differences highlight that parent-reported measures and direct measures of performance may assess different underlying constructs of EF. In both the Down syndrome and fragile X syndrome group, working memory was positively related to performance on the grammatical judgment task. Overall, the study highlights important measurement considerations for capturing language and EF ability and adds to the field’s understanding of the connection between these domains within and across IDD populations.

Two papers in this issue examined children at high likelihood of autism in the Infant Brain Imaging Study (IBIS) network, which includes IDDRCs at UNC-Chapel Hill, University of Washington, and the Children’s Hospital of Philadelphia. St. John and colleagues investigated longitudinal profiles of executive function (EF) in 83 autistic, 235 non-autistic high likelihood, and 132 non-autistic low likelihood children [4]. They found that autistic and non-autistic HL children, as well as LL children, showed distinct EF profiles from 12 months of age through school-age. On performance-based measures of working memory, inhibitory control, and cognitive flexibility, autistic and non-autistic HL children showed stable performance over time, whereas LL children’s EF improved initially between 12 and 24 months of age. Parent report indicated an accumulation of EF difficulties over time among autistic HL children. Planned comparisons at each time point showed no group differences in EF scores at 12 months. At 24 months, both HL groups had lower EF scores than the LL group. By school-age, autistic HL children scored lower than both non-autistic HL and LL children across EF measures, while non-autistic HL children differed from LL children only on parent-reported EF difficulties. This study highlights the importance of integrating multiple sources of information to better understand EF development in autistic children.

Also from the IBIS network, Zhang and colleagues examined associations between extra-axial cerebrospinal fluid volumes at infancy (from 6 to 24 months of age) and executive function at school-age in a longitudinally phenotyped cohort of children with either high (HL) or low (LL) familial likelihood for autism (i.e., HL infants who were diagnosed with autism at 24 months (HL+, n = 34), HL infants not diagnosed with autism (HL-, n = 131), and LL infants without autism (LL-, n = 74)) [5]. Using two parent rating scales of EF difficulties, they found that autistic HL children had greater EF difficulties at school-age than non-autistic HL and LL children. Higher EA-CSF volume from 6 to 24 months of age was associated with greater school-age EF difficulties regardless of autism diagnosis or familial likelihood for autism. These findings suggest that infant EA-CSF could be an early marker of later executive functioning difficulties.

Ortega and colleagues from the UCLA IDDRC examined how emotion regulation and self-inhibition relate to mental health outcomes, caregiver strain, and well-being among parents of autistic children [6]. They found that among 263 parent-dyads, stronger emotion regulation in both mothers and fathers of autistic children was associated with better mental health, less caregiver strain, and better well-being. They also found that, among fathers only, greater self-inhibition was associated with better well-being. There was no link between emotion regulation or self-inhibition and partner’s mental health, caregiver strain, or well-being. These findings indicate that emotion regulation and self-inhibition may serve as important sources of resilience for parents of autistic children.

The remaining papers in this issue examined children and adolescents with autism spectrum disorder (ASD). Sehgal and colleagues from the Boston Children’s Hospital IDDRC examined language and visuospatial working memory across three yearly timepoints in 2–4-year-old autistic preschoolers [7]. They found bi-directional cross-lagged associations between working memory and language at the earlier timepoints (when 58.8% of the sample was 2–3-years-old and 41.2% was 4–5-years-old) but not later timepoints. They suggest that the early development of language and working memory are more closely related among toddlers and younger autistic preschoolers than they are during the later preschool period as children approach school entry.

Christensen and colleagues from the University of Rochester IDDRC examined diffusion weighted imaging (DWI) and functional magnetic resonance imaging (fMRI) data from the Adolescent Brain Cognitive Development (ABCD) study. They investigated linkages between neuron density and functional activity during emotional face processing in 149 individuals with ASD compared to 10,146 individuals without ASD [8]. They found that neuron cell body density was associated with functional activation in the left amygdala in the ASD group only, suggesting that ASD is characterized by a unique relationship between neuron cell body density in the left amygdala and functional activity while processing emotional faces. This study highlights the power of leveraging a large consortium dataset to address questions about the neurobiological underpinnings of autism.

Vanneau and colleagues from the Albert Einstein College of Medicine IDDRC used EEG to investigate neural oscillatory dynamics during face processing in the context of a visual oddball task in autistic children and unaffected siblings of autistic children 8–13 years old with and without autism and siblings of autistic children [9]. The visual oddball task involved presenting upright and inverted faces and objects. Outcomes of interest were face-related event-related potentials (ERPs) including P1 and N170 and oscillatory activity associated with sensory and attentional processing (theta, alpha, and gamma). Across groups, pictures of faces elicited an earlier P1 and larger N170 amplitude than objects. The autistic group had a reduced face inversion effect (i.e., larger or delayed N170 to inverted versus upright faces) in the right hemisphere than the other groups, which may reflect less holistic face processing. Both the autistic and sibling groups evidence stronger thetas for inverted faces suggesting that they were employing more cognitive effort to process the stimuli. There was stronger gamma-band inter-trial coherence for face stimuli in the non-autistic group than autistic group than in the other two groups, suggesting differences in early network synchronization in autistic children. Altogether, these findings support altered neural synchronization/efficiency for autistic participants and siblings of autistic children that is specific to face stimuli and seen despite largely typical sensory driven encoding. Overall, findings suggest that broadband sensory-driven mechanisms for processing faces (P1 and N170) are largely intact in autistic children and their siblings. However, specific neural oscillatory processes show differences in face processing among autistic children and their siblings versus non-autistic children. These results have implications for the identification of candidate biomarkers in autism and provide new insights about the altered and non-altered aspects of face processing in autism.

Bertollo and colleagues examined self- and caregiver-completed ratings of self-determination and executive function subdomains in 226 autistic adolescents 14–22 years old. They found that, for self-reported measures, challenges with flexibility and planning predicted lower capacity for self-determination, whereas for parent-reported measures, relationships were generalized across executive function subdomains. Additionally, flexibility, planning, working memory, and emotion regulation demonstrated cross-rater relationships with self-determination. These findings link executive function to self-determination in autism and suggest that supporting flexibility, planning, flexibility, initiation, inhibition, and emotional control may be important for facilitating self-determination in autistic teens [10].

Nicklas and colleagues from the IDDRC at the University of Rochester examined cognition, movement, and visual demands in 20 autistic and 18 typically developing adolescents using mobile brain-body imaging (MoBI) [11]. They found that typically developing adolescents were more accurate on a response inhibition task while walking on a treadmill than while standing, but autistic adolescents did not show the same improvements. Optic flow—visual motion cues—increased response time on the response inhibition task for both groups but did not significantly affect task accuracy. The experimental conditions (walking and walking + optic flow) attenuated N2 and P3 ERPs across both groups which appeared to be driven by walking rather than optic flow. This indicates that motor demands increased cognitive load, while optic flow did not appear to place additional demands on the brain’s resources. These findings suggest that motor, cognitive, and sensory functions interact in complex ways, and that autistic adolescents may integrate these functions differently than their typically developing peers.

The papers in this special issue exemplify the depth and breadth of IDD research supported by the IDDRC network and connect around common themes. The body of work represented in this special issue positions EF as a central construct in IDD research. EF challenges are transdiagnostic, early emerging, linked to relevant outcomes, and impact caregivers. Using diverse neuroimaging methods, studies in this special issue examined how distinct neural structure and function related to several sensory and cognitive domains. These investigations highlight that cognitive processes in IDDs are complex and may be better understood by studying the integration and timing of neural activity rather than by focusing on a single biomarker. In summary, the articles featured in this special issue, supported by the IDDRC network, reflect significant progress and continued momentum in our understanding of memory, attention, and executive function in IDDs. More broadly, these studies also highlight the importance of leveraging large consortium and prospective, longitudinal datasets to address complex questions about cognitive development in IDD.

Authors’ contributions

TSJ, GSD, and SH each drafted sections of this editorial. The author(s) read and approved the final manuscript.

Funding

GSD was supported by P50 HD103573.

SLH was supported by P50 HD105353.

TSJ was supported by U54HD083091 and R01-HD055741.

Data availability

Not applicable.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.