Diane L. Williams
What is autism?
Autism, or what is now referred to as autism spectrum disorder (ASD), is a behaviorally-defined and diagnosed neurodevelopmental disorder (Amaral, Schumann, & Nordahl, 2008). Because there is no generally accepted biomarker for ASD, researchers and medical practitioners have to rely on behavioral char - acteristics when making a diagnosis. The defining characteristics of ASD were agreed upon by a panel of experts in the field and are published in the Diagnostic and Statistical Manual of Mental Disorders, 5th ed. (DSM-5; American Psychiatric Association, 2013).
In the prior edition of the DSM, autism was included within the multicategorical diagnosis of Pervasive Developmental Disorder (PDD). This diagnosis included the categories of Autistic Disorder, Asperger syndrome, PDD-not otherwise specified (PDD-NOS), childhood disintegrative disorder, and Rett’s disorder (DSM-4-TR;
American Psychiatric Association, 2000). Subsequent research identified problems with this multicategorical approach with limited reliability in the assignments of the DSM-4 subtypes (e.g. Walker et al., 2004).
The DSM-5 model recognizes the spectrum nature of autism and focuses on the two primary domains, impaired social communication and restricted, repetitive behaviors, that have been shown to improve the specificity of the diagnostic process (e.g., Frazier et al., 2012; Mandy, Charman, & Skuse, 2012). The DSM-5 model also allows for variability in other symptoms such as cognitive ability, expressive language ability, type of onset, and comorbid psychopathologies. These are not core symptoms because they are not specific to ASD, that is, they are shared with other neurodevelopmental disorders. However, the variability of these symptoms may provide a means for the identification of subtypes within ASD (Grzadzinski, Huerta, & Lord, 2013).
Cognitive functioning of individuals with ASD varies from severe intellectual disability to performance in the gifted range. More severely affected individuals may be minimally verbal with use of 10 or fewer spoken words or echolalic or
stereotyped phrases without clear communicative intent, and may need to use augmentative means of communication such as sign language, picture exchange systems, or speech-generating devices (Tager-Flusberg & Kasari, 2013). Other individuals with ASD may use conversational speech with mastery of the structural aspects of language (syntax, morphology, and phonology) but have deficits in pragmatics or the functional use of language and communication (Tager-Flusberg, Paul, & Lord, 2001). Mildly affected individuals with ASD may function well academically but may be challenged in adaptive functioning; as an adult, they may have difficulty securing and keeping a job and living independently (Taylor, Henninger, & Mailick, 2015).
A variety of observational tools and questionnaires are used when making a diagnosis of ASD. In recent years, research standards for determining diagnosis are typically met through the use of the Autism Diagnostic Interview—Revised (ADI-R; Lord, Rutter, & Le Couteur, 1994), the Autism Diagnostic Observation Schedule (ADOS-2; Lord, Rutter, DiLavore, Risi, Gotham, & Bishop, 2012), with verification by expert clinical opinion. The Social Responsiveness Scale (SRS-2;
Constantino & Gruber, 2012), a 65-item questionnaire completed by raters, who have known the individual being rated for at least one month, may be used to measure social deficits associated with ASD. Other common clinical instruments for the diagnosis of ASD include the Childhood Autism Rating Scale (CARS-2;
Schopler, Van Bourgondien, Wellman, & Love, 2010) and the Gilliam Autism Rating Scale (GARS-3; Gillam, 2014).
Theoretical models
Several theoretical models have been proposed to explain the behavioral presentation of ASD. The most frequently cited ones are theory-of-mind (Baron- Cohen, 1989), weak central coherence (Frith, 1989), and executive dysfunction (Hill, 2004). A fourth model, based on neuropsychological research, describes ASD as a disorder of complex information processing (Minshew, Goldstein, & Siegel, 1997).
Theory-of-mind is the ability to understand that other people have thoughts and to make an inference about what those thoughts might be. Problems with the development of theory-of-mind are thought to underlie the difficulty that individuals with ASD have in determining or misinterpreting the motives and intentions of others. This model of ASD explains how the lack of understanding what other individuals know makes effective communication and social interactions very difficult; however, it does not explain additional difficulties individuals with ASD have with cognition, language, and learning nor does it explicitly incorporate other cognitive functions such as Working Memory.
The second model of ASD, weak central coherence, attempts to explain the cognitive and learning differences in individuals with ASD. According to this explanation, individuals with ASD have a tendency to focus on local elements with concurrent difficulty processing the global features of stimuli or integrating the parts
into a cohesive whole (Frith & Happé, 1994). With respect to memory, individuals with ASD are observed to remember details of an event but to have difficulty extracting the most important elements of the event. This model provides an explanation for behaviors observed when individuals with ASD perform visual and linguistic tasks (Vanegas & Davidson, 2015). However, the predictions of this model have not been universally supported (e.g. Hahn, Snedeker, & Rabagliati, 2015).
Nor does it provide an adequate explanation of behaviors observed across the cognitive domains.
The third model of ASD arose from the challenges in Executive Functions such as Working Memory, attention, planning, organization, response inhibition, set shifting, and goal monitoring demonstrated by persons with ASD (Hill, 2004;
Pennington & Ozonoff, 1996). Unlike the first two models of ASD, the executive dysfunction model explicitly incorporates the domain of Working Memory and a large number of studies based on this model have provided greater understanding about Working Memory in ASD.
The fourth model of ASD, the complex information processing model (Minshew et al., 1997), is based on information processing theories of cognition and language. A basic assumption of this model is that individuals with ASD have underlying differences in neurofunction that present challenges during learning and processing of information (Minshew, Williams, & McFadden, 2008). This model also asserts that these challenges present across the cognitive domains beyond social cognition and language (Minshew, Webb, Williams, & Dawson, 2006). That is, relatively impaired performance will be found in skilled motor, memory, language, concept formation, and reasoning domains when the processing demands in these domains exceed the cognitive resources of the individual with ASD (Minshew et al., 1997; Williams, Goldstein, & Minshew, 2006). This observation is, of course, true of all learners. However, for individuals with ASD, overall cognitive functioning level is not predictive of performance in the same way that it is for individuals with typical development (Liss et al., 2001). Individuals with ASD have difficulty in performing tasks at lower levels of demand than generally expected.
The term “complex” in the name of the model refers to the type of demand placed on the brain’s processing system by tasks or situations (the need for a highly coordinated network of processing resources) rather than the type of information being processed. This model incorporates elements of cognitive resource theory such as allocation of cognitive resources and competition among task demands to understand what happens to individuals with ASD when they are challenged with different types of processing tasks. Working Memory, an important cognitive resource, has been considered within this model.
Working Memory (WM) and related Executive Function (EF) deficits
Given the reported difficulty individuals with ASD have with a number of Executive Functions, it is not surprising that Working Memory has been reported
to be affected in ASD; however, this has not been a consistent finding. The discrepancies have been attributed to various factors such as differing sample sizes and the related power to detect clinically significant differences, the ages of the participants and possible effects of developmental stages, and to overall heterogeneity within the ASD population. Alternately, the inconsistencies may actually provide clues to the functioning of Working Memory in ASD. For example, an important factor appears to be the level of demand of the task used to assess Working Memory.
That is, individuals with ASD may have no difficulty with Working Memory tasks that only require a brief maintenance before repeating or using the information;
however, a decrement in performance may occur when information must be maintained while another task is performed.
A related issue in Working Memory in ASD is the differential effect on visuospatial and verbal Working Memory systems. Whereas some studies view Working Memory as a single cognitive function (e.g. Schuh & Eigsti, 2012), most of the studies examine visuospatial Working Memory and verbal Working Memory separately (e.g. Steele, Minshew, Luna, & Sweeney, 2007; Williams, Goldstein, Carpenter, & Minshew, 2005a; Williams, Goldstein, & Minshew, 2006). For example, even in the Schuh and Eigsti study, the performance of the group with ASD was comparatively poorer than that of the comparison group with typical development on the visuospatial Working Memory measure but not on one of the verbal Working Memory measures. The results of studies of visuospatial and verbal Working Memory and the development of Working Memory in ASD are reviewed in the following sections.
Visuospatial Working Memory
Individuals with ASD have frequently been reported to have visuospatial Working Memory deficits even if no deficits occur on verbal Working Memory tasks ( Joseph, Steele, Meyer, & Tager-Flusberg, 2005; Williams et al., 2005a; Williams, Goldstein,
& Minshew, 2005b). Studies that have used visuospatial tasks that did not have any inherent organization or explicit strategy have generally reported relative deficits in visuospatial Working Memory for individuals with ASD ( Jiang, Capistrano,
& Palm, 2014; Schuh & Eigsti, 2012; Williams et al., 2005a, 2005b, 2006). For example, children with ASD have been reported to perform more poorly than age and ability matched controls on a “Finger Windows” task (Sheslow & Adams, 1990).
In this task, the examiner holds up a card with window-like openings in a 3 ⫻3 grid. The examiner pokes the end of the pencil in turn through the holes, modeling a pattern. The participant uses a finger to repeat the pattern in the correct sequence. The position of the pencil is not easily encoded verbally requiring the participant to maintain the image of the pencil pokes in Working Memory to recall what pattern was produced. This task is generally difficult for individuals with ASD.
Findings are more inconsistent when other measures have been used. For example, a Corsi block-tapping task (Lezak, 1995) is a visual spatial span task that is frequently used with individuals with ASD. In this task, an array of cubes is
presented; the examiner taps the cubes in sequences of increasing numbers of taps or, if presented in a computerized version, the squares change color. The participant touches the blocks with one finger or points to the squares with a computer mouse to reproduce the modeled sequence. When only a forward span condition was used, the performance of individuals with ASD has been reported to be unimpaired on this task as compared to controls with typical development (Macizo, Soriano,
& Paredes, 2016; Verté, Geurts, Roeyers, Oosterlaan, & Sergeant, 2006). However, when span forward and backward scores have been combined, the individuals with ASD had significantly more difficulty on this task than the age and ability-matched controls (Williams et al., 2005a). On a composite measure comprised of three visual–
spatial Working Memory tasks (odd-one-out, Mister X, and spatial recall tasks), children with ASD performed relatively lower than children with TD and children with SLI; however, the mean performance of the ASD group was in the low average range (Alloway, Seed, & Tewolde, 2016). On a self-ordered pointing task with abstract symbols (Petrides & Milner, 1982) in which the children had to remember what symbol they had pointed to so as not to point to that symbol again, children with ASD have been reported to be impaired (Verté et al., 2006) and unimpaired ( Joseph et al., 2005) relative to children with typical development.
Memory load appears to be an important factor in the performance of individuals with ASD on visuospatial Working Memory tasks. For example, when using a variation of the self-ordered pointing task presented as golf holes into which golf balls had been putted, Morris and colleagues (1999) reported that adults on the autism spectrum had a deficit in visuospatial Working Memory as compared to age- and ability-matched controls without ASD but only when the memory load was high (6 to 8 golf balls). Similar effects for memory load were found using a slightly different visuospatial Working Memory task (searching for blue tokens in
“boxes” on a computer screen without returning to an empty box) for children and adolescents with ASD (Landa & Goldberg, 2005). According to Steele et al.
(2007) the memory load, or the amount of information that needs to be maintained, has a greater impact on the performance of individuals with ASD than that of the age and ability matched controls and may explain the inconsistent findings across the various studies.
Verbal Working Memory
Verbal Working Memory has been reported to be affected and unaffected in ASD depending on the measure used and the age and ability level of the participants.
A number of studies have reported that verbal Working Memory is not affected in ASD when lower level tasks are used. For example, adults and children with ASD performed similarly to age and ability-matched controls on a classic n-back verbal Working Memory task in which individuals must press a button whenever two letters occur back to back (1-back) or after an intervening letter or character (2-back) (Williams et al., 2005a, 2005b). Several studies have noted that the individuals with ASD have more difficulty than the individuals with typical
development as the verbal material in the Working Memory task becomes more complex (e.g., Schuh & Eigsti, 2012). For example, children with ASD, 5 to 7 years of age, had difficulty on nonword repetition tasks but had even more difficulty on digit span and sentence imitation tasks (Gabig, 2008). Similarly, the effect of the level of task demand on Working Memory was demonstrated in a study that used a low demand, verbal span task (pointing to a series of pictured objects in the order they had been spoken) contrasted with a self-ordered pointing task (remembering what pictured objects they had pointed to in order to point to a different picture in each newly presented set) ( Joseph et al., 2005). The performance of the children with ASD, ages 5 to 14 years of age, was similar to that of the children with typical development on the verbal span task; however, they performed more poorly than that same group on the self-ordered pointing task ( Joseph et al., 2005). The differences in performance on these tasks may reflect differing demands of the tasks for holding information temporarily versus a greater need for maintenance and storage and the need for executive control (Bayliss, Jarrold, Gunn, & Baddeley, 2003). When a composite of three tasks that required maintenance and storage with executive control were used to measure verbal Working Memory, children with ASD, ages 4 to 13 years, scored significantly lower than the TD group but comparable to a group of children with SLI and a group of children with intellectual disabilities (Alloway et al., 2016).
In general, it has been difficult to separate the effects of ASD on language and the effects on verbal Working Memory with these two cognitive domains being closely connected (Schuh & Eigsti, 2012). For example, children with ASD who had more difficulty with language tasks also had increased difficulty on tasks requiring phonological Working Memory, supporting a link between Working Memory ability and language ability in ASD (Kjelgaard & Tager-Flusberg, 2001). In Hill et al. (2015), children with ASD and language impairment had more verbal Working Memory deficits than children with ASD without language impairment.
Related EF deficits
The importance of differing task demands and the need for executive control in the function of visuospatial and verbal Working Memory in individuals with ASD is supported by research on related Executive Functions such as inhibition and attention. As for Working Memory in ASD, the findings for inhibition and attention in ASD are inconsistent, possibly the result of differences in the cognitive load and the need for executive control of various tasks (Mostert-Kerckhoffs, Staal, Houben, & de Jonge, 2015). For example, when lower level measures of inhibition are used such as on a Go-no-Go task (e.g., press the button for planes but with hold response to bombs on a computer screen), the group with ASD has generally been reported to be unimpaired relative to the comparison group with typical development (Happé, Booth, Charlton, & Hughes, 2006). However, for tasks with an increased demand for executive control such as inhibition of a prepotent response (e.g., pressing a button corresponding to the opposite direction
of the movement of the target object), the group with ASD is generally reported to have more difficulty in comparison to typically developing controls (Mostert- Kerckhoffs et al., 2015). Similarly, basic reaction time measures of attention to auditory or visual stimuli or shifting attention within a single modality yield no difference in the performance of children and adults with ASD as compared to age- and ability-matched controls; however, differences may appear when shifting attention between modalities or when a memorized rule has to be applied to complete the task (Stoet & López, 2011; Williams, Goldstein, &
Minshew, 2013).
Developmental trajectory
Some of the differences in the results of studies of Working Memory in ASD may be related to the developmental stage of the group with ASD and the comparison group at the time of the study. ASD is a developmental disorder that changes in presentation with increasing age and level of experience. Working Memory, even in individuals with typical development, is not a static skill but changes with age and experience (Alloway & Alloway, 2013). Research on the developmental trajectory of Working Memory in individuals with ASD is sparse but suggests that it differs from that of typically developing individuals (O’Hearn, Asato, Ordaz, &
Luna, 2008). The development of Working Memory in ASD from childhood to adolescence in ASD may not differ significantly from the progression of other children (Happé et al., 2006). However, initial evidence from a cross-sectional study suggests that individuals with ASD may reach maturity in Working Memory development at later ages (Luna, Doll, Hegedus, Minshew, & Sweeney, 2007) with protracted development into young adulthood (O’Hearn et al., 2008). In a longi - tudinal study with children ages 9 to 16 years with ASD, ADHD, and typical development, the children with ASD did not improve in their performance on a verbal Working Memory task (letter/number sequencing) after two years (Andersen, Skogli, Hovik, Geurts, Egeland, & Øie, 2015). However, the performance of the children with ADHD and typical development did improve, supporting the contention that children with ASD have a different developmental trajectory for Working Memory.
Research on Working Memory in older adults with ASD is very limited.
A small, cross-sectional study reported an overall reduction of Working Memory abilities in older individuals with ASD compared to older individuals with typical development with the expected age-related decline (Guerts & Vissers, 2012).
A larger cross-sectional study found that the adults with ASD had longer reaction times but did not differ in Working Memory performance as compared to adults without ASD (Lever, Werkle-Bergner, Brandmaier, Ridderinkhof, & Geurts, 2015). Surprisingly, in the latter study, the adults with ASD did not show the expected age-related decline in Working Memory performance that was seen in the adults without ASD.