Elsevier

Research in Autism Spectrum Disorders

Volume 6, Issue 3, July–September 2012, Pages 1099-1106
Research in Autism Spectrum Disorders

Relationship between executive functions and motor stereotypies in children with Autistic Disorder

https://doi.org/10.1016/j.rasd.2012.03.001Get rights and content

Abstract

This study reports on the relationship between motor stereotypies and impairments in executive functions (EF) in children with Autistic Disorder (AD) and in children with Developmental Language Disorders (DLD). We hypothesized that low EF performance would predict higher frequency and longer durations of stereotypies in the AD group only. Twenty-two children (age range = 7–9 years, 6 months, girls = 5) with AD were recruited from a longitudinal multi-site study and compared to twenty-two non-autistic children with DLD (age range = 7–9 years, 6 months, girls = 5). The two groups were matched on non-verbal IQ and demographic characteristics. Frequency and duration of stereotypies were coded from videotaped semi-structured play sessions. EF measures included the Wisconsin Card Sorting Task (WCST) Categories, Wechsler Intelligence Scale for Children-Revised (WISC-R) Mazes, and Stanford-Binet Fourth Edition (SB-IV) Matrices. The scores for frequency and duration of stereotypies were higher in the AD group. Separate linear regressions revealed that group status, EF, and their interactions predict stereotypies. Specifically, lower EF scores predicted higher frequencies and longer durations of stereotypies in the AD group only. Analyses controlled for age, gender, and parent education. Findings suggest that in AD, EF impairments and stereotypies may be linked to shared brain pathways.

Highlights

► The relationship between motor stereotypies and executive functions in AD is not well understood. ► One reason may be the lack of standardized quantitative measures of stereotypies. ► We used videotape coding to assess stereotypies in children with AD and controls. ► More motor stereotypies predicted EF performance, only in the AD group.

Introduction

Restricted and repetitive behaviors (RRBs) represent the third core criteria for a diagnosis of Autistic Disorder (AD) in the DSM-IV-TR (American Psychiatric Association [DSM-IV-TR], 2000). RRBs are present in children and adults with Autism Spectrum Disorder (ASD) at higher rates than in any other developmental disability (Matson et al., 2009a, Morgan et al., 2008) and hamper normal development, learning, and social adaption (Leekam, Prior, & Uljarevic, 2011).

Among the different subtypes of RRBs, motor stereotypies are defined as patterned, repetitive, and purposeless movements (e.g., hand flapping, finger flicking, rocking). A recent review of the assessment and treatment of motor stereotypic behaviors in children with autism and other pervasive developmental disabilities, found that 25 unique categories of stereotypies have been identified in the literature (Di Gennaro Reed, Hirst, & Hyman, 2012). In ASD, motor stereotypies are prevalent, enduring, and present in all age groups (Bishop et al., 2006, Bodfish et al., 2000, Richler et al., 2010, Zandt et al., 2007). Additionally, infant and high-risk sibling studies suggest that stereotypies represent valid early markers of ASD (Baranek, 1999, Matson et al., 2009b, Wetherby et al., 2004).

Emerging evidence has demonstrated that motor stereotypies occur not only in children with ASD, and other developmental disabilities but also in normally developing children and adolescents (Barry et al., 2011, Harris et al., 2008, Mahone et al., 2004). The nature and developmental course of stereotypies among individuals with ASD is not well understood (Symons, Sperry, Dropik, & Bodfish, 2005). Moreover, observational research has revealed that motor stereotypies may be more prevalent during times of emotional or social demand (e.g., times of excitement or stress, situations with increased social engagement) and in times of boredom (Schlaggar & Mink, 2003).

Repetitive motor behaviors have not only been associated with the severity of ASD diagnosis (Bodfish et al., 2000), but also with deficits in executive functions (EF) (Liss et al., 2001, South et al., 2007). EF are defined as higher order cognitive processes that include planning, initiating and inhibiting actions, selecting relevant sensory information from one's surroundings and general cognitive flexibility (e.g., Shallice & Burgess, 1991). The Pre-Frontal Cortex (PFC) and frontal-basal ganglia circuits have been identified as the core brain substrates associated with EF (Stuss, 1992, Stuss and Alexander, 2000).

Poor EF performance has been found in individuals with ASD on a variety of tasks including, those involving inhibition of prepotent responses (Stroop Test), planning (Tower of London), generativity (Verbal Fluency Test), cognitive flexibility (Wisconsin Card Sorting Test), and memory (Bennetto et al., 1996, Robinson et al., 2009). Impairments on EF tasks are thought to directly relate to one's ability to respond, plan, and adapt behaviors based on environmental and social cues (Ridley, 1994). The executive dysfunction hypothesis, which states that the types of symptoms present in ASD are due to deficits in the executive control of behaviors, has been linked to the prevalence of RRBs seen in ASD (Hughes et al., 1994, Sayers et al., 2011).

Only within the past decade have subtypes of RRBs in ASD been examined systematically (Leekam et al., 2011, Richler et al., 2010). One identifiable subtype is motor stereotypies, which are typically considered lower-level repetitive behaviors and usually associated with younger and lower functioning children, while restricted interests, nonfunctional routines, and rituals are considered higher-level repetitive behaviors, and are typically associated with older and higher-functioning individuals (Leekam et al., 2011, Turner, 1999).

Most validated diagnostic measures for ASD contain subsections devoted to assessing RRBs, such as the Autism Diagnostic Observation Schedule (ADOS; Lord et al., 2000) the Autism Observation Scale for Infants (AOSI; Bryson, Zwaigenbaum, McDermott, Rombough, & Brian, 2008), the Baby and Infant Screen for Children with aUtIsm Traits (BISCUIT; Matson, Wilkins, et al., 2009), and the Communication and Symbolic Behavior Scales Developmental Profile (CSBS-DP; Wetherby, Allen, Cleary, Kubin, & Goldstein, 2002). Other widely used measures include questionnaires, such as the Repetitive Behavior Scale-Revised (RBS-R; Lam & Aman, 2007) and paper-and-pencil rating scales, which typically capture global impressions of stereotypy frequency and severity, which may be subjective and biased (Pyles, Riordan, & Bailey, 1997).

While one-time observational measures aid in capturing the breadth of RRBs in autism, several factors limit their reliability, such as (1) a reduced ability to accurately document rapid stereotypies, (2) difficulty observing simultaneous motor movements, and (3) a limited capacity to identify when movements begin and end (Sprague & Newell, 1996). In contrast, the coding of videotapes allows for systematic observation and assessment of repetitive movements, so as to offer better characterization, a capability to re-watch rapid and concomitant movements, as well as the power to determine duration of these movements.

A recent study using alternative methods to precisely measure motor stereotypies utilized accelerometers and pattern recognition algorithms to automatically detect these movements in children with ASD (Goodwin, Intille, Albinali, & Velicer, 2011). Findings revealed that approximately 90% of the time these automated methods were able to correctly identify stereotypical movements. Videotape recordings and automated detection of motor stereotypies may allow for a better classification and understanding of this RRB subtype in ASD.

Motor stereotypies, a subtype of RRBs, are thought to be overt and acute forms of perseveration, which may be related to a lack of generativity (Turner, 1999). Based on this view, we hypothesize that deficits in EF in autism may underlie motor stereotypies seen in this population. In line with this expectation, positive relationships have been found between the prevalence of RRBs and deficits of specific EF tasks, such as response inhibition, generativity, flexibility, and working memory, in individuals with ASD but not in matched-controls (Lopez et al., 2005, South et al., 2007). Similarly, a recent study using self-report measures of adolescents with ASD, found greater stereotypic behaviors and restricted interests scores and poorer EF performance, especially in boys (Bölte, Duketis, Poustka, & Holtmann, 2011). Another study found that executive deficits, as measured by an informant-based rating scale, were correlated with repetitive behaviors, assessed by the RBS-R in children with high functioning autism and healthy, typical controls (Boyd, McBee, Holtzclaw, Baranek, & Bodfish, 2009). Findings also revealed that ASD diagnosis, younger age, sensory processing issues, and behavioral regulation deficits predicted more repetitive behaviors (Boyd et al., 2009).

On the contrary, other studies have failed to find any correlation between RRBs and several common neuropsychological EF tasks in school-aged children with ASD (Joseph & Tager-Flusberg, 2004), and another study did not find an association between RRBs, measured by the ADOS (Lord et al., 2000) and the ADI-R (Lord, Rutter, Le Couteur, 1994), and inhibition and working memory (Ozonoff et al., 2004). The above divergent results on the association between EF and RRBs may stem from the lack of focus on the distinct subtypes of repetitive behaviors in ASD such as motor behaviors versus rituals.

Accordingly, we sought to revisit the question of the relationship of RRBs and EF deficits. Specifically, we examined repetitive motor behaviors (i.e., stereotypies) in a group of children diagnosed with Autistic Disorder (AD) and a matched control group of non-autistic children with Developmental Language Disorders (DLD). We used quantitative objective measures of the frequency and duration of motor stereotypies collected during videotaped semi-structured play sessions. In regard to EF, we selected three tasks from the fixed research battery of neuropsychological tests, WCST Categories, WISC-R Mazes, and SB-IV Matrices. These tasks measure cognitive domains such as, inhibition, planning, and mental flexibility, as well as perseverations, which are linked to RRBs in autism.

We hypothesized greater frequencies and longer durations of stereotypies in the AD group compared to controls, replicating prior work on RRBs and autism. We expected EF measures to be related to stereotypy frequency and duration; however, AD diagnosis was expected to moderate the EF-stereotypy association such that it would be stronger (or only evidenced) in the AD group compared to a control group of children with DLD. This work advances on the literature in two key ways: (1) we utilize video-recorded quantitative measures of motor stereotypies rather than broad measures of RRBs that collapse routines, rituals, and motor behaviors, and (2) we focus on a narrow age range of children at a time in development when motor stereotypies are prevalent.

Section snippets

Participants

Children were selected from a longitudinal, multi-centric (Boston MA, the Bronx NY, Cleveland OH, and Trenton, NJ), nosological study conducted between 1985 and 1992 involving comprehensive behavioral, neurological, neuropsychological, and psychiatric evaluations that placed them into one of four diagnostic groups based on cognitive level and autism diagnosis (Rapin, 1996). The children were assessed at age three by trained psychiatrists according to the DSM-III-R (American Psychiatric

Results

The AD and DLD groups were comparable for key demographic characteristics (Table 1).

As expected, the frequency (3.82, ±2.50) and duration (8.41, ±4.15) of stereotypy episodes in the AD group were significantly greater than the frequency (2.50, ±1.78) and duration (1.17, ±0.48) of stereotypy episodes in the DLD control group. No group differences were found on the EF tasks.

The key demographic variables, AD diagnosis, the three EF tasks (WCST Categories, WISC-R Mazes, and SB-IV Matrices) and the

Discussion

This study was designed to evaluate the relationship between frequency and duration of motor stereotypies and executive functions in 22 children with AD and 22 matched control children with DLD. The findings are consistent with our hypothesis, stating that lower EF performance on tasks of inhibition, planning, and mental flexibility would predict higher frequency and longer durations of stereotypies only in the AD group, even when adjusting for age, gender, and parent education.

Our results

Financial disclosure

Sylvie Goldman was supported by the Einstein/Montefiore Autism Center and a LEND grant-Leadership Education in Neurodevelopmental and Related Disabilities from the Bureau of Maternal and Child Health in the Department of Health and Human Services.

Conflicts of interest

None declared.

Acknowledgements

We thank the children and their parents for their participation. We thank Dr. Isabelle Rapin, Principal Investigator of this original study, supported by NINDS program Project NS 20489, for her insightful comments. We also thank the two blind raters who devoted their time and effort to code the videotapes used in this study. Portions of this manuscript were presented at the 39th annual North America meeting of the International Neuropsychological Society in Boston, Massachusetts on February

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