Executive functions in children with Autism Spectrum Disorders

Abstract

Executive dysfunction is a characteristic impairment of individuals with Autism Spectrum Disorders (ASD). However whether such deficits are related to autism per se, or to associated intellectual disability is unclear. This paper examines executive functions in a group of children with ASD (N = 54, all IQ⩾70) in relation to a typically developing control group individually matched on the basis of age, gender, IQ and vocabulary. Significant impairments in the inhibition of prepotent responses (Stroop, Junior Hayling Test) and planning (Tower of London) were reported for children with ASD, with preserved performance for mental flexibility (Wisconsin Card Sorting Task) and generativity (Verbal Fluency). Atypical age-related patterns of performance were reported on tasks tapping response inhibition and self-monitoring for children with ASD compared to controls. The disparity between these and previous research findings are discussed. A multidimensional notion of executive functions is proposed, with difficulties in planning, the inhibition of prepotent responses and self-monitoring reflecting characteristic features of ASD that are independent of IQ and verbal ability, and relatively stable across the childhood years.

Introduction

The concept of ‘executive function’ refers to the higher order control processes necessary to guide behaviour in a constantly changing environment (Jurado & Rosselli, 2007). The concept includes abilities such as planning, working memory, mental flexibility, response initiation, response inhibition, impulse control and monitoring of action (Roberts et al., 1998, Stuss and Knight, 2002). Behavioural and neuropsychological studies originally linked executive functions to the frontal lobes, in particular the pre-frontal cortex (Baddeley and Wilson, 1988, Stuss and Benson, 1986). However, more recent neuroimaging studies have shown that executive functions are associated with different regions of the frontal lobes, with links between frontal and posterior areas, as well as subcortical and thalamic pathways (Monchi et al., 2006, Stuss and Alexander, 2000, Stuss et al., 2002).

Executive dysfunction has been linked to a number of developmental disorders, including Autism Spectrum Disorder (ASD) (see Russell, 1997). Behavioural similarities between patients with frontal lobe lesions and individuals with ASD led to the notion that some of the everyday social and non-social behaviours seen in individuals with ASD may reflect specific executive dysfunction (Ozonoff, Pennington, & Rogers, 1991). The behaviours proposed to be accounted for by the theory of executive dysfunction include; a need for sameness, a strong liking for repetitive behaviours, lack of impulse control, difficulty initiating new non-routine actions and difficulty switching between tasks (Hill, 2004, Rajendran and Mitchell, 2007). These non-social behaviours comprise strengths as well as weaknesses for individuals with ASD, and they are not successfully accounted for by the theory of mind deficit hypothesis (Happé, 1994), weak central coherence accounts (Frith, 1989, Frith, 2003) or the extreme male brain theory (Baron-Cohen, 2002).

Executive dysfunction in ASD has been widely investigated. In a review of the ASD literature, Hill (2004) divided studies into the executive domains of; planning, mental flexibility, inhibition, generativity and self-monitoring. Difficulties have been reported in each of these domains for individuals with ASD (e.g. Hill and Bird, 2006, Hughes and Russell, 1993, Ozonoff et al., 2004, Rumsey and Hamburger, 1988, Russell et al., 1999). However, preserved performance has also been documented (e.g. Boucher, 1988, Hughes et al., 1994, Ozonoff and Jensen, 1999, Russell and Hill, 2001). Hill (2004) attributed these inconsistencies to methodological differences, such as task selection, participant matching and ability level. In particular, the inclusion of participants with cognitive impairments means that the extent to which executive difficulties reflect autistic symptomology or intellectual disability is unclear. Hill (2004) proposed there is a need for better controlled studies to establish whether executive deficits are causally related to autistic symptomology. To address these issues, this paper reports findings from a sample of children with ASD, whose IQ’s fall within the normal range, in relation to typically developing age, IQ and vocabulary matched controls, for the executive domains of planning, mental flexibility, response inhibition and generativity, and self-monitoring.

Planning is a cognitive skill that requires constant monitoring, evaluation and updating of actions (Hill, 2004). The Tower of Hanoi (ToH) or the Tower of London (ToL) tasks are often used to assess planning and problem solving skills. On these tasks, participants must move beads from a prearranged sequence to match a goal state determined by the examiner. Children with ASD, with IQ scores at the lower end of the normal range, have been reported to be significantly impaired on these tasks compared to age and/or IQ matched controls (typically developing, intellectually impaired or other groups with other developmental disorders, such as ADHD, Tourette syndrome and dyslexia; Geurts et al., 2004, Hughes et al., 1994, Ozonoff and Jensen, 1999, Ozonoff and McEvoy, 1994, Ozonoff et al., 1991). Impaired planning of underhand reaches on the Luria bar task (Hughes, 1996) and slowed performance on the Milner mazes (Milner, 1965, Prior and Hoffman, 1990) has also been reported for children with ASD.

In contrast, on a computerised version of the ToH/ToL tasks, the Stockings of Cambridge task (SoC), Happé, Booth, Charlton, and Hughes (2006) reported normal performance for children with ASD who had IQ’s above 70. They also reported a significant reduction in the number of extra moves made by older children (11–16 years) to complete problems compared with younger children (8–10 years). This suggests that planning deficits may be related to level of general intellectual functioning and maturation. Mari, Castiello, Marks, Marraffa, and Prior (2003) also reported that impaired planning ability on a kinematic reach-to-grasp task was related to level of IQ rather than to autism. However, impaired planning on the Trail Making Test (Army Individual Test Battery, 1944, Rumsey and Hamburger, 1988) has been reported for men with ASD whose IQ’s fell within the normal range. The computerised and standard version of the ToH/ToL task may also not be equivalent. Thus, is it unclear whether discrete cognitive task demands or level of intellectual functioning contribute to the preserved performance reported by Happé et al. (2006).

Mental flexibility refers to the ability to shift to a different thought or action in response to situational changes. The Wisconsin Card Sorting Task (WCST) is a classic test of mental flexibility that requires participants to sort cards according to one of three possible rules (colour, shape or number). Difficulty in shifting to a new sorting procedure is typically taken as the primary index of executive dysfunction (Hill, 2004). Individuals with autism have been reported to be highly perseverative on this task compared to typically developing (TD) controls and controls with other developmental disorders, such as, attention deficit hyper-activity disorder (ADHD), language disorder, Tourette syndrome and dyslexia (Geurts et al., 2004, Liss et al., 2001, Ozonoff and Jensen, 1999, Ozonoff et al., 1991, Rumsey, 1985). Similarly, impaired performance has been reported on the intradimensional–extradimensional shift task of the Cambridge Neuropsychological Test Automated Battery (Cambridge Cognition, 1996) for individuals with ASD (Hughes et al., 1994, Ozonoff et al., 2004).

However, Liss et al. (2001) reported no significant difference in perseverative errors on the WCST between children with autism and children with developmental language disorder once verbal IQ was controlled for. This suggests that perseverative tendencies may be related to verbal ability. Normal perseverative performance has also been reported for individuals with autism who have IQ’s within the normal range (i.e. above 70; Ozonoff, 1995), though this has not been found by all (Minshew, Goldstein, Muenz, & Payton, 1992). Ozonoff (1995) also reported attenuated rates of perseveration for children with ASD on a computerised version of the WCST compared to the traditional card version, which may reflect reduced verbal and social task demands. In addition, multiple component skills are required for successful performance on the WCST (e.g., generation of a sorting rule, working memory to hold the sorting principle, use of feedback to inhibit prepotent responding, the ability to shift set). Thus, although many studies have reported difficulties in mental flexibility for individuals with ASD, poor performance may be confounded by level of general intellectual functioning, verbal ability and task demands.

Response inhibition is the ability to suppress irrelevant or interfering information or impulses. The Stroop (Stroop, 1935) is a classic task of response inhibition that requires participants to name the colour that words are written in, whilst ignoring the word representing colour itself (e.g. “red”/“blue”). Regardless of level of intellectual functioning, interference effects for children and adults with ASD are not reported to differ significantly from controls on traditional card versions of this task (Hill and Bird, 2006, Ozonoff and Jensen, 1999, Russell et al., 1999). This is in contrast to children with ADHD and Tourette syndrome for whom inhibitory performance on this task is reported as impaired (Ozonoff & Jensen, 1999). Typical interference effects have also been reported for children with ASD, with IQ’s within the normal range for the Go/No-Go task, Stop-Signal task and negative priming tasks (Ozonoff and Strayer, 1997, Ozonoff et al., 1994, Schmitz et al., 2005). Performance on computerised versions of the Stroop have not yet been investigated for children with ASD.

Impaired response inhibition has, however, been reported on the Windows Task, and variations of this task, for children with ASD (Bíro and Russell, 2001, Hughes and Russell, 1993, Russell et al., 2003, Russell et al., 1991). On these tasks, in order to win a desired object (chocolate) visible in a box, children are required to inhibit the prepotent response of pointing to the box with the chocolate in it and instead point to an empty box beside it. Consistently poor performance on these tasks indicates a difficulty inhibiting prepotent responding.

The Hayling test (Burgess & Shallice, 1997) is another measure of prepotent response inhibition. In the first part of this test participants are required to complete the last word of a sentence as quickly as possible, whilst in the second part they are required to complete the sentence using a word that does not fit the context. Hill and Bird (2006) reported impaired performance (increased response latencies) on this test for adults with ASD. They proposed that poor performance reflected a generative deficit rather than an executive impairment in inhibition or strategy formation; however strategy formation was not directly assessed. Performance on this task has not yet been reported for children with ASD. It is therefore unknown whether performance is impaired for children with ASD and if so whether poor performance reflects an impairment in the inhibition of prepotent responses, strategy formation, generativity or the arbitrary nature of the rules.

Generativity is the ability to generate novel ideas and behaviours spontaneously (Turner, 1997). Tests of Verbal Fluency are typically used to assess generativity. These tasks require participants to produce as many words as possible within a specified time in response to either a phonemic (e.g. the letter F) or semantic cue (e.g. the category of animals). Impaired performance has been reported for individuals with autism in relation to age and ability matched controls (Minshew et al., 1992, Rumsey and Hamburger, 1988, Turner, 1999), though this has not been found by all (Boucher, 1988, Scott and Baron-Cohen, 1996). A generative deficit has been proposed to account for impaired performance on measures of response inhibition (Hill & Bird, 2006). Generativity may therefore contribute to the pattern of performance reported for children with ASD in other executive domains.

Self-monitoring is the ability to monitor one’s own thoughts and actions (Hill, 2004). Specific tests designed to assess this executive domain are not well established and they have generally failed to find any performance differences in ASD (Hill & Russell, 2002). Impairments in self-monitoring have only been reported on a post hoc basis, for example error correction, avoidance and memory for actions (Hughes, 1996, Russell and Jarrold, 1998, Russell and Jarrold, 1999). Monitoring one’s verbal output is required on tests of Verbal Fluency to prevent item repetition. A deficit in self-monitoring might therefore be apparent in perseverative responses on these fluency tasks, again this has not yet been reported for individuals with ASD.

The aim of the present study was to provide information relevant to identifying the nature of executive functions in children with ASD. As discussed above, performance was assessed for mental flexibility, planning, inhibition and generativity. Children with ASD were individually matched to TD controls on the basis of age, IQ, receptive vocabulary and gender. To ensure that performance differences reflected autistic symptomology and not level of intellectual functioning, performance was assessed for children whose IQ’s fell within the normal range. Age-related differences in performance were also investigated. The specific research questions to be addressed by the study were:

• Do children with ASD exhibit executive impairments in planning, mental flexibility, inhibition or generativity?

• Do children with ASD exhibit typical age-related differences in executive performance?

• To what extent does intellectual disability influence executive functioning in children with ASD?