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DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY

ORIGINAL ARTICLE

An examination of the relationship between motor coordination and executive functions in adolescents DANIELA RIGOLI 1 | JAN P PIEK 1 | ROBERT KANE 1 | JAAP OOSTERLAAN 2 1 School of Psychology and Speech Pathology, Curtin Health Innovation Research Institute, Curtin University, Perth, Western Australia, Australia. 2 VU University Amsterdam, Department of Clinical Neuropsychology, Amsterdam, the Netherlands. Correspondence to Ms Daniela Rigoli at School of Psychology and Speech Pathology, Curtin University of Technology, GPO Box U1987, Perth 6845, Western Australia, Australia. E-mail: [email protected] This article is commented on by Michel on page 971 of this issue.

PUBLICATION DATA

AIM Research suggests important links between motor coordination and executive functions. The

Accepted for publication 29th May 2012. Published online 31st July 2012.

current study examined whether motor coordination predicts working memory, inhibition, and switching performance, extending previous research by accounting for attention-deficit– hyperactivity disorder (ADHD) symptomatology and other confounding factors, in an adolescent normative sample. METHOD Ninety-three adolescents (38 females, 55 males) aged 12 to 16 years (mean age 4y 2mo, SD 1y 1mo) were assessed on the Movement Assessment Battery for Children-2 (MABC-2), Wechsler Intelligence Scale for Children-IV, N-back task, the inhibition subtest from the NEPSY-II: A Developmental Neuropsychological Assessment, second edition, and the parent-rated Strengths and Weaknesses of ADHD Symptoms and Normal Behaviour Questionnaire. RESULTS The MABC-2 total score accounted for a significant proportion of the variance in visuospatial working memory (p=0.041) but not for verbal working memory. The MABC-2 aiming and catching component, however, was found to account for unique variance in both verbal (p=0.019) and visuospatial working memory (p=0.016). The MABC-2 total score was found to account for a significant proportion of the variance in inhibition total completion time (p=0.017). Finally, balance skills accounted for unique variance in a NEPSY-II inhibition total errors variable (p=0.020). INTERPRETATION The results provide support for an overlap between motor coordination and executive functions, which has important practical implications. The study also suggests shared mechanisms underpinning the relationship between these areas, including possible cerebellar involvement.

ABBREVIATIONS

DCD Developmental coordination disorder MABC-2 Movement Assessment Battery for Children-2 SES Socio-economic status SWAN Strengths and Weaknesses of ADHD Symptoms and Normal Behaviour VCI Verbal Comprehension Index WISC-IV Wechsler Intelligence Scale for Children-IV WMI Working Memory Index

It has been noted that motor control involves cognitive processes such as inhibiting frequently used movements, anticipating and updating aspects of the task to allow forward planning, resisting interference due to automatic postural control and fatigue, and the monitoring and correction of incorrect movements.1 However, although there is some suggestion that complex cognitive processes (i.e. executive functions) affect motor performance, causal evidence regarding the direction of the relationship is limited. The notion that motor development may predict cognitive functioning is partly supported by research highlighting that it is the sensory and motor functioning regions of the brain that are typically the first to mature.2 Furthermore, longitudinal studies have found that early motor development predicts later performance on complex cognitive tasks, including working memory.3 Conversely, in a study of preschool children, Niederer et al.4 found that baseline memory was not associated with an improvement in motor skills 9 months later. Diamond5 argued that the close association between motor and cognitive development is mediated by the coactivation of

the cerebellum and the prefrontal cortex. It is also important to note the role of individual differences when understanding this relationship.6 For example, there are a number of studies suggesting that physical activity and high levels of aerobic fitness during childhood may enhance neurocognition.7 This provides further evidence that motor coordination may predict executive functions. Evidence for the relationship between motor performance and executive functions also exists from behavioural studies. Normative studies1 as well as those examining developmental coordination disorder (DCD)8 have demonstrated a link between motor coordination and working memory. Baddeley’s9 model of working memory comprises separable components for the temporary storage of verbal (i.e. the phonological loop) and visuospatial (i.e. visuospatial sketchpad) information, and research in the area of DCD has found that motor coordination may be more closely linked to visuospatial working memory than to verbal working memory.8 This may be partly understood in terms of the visuospatial processing deficit found in individuals with DCD.10

ª The Authors. Developmental Medicine & Child Neurology ª 2012 Mac Keith Press

DOI: 10.1111/j.1469-8749.2012.04403.x 1025

Regarding other executive function domains, studies have found that children with coordination difficulties are slower in performing inhibition and attention shifting tasks but are not less accurate than typically developing children.6 It is possible that this reflects an automatization deficit in children with motor impairments, suggesting that cerebellar mechanisms may be implicated in the slower performances on these tasks. The available literature on the relationship between motor functioning and executive functions leaves a number of issues needing to be addressed. First, it is important to control for attention and ⁄ or hyperactivity–impulsivity (attention-deficit– hyperactivity disorder [ADHD]) symptomatology as ADHD has been linked with motor problems11 as well as executive function areas such as working memory and inhibition.12 Very few studies have employed normative samples of children. Normative studies are important given methodological problems associated with clinical samples such as overestimating associations between domains.1 In addition, as there is evidence from normative samples1 and studies examining motor impairment6 that specific components of motor coordination have a relationship with certain aspects of executive function, whereas others do not, it is important to examine these components separately. Furthermore, research is needed in adolescent samples given that previous studies have involved younger children or a mixed sample of children and adolescents.13,14 The current study examined the relationship between motor coordination (namely overall motor performance, manual dexterity, aiming and catching, and balance) and executive functions (namely working memory, response inhibition, and switching) in an adolescent normative sample, whilst controlling for ADHD symptomatology, age, gender, socioeconomic status (SES), and verbal ability. It is hypothesized that motor coordination will show a significant relationship with working memory, and this may be stronger for visuospatial working memory than for verbal working memory.8 It is also hypothesized that a significant relationship will be found between motor coordination and the timing measures from the response inhibition and switching tasks, but not with motor coordination and the accuracy variable.

METHOD Participants Recruitment occurred across five randomly selected secondary schools and through public advertisements (e.g. community newspapers). Adolescents aged 12 to 16 years were eligible for inclusion and had a minimum Verbal Comprehension Index (VCI) of 80 as measured by the Wechsler Intelligence Scale for Children-IV (WISC-IV), in order to exclude any adolescent whose difficulties might be attributed to general delayed development.15 Furthermore, a parent-rated developmental history questionnaire was used to ascertain the absence of physical disability, chronic illness, pervasive developmental disorder, and neurological disorder. Ninety-four participants responded and consented to the project; however, one participant with undiagnosed hand tremor was excluded. The final sample included 93 adolescents (38 females and 55 males) with 1026 Developmental Medicine & Child Neurology 2012, 54: 1025–1031

What this paper adds • The results show that motor coordination may be more closely linked to visuospatial working memory than to verbal working memory. • `Aiming and catching' skills may be linked to both verbal and visuospatial working memory. • Motor coordination is related to performance speed on inhibition tasks. • Balancing skills are related to interference control.

a mean age of 14 years 2 months (SD 1y 1mo). The Australian Prestige Scale16 was used to provide SES scores. The scale assesses the prestige of occupations, with scores ranging from 1 (reflecting high prestige) to 6.9 (reflecting low prestige). For the current study, the occupation rated as most prestigious out of mother’s and father’s occupation was used as the SES score (mean 3.8, SD 1.0, range 1.8–6.6).

Measures Movement Assessment Battery for Children-2 (MABC-2) The MABC-2 is a standardized test used for the identification and description of children with movement difficulties.17 Age-based standard scores for manual dexterity, aiming and catching, and balance components and a total test score are provided (mean 10, SD 3), with higher scores demonstrating better performance. A total test score at or below the 5th centile indicates significant movement difficulty, whereas a score between the 5th and 15th centile indicates that a child is ‘at risk’. Henderson et al.17 provide evidence suggesting favourable psychometric properties for the MABC-2. A reliability coefficient of 0.80 for the total test score and coefficients ranging from 0.73 to 0.84 for the individual component scores are reported.17 Wechsler Intelligence Scale for Children-IV – Australian The WISC-IV is a measure of cognitive ability for children aged 6 years to 16 years 11 months.18 The 10 core subtests yield a full-scale IQ and four indices of verbal comprehension (i.e. VCI), perceptual reasoning, working memory (i.e. WMI), and processing speed. For the current study, the VCI was used as a potential control variable and to exclude any adolescent whose difficulties might be attributed to general delayed development. The WMI was employed as measure of verbal working memory. The WISC-IV is widely used and has excellent internal consistency, test–retest reliability, criterion validity, and construct validity.18 N-back task The N-back task was used to assess visuospatial working memory, designed after Gevins and Cutillo19 and Jansma et al.20 The task has also been adapted to make it more attractive and appropriate for children.21 An apple with four holes from which a caterpillar appears is presented on the computer screen. Respondents are required to press one of the four buttons that corresponds spatially with the hole from which the caterpillar emerged. There are four conditions of graded difficulty requiring the respondent to indicate where the caterpillar was one move back, two moves back, three moves back, or four moves back. Each condition comprises a practice block

(10 trials) and an experimental block in which performance is measured (32 trials). Respondents move to the next level of difficulty only if they score a minimum of eight correct responses (indicating performance above chance levels) in the experimental blocks. For this study, task performance is measured by the total number of correct responses across the conditions (maximum raw score of 128). The N-back task is a widely used measure of working memory, and in a study involving a sample of adolescents test–retest reliabilities of 0.70 and 0.66 were reported for 3- and 4-back, respectively.21

followed. Approval was also granted from the participating schools’ representative bodies and, subsequently, from interested school principals in Perth, Western Australia. Adolescents and their parents provided written consent and were then individually tested by a trained examiner at home or at the university, depending on family preference. Testing duration was 4.5 hours over two sessions. Measures were administered in a standard manner. Parents completed questionnaires including a developmental history questionnaire and the SWAN scale.

NEPSY-II: a developmental neuropsychological assessment The NEPSY-II provides a comprehensive neuropsychological assessment for children and adolescents aged 3 to 16 years.22 The ‘naming’, ‘inhibition’, and ‘switching’ sections of the inhibition subtest were administered for the purposes of this study. These sections assess, respectively, simple naming skills, the ability to inhibit automatic responses in favour of novel responses, and the ability to switch between response types. The age-standardized total completion time scaled score for the inhibition and switching sections were utilized for this study, with higher scores representing faster completion times. A total errors scaled score was also used, which combines errors across all sections in the inhibition subtest (namely naming, inhibition and switching sections). A higher total errors scaled score corresponds to better performance (i.e. fewer errors made). The inhibition subtest has shown adequate to high internal consistency, for example average reliability coefficients for the inhibition and switching combined scaled scores range from 0.73 to 0.87 for ages 12 to 16 years.22 The NEPSY-II also demonstrates adequate stability across time, as well as good content, construct, and criterion-related validity.22

Statistical analysis A series of hierarchical regressions were conducted to determine whether the MABC-2 total score or its component scores (manual dexterity, aiming and catching, and balance) accounted for incremental variance in working memory (N-back accuracy, WISC-IV WMI), inhibition (NEPSY-II inhibition total completion time scaled score), switching (NEPSY-II switching total completion time scaled score), and the NEPSY-II total errors scaled score, after controlling for covariates (WISC-IV VCI, SWAN attention and hyperactivity ⁄ impulsivity symptoms). In a hierarchical regression analysis, DR2 represents the increase in the proportion of variance in the criterion variable explained from step N)1 to step N. The term sr2 represents the unique amount of variance that a predictor brings to the model. In a hierarchical regression analysis where just one predictor is added at step N, then the DR2 from step N)1 to step N will be equivalent to the sr2 for the added predictor. The most complex regression model included three control variables and three primary predictors. Our sample size of 93 was sufficient to detect moderate relationships (i.e. f2=0.12) between the criterion variables and the primary predictors.26

Strengths and Weaknesses of ADHD Symptoms and Normal Behaviour (SWAN) The parent-rated SWAN scale includes 18 items based on ADHD symptoms listed in DSM-IV.23 Parents are asked to rate the items based on observations from the last month and with reference to age-matched peers. Scores for each item range from +3 (i.e. ‘far below average’) to )3 (i.e. ‘far above average’). For the current study, attention and hyperactivity ⁄ impulsivity scores were calculated by averaging the total of the nine corresponding items, with positive scores indicating presence of symptoms and negative scores indicating absence of symptoms. The SWAN scale has been found to yield a normal distribution of scores, making it useful for examining variability in (hyper)activity and (in)attention in the general population.24 Martin et al.25 found the prevalence rate of ADHD, as assessed using the SWAN scale, to be similar to what has been reported in previous studies. Procedure The Curtin University Human Research Ethics Committee granted approval for the project and National Health and Medical Research Council of Australia ethical guidelines were

RESULTS Descriptives Table I shows the means, standard deviations, and ranges for the study variables. Five adolescents scored at or below the 5th centile on the MABC-2 total score, indicating significant movement difficulty. The prevalence of significant movement difficulty was 5.4%, which is similar to previous estimates of 6%.27 Two adolescents scored between the 6th and 15th centiles, suggesting that they were ‘at risk’ of movement difficulty. Bivariate correlations The correlations between the criterion variables, predictors, and control variables are shown in Table II. Multiple linear regression analyses As expected, there were strong correlations between the MABC-2 total score and each of its component scores (see Table II). Because the MABC-2 total score was a reliable predictor of the component scores, it was included as a proxy for the component scores in the primary analysis, thereby reducing the complexity of the regression model and optimizing statistical power. Because there was no correlation between the Motor Coordination and Executive Functions Daniela Rigoli et al. 1027

Table I: Means, SDs, and range of scores for the study variables

MABC-2 total scorea MABC-2 manual dexteritya MABC-2 aiming and catchinga MABC-2 balancea WISC-IV Working Memory Indexa N-back accuracyb,c NEPSY-II inhibition completion timea NEPSY-II switching completion timea NEPSY-II total errorsa SWAN attentionb,d SWAN hyperactivity ⁄ impulsivityb,d WISC-IV Verbal Comprehension Indexa SESb,e

Mean

SD

Range

10.63 9.57 11.03 11.42 103.75 88.17 10.68 10.64 8.88 )0.83 )1.17 106.63

2.56 2.47 2.73 2.98 12.47 19.69 2.9 2.42 3.19 1.17 1.03 11.25

3.0–16.0 3.0–15.0 4.0–16.0 4.0–14.0 59.0–141.0 6.0–124.0 4.0–19.0 3.0–16.0 1.0–16.0 )3.0 to 2.33 )3.0 to 1.11 81.0–132.0

3.77

1.00

1.80–6.60

a

Age-standardized score. bRaw score. cTotal number of correct responses. dScores are calculated by averaging the total of the nine attention or hyperactivity ⁄ impulsivity items. eThe occupation rated as most prestigious out of mother’s and father’s occupations. MABC-2, Movement Assessment Battery for Children-2; WISC-IV, Wechsler Intelligence Scale for Children-IV; SWAN, Strengths and Weaknesses of ADHD Symptoms and Normal Behaviour; SES, socioeconomic status.

MABC-2 aiming and catching and manual dexterity components (r=0.071), individuals with the same total score can be fundamentally different at the component level. It was important to conduct secondary regression analyses that replaced MABC-2 total score with its component scores. Only those outcomes that were significantly associated with the MABC-2 score total, or at least one component score, were analysed. The VCI was entered first, followed by SWAN attention and hyperactivity ⁄ impulsivity (Table II indicates that these were the only covariates), and then the MABC-2 total score or its component scores.

Working memory After controlling for the three covariates, the MABC-2 total score explained a significant 4.2% of the variance in N-back accuracy (DR2=0.042; p=0.041). When the MABC-2 total score was replaced by its component scores, however, the combined scores explained no additional variance over and above that already explained by the covariates (DR2=0.069; p=0.077), although aiming and catching uniquely explained a significant 5.8% of the variance in N-back accuracy (sr2=0.058; p=0.016). After controlling for the three covariates, the MABC-2 total score explained no additional variance (DR2=0.011; p=0.272) in WISC-IV WMI performance. Similarly, when the MABC-2 total score was replaced by its component scores, the combined scores explained no additional variance over and above that already explained by the covariates (DR2=0.050; p=0.123), although aiming and catching uniquely explained a significant 4.8% of the variance in WMI performance (sr2=0.048; p=0.019), and VCI uniquely explained 12.2% of the variance (sr2=0.122; p