Review article
Differential activation of brain areas in children with developmental coordination disorder during tasks of manual dexterity: An ALE meta-analysis

https://doi.org/10.1016/j.neubiorev.2018.01.002Get rights and content

Highlights

  • Compromised manual dexterity is a hallmark of the DCD symptom profile.

  • This is the first ALE analysis to detect reliable neural correlates of this symptom.

  • Data suggest differential recruitment of motor systems for manual function in DCD.

  • Interestingly, results may also implicate atypical activation of executive systems.

Abstract

Recent neuroimaging studies have reported atypical neural activation in children with Developmental Coordination Disorder (DCD) during tasks assessing manual dexterity. However, small sample sizes and subtle differences in task parameters have led to inconsistent findings, rendering interpretation difficult. The aim of the present meta-analysis was to quantitatively summarize this body of evidence using activation likelihood estimation (ALE) analysis to identify reliable regions of differential neural activation in children with DCD, compared to age-matched controls. Seven studies that adopted fMRI to compare children with and without DCD during manual performance were identified following a literature search. All were included in the ALE analysis. Compared to controls, children with DCD showed reduced activation during a manual dexterity task in the middle frontal gyrus, superior frontal gyrus, cerebellum, supramarginal gyrus, and inferior parietal lobule. Children with DCD showed greater activation in parts of the thalamus. Findings provide much needed clarification into the possible neural contributors to atypical manual dexterity in DCD and highlight the need for neuroimaging studies to include manual performance outcomes.

Introduction

Developmental coordination disorder (DCD) is a neurodevelopmental condition characterized by significantly reduced motor competence in the absence of neurological or intellectual deficit (Geuze et al., 2001). DCD affects around 6% of school-aged children (Blank et al., 2012), significantly impacting their capacity to undertake fundamental, motor-related day-to-day activities (Blank et al., 2012; Miller et al., 2001; Missiuna et al., 2007; Summers et al., 2008). It is now well-documented that the impact of DCD extends beyond the motor domain, with those affected presenting with an increased risk of cognitive executive dysfunction (Leonard et al., 2015; Wilson et al., 2013; Leonard and Hill, 2015; Alloway et al., 2009; Piek et al., 2007), and developing disordered affective (Kristensen and Torgersen, 2008), interpersonal (Campbell et al., 2012), and academic functioning (Cantell et al., 2003; Dewey et al., 2002). The physical health of individuals with DCD also appears to be compromised, with increased incidence of obesity, cardio respiratory and vascular disease and arterial stiffness reported (Cairney et al., 2017). These issues may reflect a reluctance to participate in active play, organized sport and physical activities as a consequence of poor coordination (Cairney and Veldhuizen, 2013; Joshi et al., 2015).

Although DCD is not attributable to a known neurological condition, there has long been acknowledgement that the neuropsychological profile of individuals with DCD is consistent with atypical neurological function (for recent reviews see Gomez and Sirigu, 2015; Biotteau et al., 2016; Reynolds et al., 2015a; Brown-Lum and Zwicker, 2015; Wilson et al., 2017). Elucidating the neural substrate of common symptoms of DCD is fundamental to developing a unified account of poor motor development, and its eventual remediation. Indeed, poor manual dexterity is one of the more common and debilitating features of DCD, significantly impacting fundamental academic (e.g., handwriting) and daily (e.g., dressing and self-care with utensils) functions (Miller et al., 2001; Cantell et al., 2003; Dewey et al., 2002). Accordingly, a number of imaging studies have investigated neural activity during complex manual movement in DCD using finger tapping and tracing tasks [see Peters et al. (2013) for a recent review]. Consistent with earlier neuropsychological accounts, these studies collectively provide broad support for differential activation in DCD (both loci and magnitude) during manual performance, particularly with respect to fronto-parietal (Kashiwagi et al., 2009; Zwicker et al., 2010; Zwicker et al., 2011) and fronto-cerebellar motor circuitry (Zwicker et al., 2010; Biotteau et al., 2017; Debrabant et al., 2013). However, activation patterns across studies remain inconsistent (Peters et al., 2013). While this variation possibly reflects the heterogeneity of the disorder, it is also likely to be the consequence of a combination of small sample sizes across studies (i.e., the average sample size for DCD groups is around 10 participants) and subtle differences in the experimental paradigms used. Hence, it is difficult to discern the core neural correlates of poor manual control in DCD from what might be task specific anomalies. A quantitative summary of neural activation during complex manual dexterity in DCD is required to minimize the influence of study specific ‘noise’ and bring those primary regions of influence to the fore. The recent meta-analytic technique ‘activation likelihood estimation’ [ALE, Eickhoff et al., 2009; Eickhoff et al., 2012; Turkeltaub et al., 2012] provides the ideal means with which to achieve this.

During functional magnetic resonance imaging (fMRI), neural locations of peak activation elicited by performance of functional tasks are typically recorded in stereotaxic coordinates. ALE meta-analysis takes these activation coordinates from multiple studies to identify voxelwise regions of spatial convergence across studies (Eickhoff et al., 2009; Hardwick et al., 2013). The final product is a whole brain map that provides the means for determining how likely a neural locus is to be involved in a symptom based on multiple studies, partialing out trivial effects due to variations in experimental tasks (Eickhoff et al., 2012; Dickstein et al., 2013; Houdé et al., 2010). In other words, ALE provides a powerful method for aggregating data from small sampled imaging studies that use similar yet distinct experimental tasks (such as those requiring manual dexterity in DCD) to quantitatively identify common regions of de/activation. ALE analysis will therefore provide much needed clarification of the core neural correlates of compromised manual dexterity in DCD. Accordingly, the aim of the present study was to conduct an ALE meta-analysis to detect reliable differences in activation patterns between individuals with and without DCD during tasks of manual dexterity.

Section snippets

Study selection

Articles were obtained from an online search of the PubMed and ISI Web of Science databases on 8 March 2017. Based on recent narrative meta-analyses of fMRI studies of DCD (Peters et al., 2013), the search string included a combination of the words ‘developmental coordination disorder’ and ‘imaging’, or equivalents (see Table 1). Further, reference sections of the reviewed articles were inspected to identify additional articles of interest. Studies were included in the analysis if they met the

Areas of reduced activation in children with DCD

Children with DCD showed reduced activation across cortical association areas and the cerebellum. Specifically, brain regions showing reduced activation in children with DCD were observed in the posterior part of the left cerebellum (lobule VI / Crus 1), the left inferior parietal lobe (IPL, BA 40), the right supramarginal gyrus (SMG, BA 40), the left superior frontal gyrus (SFG, BA9) and the right middle frontal gyrus (MFG, BA 9). Talairach coordinates of the differential activation maxima are

Discussion

A series of recent fMRI studies have reported differential neural activation between individuals with and without DCD during tasks of manual dexterity. However, small sample sizes and subtle differences in task parameters across studies have led to inconsistent findings, rendering interpretation difficult. By combining neural locations of peak activation from 86 school-aged children with DCD and 84 controls performing tasks of manual dexterity, the present ALE meta-analysis has been the first

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      Moreover, visuo-motor integration dysfunction has been reported in children with DCD (Ruddock et al., 2016) and it is hypothesized that the motor deficits observed in DCD could be attributable to an internal model deficit (Wilson et al., 2013). Certain neural pathways are associated with the internal model and a recent meta-analysis of DCD research by Fuelscher et al. (2018) concluded that children with DCD (mainly aged 9–10 years) showed reduced magnitude of activation in five regions of the brain and increased activation in the thalamus compared to controls during tasks of manual dexterity, seemingly lending support to this hypothesis. Poor manual dexterity can result in problems with ADL including dressing, writing and utensil use and impact negatively on everyday life, so follow up and possible intervention for children with moderate motor coordination difficulty will be important to avoid these negative consequences.

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