Systematic Review on Executive Functions in Children with Poor Motor Skills and With Development Coordination Disorder Volume 2 - Issue 3

RF Sartori¹*, N. CValentini², GC Nobre³ and RP Fonseca⁴

• ¹Department of Physical Education at the Pontifical Catholic University of Rio Grande do Sul and Serra Gaucha University, Brazil
• ²Department of Physical Education, School of Physical Education, Physiotherapy and Dance, Federal University of Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil
• ³Department of physical Education, Federal Institute of Education, Science and Technology of Ceará, Fortaleza, Brazil
• ⁴Pontifical Catholic University of Rio Grande do Sul Rio Grande do Sul, Brazil

Received: July 23, 2019   Published: August 09, 2019

Corresponding author: RF Sartori, Department of Physical Education at the Pontifical Catholic University of Rio Grande do Sul, Brazil

DOI: 10.32474/PAPN.2019.02.000138

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Abstract

Objective: The aim of this study was to describe the tests used to assess working memory, inhibition, and cognitive flexibility, and analyzed the main research results related to executive functions in children with Developmental Coordination Disorder or with poor motor skills. Methods: This review used as data sources studies in MEDLINE, Web of Science, APA PsycNET, EMBASE, and Google Scholar with children with poor motor skills, DCD, and typical development. Quality of the studies was conducted using the Newcastle Ottawa Scale. Results: 1475 papers found, 31 matched the review criteria; 31 different executive function tests used to assess children with poor motor skills and DCD. Across the 31 studies, included in this systematic review, eleven studies examined only the working memory; ten studies measured only inhibition, a single study measured only cognitive flexibility, three studies examined the working memory and inhibition, one study examined inhibition and cognitive flexibility, one study examined working memory and cognitive flexibility and four studies examined the three executive functions. In conclusion, many tests were used to assess children with poor motor skill and DCD requiring verbal, nonverbal, or complex visuospatial processing, with or without motor demand involved. In some tests the different demands or different types of stimulus involved cause secondary loss in execution. The executive functions deficits in children with poor motor skills and DCD are in a wide ranging and extend across basic all functions assessed (working memory, inhibition, and cognitive flexibility). The pervasive and persistent nature of the executive function deficits suggests a need for a more aligned methodological approach to investigate this phenomenon.

Keywords: Working Memory; Inhibition; Cognitive Flexibility; Dcd and Poor Motor Skill

Introduction

The Developmental Coordination Disorder (DCD) can present itself in an isolated manner, with the child showing difficulties in executing motor skills [1], or associated with academic contents [2], and movement planning (Brown-Lum & Zwicker, 2015; Zwicker et al., 2012)difficulties. Social and emotional [3], and cognitive development [4] are also affected. The close relation between motor and cognitive development is explained by cerebral areas activation, when motor control areas show neural activation during the execution of an movement certain cognitive areas are also coactivated (Diamond, 2000). Moreover, there is evidence of a specific relation between motor delays and deficits in executive functions [5].Executive functions are cognitive processes that allow the individual to direct behaviors to goals, evaluate the efficiency and adequacy of these behaviors, abandon inefficient strategies in favor of others that are more efficient, and solve immediate and long term problems [6]. Executive functions, therefore, regulate human behavior [7] by find the solution of problems, selective inhibit a behavior, control and change an action, and remember components necessary to act [8]. The executive functions are studied in three main components, the working memory (i.d. storing and updating information while the individual does some activity related to it), inhibitory control (i.d. inhibition of automatized response when the individual is engaged in the execution of a task), and cognitive flexibility (i.d. changing the focus of attention and cognition between dimensions related to a given task) [9].

Several times the use of tests or tasks that are highly complex cover more than one component of the executive functions depend on other cognitive abilities to be performed successfully (Leonard & Hill, 2015; Wilson et al., 2012). Depending on the complexity of test various executive functions are measured since the tests lack purity [10]. Besides, many measurements of executive functions demand motor responses or complex visuospatial processing that may affecting the performance of children with DCD or with motor difficulties due to the poor motor skills and not necessarily to limited executive functions. The characteristics of the tests to assess executive functions and the results of assessments need to be further investigated in order to better understand the subjacent mechanisms affecting executive function in children with DCD or with motor difficulties. The aim of this study was to describe the tests used to assess working memory, inhibition, and cognitive flexibility, and analyzed the main research results related to executive functions in children with DCD or with poor motor skills.

Methods

This systematic review (registered at the international prospective register of systematic reviews PROSPERO network - http://www.crd.york.ac.uk/prospero/: Registration CRD42016047299) was conducted using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) (Moher, Liberati, Tetzlaff, & Altman, 2009).All the original studies investigating executive function in children and adolescents with DCD or poor motor skills were eligible. We used the acronyms PECOT (Population, Exposure, Comparing, Outcome and Type of study) in accordance with the PRISMA protocol as an auxiliary method for the inclusion of studies. Therefore, we included studies with: (P) Population of children and adolescents, from 5 to 16 years old, with probable DCD [11], with DCD, or poor motor skills; (E) Exposure of instruments of clinical evaluation that assess working memory, inhibition or cognitive flexibility [12]; (O) Outcome that measure executive functions capacity;(T) Type of study included observational, intervention, and peer reviewed studies.

The MEDLINE (accessed by PubMed), Web of Science, APA PsycNET, EMBASE and Google Scholar databases were search, until December of the 2018. We used specific descriptors, Boolean operators (AND & OR), and specific keywords for working memory (“working memory”[All Fields] OR “visuospatial working memory”[All Fields] OR “verbal working memory”[All Fields]), inhibition(“Inhibitory control”[All Fields] OR “inhibitory function”[All Fields] OR “Response inhibition”[All Fields] OR “Inhibitory controls”[All Fields] OR “inhibition”[All Fields]), and cognitive flexibility(“cognitive flexibility”[All Fields] OR “Flexible cognition”[All Fields] OR “Shifting”[All Fields] OR “Set-shifting”[All Fields] OR “mental flexibility”[All Fields]). Executive functions were associated with keywords regarding the motor skills difficulties (“Developmental Coordination Disorder”[All Fields] OR “Motor Disorder”[All Fields] OR “DCD”[All Fields] OR “Dyspraxia”[All Fields] OR “Motor Skill Disorder” OR “poor motor skill” [All Fields]);none filters were used. We extracted categories for background (aim of the study and construct or domain of the executive function), methods (instruments or procedures for assessing the executive function, samples age,sex,number of participants with and without DCD, motor tests and cut off points used; confounding factors), and main findings and other relevant information reported by studies.

Assessment of Study Quality

The quality of the studies was assessed using the Newcastle/ Ottawa Scale (NOS: Takahashi & Hashizume, 2014);each study was evaluated using the point system. Two authors did a critical evaluation of the included studies for potential sources of bias (selection bias, detection bias, reporting bias, performance bias, attrition bias), methods of participant allocation and allocation concealment, and blind assessment. Study design was assessed regarding selection (representativeness of the sample, sample size, description of groups, ascertainment of exposure), confound comparability (based on design and analysis), and outcome (assessment of outcome and statistical test) considering recognize cut offs points, maximum score of five for cross-sectional studies (5 = very good; 4 = good; 3 = satisfactory; 0-2 = unsatisfactory) and eight for cohort studies (7-8 = very good; 5-6 = good; 4 = satisfactory; 0-3 = unsatisfactory). The two raters achieved consensus through discussion (K=0.90); the third author settled discrepant results.

Results

In the selection process, we identified 1475 papers using title and abstract screening; 31 matched review criteria. Approximately 90.3 % (n = 28 studies) were conducted within the last 10 years. In addition, 33 different tests to assess executive function were found within 31 studies. Sample sizes, including children with DCD or poor motor skills, ranged from 11 to 71 participants from England, Germany, Australia, Italy, Canada, France, Finland, Taiwan, and US. Figure 1 provided a selection process synthesis.

Inhibition Measurements in Children with DCD or Poor Motor Skills

Descriptive studies were first conducted, regarding inhibition and motor development, using the Simon Task [13].Latter on, the Go/no-Go test [14], the Stop-Signal Task and Day/Night Stroop tests (Livesey, Keen, Rouse, & White, 2006; Pratt et al., 2014), and the Verbal –Motor Inhibition tests [15] were used with the same objective. Yet, the Covert Orienting of Visuospatial Attention Task (COVAT) were used to investigate the associations spatial attention and motor difficulties [16]. The Go/no-Go test and neuroimaging was used to investigate the neural processes of inhibitory control in children with DCD [17]; and also in a experimental study investigating the impact of a neutral or positive reinforcement in inhibitory control of children with DCD [18]. And finally, Animal Stroop Task was used to compare results between children at risk for DCD and typical children [19].
Regarding intervention studies, two were conducted for children with DCD using Posner Paradigm to investigate changes in inhibition [20]; the visuospatial selective attention paradigm provides a measurement of conflict resolution that has been acknowledge as a trustworthy index of inhibitory control [21]. Two follow-up studies conducted during one-year [22]and two-years [23], assessed inhibitory control in children with and without motor difficulties using the Fruit Stroop Task test; and another studied conducted in England used the Verbal and Motor Inhibition tests to assess association of inhibition, poor motor skills and academic achievement in two-years follow‐up study [24].

Working Memory Measurements in Children with DCD or Poor Motor Skills

Regarding to descriptive studies, working memory has been investigate in children with DCD in relation to the proficiency of motor skills using the Trail Making Test [25] the N-Back task [26,27]; and the Automated Working Memory Assessment [28]. Yet, a study investigated the visuospatial working memory mechanisms using the Visuospatial Working Memory Paradigm (VSWM) and compared the brain activity (electroencephalography) of typical and atypical children [29]; and the relation between motor coordination and visuospatial working memory in children with DCD, was investigated using the Cog State One-Back [30]. To verify attention and working memory in children with poor motor skills, the Cambridge Neuropsychological Test Automated Battery was used [31]. To compare results between children at risk for DCD and TD children three verbal and three visuospatial tasks were used [32].
A study conducted in England [33] investigate several executive functions in children with poor motor skills and DCD, using the Working Memory Battery for Children [34] to assess verbal working memory and the Odd-One-Out test [35] for the nonverbal working memory. Yet, a studied conducted in Italy using the Motor Observation Questionnaire for Teachers to investigate the relation between the poor motor skills and visuospatial working memory in children with DCD [36]. Regarding to a follow-up studies, a one-year [37] and two- years [38] studies assessed visuospatial working memory using the Backwards Color Recall task and the Corsi-Blocks Backwards tests. And another follow-up study used the Working Memory Battery for Children and Odd-One-Out in children with poor motor skills and DCD children over 2 years [38].

Cognitive Flexibility Measurements in Children with DCD or Poor Motor Skills

Deficits in cognitive flexibility tasks were assessed in children with DCD using an Inspection Time Task in an Australian study [39]. The Wisconsin Card Sorting test [40] and the Wisconsin Card Sorting Test has been developed to assess reasoning and the ability of changing cognitive strategies in response to environmental changes. Regarding to follow-up studies, in a one-year study the Cognitive Flexibility Test was used [41] and in a two-years period the Flanker Task [42] were used to assess cognitive flexibility in children with DCD. Another study conducted in France used the Trail Making Test [43] to compare the development of cognitive flexibility in children with motor difficulties. And the Intra-Extra Dimensional Test Set Shift to follow-up changes in nonverbal cognitive flexibility of the children over 2-years period [44]. Table 1 provided the main results of the testes used to measure executive functions in children with poor motor skill and DCD. Table 1 describes the tests and outcomes in studies design to assess executive functions in children.

The studies used three motor batteries to assess children motor skills; the majority of the studies (n=22) studies used the Movement Assessment Battery for Children-2, five studies used a Mc- Carron Assessment of Neuromuscular Development-MAND. Some assessments (Bruininks–Oseretsky Test of MotorProficiency-2, KörperkoordinationstestFür Kinder) and interviews and questionnaires (multidisciplinary assessment of developmental dyspraxia, Motor Observation Questionnaire for Teachers, Ideomotor test questionnaire) were used with less frequency. Regarding the main results of the executive functions in children with poor motor skills or DCD compared to children with typical development the majority of the studies indicate that there is a deficit of inhibition in children with DCD, however effect size was rarely reported. Regarding, inhibition tasks 15 studies compare children with DCD with a typical development; three studies (code 13, 25, 26) found no difference between groups. One study (code 26) showed that children with DCD and with typical development had similar accuracy in Go/No-go tasks and similar errors during the task, except when the No-go stimulus was associated with conditions receiving positive reinforcement.
Regarding working memory, 15 studies compare children with DCD with children with typical development and only one study (code 14) found no difference between groups. Regarding cognitive flexibility tests, 6 studies were found comparing children with DCD or with poor motor skills with children with typical development. The results showed deficits in cognitive flexibility in children with DCD or with motor difficulty, independently of tests used, compared to control group. Table 2 presents themain results of the studies that assessed executive functions in children with poor motor skill and DCD.Insert Table 2 Using the NOS parameters, five studies implemented experimental design with very good quality; and 26 cross-sectional designs, ten with very good quality, nine with good quality, and the remaining six studies were satisfactory due to the lack of procedures adopted to control the influence of the researcher’s knowledge about the sample in relation to the measurement of the outcome. However, in general, the methods of recruitment of subjects, controlling for the confounders, and outcome assessment were appropriate for all studies.

Discussion

Executive functions play a critical role in everyday life. However, despite the obvious relevance of executive functions of children with poor motor skills and DCD, much is still unknown about individuals ‘ability. We addressed this gap in the literature by conducting a systematic review to identify tests used to measure inhibition control, cognitive flexibility and working memory. A large number of tests were designed to measure inhibition in children with typical development, with poor motor skills and with DCD. A possible explanation is the fact that inhibition presents a greater representation about the other possible components in executive functions. In other words, the satisfactory development of inhibition is essential for the typical performance of the other neuropsychological abilities, such as working memory, internalization of speech, self-regulation, reconstitution, and motor control [45].Inhibition studies with children with DCD, showed great variety of tests used, however the Go/No-Go test were used more often (3 studies) to assess a participant’s capacity for sustained attention and inhibition behavior. Yet, in studies using neuroimaging to investigate the neural processes of inhibitory control of children with DCD, the Go/No-test was used [46]. Besides that, two versions, “cool Go/No-Go test” (the stimulus were faces with neutral facial expressions) and “hot Go/No-Go tests” (the stimulus were happy or fear emotions faces) were used to investigate the effects of this motivational strategy in the inhibition outcomes of children with DCD [47].

The diversity of tests used in the researches may be due to the multiple components of the executive functions and the lack of methodological agreement in the field [48]. In terms of inhibition control and working memory some tests were used to assess both functions (i.e. the trail making/updating task used by [49] while some other researchers used separate tests for these two functions [50]. It is also important to notice that the tests also differ in the extent to which they required motor skills, with tests such as the trail making/updating task requiring button pressing responses, while the Fruit Stroop task used having no motor demands [51]. Motor demands may mask the outcomes for the executive function. It would be worth mentioning that other factors such as the lack of executive function “purity” of the tests, tests interaction with age, and other aspects of inhibition could also play an important role in the test outcome [52]. For example, results indicate that there is no relation between the Stop-Signal Task with other assessment of inhibitory control in children five-to six-years-old [53]. There is an agreement that the Stop-Signal and the Day/Night Stroop tests present aspects that are very different regarding the inhibition of behavior in children with DCD; the lack of association between both tests do not pose any doubt about the validity of the tasks as a measurement of response inhibition.

Another important condition refers to tests that involve motor demands. Many tests used to assess executive functions in children require verbal, nonverbal or complex visuospatial processing, with and without motor demands. In some tests, the different demands and types of stimulus may cause secondary loss during the execution, masking the primary executive function that should be examined (motor performance or visual perception bias) and limiting the acquisition of specific information. For example, inhibition tests was often involve press a button or other kind of motor responses, therefore in this kind of tests it is important to assess the extent to which any motor difficulties or additional processing load were associated with producing the responses effects on the inhibition performance of children with DCD [54].Consequently, researchers should ensure that they account for the tests of visuospatial and motor demands when interpreting the results of children with DCD [55]. The studies review underlined wide ranging of deficits across working memory, inhibition, and cognitive flexibility in children with poor motor skills and DCD compared to children with typical development; these deficits have been previously reported [56]. Specifically, since inhibition contributed to an efficient performance of several executive function by allow the motor execution to be fluent and efficient [57], this cognitive function is essential for tasks that suddenly prevent one’s self from executing an inappropriately prepared action such as riding a bicycle, playing dodge ball or football [58]. Deficits in this control process underline motor coordination problems [59]. For instance, additional taps in a motor inhibition test with children with DCD could reflect a deficit in motor control resulting in involuntary repetition of the taps of the same thumb [60].This assumption is in accordance with previous studies showing a global inhibition deficit in tasks that not requiring a motor response in DCD [61]. Consequently, clumsiness could partially result from executive functions deficit demonstrated by children with DCD resulting from early cerebral lesion [62].

Regarding working memory, the majority of studies found deficits for children with poor motor skills and DCD. Working memory is an temporary information storage system that allows the management of information, and is related to the retention of the information in the brain and to the possibility of using clues of this information to solve a problem [63].This retention capacity makes us capable of connecting unrelated elements as well as separating integrated elements [64] which support the fact that children with poor motor skills and DCD have worse results than children with typical development. These processes of disassembly and recombination of the elements are fundamental for creativity and decision making [66]. Children with DCD were significantly slower and had greater variability in performance of cognitive flexibility tests compared to the typical develop children. Cognitive flexibility requires the individuals to modulate their behavior and adapt to different requirements of a particular tests [67] and change the course of actions according to the environment’ requirements [68].

This capability suggests a change in perspectives or differentiated approaches to a problem, flexibility, adjusting to the demands, rules, or priorities of each task providing the basis for higherorder functions such as planning and reasoning [68]. However, cognitive flexibility appears later in the development compared to working memory and inhibition [69], which may be the reason for a smaller number of studies found and the absence of differences between the children with DCD and with typical development. For future studies, it would be important to standardize the tests and the methods in research enrolling children with poor motor skills and DCD, to enable more precise evidences. Although, practically it may be difficult to achieve since different measures of executive function are used across countries. We also argue that there may be moderators of the associations between poor motor skills and executive functions that are unaccounted in analyses. Some studies failed to report important information such as clinical status of participants, education, economic status, medication, psychiatric disorders precluding moderator analyses on these variables. However, it is worth emphasizing that the multiple characteristics and the recognized the overlap of different comorbidities of this disorder is a great challenge [70]. Yet, to further the understanding of the association between executive function and motor skills, the definitional and measurement problems of the executive function need to be solved [71]. Without a set of clearly defined terms and measurements, it will be difficult to be more assertive about how executive function relates to children poor motor skills [72].

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