1.1

Introduction

Developmental dyspraxia is a developmental disorder covering a heterogeneous group of motor skills and coordination disorders associated or not to perceptual-motor difficulties, in children with no neurological or psychiatric pathologies. Its prevalence is estimated at 5 to 6% according to the WHO . These disorders lead to difficulties in completing daily life tasks and impact the child’s ability to learn in school. Furthermore, disorders linger into adolescence and adulthood . Developmental dyspraxia is very often associated with other developmental disorders , such as Attention Deficit Disorder with or without Hyperactivity (ADD/ADHD) and specific speech disorders .

The international terminology, stemming from the DSM-IV , uses the term Developmental Coordination Disorder (DCD). Today, there is a real wish to harmonize the terms for this disorder . However, in clinical practice, there is often a difference between the two concepts that remain distinct from one another , developmental dyspraxia was most often presented as a subgroup of DCD . In this study, we chose to refer to the concept of developmental dyspraxia proposed by Gérard promoting a neuropsychological approach of the disorder.

Executive Functions (EF) are control functions used to implement or execute a task in order to face new situations; these functions are involved in all types of cognitive activities. Pediatric neuropsychological research has only recently focused on the development of executive functioning in children . However, we know that in humans the prefrontal cortex is one of the last regions of the brain to reach maturation. Anderson proposed a model of executive function including four distinct but inter-related domains: attentional control (ability to select specific stimuli, inhibit automatic responses and focus attention), information processing (efficiency and speed of information processing), cognitive flexibility (ability to change strategy, divide attention and process multiple sources of information) and finally goal setting (ability to plan, use a strategy, and develop new initiatives or concepts). Barkley proposed a model based on observations in children with ADD/H, focused on inhibition impairment. It is now well known that executive functions are essential in the cognitive development of children and are involved in learning acquisitions. Assessment of EF in children is difficult and mainly based on tests used in adults . Furthermore, EF are only evaluated through instrumental functions and finally only partially assessed by so-called “paper-and-pencil” tests (i.e. in an office, with a clearly determined objective, linear course, short duration and very structured context), which do not always reflect the difficulties experienced in daily life situations . Dissociations have been described between performances in the neuropsychological tests (which can be normal or normalized) and abilities observed in daily life. Paper-and-pencil EF assessment should therefore ideally be completed by ecological tests, i.e. requiring more self-management and open to more conflicting stimuli and situations in order to complete the interpretation derived from standard tests .

Three types of ecological assessments have been developed and studied mainly in acquired brain injury, epilepsy or ADD/H: paper-and-pencil tasks simulating situations close to daily life tasks; questionnaires evaluating executive functioning in common daily situations (home or school), and finally implementing real-life situations. Recently, Chevignard et al. proposed an assessment in a real-life open-ended setting, i.e. the Children’s Cooking Task (CCT).

In the French literature, at the time of this study and to the best of our knowledge, we did not find studies assessing executive functioning in children with developmental dyspraxia. However, the issue of EF impairment in development dyspraxia has been raised by several authors and is routinely seen in clinical practice. In the international literature, studies evaluating executive functions in DCD children are stemming from research on children with ADD/H. Some authors have brought up the hypothesis of a common neurocognitive mechanism such as executive dysfunctions ; others underlined the possibility of a relationship between motor performance, attention and executive functions . But these studies are very rare in DCD and most often only focused on one domain of executive functioning.

The aims of this study were:

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  to conduct an in-depth, specific and standardized assessment of executive functions in children with developmental dyspraxia;

  
  
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  to combine previously validated paper-and-pencil tests with more ecological evaluations;

  
  
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  to compare the respective sensitivity of the various tests used, and specially the CCT in this population.

Our hypotheses, based on our clinical experience and data from the literature, were the following:

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  the CCT would be feasible in this population of patients with impaired motor skills;

  
  
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  some children with developmental dyspraxia are likely to have executive dysfunctions, which can be observed in various examination modalities and should be taken into account in rehabilitation;

  
  
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  the ecological tests would be more sensitive to a dysexecutive syndrome than the neuropsychological paper-and-pencil tests.

1.2

Methods

1.3

Results

1.4

Discussion

The main objective of this study was to evaluate EF in children with developmental dyspraxia in a systematic manner using classical neuropsychological and ecological tests. Overall, the assessments suggest that some of these patients exhibit EF disorders in various domains. Common neuropsychological tests highlighted a deficit for the non-verbal planning ability on the NEPSY tower test and BADS-C 6-part test, with a very low strategy score. Results of the dysexecutive questionnaires were similar, for the BRIEF, the subscales working memory, plan/organize and monitor (ability to check the work and evaluate performances) were the most disrupted. Slow information processing was also highlighted (TMT and paired-images test), related in part to these children’s visual spatial disorders. There did not seem to be flexibility disorders. Regarding inhibition deficits, almost half the children exhibited a pathological impulsivity index at the paired-images test. These results could in part be explained by the associated ADD/H condition present in half of the group, indicating an inability to inhibit inappropriate responses . However, based on the results from the auditory attention test and BRIEF’s inhibit subscale, the ability to inhibit an automatic response was retained. Prospective memory (RBMT subtests) was impaired. Furthermore, BRIEF’s cognitive working memory subscale was among the most disrupted elements. The observed results matched some of the data from the literature, mainly regarding children diagnosed with Developmental Coordination Disorders (DCD) and, as previously described in the introduction, these diagnoses do not always overlap.

Planning disorders are rarely described in the international literature, where DCD is considered as motor control impairment. In fact, for some authors this motor control impairment would stem from the cerebellum. In the literature on developmental dyspraxia, gesture disorders are also considered as motor control impairments but some authors bring up the issue of executive dysfunctions. Leroy-Malherbe reported that impaired gesture organization could be caused by frontal lobe injury. Gerard and Dugas brought up difficulties in executive control of action, thus disrupting practognostic pathways, sometimes associated to attention disorders with or without hyperactivity in the subtype 3 of their classification. Recently, Feige et al. explored the role of executive and attention disorders in praxis disorders and thus dyspraxia, asking if they could be associated disorders, or a common underlying neurocognitive mechanism? They proposed the term of “executive dyspraxia” to underline the integration of gesture and construction disorders within a larger executive system. Our results suggest an overall planning dysfunction, beyond gesture planning.

Slow information processing has been well described in this population , as well as perception and attention visual spatial disorders . Mandich reported a selective visual spatial deficit at the level of endogenous attention related to impaired inhibition. However, this impaired inhibition has not been validated by Pieck et al. , who suggested that slow information processing was related to impaired working memory, especially the visual spatial sketchpad.

Alloway also studied the components of the short-term and working memory in children with DCD and showed that visual spatial abilities were impaired, related to movement planning and control. We did not use specific tests to assess working memory and its different components , however the results from the BRIEF suggested that the working memory subscale was the most disrupted. To our knowledge, no other studies used this questionnaire in children with DD or DCD.

Regarding the CCT, it proved to be feasible in children with developmental dyspraxia, in spite of their gesture disorders. Moreover, children enjoyed this task. Results showed that children with dyspraxia made significantly more errors than children in the control group; all types of errors discriminated patients from controls, as well as the qualitative analysis.

There was quite a very high number of ‘commentary-questions’, indicating the need for patients to verbalize their actions. This need to verbalize could be due to praxis disorders (children speak in order to compensate their difficulties in completing the gestures) or their planning and/or working memory difficulties. Nevertheless, children were not able to inhibit this behavior to adapt to the task’s guidelines (the latter clearly stated that children should act as if they were alone and not speak to the examiner).

More precisely, within the ‘commentary-questions’, the number of ‘dependency’ was also significantly higher in children with dyspraxia, suggesting a limited search for strategies/solutions to face a problem without an immediate solution, as described in adults and children with brain injury . Furthermore, similar to children with brain injury , the most common error noted in the neuropsychological analysis was ‘context neglect’. Children with dyspraxia have a hard time integrating environmental parameters in order to adapt their behavior.

For the qualitative analysis of the cooking task, the patient group required adult help; this dependence was significantly lower in controls. Two patients did not spontaneously start the cocktail, which brings up potential prospective memory disorders, even if only one of them failed one of the RBMT subtests. One patient finished the cocktail but not the cake, which brings up the suspicion of “goal neglect”, described in the dysexecutive syndrome . Finally, three children exhibited a dangerous behavior, which did not happen with the controls, highlighting patients’ poor environmental and instructions management .

In summary, the cooking task is feasible in children with developmental dyspraxia. It seems sensitive enough to detect a dysexecutive syndrome, even mild, similar to children with acquired brain injury . Of course, it remains a global task, not allowing the in-depth analysis of impaired cognitive mechanisms, but it could be a good complementary assessment to analyze a child’s ability to follow guidelines while abiding by certain rules in a more open environment.

Our objective was also to compare the sensitivity of the various types of tests used to assess executive functions in children with developmental dyspraxia.

EF assessment in children is a well-debated issue and studies are ongoing in France to validate a test battery for children. In our study, the neuropsychological tests sometimes lacked sensitivity as previously described . It seems thus essential to include more ecological tests that are more sensitive and more similar to daily life tasks. Input from questionnaires was interesting and has proven essential in the evaluation process to explore several domains of daily life related to executive functions and they seem more sensitive than the paper-pencil tests. Nevertheless, similar to the pilot study in children with traumatic brain injury, a certain number of families did not complete, or incorrectly completed the questionnaires, rendering the data useless and underlining the limits of these assessments.

One of the limits of our study was the small sample size, which does not allow to extrapolate the results to the population of children with developmental dyspraxia. The sample was also biased, since the patients are usually sent to this department when diagnosis is particularly difficult to establish, and children often have co-morbidities. The concept of developmental dyspraxia probably comprises of heterogeneous clinical entities.

Another limit is the choice of neuropsychological tests. A more in-depth assessment of working memory, especially its visual spatial component, would have been interesting. But we did not want to lengthen the duration of the assessment for these children. Finally, we did not report on the anatomical-functional mechanisms of dyspraxia since it was not the objective of this work. We suggest looking at the integrative model reported by Lussier and Flessas , which is a synthesis of all developmental dyspraxia models, proposed by various authors.

1.5

Conclusion

This study is relevant on two levels. First, we showed that some children with developmental dyspraxia also have a dysexecutive syndrome. In fact, we observed EF disorders both in common neuropsychological tests, in dysexecutive questionnaires and the ecological cooking task. To our knowledge, and even if several authors have already brought up this issue, very few studies have comprehensively explored executive functions in these patients. These first results need to be completed with further studies in order to better understand the disorders of children with developmental dyspraxia. We should however take into account the presence of executive function disorders and systematically screen for them during neuropsychological assessments. Indeed, when EF disorders are identified, children should benefit from specific care using rehabilitation methods not only centered on gesture control, but also on executive functions.

Secondly, assessment of executive functions in children is very important, and should be performed using neuropsychological tests, but also more ecological tests, allowing to better characterize the consequences of the dysexecutive syndrome on a child’s activities of daily living. This study also highlighted the relevance of the CCT, a multitask assessment performed in a real-life setting, in interpreting the children’s difficulties in carrying out complex tasks.

Disclosure of interest

The authors declare that they have no conflicts of interest concerning this article.

Acknowledgements

We would like to thank the patients and their family for their participation. Also many thanks to the rehabilitation team in the congenital neurological pathologies department in the Saint Maurice Hospitals, especially occupational therapists and neuropsychologists for sharing their clinical experience. Many thanks to the occupational therapists in the rehabilitation department for children with acquired brain injury.