Children with developmental coordination disorder are equally able to generate force but show more variability than typically developing children

Abstract

Several studies have suggested that children with developmental coordination disorder (DCD) have difficulties in the fine-tuning of manual force. However, parameterization of the generated force per se is hard to test under normal circumstances as movement planning and execution are also involved. In the present study, an isometric force production task was used to test the hypothesis that children with DCD have a decreased ability to scale force to a required force level and to maintain steady low to submaximal forces. We also tested if the developmental trends were different between the children with DCD and typically developing (TD) children. Twenty-four children with DCD and 24 matched TD children, divided over three age groups (7–9–11 years) participated in this study. Analysis of the data showed that DCD and TD children are equally able to adapt their generated force to the required levels, however DCD children produced a less steady force, even more variable than in the youngest TD children. These results suggest that problems in force control in children with DCD are caused by a higher level of inherent noise of the output system. Since younger DCD children are much more affected than older ones it is suggested that these children are able to learn a strategy to cope with their increased stochastic variability, especially at higher force levels.

Introduction

Recently, there has been growing interest in, and debate about, the importance of cognitive neuroscience in relation to developmental disorders (Fawcett & Nicolson, 2007). Developmental cognitive neuroscience may offer methods for the early identification of developmental disorders and for differential diagnoses. Furthermore, it may enable theory-based assessment and intervention for children with special needs. Several studies in the last decades identified the kind and severity of problems in neuromotor control in children with developmental coordination disorder (DCD) (Geuze, Jongmans, Schomaker, & Smits-Engelsman, 2001). Literature reviews have linked these deficits to visuo-spatial processing, kinesthetic perception, cross-modal perception, and poor sensory-motor coordination (Piek and Dyck, 2004, Wilson and McKenzie, 1998). Overall it can be stated that when children with DCD move towards an object, they make large endpoint errors, need more time and have less fluent movement profiles than their well-coordinated peers (Smits-Engelsman et al., 2001, van Galen et al., 1993). Based on many studies, we can now describe the features of the less coordinated movements in children with DCD; however the underlying causes are still not clear. Especially higher levels of motor control did get attention as an explanation for the observed deficient performance, more specifically internal models (Katschmarsky et al., 2001, Wilson et al., 2001), feed forward processing (Smits-Engelsman, Wilson, Westenberg, & Duysens, 2003) and motor planning (Schoemaker, Hijlkema, & Kalverboer, 1994). However, dexterity requires not only a capability to process sensory-motor information but also a capability to precisely grade forces.

Our general research goal is to advance the debate about underlying processes in DCD by clinically testing one step in the process of movement generation that has not received much attention and is potentially important to understand the relation between the measured behavior and the cognitive neuromotor processes, specifically the precision of force generation. Recent evidence indicates that several brain areas are involved in this type of task. For example, an fMRI study showed that precise force generation led to an increase in regional cerebral blood flow in contralateral primary and non-primary motor cortices (Bonnard, Gallea, de Graaf, & Pailhous, 2007). Moreover, differences are reported in the activation of these parts of the cortex during different levels of precision grip. It was shown that the contralateral primary sensory-motor cortex, dorsal premotor area, ventral premotor area, and bilateral supplementary motor area were more activated during a gentle (with lower force levels) than a normal precision grip (Ehrsson et al., 2000, Kuhtz-Buschbeck et al., 2001).

The ability to manipulate small objects with the tip of the thumb and fingers, requiring precise force control, is known to be often implicated in children with DCD. The high level of dexterity obtained during normal development in activities that continuously require a precise control of dynamic forces such as writing, drawing, and picking up objects, is often lacking in children with DCD (DSM-IV, 1994). However, there is not much evidence to illustrate if this lack of dexterity is caused by a reduced ability to respond adequately to the force precision demands. Therefore this topic was taken as the basis for the present experimental study.

It is known that development of the corticospinal system, connecting the motor control to the output system, is an essential anatomical substrate for organizing dexterous hand movements (Porter & Lemon, 1993) but quantitative studies along these lines are scarce. In a recent study we used an isometric paradigm to examine development of force control (Smits-Engelsman, Westenberg, & Duysens, 2003). The finding of that study was that for a simple force control task using a single finger, the maturation of force regulation measured by the relative variability is almost complete by 10 years of age despite further increase in maximum produced force until adulthood. The authors concluded that the control of a constant force of the fingers relies primarily on the maturation of the corticospinal system (up to age 9–10). We therefore hypothesized that a maturational delay could be reflected in more variability in force generation in children with DCD and therefore tested children in the specific age range (7–11 years of age) where the developmental changes are to be expected.

There are only a few controlled studies on the steadiness of force control in DCD. First, there is the study of Oliveira, Shim, Loss, Peterson, and Clark (2006), who investigated finger strength and the ability to control digit force production in children with DCD. In their task, no significant differences in strength or force variability between DCD and typically developing children during constant index finger pressing force production emerged. In one other study, using tasks in which children with DCD had to lift an object, Pereira, Landgren, Gillberg, and Forssberg (2001), showed that children with DCD used higher grip forces and safety margins but also larger variability in the control of the grip force in comparison to the controls.

Variability is a fundamental feature of human motor control (Frank, Friedrich, & Beek, 2006). To cope with this inherent noise in the system one may expect that developmental strategies will develop. Wolpert (2007) proposed that noise in the motor output is the fundamental limitation of the neuromotor system and it is known that the level of noise is implicated in some motor disorders like Parkinson’s disease (Contreras-Vidal & Buch, 2003). The reported increased movement variability in DCD is consistent with the hypothesis that either increased noisiness of the motor system or inadequate removal of noisy signals could be one of the causes of DCD (Smits-Engelsman & van Galen, 1997), since this noise makes perception and action computationally more difficult.

So far there is a lack of evidence to conclude that decreased capabilities to control variability in the generated force are one of the possible underlying causes of poor manual dexterity. The present study considers whether force control in a range comparable to that for daily living activities, is implicated in children with DCD. For this purpose force variability at different force levels is studied in a simple isometric task in individuals with DCD and in their typically developing matched peers. To test for maturational delays three age groups of children participated in this study with a mean age of 7, 9, and 11 years.

In short, this study systematically investigated finger force accuracy and steadiness using an isometric task. Moreover, we studied the ability of children with DCD to adapt finger force to five different levels of force (12–60% of MVC) comparable to levels required in daily activities. To further understand the development of children with DCD in relation to typically developing (TD) children, differences between groups in age-related changes of finger force and force control were also examined.

Based on previous studies, we hypothesized that children with DCD, compared to TD children, would have a higher variability in controlling finger forces and would show a developmental delay. Moreover, it was expected that children with DCD would show a decrease in accuracy in force tasks (as measured by the Error) and an increase in variability as measured by the standard deviation of the force signal and the ratio of the force signal to the noise (force/SD).