International Journal of Neuroscience, Early Online, 1–8, 2010
Copyright © 2010 Informa Healthcare USA, Inc.
ISSN: 0020-7454 print / 1543-5245 online
DOI: 10.3109/00207454.2010.535936
The Inability To Mentally Represent Action May Be
Associated With Performance Deficits in Children With
Developmental Coordination Disorder
Carl Gabbard and Tatiana Bobbio
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Department of Health and Kinesiology, Texas A&M University, College Station, Texas, USA
AB STRA CT
Several research studies indicate that children with developmental coordination disorder (DCD) show delays with
an array of perceptual-motor skills. One of the explanations, based on limited research, is that these children have
problems generating and/or monitoring a mental (action) representation of intended actions, termed the “internal
modeling deficit” (IMD) hypothesis. According to the hypothesis, children with DCD have significant limitations
in their ability to accurately generate and utilize internal models of motor planning and control. The focus of this
review is on one of the methods used to examine action representation—motor imagery, which theorists argue
provides a window into the process of action representation (e.g., Jeannerod, 2001. Neural simulation of action:
A unifying mechanism for motor cognition. Neuroimage, 14, 103–109.). Included in the review are performance
studies of typically developing and DCD children, and possible brain structures involved.
KEYWORDS: Action representation, developmental coordination disorder, internal modeling deficit, motor imagery
THE INABILITY TO MENTALLY
REPRESENT ACTION MAY BE
ASSOCIATED WITH PERFORMANCE
DEFICITS IN CHILDREN WITH
DEVELOPMENTAL COORDINATION
DISORDER
A literature search of published work clearly indicates
that the topic of developmental coordination disorder
(DCD) has emerged as a vibrant line of inquiry over the
last two decades. Wilson and Larkin (2008) point out
that, not only has this research impacted thoughts on
developmental disabilities in general, it also has stimulated the bonding of several relevant cross-disciplines to
work on a single project. By definition, DCD is a term
describing motor impairment in the absence of neurological disease, any known physical disorder, developmental delay, mental retardation, and low IQ (American Psychiatric Association, 2000). The movements of
children with DCD are often described as clumsy and
uncoordinated and lead to difficulties with performing
Received 24 September 2010.
Address correspondence to Carl Gabbard, TAMU 4243, College Station, TX
77843-4243, USA. E-mail: [email protected]
many of the activities of daily living and sports that typically developing children perform easily. The prevalence
of DCD has been estimated to be as high as 6% for children in the age range of 5–11 years (NIH, 2006); estimates range from 5% to 20% with at least 2% being affected severely. More recently, evidence has shown that
a significant number of children will continue to have
persistent difficulties into adulthood (Kirby, Edwards,
Sugden, & Rosenbaum, 2010).
In regard to motor control, the literature indicates
quite clearly that children with DCD display deficits
with an array of perceptual-motor skills (Astill & Utley,
2006; Cherng, Liang, Chen, & Chen, 2009; Deconinck
et al., 2006, 2008a; Tsai, Pan, Cherng, Hsu, & Chiu,
2009; Tsai, Wilson, & Wu, 2008). The present review
and commentary focuses on the idea that an underlying
problem may be a deficit in generating and/or monitoring an action representation termed the “internal
modeling deficit” (IMD) hypothesis. According to
the hypothesis, children with DCD have significant
limitations in their ability to accurately generate and
utilize internal models of motor planning and control.
From another perspective, these children have deficits
in their ability to mentally represent action—known
as action representation. These representations, that
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C. Gabbard and T. Bobbio
are associated with internal models, are hypothesized
to be an integral part of action planning. Furthermore,
there are indications that motor imagery (MI) provides a
window into the process of action representation. This paper
reviews the literature that highlights the notion that with
DCD, there may be a significant deficit in the ability to
mentally represent action. Included in the review are
performance studies of typically developing and DCD
children, and possible brain structures involved.
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ACTION REPRESENTATION
Motor programming theory suggests that an integral
component in an effective outcome is an adequate action representation of the movements. This view contends that action representation is a component of an
internal forward model, which is a neural system that
simulates the dynamic behavior of the body in relation to the environment (e.g., Wolpert, 1997; Wolpert
& Kawato, 1998). This theory proposes that internal
models make predictions (estimates) about the mapping of the self to parameters of the external world; processes that enable successful planning and execution of
action. These representations are hypothesized to be an
integral part of action planning (Caeyenberghs, Roon,
Swinnen, & Smits-Engelsman, 2009; Choudhury,
Charman, Bird, & Blakemore, 2007a, 2007b; Molina,
Tijus, & Jouen, 2008; Skoura, Papaxanthis, Vinter, &
Pozzo, 2005; Wolpert, 1997); Choudhury et al. and
Molina et al. reference this idea to children. Skoura,
Vinter, and Papaxanthis (2009) suggest that improvement in action representation in childhood may be due
to refinement of internal models.
Complementing the forward model idea and central to the present discussion is the suggestion that MI
provides a window into the process of action representation; that is, it reflects an internal action representation
(Jeannerod, 1997, 2001; Munzert, Lorey, & Zentgraf,
2009).
ACTION REPRESENTATION AND MI
MI is defined as an internal rehearsal of movements
from a first-person perspective without any overt physical movement. From another perspective, MI, also
known as kinesthetic imagery, is an active cognitive process during which the representation of a specific action
is internally reproduced in working memory without
any overt motor output (Decety & Grezes, 1999). In
addition to the reasonable case that MI is a reflection of
action representation and motor planning, studies have
found that there is a high correlation between real and
simulated movements (e.g., Glover, Dixon, Castiello,
& Rushworth, 2005; Heremans, Helsen, & Feys, 2007;
Nikulin, Hohlefled, Jacobs, & Curio, 2007; Michelon,
Vettel, & Zachs, 2005; Sharma, Jones, Carpenter, &
Baron, 2008; Young, Pratt, & Chau, 2009). Complementing those findings is the idea that motor control
and motor simulation states are functionally equivalent
(Jeannerod, 2001; Kunz, Creem-Regehr, & Thompson,
2009; Lorey et al., 2010; Munzert & Zentgraf, 2009).
Also known as “simulation theory,” this idea postulates
that mental (covert) and executed (overt) actions rely
on similar motor representations. Such research has
drawn the interest of (for example) clinicians working to
stimulate neuromuscular pathways. For example, with
stroke patients, injured athletes, and those with cerebral
palsy, imagery is considered an attractive means to
access the motor network and restore motor function
without actual overt action. Also, a relatively large
body of literature indicates that sport psychologists
use mental rehearsal as a means to facilitate practice
and improve performance in athletes (see reviews by
Munzert, Lorey, & Zentgraf., 2009; Sharma et al.,
2009; Steenbergen, Craje, Nilsen, & Gordon, 2009).
Furthermore, evidence has been reported showing that
MI follows the basic tenets of Fitts’ Law (Solodkin,
Hlustik, Chen, & Small, 2004; Stevens, 2005). That
is, simulated movement duration like actual movement,
decreases with increasing task complexity.
As opposed to visual imagery (VI), defined as the
internal enactment or reenactment of perceptual experiences (Barsalou, 2008), neuroimaging and neuropsychological studies indicate that MI is more affected by
biomechanical (kinesthetic) constraints, which are commonly associated with action processing (see review by
Pelgrims, Andres, & Olivier, 2005; Stevens, 2005). The
notion that MI elicits corticomotor excitability associated with action is supported by the work of Neuper, Scherer, and Pfurtscheller (2005), Stinear, Byblow,
Steyvers, Levin, and Swinnen (2006), and Takahashi
et al. (2005).
It has also been hypothesized that MI plays an
important role in the prediction of one’s actions (e.g.,
Bourgeois & Coello, 2009; Kunz, Creem-Regehr,
& Thompson, 2009; Lorey et al., 2010). Arguably,
one of the important aspects of an action plan is the
ability to predict the outcome and consequences of
intended actions. Imagining an action can serve several
useful goals to that endeavor. For example, during
imagery important timing information is provided
by the forward model which aids in predicting the
sensory consequences of the movement. According to
Bourgeois and Coello (2009), motor representation
can be viewed as a component of a predictive system,
which includes a neural process that simulates through
MI the dynamic behavior of the body in relation to the
environment.
International Journal of Neuroscience
Children with DCD 3
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STUDIES OF TYPICALLY DEVELOPING
CHILDREN
Studies of typically developing children indicate that
the emergence of MI begins around age 5 (Funk,
Brugger, & Wilkening, 2005; Gabbard, Cordova, &
Ammar, 2007; Kosslyn, Margolis, Barrett, Goldknopt,
& Daly, 1990) with considerable refinement in ability
shown between early adolescence (12 years >) and early
adulthood (Choudhury et al., 2007a, 2007b; Gabbard,
2009). As a general observation of studies involving
a range of age, older populations perform better than
younger groups (e.g., Caeyenberghs, Tsoupas, Wilson,
& Smits-Engelsman, 2009; Molina, Tijus, & Jouen,
2008; Skoura, Vinter, & Papaxanthis, 2009). Furthermore, those findings suggest that the ability to mentally
represent actions (i.e., action representations) follows a
similar age-related trend.
Association With Brain Development
Work with typically developing children and adults suggests that there is a close link between development of
the parietal cortex, action representation, and the ability to formulate internal models associated with MI;
suggesting that both are refined through the adolescent years (e.g., Blakemore & Sirigu, 2003; Choudhury
et al., 2007a, 2007b; Gerardin et al., 2000; Koscik,
O’Leary, Moser, Andreasen, & Nopoulos, 2009; Lacourse, Orr, Cramer, & Cohen, 2005; Skoura, Vinter, &
Papaxanthis, 2009). According to Skoura and colleagues (2009), one could also speculate that deficits in
action representation in children could be related to the
maturational processes in the parietal cortex. With increasing age, the maturational processes in parietal cortex increase neural efficiency and may aid older children
(10 years >) to progressively improve their ability to generate accurate motor predictions. The researchers also
brought attention to the idea, as others have noted, that
we cannot rule out other factors, such as attention and
the capacity to understand and follow task instructions,
as influences on children’s MI performance.
Another aspect associated with the cognitive aspects
of action representation is development of the prefrontal
cortex (e.g., Skoura et al., 2009). That is, evolution of
a general capacity to establish relations between data
separated in space and time (Diamond, 2002). Molina,
Tijus, and Jouen (2008) suggest that MI in children can
be interpreted in terms of a general development of cognitive processes involved in motor representation principally determined by internal changes in the prefrontal
and parietal structures of the brain.
Interestingly, the cerebellum, although not given the
attention of the structures previously mentioned, has
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been associated with the ability to internalize representations, as noted in the internal (forward) model
literature (e.g., Bastian, 2006; Blakemore, Frith, &
Wolpert, 2001; Blakemore & Sirigu, 2003; Shadmer &
Krakauer, 2008). The general notion is that the cerebellum is presumed to be involved in motor prediction,
a function of the internal model, and thus would be
critical for action representation and processing. For
example, activation of the cerebellum early in learning
might correspond to the error signals between the
predicted and actual outcomes of movements, which
are used to refine the forward model’s predictions and
guide acquisition of new internal models (Blakemore,
Frith, & Wolpert, 2001). Some investigators suggest
that the cerebellum acquires and stores internal models
of the motor system (Miall, Weir, Wolpert, & Stein,
1993; Wolpert, Miall, & Kawato, 1998; Kawato, 1999;
Imamizu et al., 2000). Support for these ideas is largely
based on deficits in patients with cerebellar dysfunction
or on functional imaging studies (Maschke, Gomez,
Ebner, & Konczak, 2004; Smith & Shadmehr, 2005).
Interestingly, Blakemore and Sirigu (2003) reported
that both the parietal cortex and the cerebellum provide
internal models of different nature. The researchers
speculated that whereas a cerebellar internal model
makes rapid predictions about the sensory consequences of self-generated movement at a very low level
of movement execution, a model in the parietal cortex
might address more cognitive aspects of movements.
More specific to MI in children, Caeyenberghs and colleagues (2009) have suggested that the cerebellum plays
an important role in the reduction of MI accuracy, since
it is thought to encode internal models that reproduce
the essential properties of action representations.
Children With DCD
As noted earlier, the literature presents a rather convincing case that children with DCD are likely to show
an IMD (e.g., Deconinick, Spitaels, Fias, & Lenior,
2008b; Lewis, Vance, Maruff, Wilson, & Cairney, 2008;
Maruff, Wilson, Trebilcock, & Currie, 1999; Pettit
et al., 2008; Van Waelvelde et al., 2006; Williams,
Thomas, Maruff, Butson, & Wilson, 2006; Williams,
Thomas, Maruff, & Wilson, 2008; Wilson et al., 2004).
Those experiments used an array of (so-called) MI tasks
and paradigms. For example, mental rotation involving the hand and whole-body, distance estimation with
the effector (hand), and tasks involving the comparison
(chronometry) of actual and simulated actions such as
pointing, aiming, and walking; tasks that for the most
part, have been reported as valid with adult populations. Typically, with the chronometry tactic, MI ability is judged by the closeness of the relationship (time)
between simulated and actual movement. Similar to this
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C. Gabbard and T. Bobbio
method, is the association with Fitts’ law—that is, simulated movement duration like actual movement, should
decrease with increasing task complexity.
For example, Van Waelvelde and collegues (2006)
used a rhythmic finger-tapping task in combination
with a jumping and a drawing activity to evaluate children with DCD and a matched control group. In children with DCD, an increased temporal variability was
found with finger tapping when compared with a control
group. Errors in time correlated significantly with the
jumping and drawing task, while errors in space did not.
It was concluded that children with DCD have more
problems in building up an internal representation of
the movement. The researchers went on to suggest that
deficits in temporal movement parameterization might
be one of the underlying causes of poor motor performance in some children with DCD.
Williams and colleagues (2006) also investigated the
so-called IMD hypothesis using the mental rotation
paradigm with typically developing children and a sample of children with DCD (ages 7–11). Results indicated partial support for the hypothesis that children
with DCD would display an atypical pattern of performance on the hand rotation task, requiring implicit
use of MI. Overall, there were no significant differences
between the DCD and control groups when the hand
task was completed without explicit instructions, on either response time or accuracy. However, when imagery
instructions were introduced, the controls were significantly more accurate than the DCD group, indicating
that children with DCD were unable to benefit from explicit cuing. In essence, the researchers found support
for the IMD hypothesis with DCD children.
In a subsequent study, Williams, Thomas, Maruff,
and Wilson (2008) examined MI ability in children
with DCD aged 7–11 years with the intent to determine whether children with varying degrees of motor
impairment differed in their ability to perform MI tasks.
DCD children were split into two groups (DCD severe [DCD-S], DCD mild [DCD-M]) and compared to
age-matched controls. Participants performed two MI
tasks—hand (performed without and with specific imagery instructions) and whole-body rotation. Results indicated that children in the DCD-S group had a generalized MI deficit in that they were less accurate across
tasks than controls (and the DCD-M group on the hand
task) and showed little benefit when given specific imagery instructions. The DCD-M group appeared capable of performing simpler MI transformations, but was
less successful as task complexity increased. Unlike the
DCD-S group, the DCD-M group did show some benefit from specific imagery instructions with increases in
accuracy on the hand task. The findings suggested that
a MI deficit does exist in many children with DCD but
that its degree can vary. That is, factors such as individ-
ual ability level and task complexity appear to be linked
to the deficit.
In 2008, Lewis et al. examined movement durations
for real and imagined movements in a visually guided
pointing task in children aged 8–12 years old and (similar to previous studies noted) found that the DCD group
demonstrated an inability to generate imagined movements that was not present in the typically developing
participants. Deconinck and colleagues (2008b) investigated the IMD hypothesis with 9-year-old children with
DCD using a mental (hand/letters) rotation paradigm.
Results indicated that children with DCD were generally
slower and made more errors than the typically developing control sample. The researchers concluded that
both groups did use an imagery strategy; however, judgments of the DCD group seem to be compromised by a
less well-defined internal model.
IMD and Other Disabilities
In addition to children with DCD, there are reports of
children with other disabilities having exceptional difficulty in mentally representing action. For example, in
their review of MI and children with hemiplegic cerebral
palsy (CP), Steenbergen and colleagues (2009) noted
that converging evidence indicates that motor decits in
those children are not only associated with execution,
but also with impaired motor planning. For example,
Mutssarts, Steenbergen, and Bekkering (2007) reported
that a group of adolescents with CP displayed impaired
MI, which they associated with that of anticipatory motor planning. The researchers did differentiate the side
of CP impairment by observing that participants with
left hemiparetic CP (right congenital brain damage)
were less affected than those with right hemiparetic CP.
In 2009, Caeyenberghs, Swinnen, and SmitsEngelsman examined MI ability of children with
acquired brain injury (ABI). The researchers used
a chronometry, executed compared to imagined
paradigm, to investigate the speed-accuracy trade-offs
(or Fitts’ law) with an aiming task. Whereas performance of the control group conformed to Fitts’ law, in
the ABI group, only executed movements aligned with
Fitts’ law. Their conclusion was that children with ABI
show an inferior ability to imagine the time needed to
complete goal-directed movements.
Another piece of research that appears to hint at the
notion of an IMD was reported by Van Roon, Caeyenberghs, Swinnen, and Smits-Engelsman (2010). Children with a learning disorder (LD) and matched controls were asked to smoothly track an accelerating dot by
moving an electronic pen on a digitizer. The researchers
were examining the children’s prospective motor control. That is, the ability to “predict future responses,”
and from one perspective, create a forward (internal)
International Journal of Neuroscience
Children with DCD 5
model. Results indicated that children with LD performed worse than controls. It was suggested that part
of the problem was the inability to create an effective
internal model. Interestingly, no differences in tracking
performance were found between children with LD who
scored in the normal range on the MABC (above the
15th percentile) and those who scored in the clinical
range (below the 15th percentile).
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Brain Deficits Associated With IMD
Obviously, some of the same structures noted with typically development children are relevant with DCD populations. Mentioned with DCD studies are: cortical areas involved in motor processing, such as the premotor
area (plays a role in motor planning and sequencing and
movement readiness), parietal cortex, and the dorsolateral prefrontal cortex, which are also associated with premotor planning (Deconinck et al., 2008b; Wilson et al.,
2004).
In regard to the role of the cerebellum mentioned
earlier, there are hints that this structure may have specific relevance to children with DCD. Whereas strong
evidential support has not been established, some researchers have suggested that these children might have
a cerebellar impairment that underscores the general
disorder; the idea is described as the cerebellar hypothesis (e. g., Cantin, Polatakjko, Thach, & Jaglal, 2007;
Geuze, 2005; Stoodley & Stein, 2009). One of the
key arguments is that children with DCD typically display difficulty with the coordination of voluntary movements, including balance and equilibrium; problems
that are associated with cerebellar function (ShumwayCook & Woollacott, 2006; Slobounov, Hallett, Stanhope, & Shibasaki et, 2005). And, as noted earlier, the
cerebellum has been associated with internal modeling
and the ability to mentally represent action via MI. One
key aspect related to internal modeling is that the cerebellum is thought to correct discrepancies between the
intended movement and the actual movement through
its connections with lower motor neurons and the motor cortex (Barlow, 2002). A problem with this process
would theoretically account for inaccurate predictions
of the motor plan. Speculatively, if children with DCD
have a cerebellar impairment or, many would argue lack
of maturity, it seems reasonable to predict difficulties
with the ability to mentally represent action with tasks
requiring coordination and postural control.
In general, most researchers agree that the deficits
displayed by these children are the result of a general processing deficit of the motor system as a whole.
For example, when information “flows” from the prefrontal to the motor cortex, DCD children, especially
younger ones, may be forced to maintain a high level
of preprogramming to compensate for difficulties in the
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perceptual-motor and executive aspects of the movement related to their coordination disorder (Castelnau,
Albaret, Chaix, & Zanone, 2008).
CONSIDERATIONS (CAUTION) IN
EXPERIMENTAL PARADIGMS
Underscoring the use of tasks for eliciting MI is the
notion that it engages MI and that the child has the cognitive ability and attentiveness to understand and complete the task. Of these considerations (constraints), arguably the most debatable is the MI issue. For example,
is the child engaging in VI, rather than MI? MI involves
the first-person mental simulation of action that “focuses” on the effector (body part involved). An important point is the hypothesized distinction between MI
and VI and its connection to the visual systems (dorsal/ventral substrates). Stevens (2005) contends that
MI represents the kinesthetic and biomechanical constraints connected with action, associated with the dorsal
stream, whereas VI is linked with the spatial component
of the perceived environment via the ventral stream. Furthermore, MI elicits corticomotor excitability associated
with action and several reports suggest that there is a high
correlation between real movements and MI; neither of
those observations is associated with VI (Solodkin et al.,
2004; Stinear et al., 2006). VI relies heavily on connectivity patterns originating in the occipital areas, which
supports the idea that this behavior may be classified as
a visual task. Solodkin et al. add to the distinction by
concluding that MI complements Fitts’ Law, whereas VI
does not. Farahat, Ille, and Thon (2004) reported that
the difference in duration of actual and imagined movement for learning to draw graph forms was much smaller
when using kinesthetic (motor) imagery compared
to VI.
A close review of the studies described here noted
that very few indicated in the methodology specific instructions or training regarding the elicitation of MI.
One exception stated, “participants were trained and
asked to kinesthetically ‘feel’ themselves executing the
movement (‘feel your arm extending. . .’)” (Gabbard,
Cordova, & Ammar, 2007; Gabbard, Cordova, & Lee,
2009); a statement that suggests being more sensitive
to the biomechanical constraints of the task (Johnson,
Corballis, & Gazzaniga, 2001; Sirigu & Duhamel, 2001;
Stevens, 2005). Obviously, without brain activity verification there is no way to really know the extent that MI
or VI is processing. However, more specific instructions
and training, especially with younger children would be
better science and necessitate a summary in any scientific report.
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C. Gabbard and T. Bobbio
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CONCLUSIONS AND FINAL
COMMENTS
There appears to be substantial evidence that in typically
developing children and especially those with DCD (and
other motor-related disorders), the inability to mentally represent action may be associated with deficits
in motor planning. Primary brain structures and possible impairments or delayed development have focused
on the parietal cortex, prefrontal cortex, and cerebellum.
Furthermore, there appears to be a general processing deficit of the motor system associated with the
flow of information from the prefrontal to the motor cortex. In regard to methodology used to examine
action representation, caution should be taken in regard to use of motor (kinesthetic) imagery, rather than
VI.
Obviously, further inquiry is needed and relevant
research questions remain unclear. Two of the more
frequent observations (and some would say criticism)
addresses—is the delay displayed in children with DCD
different from the developmental immaturity of typically developing children? And, could it be that children with DCD might be poor at using MI because they
are clumsy not clumsy because they have poor MI ability? This line of inquiry also needs to include more aspects of both visual and MI (tasks). For example, a study
that finds no difference between children with DCD and
typically developing peers, may not provide evidence
against the internal model deficit theory; only that the
children with DCD were not impaired on this particular task. In addition, more specifically, what is/(are)
the common neuropsychological deficit(s) among children with different impairments (CP, LD, and ABI)
that identify them as having IMD? Perhaps additional
studies of brain activity involvement will provide more
insight.
In regard to the applied implications of this information, according to Williams et al. (2008), the applied significance relates foremost to teaching methods. Given
that children with DCD may have difficulty in mentally
representing movements, it is suggested that more kinesthetic approaches are used. That is, approaches to teaching motor skills that focus on “actual” bodily movement
and touching to learn, as opposed to the predominant
use of visual or verbal stimuli. These modalities reduce
the reliance on internal models that are likely to be less
than effective. In addition, it has been suggested that
early training and movement experience with these children involve a strong emphasis on the development of
body and spatial awareness. Underscoring this idea is
the importance of a solid fundamental movement foundation with knowledge of what the body can do and how
to do it.
Declaration of Interest: The authors report no conflicts of interest. The authors alone are responsible for
the content and writing of the article.
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Children with DCD 7
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