Research in Developmental Disabilities 34 (2013) 2047–2055

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Research in Developmental Disabilities

Review article

Motor skill learning in children with Developmental

Coordination Disorder
Jin Bo *, Chi-Mei Lee
Department of Psychology, Eastern Michigan University, 341 MJ Science Building, Ypsilanti, MI 48197, United States

A R T I C L E I N F O A B S T R A C T

Article history: Children with Developmental Coordination Disorder (DCD) are characterized as having
Received 17 December 2012 motor difficulties and learning impairment that may last well into adolescence and
Received in revised form 13 March 2013 adulthood. Although behavioral deficits have been identified in many domains such as
Accepted 13 March 2013 visuo-spatial processing, kinesthetic perception, and cross-modal sensory integration,
Available online 11 April 2013 recent studies suggested that the functional impairment of certain brain areas, such as
cerebellum and basal ganglia, are the underlying causes of DCD. This review focuses on the
Keywords: ‘‘motor learning deficits’’ in DCD and their possible neural correlates. It presents recent
Developmental Coordination Disorder
evidence from both behavioral and neuroimaging studies and discusses dominant neural
Motor adaptation
hypotheses in DCD. Given the heterogeneity of this disorder, a successful intervention
Motor sequence learning
Cerebellum
program should target the specific deficits on an individual basis. Future neuroimaging
Basal ganglia studies are critical steps in enhancing our understanding of learning deficits in DCD.
ß 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2048
2. Motor learning deficits in children with DCD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2048
2.1. Sensorimotor adaptation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2048
2.2. Motor sequence learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2049
3. Neural hypotheses related to motor learning deficits in DCD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2050
3.1. Cerebellum hypothesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2050
3.2. Basal ganglia hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2051
3.3. Parietal hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2051
3.4. Other areas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2052
4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2052
4.1. From behavioral to neuroimaging studies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2052
4.2. From group-comparisons to subtypes of DCD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2052
4.3. From lab-based learning to intervention strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2052
4.4. Final notes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2053
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2053

* Corresponding author. Tel.: +1 734 487 3416; fax: +1 734 487 1155.
E-mail address: jbo@emich.edu (J. Bo).

0891-4222/$ – see front matter ß 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ridd.2013.03.012
2048 J. Bo, C.M. Lee / Research in Developmental Disabilities 34 (2013) 2047–2055

1. Introduction

Children with Developmental Coordination Disorder (DCD), sometimes known as ‘‘clumsy children,’’ demonstrate motor
difficulties (Bo, Bastian, Kagerer, Contreras-Vidal, & Clark, 2008; Henderson, Barnett, & Henderson, 1994) and learning
impairment (Alloway & Archibald, 2008; Dewey, Kaplan, Crawford, & Wilson, 2002; Kagerer, Bo, Contreras-Vidal, & Clark,
2004) that interfere with academic achievement (Henderson & Sugden, 1992; Tucha & Lange, 2004) and activities of daily
living (e.g., dressing, playground skills and handwriting; Kennedy et al., 2007). If without appropriate intervention during
childhood, these deficiencies may last well into adolescence (Cousins & Smyth, 2003) and adulthood (Kirby & Sugden, 2010).
Up to 6% of American school children are thought to be affected by DCD (American Psychiatric Association (APA), 2000) and
as high as 87% of these children will not ‘‘grow out’’ of their difficulties (Cousins & Smyth, 2003).
Although a number of terms have been used to describe children with motor difficulties in the literature (see review in
Henderson & Henderson, 2003), we use the term Developmental Coordination Disorder (DCD) in this review in accordance
with the Diagnostic and Statistical Manual of Mental Disorders IV-TR ([DSM IV-TR]; APA, 2000) to avoid confusion among
terms and potential bias on causality. Based on DSM IV-TR, criteria for the diagnosis of DCD include (1) performance in daily
activities that require motor coordination that is substantially below that expected given the person’s chronological age and
daily living; (2) the motor disturbance (significantly) interferes with academic achievement or activities of daily living; and
(3) the motor disturbance is not due to a general medical condition (e.g., cerebral palsy, hemiplegia, or muscular dystrophy)
and does not meet the criteria for a Pervasive Developmental Disorder (APA, 2000).
In this review, we focus on the ‘‘motor learning’’ aspect of DCD due to its classification as a ‘‘learning disorder,’’ although
behavioral deficits have been identified in many other domains such as visuo-spatial processing, kinesthetic perception, and
cross-model sensory integration (see Wilson & McKenzie, 1998, for detailed review). It has been suggested that DCD may be
related to central nervous system pathology (Ivry, 2003; Querne et al., 2008; Zwicker, Missiuna, Harris, & Boyd, 2011).
Therefore, the purpose of this review is to present a synopsis of the current literature on the motor learning deficits in DCD
and their possible neural correlates, discuss dominant hypotheses, and suggest a direction for future research.

2. Motor learning deficits in children with DCD

The ability to learn a variety of motor skills is critical for many daily activities throughout the lifetime (e.g., dressing
oneself, writing letters, or communicating via computers). Here, the term ‘‘motor learning’’ refers to relatively permanent
behavioral changes associated with practice or experience (Schmidt, Sherwood, & Walter, 1988). Wolpert, Diedrichsen, and
Flanagan (2011) have recently provided an extensive review on the principles of motor learning as we adapt to changes in
our environment, manipulate new objects, and refine existing motor skills. Although there are multiple ways to classify
motor learning (e.g., error-based learning, reinforcement learning, and use-dependent learning in Wolpert et al. (2011)), the
current review focuses on two broad experimental categories: sensorimotor adaptation and sequence learning (Doyon &
Benali, 2005; Willingham, 1998). In sensorimotor adaptation paradigms, participants modify movements to adjust to
changes in either sensory input or motor output characteristics. For sequence learning, individuals learn to combine isolated
movements into one smooth, coherent action (Bo, Langan, & Seidler, 2008).

2.1. Sensorimotor adaptation

Sensorimotor adaptation tasks are used to gain insight into how humans represent their environment, the mechanics of
the body, and interactions between the two during movement planning and production (Bo, Block, Clark, & Bastian, 2008). A
useful experimental approach to understand adaptation is to investigate how motor performance changes through
repetition or practice when the relationship between the hand movements and the sensory feedback of those movements is
altered. In this case, participants have to adaptively adjust their movement to compensate for the changed environment.
In the literature, there are two broad types of sensorimotor adaptation. One is kinematic adaptation, where the sensory
feedback of movements is distorted through the use of computer programs (e.g., Cunningham, 1989; Pine, Krakauer, Gordon,
& Ghez, 1996) or the use of laterally displacing prisms (e.g., Held & Bossom, 1961; von Helmholtz, 1962). The other is
dynamic (or kinetic) adaptation, where the anticipated proprioception is altered by having participants move their limb
through an opposing force field (e.g., Izawa, Criscimagna-Hemminger, & Shadmehr, 2012; Shadmehr & Holcomb, 1997,
1999).
A real-world example of sensorimotor adaptation is driving a rental car that is a different model from one’s own car. The
magnitude of vehicle movement in response to the amount of wheel turn and accelerator depression varies across vehicles.
Thus, the driver must learn the new mapping between his or her actions and the resulting vehicle movements.
Experimentally, a sensorimotor adaptation task consists of three phases: (1) baseline with normal visual feedback of the
hand movements (e.g., you drive your own car without making errors), (2) learning trials (i.e., distorted trials) where
the visual feedback of the hand movement is changed (e.g., you drive a rental car for the first time and make mistakes since
the scale of the wheel turn is not the same), and (3) post-learning trials where the visual feedback of the hand movement is
changed back to normal. Successful learning can be measured by the presence of an after-effect during post-learning trials
(e.g., making errors when you change back to your own car after driving a rental car for quite a long period of time).
 J. Bo, C.M. Lee / Research in Developmental Disabilities 34 (2013) 2047–2055 2049

Using computer-manipulated adaptation paradigms, previous work on children with DCD suggests that ‘‘noisy’’
sensorimotor mapping (i.e., large variability under normal setting) underlies their learning deficits in visuomotor adaptation
tasks (Kagerer et al., 2004; Kagerer, Contreras-Vidal, & Stelmach, 1997). Kagerer et al. (2004) reported a study where children
with and without DCD were required to adapt to a novel visuomotor relationship, which involved visual feedback that was
rotated by 458 whilst they performed a center-out drawing task. The results showed that the movement errors during
learning trials were considered as normal performance for children with DCD and therefore remained uncorrected. In other
words, children with DCD did not realize that the relationship between their hand movements and visual feedback was
altered because of the large variability at the baseline condition. Thus, they were less affected by the feedback distortion and
had less learning than the controls. The authors argued that children with DCD had a less well-defined ‘‘noisy’’ visuomotor
mapping (Kagerer et al., 2004). To address the issue of small sample size (i.e., only 7 DCD in the original study) and evaluate
the scope of ‘‘noisy’’ mapping, Kagerer, Contreras-Vidal, Bo, and Clark (2006) performed a follow up study to examine
whether children with DCD could adapt differently when the distortion was introduced abruptly or gradually. Consistent
with the idea of the ‘‘noisy’’ sensorimotor mapping, the children with DCD did not appear to be able to utilize the small error
signals provided during the gradual perturbation, but they could perform as well as the typically developing children when
exposed to larger error signals in abrupt visuomotor perturbation. These results suggest that impaired adaptation is mainly
due to their less-defined baseline performance. When the error messages are significantly distinguished from their ‘‘noisy’’
range of ‘‘normal’’ sensorimotor mappings, children with DCD may be able to adapt to changes to their environment.
Another way to introduce the discrepancy between visual space and motor space is to expose someone to laterally
displacing prisms. Prism adaptation studies on throwing, revealed no learning deficits in children with DCD (Dickey, Bo,
Contreras-Vidal, Kagerer, & Clark, 2006). Similarly, Cantin, Polatajko, Thach, and Jaglal (2007) reported that, in general, the
DCD group was more variable and less accurate throughout the whole test. No group differences were found for adaptation.
The authors argued that the poor throwing accuracy and large variability might mask the learning deficit in this prism
adaptation task. This finding was consistent with the results from the computer-manipulated adaptation studies in Kagerer’s
group (2004, 2006), where the distortion was within the ‘‘noisy’’ baseline performance, and therefore, was not detected.
Interestingly, further individual analysis revealed that only three children in the DCD group adapted within the range of the
controls. Six out of nine children with DCD showed less adaptation compared to the controls. In another study using a similar
throwing prism task, Brookes, Nicolson, and Fawcett (2007) reported that all the DCD children, 5 of the 6 children with
comorbid DCD and dyslexia, showed an impaired rate of adaptation. These findings suggest most children with DCD are
impaired in motor adaptation, and among them, there are substantial individual differences.
Beyond the kinematic domain, a representation of limb dynamics is another basis of voluntary motor control. The basic
operation is to transform planned kinematic trajectories into appropriate patterns of muscular enervation (Jordan, Flash, &
Arnon, 1994; Konczak, Borutta, Topka, & Dichgans, 1995). In typical dynamic adaptation tasks, participants are exposed to
an unknown force field while they attempt to execute goal-directed arm movements (Jansen-Osmann, Richter, Konczak, &
Kalveram, 2002; Konczak et al., 1995). In such situations, participants have to adjust the relationship between their
planned kinematic trajectories and muscular forces in order to compensate for the new force field. Jucaite, Fernell,
Forssberg, and Hadders-Algra (2003) have investigated adaptation to different lifting weights and its correspondent
anticipatory postural adjustment in children with DCD, Attention Deficit Hyperactivity Disorder (ADHD), and a
combination of ADHD and DCD. Results showed that children with ADHD and DCD could not scale manual and postural
forces in both amplitude and temporal domains. Children with DCD did show adjusted grip forces, but had temporal delays
in correspondent postural adjustment. It appears that impaired force control may be partially due to the ‘‘timing’’ deficits in
DCD that have been consistently reported in multiple behavioral studies (Bo, Block, Clark, et al., 2008; Lundy-Ekman, Ivry,
Keele, & Woollacott, 1991). Other studies have reported that children with DCD have difficulties in the fine-tuning of
manual force (Smits-Engelsman, Niemeijer, & van Galen, 2001). Smits-Engelsman, Westenberg, and Duysens (2008) used
an isometric force production task to test the hypothesis that children with DCD have a decreased ability to scale force to a
required force level. Results showed that children with and without DCD were equally able to adapt their generated force to
the required levels. However, DCD children produced a less steady and more variable force than controls. In addition, the
force control of younger children with DCD was more affected than older children. All these results suggest ‘‘noisy’’ baseline
dynamic control that is similar to kinematic control (e.g., Kagerer et al., 2004, 2006). Since there are very few force
adaptation studies that have been reported, it is not clear how such ‘‘noisy’’ dynamic control affects the force adaptation
performance in children with DCD. Based on the findings reported by Smits-Engelsman’s group (2008), we may
hypothesize that, similar to the kinematic adaptation, the ‘‘noisy’’ baseline force controls will affect force adaptation in
children with DCD.

2.2. Motor sequence learning

Sequence learning refers to an ability to combine isolated movements into one smooth, coherent action. It can be either
explicit, where participants are aware of the sequence and the goal of learning, or implicit, where learning occurs outside of
conscious awareness. A widely used paradigm to investigate sequence learning is the serial reaction time (SRT) task, where
stimuli appear successively at different locations in a repeating sequence, and participants respond to each by pressing a
corresponding key (Nissen & Bullemer, 1987). Typically, implicit sequence learning is said to occur when participants
demonstrate improvements in the speed and/or accuracy of their responses, but are unable to explicitly describe what they
2050 J. Bo, C.M. Lee / Research in Developmental Disabilities 34 (2013) 2047–2055

have learned. On the other hand, explicit sequence learning is concluded if participants show any signs of sequence
awareness.
Despite the fact that DCD has been characterized by a deficit in the ability to learn motor skills, few studies have been
reported on motor sequence learning. Wilson, Maruff, and Lum (2003) have focused on implicit learning in a group of 10
children with DCD and 10 controls. They employed the classic SRT task (Nissen & Bullemer, 1987) in which children were
required to learn a 10-element spatial sequence. Results showed that both groups learned the sequence and there were no
group differences in the magnitude of learning. The authors concluded that implicit learning for simple sequential
movements appears to be intact in children with DCD (Wilson et al., 2003).
However, a different finding has been reported by Gheysen, Van Waelvelde, and Fias (2011). They questioned the small
sample size and the liberal significant cut-off (p < .10) reported by Wilson et al. (2003). It was also problematic to have
random testing blocks to assess final learning. Thus, Gheysen et al. (2011) used the same experimental design to ensure a
reliable comparison with Wilson et al. (2003), but modified the random testing blocks to match the structure of sequence
blocks. Results revealed that children with DCD did not significantly improve their performance over the sequence blocks,
suggesting a sequence learning deficit. Furthermore, an awareness test, administered after the SRT task, indicated some
consciousness of the repeating sequence pattern. Thus, it is possible that the sequence learning deficits reported in
Gheysen et al. (2011) may related to the difficulties in explicit, implicit, or both types of learning. Further individual
analysis or subgroup analysis among children with and without awareness of the sequence will be helpful to clarify these
possibilities.
It is surprising that sequence learning has been rarely studied in this population although it is crucially important for
efficient daily activities. At this point, we argue that, at least, there is a group of children with DCD that have significant
motor learning deficits. Such deficits may be partially due to less fine-tuned ‘‘noisy’’ kinematic and dynamic control.
Further studies are needed to explore whether there are any ‘‘overlapping’’ or ‘‘differential’’ learning deficits among
different motor tasks in different groups of DCD, as well as the relationship between implicit and explicit learning in these
groups of children.

3. Neural hypotheses related to motor learning deficits in DCD

Despite hundreds of behavioral neuroscience investigations of skill learning performed for more than a century
(James, 1890), it was not until the last two decades that studies using brain imaging techniques to examine the
neural mechanisms of motor learning exploded (detailed reviews see Ashe, Lungu, Basford, & Lu, 2006; Bo, Langan, et al.,
2008; Doyon et al., 2009; Seidler, 2010) and set a foundation to understanding the neural mechanism in the pediatric
context. But, to date, there has been very few brain imaging studies examining neural mechanisms of motor learning
deficits in DCD. The neural correlates of DCD have essentially been hypothesized from behavioral data. Zwicker,
Missiuna, and Boyd (2009) have reviewed the behavioral evidence for neural correlates of DCD. Here, we focus on
the ‘‘motor learning aspect’’ in this population and combine evidence from both behavioral and recent neuroimaging
studies to explore several dominant hypotheses and their relationships with motor skill learning in children with
DCD.

3.1. Cerebellum hypothesis

The cerebellum is especially vulnerable in developmental disorders because it develops relatively later and slower
than most of the other areas of brain (Giedd, 2001; Griffiths et al., 2004; Huttenlocher, 1990). An increasing number of
animal studies have suggested the role of delayed cerebellum development on uncoordinated behaviors. For example,
under-nourishment during the brain-growth spurt period in rats leads to a smaller cerebellum containing fewer neuronal
and glia cells, fewer synapses, and decreased myelination, and the rats showed long-lasting signs of clumsiness
(Gramsbergen & Westerga, 1992). In another study (Gramsbergen, 2003), dexamethasone (a steroid that may affect the
cerebellar maturation during late pregnancy) injected into young rats during the last-trimester (cerebellum maturation
stage) induced long-lasting abnormalities and clumsiness in a wide range of motor skills. Thus, although there is still lack
of direct linkage between the role of the cerebellum and uncoordinated behaviors, converged evidence from
morphological and animal studies implies that a disturbed cerebellum development may be one of the key players in
children with DCD.
Behaviorally, children with DCD have demonstrated difficulties in a wide range of motor tasks similar to that observed in
patients with cerebellar lesion (Geuze & Kalverboer, 1987; Ivry, 2003; Lundy-Ekman et al., 1991; Williams, Woollacott, &
Ivry, 1992). It is known that the cerebellum plays a unique role in adaptation, especially for storage of long-term
sensorimotor representations (Imamizu, Kuroda, Miyauchi, Yoshioka, & Kawato, 2003; Imamizu, Kuroda, Yoshioka, &
Kawato, 2004; Imamizu et al., 2000). Multiple studies have reported that patients with cerebellar lesion cannot adapt to
sensorimotor distortions (Bo, Block, Clark, et al., 2008; Earhart & Bastian, 2001; Lang & Bastian, 2002; Morton & Bastian,
2004, 2006). Similarly, Kagerer et al. (2004) have previously found a complete lack or poor visuomotor adaptation in a group
of children with DCD (Kagerer et al., 2004). In another study, Kagerer et al. (2006) examined the motor adaptation in children
with DCD under different types of distortion (Kagerer et al., 2006). The results showed that children with DCD could update
their internal model more effectively during exposure to an abrupt visuomotor perturbation than to a gradual one. Robertson
 J. Bo, C.M. Lee / Research in Developmental Disabilities 34 (2013) 2047–2055 2051

and Miall (1999) showed that adaptation to gradual visuomotor distortions was blocked by inactivation of the dentate
nucleus, whereas adaptation to abrupt visuomotor perturbations was spared in non-human primates. In the context of
gradual adaptation, learning is driven by an error signal between the planned movement and the movement outcome. The
primary goal for the cerebellum is to minimize this error signal. An imaging study by Miall and Jenkinson (2005) showed that
cerebellar activations represented a predictive signal used for error correction. Given the known role of the cerebellum in
providing an error signal necessary for updating the sensorimotor mapping in response to a gradual visuomotor distortion,
findings from Kagerer et al. (2006) implicated compromised cerebellar function in children with DCD.
Regardless of emerging behavioral evidence relating cerebellum and DCD, the neuroimaging data are desperately
deficient. In one recent functional MRI study, Zwicker et al. (2011) measured brain activation when seven children with DCD
and seven age-matched controls performed a trail-tracing task. Behaviorally, there were not statistical differences on the
motor performance changes (i.e., tracing errors, time per tracing, number of trace completed, all p > 0.23; Zwicker et al.,
2011) between groups. However, blood-oxygen-level-dependent (BOLD) signals revealed that children with DCD had less
activation in the right cerebellar crus I, left cerebellar lobule VI and IX, bilateral inferior parietal lobules, and right middle
frontal gyrus compared to controls (p < 0.005 corrected). Although the results may be limited by its small sample size, to our
knowledge, this is the first task-related functional MRI study supporting the close relationship between cerebellar under-
recruitment and poor motor performance in DCD. In a clinical case study, structural MRI confirmed the cerebellar
involvement in a 19-year-old patient with DCD with minor ataxia and other behavioral problems, indicating functional
disruption of the cerebellum (Marien, Wackenier, De Surgeloose, De Deyn, & Verhoeven, 2010). Future brain imaging studies
using motor learning tasks will be critical to further understand the importance of cerebellum on motor learning deficits and
pathophysiologcial mechanisms of DCD.

3.2. Basal ganglia hypothesis

It is known that the basal ganglia plays a key role in motor control and learning (Doyon & Benali, 2005; Doyon, Penhune, &
Ungerleider, 2003). In terms of brain development, the basal ganglia and thalamus mature earlier than most areas of the
cerebral cortex (Chugani, Phelps, & Mazziotta, 1987; Huttenlocher, 1990) while the cerebellum develops slower and later
than most of other areas of the brain (Giedd, 2001; Griffiths et al., 2004; Huttenlocher, 1990). Although the basal ganglia
mature earlier than most areas of the cerebral cortex (Chugani et al., 1987; Huttenlocher, 1990), converging evidence
suggests the possible involvement of basal ganglia in DCD.
Groups of studies reveal that children with DCD have poor motor performance that relies on basal ganglia function,
such as force control (Pitcher, Piek, & Barrett, 2002; Smits-Engelsman et al., 2008) and motor sequence learning (Gheysen
et al., 2011). For example, Oliveira, Shim, Loss, Petersen, and Clark (2006) found that children with DCD showed larger
variability than typically developing children in the constant thumb-index finger pinching torque production. Jucaite
et al. (2003) has reported that children with DCD could not properly scale grip forces. Gheysen et al. (2011) reported that
children with DCD could not significantly improve their performance in a spatial sequence learning task. In an adaptation
study, although children with DCD, as a group, could effectively adapt to an abrupt visuomotor perturbation, there were
several individuals with DCD that showed poor adaptation in the abrupt condition, a phenomenon that was similar to
patients with Parkinson’s disease (Contreras-Vidal & Buch, 2003). Lundy-Ekman et al. (1991) revealed that children who
presented soft neurological signs of basal ganglia dysfunction were selectively impaired on force control tasks. In
contrast, children who presented cerebellar signs were selectively impaired on tasks that required precise timing. It
seemed that there was at least a subgroup of children with DCD, whose learning deficit might be attributable to the
function of basal ganglia. Unfortunately, to date, there is lack of neuroimaging data supporting abnormality of the basal
ganglia in children with DCD.

3.3. Parietal hypothesis

Besides the hypotheses on the compromised subcortical functions in DCD, suboptimized cortical functions have also been
proposed recently. One of those is the parietal region. Frontal–parietal connections have been considered to be involved in
serial processing of sensory motor transformation and learning (such as visuospatial processes during motor skill learning;
Burnod et al., 1999). Multiple studies have revealed poor visual spatial processing in children with DCD (de Oliveira & Wann,
2010; Wilson & McKenzie, 1998). For example, de Oliveira and Wann (2010) asked participants with and without DCD to
perform a steering motor task where the visual information was manipulated during motor execution. The DCD group
moved significantly slower and was more variable than the control group. The authors argued that suboptimal parietal and
cerebellar networks in DCD is due to poor visual spatial integration for online movement controls and poor motor
preparation.
While the involvement of parietal area in visuomotor adaptation and sequence learning is clear (e.g., Bo, Peltier, Noll, &
Seidler, 2011; Seidler, Noll, & Chintalapati, 2006), few brain imaging studies focus on the parietal dysfunction in DCD. As
discussed in Section 3.1, Zwicker et al. (2011) reported under-activated frontal–parietal and frontal–cerebellar networks
when children with and without DCD performed a trail-tracing task in a functional MRI study. In another joystick-tracing
experiment, Kashiwagi, Iwaki, Narumi, Tamai, and Suzuki (2009) reported lower brain activation in the left posterior parietal
cortex and postcentral gyrus. Abnormal functional connectivity has also been found in the parietal-related networks in DCD
2052 J. Bo, C.M. Lee / Research in Developmental Disabilities 34 (2013) 2047–2055

(Querne et al., 2008). These studies suggest that the suboptimal parietal function may be another neural underpinning of
impaired motor skill in DCD children. However, the effect of these areas on motor skill learning is far less clear. Future work
will be needed to verify this hypothesis.

3.4. Other areas

Several other brain areas besides basal ganglia, cerebellum, and parietal networks have been proposed in DCD recently.
For example, Querne et al. (2008) has claimed that abnormal brain hemispheric specialization due to the imbalanced
communication at the corpus callosum. However, de Castelnau, Albaret, Chaix, and Zanone (2008) did not find abnormal
interhemispheric communication based on the spectrum electroencephalography (EEG) coherence between left and right
central motor sites. Significant higher coherence was only found between fronto-central regions in a group of 8 and 9 year
old children with DCD, suggesting impaired frontal function. Other proposed areas related to DCD include insula (Hadjikhani
& Roland, 1998), anterior cingulate, and dorsal lateral prefrontal cortex (Banati, Goerres, Tjoa, Aggleton, & Grasby, 2000). The
functions of these areas in motor learning need to be extensively tested.

4. Discussion

Converging evidence have suggested that poor motor performance in children with DCD may be attributed to disrupted
brain function (e.g., Ivry, 2003; Querne et al., 2008; Zwicker et al., 2011). In addition, some evidence suggests that children
with DCD have learning deficits that rely on basal ganglia function such as sequence learning (e.g., Gheysen et al., 2011).
Others indicate that children with DCD have difficulties in adaptation similar to that observed in patients with cerebellar
lesion (e.g., Kagerer et al., 2006). Recent evidence supports the idea that abnormal frontal–parietal networks play a
significant role in impaired motor performance in children with DCD (e.g., Zwicker et al., 2011). However, the role of parietal
area in learning deficit is not clear yet. Here, we highlight three overarching aspects for future studies that will help us to
understand the underlying mechanisms of learning deficits in DCD.

4.1. From behavioral to neuroimaging studies

Most evidence suggesting compromised brain functions in DCD is based on behavioral studies. Only a few
neuroimaging studies can be found. Most of them employed simple motor performance tasks that do not have clear
learning components (e.g., performance changes over practice in Zwicker et al., 2011). Thus, determining the neural
mechanisms of learning deficits has lagged far behind. This may in part be due to the complexity of the performance (e.g.,
confounds of age differences in behavioral tasks) and the constraints (e.g., attention span, anxiety, and excessive head
motion) associated with most of brain imaging technologies in the pediatric population. Recently, some new procedures
have been developed, which open a window to understand the neural bases of special populations. For example, resting
state functional connectivity (fcMRI) measures regions with similar functions and known anatomical connections that
have strong correlations in the low frequency BOLD signals. It is a completely non-invasive technique with fast data
acquisition. It allows more integrative assessments of brain networks instead of isolated regions and does not contain
confounds of age differences in task difficulty effects that often complicate interpretation of task-driven fMRI. Future
results from neuroimaging studies are very critical in enhancing our knowledge on the neural specificity of learning
deficits in DCD.

4.2. From group-comparisons to subtypes of DCD

The issues of DCD subtypes can also be addressed with more neuroimaging studies. Multiple behavioral evidences
indicate subtypes of DCD with a dominant one being related to compromised cerebellar function (e.g., Ivry, 2003). Other
types have been associated with disrupted basal ganglia function (e.g., Lundy-Ekman et al., 1991), abnormal frontal–parietal
network, and imbalanced cross-hemispheric communication (e.g., Zwicker et al., 2011). It is known that these networks (i.e.,
cortico-striatal, cortical–cerebellar, and frontal–parietal) are critical for motor learning, but there is no clear evidence to
show how these networks relate to subtypes of DCD.

4.3. From lab-based learning to intervention strategies

Lack of understanding of the neural mechanisms of DCD may also explain why children with DCD are likely to have
continuing difficulties despite progressive interventions (e.g., Green, Chambers, & Sugden, 2008). Earlier interventions in
DCD focus on intensive motor practice (Burns, 1962; Freeman, 1914). Later process-oriented interventions normally
include a wide variety of tasks with a hope to have successful generalizations across all motor skills even if the intervention
has little relationship to the deficits, e.g., handwriting (Weintraub, Yinon, Hirsch, & Parush, 2009). Due to the heterogeneity
of DCD, it is not surprising that these interventions, which mostly rely on behavioral evidence, have limited success
(Cermak & Larkin, 2002; Mandich, Polatajko, Macnab, & Miller, 2001; detailed reviews see Barnhart, Davenport, Epps, &
Nordquist, 2003; Wilson, 2005). We believe that the understanding of the neural specificity of an individual with DCD is the
 J. Bo, C.M. Lee / Research in Developmental Disabilities 34 (2013) 2047–2055 2053

key for successful evaluation, diagnosis, and intervention. Further studies focusing on long-term clinical outcomes should
be emphasized.

4.4. Final notes

Children with DCD frequently co-morbid with other developmental disorders, such as ADHD (Wilson et al., 2004),
learning disabilities (Jongmans, Smits-Engelsman, & Schoemaker, 2003), dyslexia (Fawcett & Nicolson, 2007; Iversen, Berg,
Ellertsen, & Tonnessen, 2005), and speech language impairment (Alloway & Archibald, 2008). Studies have reported that as
high as 50% of children with DCD meet the diagnostic criteria for ADHD (Kadesjo & Gillberg, 1999; Wilson et al., 2004). Up to
50% children with dyslexia showed motor problems that were very similar to DCD (e.g., Iversen et al., 2005). Over half of
children with DCD performed similarly to children with specific language impairment in measures of expressive language
(Alloway & Archibald, 2008). Moreover, some children with DCD may have more than one co-morbid disorder (Lingam et al.,
2010; Tseng, Howe, Chuang, & Hsieh, 2007). The issues of co-morbidities can significantly impact the research findings,
symptom presentations, severity, and prognosis of DCD. Thus, it is important to recognize and differentiate the co-
morbidities while we discuss the neural networks of DCD (e.g., Fawcett & Nicolson, 2007).
Finally, it is important to note that there is no straightforward linkage between brain structure and observed behavior.
The development of motor skill learning is the product of dynamic processes involving interactions among different kinds of
factors from genetics to environment. Behavioral studies are just the first step toward examining the hypotheses that
compromised brain function might play an important role in the motor learning deficits in DCD. Additional neuroimaging
studies would be extremely valuable in matching neural sources to behavioral performance for a clearer understanding of
the underlying mechanisms in learning deficits. The understanding of relationships between behaviors and brain functions
will enhance our knowledge of the neural mechansims of DCD and set a foundation to examine neural plasticity in future
studies.

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