developmental coordination disorder: core sensori-motor deficits, neurobiology and etiology

Neuropsychologia ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Developmental coordination disorder: core sensori-motor deficits,neurobiology and etiology

Alice Gomez a,b,n, Angela Sirigu a

a Centre de Neuroscience Cognitive, CNRS, UMR 5229, 67 Boulevard Pinel, 69675 Bron, Franceb Université Claude Bernard Lyon 1, ESPE, Lyon, France

a r t i c l e i n f o

Article history:Received 25 May 2015Received in revised form24 September 2015Accepted 25 September 2015

Keywords:Motor disabilityEtiologyNeuropsychologyGeneticClumsinessDyspraxiaBrain bases

x.doi.org/10.1016/j.neuropsychologia.2015.09.032/& 2015 Published by Elsevier Ltd.

esponding author. Fax: þ33 4 37 91 12 10.ail addresses: [email protected] (A. Gomsc.cnrs.fr (A. Sirigu).

e cite this article as: Gomez, A., Siriogy. Neuropsychologia (2015), http:/

a b s t r a c t

Among developmental disorders, DCD is one of the least studied and less understood one (Bishop, 2010).This review summarizes the current understanding of developmental coordination disorder in neu-ropsychology with a focus mainly on high level sensorimotor impairments, its etiology and its neuralbases. We summarize these core deficits in the framework of an influent motor control model (Blake-more et al., 2002). DCD has several environmental risk factors which probably interplay with geneticfactors but those have not been sufficiently identified. High-level sensori-motor deficits are probablymultifactorial in DCD and involve predictive coding deficits as well as weaknesses in perceptual andsensory integration. At the brain level, DCD is associated with impaired structure and functions withinthe motor network. Throughout the review we highlight exciting new findings as well as potential futurelines of research to provide a more comprehensive understanding of this disorder.

& 2015 Published by Elsevier Ltd.

This review summarizes current knowledge regarding Devel-opmental Coordination Disorder (henceforth, DCD) by using a le-vel-of-analysis framework (Pennington, 2002). The guiding prin-ciple behind this framework is that a complete explanation of anydisorder- or indeed, of any atypical developmental phenomenon-requires understanding of the phenomenon across multiple levels:its defining symptoms or behaviors; its etiology, or distal causes,including genetic and environmental factors; its neuropsychology(underlying cognitive processes that are not directly observableand not part of the disorder’s definition); its pathophysiology(changes in brain structure and function). This framework postu-lates that no level is fully reducible to a “lower” level because ofthe emergence of new phenomena as systems become increas-ingly complex, and no level has priority over the others in terms ofscientific value.

The sections below cover DCD's definition and etiology, neu-ropsychology and brain bases. We particularly highlight futuredirections that should be undertaken in this domain and actuallimits of the research conducted so far.

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gu, A., Developmental coor/dx.doi.org/10.1016/j.neurop

1. Definition of developmental coordination disorder

DCD is a neurodevelopmental disorder which indicates thatsymptoms must begin in the early developmental period and notbe acquired through lesions. According to the Diagnostic andStatistical Manual (DSM) IV-TR, individuals with DCD have markedimpairment in the acquisition and performance of coordinatedmotor skills given the child’s chronological age and appropriateopportunities for skill acquisition. The marked impairment has asignificant, negative impact on activities of daily living- such asdressing, feeding, riding a bicycle- and/or on academic achieve-ment such as poor handwriting skills which is one of the mostcommon reason for referral to occupational therapy service as itcan have strong academic consequences for children with DCD (Boet al., 2014; Chang and Yu, 2010; Cheng et al., 2011; Huau et al.,2015; Jolly and Gentaz, 2013, 2014; Jollyet al., 2010; Pruntyet al.,2013, 2014; Rosenblum and Livneh-Zirinski, 2008; Rosenblumet al., 2013). These impairments occur despite any medical con-dition such as cerebral palsy, hemiplegia or muscular dystrophyand any mental retardation1 (American Psychiatric Association,2000). It is a chronic disorder in the sense that adolescents andadults still suffer from this condition (e.g., Cantell et al., 2003;Losse et al., 1991), with considerable consequences in daily life and

1 or the motor difficulties should be in excess with the assumed risk of motordifficulties expected in mental retardation.

dination disorder: core sensori-motor deficits, neurobiology andsychologia.2015.09.032i

www.elsevier.com/locate/neuropsychologia

http://dx.doi.org/10.1016/j.neuropsychologia.2015.09.032



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A. Gomez, A. Sirigu / Neuropsychologia ∎ (∎∎∎∎) ∎∎∎–∎∎∎2

academic achievement.Prevalence estimates are definition dependent2. Using the

DSM-IV at 7 years of age in the UK population the prevalence ofDCD was estimated at 1.8% of the population with strict 5th centilecutoffs and up to 5.5% with the 15th percentile cutoff (Lingam etal., 2009). Future studies may provide increased prevalence withnew defining criteria including low IQ as proposed by the DSM-53.However, in Lingam's study exclusion of children with an IQo70were not expected to alter significantly the prevalence. There is arelatively small but significant male predominance (1.9:1–2.8:1males to females, Faebo et al., 2013; Lingam et al., 2009).

Nonetheless, DCD is still underecognized by healthcare andeducational professionals (Peters et al., 2001). Research is sig-nificantly behind compared to similar neurodevelopmental dis-orders (Bishop, 2010). Interest in this pathology has increased andhas concentrated under the term of DCD. In fact, Pubmed refer-encing of the term Developmental Coordination Disorder hasnearly tripled over the last decade compared to the previous one,from 133 ref./y. up to 332/y.

To provide a complete overview of the different level of ana-lysis, we now turn to the etiology of DCD. The genetic but also thesocial and cultural context provide interesting highlights on themechanisms responsible for this disorder and highlight potentialremediation that could be embraced in the future.

2. Etiology

Since DCD is defined as a continuous disorder, it does not ne-cessarily have one discrete etiology, unlike Down syndrome(which reflect a mutation in a single gene), and thus its boundarieswith other continuous disorders have been questioned.

2.1. Insights from comorbidities, co-occurrence

“It is an unusual child whose atypical development is limited to asingle area”

(Kaplan et al., 2001, p. 556)One of the main comorbidity of DCD has been estimated to be

ADHD with an overlap ranging between 35 and 50% of the cases(Dewey et al., 2002; Ghanizadeh, 2010; Kadesjö and Gillberg, 1999;Kaplan et al., 2006; Loh et al., 2011; Martin et al., 2006; Piek et al.,1999). Another very common comorbidity is Specific LanguageImpairment (SLI) with an overlap estimated at 32% and readingdisorders (Flapper and Schoemaker, 2013; Hill, 1998; Kaplan et al.,2006; Scabar et al., 2006). Other comorbid disorders have beenidentified such as ophthalmic abnormalities (Creavin et al., 2014),Joint hypermobility syndrome (Kirby et al., 2005; Kirby and Davies,2007) and migraines (Esposito et al., 2012).

2 Essentially all behaviorally defined disorders, including DCD, are continuousdisorders, in the sense that they do not represent categories (so that you eitherhave the disorder or you do not), but just extremes on a continuous distribution.DCD is mainly defined as the low end of a normal distribution of motor skills. Thus,in order to diagnose the disorder, a somewhat arbitrary cutoff must be set on acontinuous variable. This cutoff greatly varies across studies ranging from the 5thpercentile to the 20th percentile for instance, which may have incidence on theestimated prevalence but also for comparisons across studies.

3 The previous version of the Diagnostic and Statistical Manual of MentalDisorders (DSM (version IV-TR; APA 2000) required that motor skills achievementbe below the level expected for both age AND IQ. The most recent version of theDSM (DSM-5, APA, 2013) now requires that motor skills be below age expectationsonlyThe logic behind the IQ-discrepancy definitions is that the cause of poor motorskills might differ between low-IQ and normal or high-IQ. In DCD no research hasbeen conducted on the impact of low or high IQ on etiology and treatment effectsfor instance. This is not surprising given that norms to identify a child with a motordifficulties in excess given mental retardation have only recently been published(Smits-Engelsman and Hill, 2012).

Please cite this article as: Gomez, A., Sirigu, A., Developmental cooretiology. Neuropsychologia (2015), http://dx.doi.org/10.1016/j.neurop

Clinical samples studies have shown that motor impairmentsco-occur with other neurodevelopmental disorders in 40% of thecase (Lingam et al., 2010; Pieters et al., 2012a, 2012b). The pre-valence of motor difficulties in other neurodevelopmental dis-orders have also been examined, in particular in reading disability(Fawcett et al., 1996; Fawcett and Nicolson, 1995; Nicolson andFawcett, 1994) and socio-emotional disorders (Cairney et al., 2010;Green et al., 2006; Pieters et al., 2012) such as Autism SpectrumDisorder (Gillberg and Billstedt, 2000; Matson et al., 2011; Minget al., 2007). For instance, Ming et al. (2007) tested 154 childrenand adolescents with autism from 2 to 18 years old. They foundthat gross motor delay was reported in 9% and apraxia in 34% ofchildren with ASD. The author suggest that some potential pa-thophysiological mechanisms of ASD such as abnormal transmis-sion in serotoninergic, dopaminergic and GABAergic systems (Fa-nelli et al., 2013; Gadow et al., 2014; Man et al., 2015) could beresponsible for these poor motor performance. Hence, these largesamples studies suggest that motor impairments are likely asso-ciated to other cognitive deficits in large samples.

An intriguing question is what kind of relationship exists be-tween these co-occurring disorders?

Regarding the mechanisms of comorbidity, disorders comorbidwith a given condition could be (a) coincidental, (b) causally di-rectly related, one condition leading to the other one or(c) causally indirectly related, another underlying cause leadingboth to the comorbid disorder and (d) the cognitive sub-types (SeeFig. 1 Gillberg and Billstedt, 2000; Kaplan et al., 2006). This in-direct causality can also be referred to as the common etiologyhypothesis which states that there is a shared etiological basis (forinstance genetic) for both disorders and that the more severeform, will result in a combination of both disorders. Finally, thecognitive subtype hypothesis suggests that comorbid develop-mental disorders are a third disorder due at least in part to etio-logical factors that are distinct from those that increase suscept-ibility for a single disorder alone. Therefore, this hypothesis

Fig. 1. Conceptual models of relationships between coexisting disorders. (a) Co-incidental disorders with independent etiologies; (b) direct causality of disorderswith one disorder leading to another disorder; (c) Indirect causality, with onecommon etiology leading to both disorders; (d) the cognitive sub-types hypothesiswith unrelated etiologies for each separate disorders as well as a third etiologyleading to the comorbidity.





4 A stimulating home with “availability of stimulating play materials”.

A. Gomez, A. Sirigu / Neuropsychologia ∎ (∎∎∎∎) ∎∎∎–∎∎∎ 3

predicts that the comorbid group will exhibit a different pattern ofexternal correlates than a simple additive model of each disorderseparately (Gillberg and Billstedt, 2000).

Research to characterize the mechanisms involved in the re-ported comorbidity are only starting and to date, more attentionhas been paid to its overlap with ADHD (for a review, Goulardinset al., 2015). Existing results support the view that ADHD and DCDmay have different etiology. For instance, studies on the under-lying anatomical substrate of the DCD ADHD comorbidity haveshowed that children exhibiting both DCD and ADHD showedpatterns of white matter connectivity which can be seen as asimple addition of DCD plus ADHD (Langevin et al., 2014). More-over, the co-occurrence of DCDþADHD has been associated with adistinct global pattern of regional cortical thickness decrease,highlighting the unique neurobiology of these comorbid neuro-developmental disorders (Langevin et al., 2015). However, the di-rect or indirect causality hypothesis cannot be fully discarded yet.Further studies are necessary on the overlap of neuropsychologicalprocess between DCD and ADHD for instance. Moreover, futurestudies will need to assess if the other mentioned comorbid dis-orders share common or distinct etiologies with DCD.

It is clear from this review that comorbidity is common, if notthe rule in DCD. First, this may have important clinical implica-tions: comorbidity is to be expected and looked for, whenever adiagnosis of DCD is made, to allow proper treatment. For instance,if DCD is the only diagnostic made in the case of a co-occurrentDCDþADHD, it is likely that stimulant medication will not be of-fered when they could help. Second, this has implication for futureresearch: small-scale studies on brain bases or neuropsychologicalprocesses should include ‘pure’ cases (DCD alone group) and caseswith comorbid disorders (DCD with a comorbid disorder group) tofurther our understanding of the specificity of this disorder, itsmechanisms and etiology; Genetic linkage studies are needed tosearch for chromosomal regions that may contain a gene or genesthat increase risk of comorbid disorders.

The etiology of developmental coordination disorder is cur-rently thought to be multifactorial as no single cause has beenidentified. Based on the above-mentioned and on clinical reports,both genetic and environmental influences have been suspected.We will now review available evidence and discuss their potentialinterplay.

2.2. Environmental influences

2.2.1. Socio-economic influenceThe effect of SES on motor skills has recently received attention

due to the potential repercussions of DCD on health, as it has beenidentified as an obesity risk factor (for a review, Hendrix et al.,2014; Lifshitz et al., 2014; Zhu et al., 2014).

Socio-economic status has been associated with motor skills (aswith almost all other measures of achievement) and in return,developing fundamental motor skills facilitates successful aca-demic achievement (Bradley and Corwyn, 2002). The studiesavailable have repeatedly observed a greater risk of low motorskills in families with lower socio-economic status with 21% of theestimated Movement Assessment Battery for Children (M-ABC,one of the standard battery for the diagnosis of poor motor skills,Henderson and Sugden, 1992) score variance accounted by the SES(Birnie et al., 2011; Faebo Larsen et al., 2013; Hardy et al., 2012;Valentini et al., 2014). However, it also says that we can considerthat more than 79% of the variance in motor skills is independentof SES and thus many children from disadvantaged backgroundswill develop strong motor skills while many children with weakmotor skills will come from advantaged families.

Using the DSM procedure, Lingam and colleagues showed thatseveral economic parameters (such as rented housing tenure and


lower maternal socio-economic group) increased the risk of DCDassessed with sub-scales of the M-ABC (2009).

The reasons for such impact of the SES on DCD are still elusive.The socio-economic status probably modify several environmentalvariables that adversely affects motor skills development such ashome affordances4 for instance (Miquelote et al., 2012). Somespecific environmental factors can directly influence motor skillsdevelopment, such as environment affordances, availability ofstimulating play materials, sleeping position, equipment, access tosports activity, quality and nature of physical fitness education(Miquelote et al., 2012; Myer et al., 2015; for a review, Pin et al.,2007; Saccani et al., 2013). Importantly, although these above-mentioned research tell us about environmental causes of in-dividual differences in motor skills, it does not tell us about theextent to which particular environmental treatments (such asproviding a systematic guidance in home affordance and advicesregarding physical fitness) may help reduce the risks of developingDCD (Saccani et al., 2013).

2.2.2. Cross-cultural influenceAlthough research on developmental coordination disorder

was initially confined to developed world and in particular to theUK and USA, some interest has been paid to the nature of devel-opmental coordination disorder across countries.

Several studies assessed the potential cross-cultural factorsindicative of cultural differences in motor skills development(Lebanese: Ammar et al., 2013; Israel: Engel-Yeger et al., 2010; e.g.,Portuguese: Lopes et al., 2012; Japan: Nakai et al., 2011; Brazilian:Valentini et al., 2014). Overall, the studies suggest that the socio-economic status which can be different across countries greatlyimpact factors such as availability of stimulating play materialsetc.. However, across developed countries, the prevalence acrosscountries is also found to greatly vary : using a 12th percentilecutoff, the prevalence of DCD was estimated at 8% in the Canadianpopulation and 19% in the Greek population suggesting that life-style and culture may also impact the level or motor coordination(Tsiotra et al., 2006). The difference across these countries hasbeen ascribed for instance to the relatively inactive lifestyle ofGreek compared to other countries.

These studies raise the question of whether the criterion usedshould be lowered or increased in different countries, or if itshould remain an absolute standard. At the moment there is noworld-wide criterion-referenced test for DCD. Furthermore, assuggested by Niemeyer and colleagues, future research shouldhelp describe what it means that the “child is given enough op-portunity for skill learning and use of skill”, given their culturalcontext.

2.2.3. Natal and perinatal and other risk factorsOther factors have been suggested as risk factors such as pre-

mature birth, low birth weight and postnatal steroids exposure(for a recent meta-analyses, Edwards et al., 2011; Faebo Larsenet al., 2013; Zwicker et al., 2013). For instance, the study by Larsenand colleagues assessed several determinants of developmentalcoordination disorders concerning the child, including sex, in-trauterine growth restriction, gestational age at birth; concerningthe mother, age at conception, occupational status during preg-nancy, smoking during pregnancy, tobacco use, alcohol use duringpregnancy. They showed that children born preterm had poorermotor development than born term or post-term especially whenborn very preterm, but toxic use for instance did not reveal as arisk factor (Faebo Larsen et al., 2013). Future studies might try toassess if the neurocognitive deficits can be distinguished on the






basis of environmental influences by comparing for instancechildren with DCD born preterm to children with DCD born atterm.

Using a monozygotic twin study, Pearsall-Jones and colleagues(2009) showed that second-bor monozygotic twins aged from 8 to17 have twice as many chances to meet the criteria for DCD thanfirst born. Seven of the 9 twins who met the criteria for DCD ex-perienced perinatal oxygen perfusion problems. The use of co-twincontrol, or twin-differences design such as this one, provides aunique mean to control for potentially confounding factors such asgenotype, gender, age, SES and shared family environment andsuggest that perinatal hypoxia may be a relevant risk factor.

Beyond these environmental influences, genetic influences arestill not well understood in this pathology.

2.3. Genetic and genetic environment interplay

Only two studies have focused on the genetic etiology of DCD,and they both questioned the potentially shared genetic etiologyof DCD and ADHD (Fliers et al., 2009; Martin et al., 2006). How-ever, although both studies showed a high shared heritability ofADHD and probable DCD (ranged from 0.29 to 0.51), only Martinand colleagues showed a high heritable component of 0.69 forprobable DCD in a population-based twin sample5. They also no-ticeably highlight a common family environment contribution tothe determinants of DCD (some of which have been noted pretermbirth, perinatal experiences, and interactions in the home).

Behavioral geneticists should further document the heritabilityof this disorder using real motor testing rather than self-ad-ministered questionnaires. Moreover, molecular genetic may try toidentify potential risk loci through replicated linkage studies.Candidate genes which affect other developmental disorders suchas dyslexia may be analyzed (e.g., DYX1C1, DCDC2, KIAA0319 andROBO1). In fact, these loci have been shown to play a specific rolein brain development in rodents, specifically in neuronal migra-tion and the formation of connections once neurons reach theirfinal destination in the brain.

Genetic determinant of reading disorder may also be assessedin children with DCD given the involvement of the following genesin motor coordination and the high prevalence of comorbidityfound between DCD and reading disorders (see for instance, Vi-holainen et al., 2011).

Because there are genetic influences on individual differencesthat impact people's ability to achieve higher levels of education,income, and occupational status, SES impact might not solely bean environmental construct (Baker et al., 1996). In fact, given thatsome aspects of motor ability are predictive of future cognitiveabilities, the relationship between low SES and higher DCD mightreflect the difficulties of parents' with poor motor skills to reachhigh SES (Burns et al., 2004; Murray et al., 2006; Piek et al., 2008).

Thus, the SES-low skills association may be due to a thirdvariable: genes shared by parents and children that influencemotor skills or cognitive abilities more broadly. A more complexrelationship at the intersection of genes and environmental in-fluence may exist. The fact that low and high professions havebeen related to poor motor skills might suggest different gene andenvironmental influences. In fact, it is possible that children withDCD in higher socio-economic status families may be more ge-netically determined than children from lower SES families, asfound in other neurodevelopmental disorders, such as dyslexia.Children with dyslexia in higher socio-economic status familieswere found to be more genetically determined than children from

5 In fact, twin studies allow to control some of the environmental contributionsto the disorder.


lower SES families (Friend et al., 2008). Such result would high-light the critical role of the society to provide adapted educationfor such vulnerable children.

Overall, environmental and genetic influence on the etiology ofDCD is only starting to be unraveled. On the other hand, char-acterization of neuropsychological deficits has already advanced inthe last century and researchers are starting to identify core sen-sori-motor deficits.

3. Neuropsychology

3.1. History

3.1.1. TerminologyIn the literature, descriptions of children with motor co-

ordination difficulties and clumsy movements have been largelydiscussed in the last century (Ford, 1966; Geschwind, 1975; Gub-bay et al., 1965; Lesny, 1980). First, several authors used the termchild dyspraxia to discuss the disorder (Ajuriaguerra and Hecaen,1964) because they theoretically referred to the constructionalapraxia of adults (Ajuriaguerra and Hecaen, 1964). But this historyof description often lead to the confusion that DCD can be reducedto a simple child version of adult apraxia. However, apraxia is anacquired disorder due to brain damage often located in the leftparietal lobe, the pre-motor cortex, the temporal or the supple-mentary motor area (e.g., Buxbaum et al., 2014, 2003; for a recentreview, Goldenberg, 2009) whereas DCD or dyspraxia is a devel-opmental disorder. However, as mentioned above, children appearto fail to ever acquire the ability to perform age-appropriatecomplex motor actions. A modular approach to cognitive abilities(Fodor, 1983, 1985; Pinker, 2005) suggest that domain-specificabilities can function independently of one another, and can beseen to be dissociated in cases of adult neuropsychological pa-tients. One of the difficulty child neuropsychologist have facedwhen trying to characterize neurodevelopmental disorders such asWilliams syndrome or DCD is the lack of clear double dissocia-tions. In fact, it is possible that a core cognitive deficit which ap-pear early in the development will impact the development ofother cognitive abilities, as such when assessing a young child oran adult it becomes difficult to distinguish between core cognitiveimpairments and cascading impairments (Karmiloff-Smith andFarran, 2012b; Karmiloff-Smith et al., 2003). This problem existswith DCD as well.

Moreover, there still exists a difficulty in medical and scientificcommunities in using a common terminology given its historicalbackground (Vaivre-Douret, 2014). A survey of health and educa-tional professionals showed widespread uncertainty about thedefinition of, and distinction between them (Peters et al., 2001).Nowadays, however, since its adoption at the Leed consensus, DCDis the term preferred among scientists (Sugden, 2006).

3.1.2. Clustering and subtypes?To date, no subtyping exists in the DSM-V. In the scientific

literature, the process of subtyping can be summarized by the factthat about each different study has yielded a different subtypingand are at best inconclusive (Vaivre-Douret, 2014; Visser, 2003,2007), in particular because heterogeneous sets of tests are used.

An alternative to the subtyping approach is to consider thatimpairments that are not found in all children with DCD do notreflect a core deficit and that these impairments reflect secondaryacquired disorders which are a consequence of primary deficits assuggested by the neuroconstructivist approach (Karmiloff-Smithand Farran, 2012a).Subtyping studies should make a clear point todefine possible common etiology within a subtype or possiblecommon help from a remediation within a subtype to provide a






step forward. To date however, no such studies are available andstudies which exist have failed to show a differential outcome ofremediation tools based on subtyping (Green et al., 2008).

3.2. What is the core neurocognitive deficit of developmental co-ordination disorder?

In the following section, we will briefly survey different hy-potheses formulated on perceptual deficits and sensory-motorintegration in DCD. We will further focus on the predictive codingdeficit hypothesis6.

Deficits in other cognitive domains have been reported (such asmathematical, memory or “hot” executive functions impairments;e.g., Chen et al., 2013; Gomez et al., 2015; Rahimi-Golkhandanet al., 2015) but will not be reviewed here.

3.2.1. A perceptual or sensory-motor integration deficit?Perceptual modalities have been tested in children with DCD

with a particular focus on motor control, involving the visual (DeCastelnau et al., 2007; Gubbay et al., 1965; Hulme et al., 1982,1983; Lord and Hulme, 1987b; Schoemaker et al., 2001; Tsai et al.,2008; Van Waelvelde et al., 2004), and the kinesthetic modalities(Hoare and Larkin, 1991; Hulme et al., 1982; Li et al., 2015; Lordand Hulme, 1987a). Proprioceptive impairment in the localizationof tactile and double tactile stimuli have also been reported (El-basan et al., 2012).

3.2.1.1. Kinesthetic and visual-spatial deficits. Kinesthesia can bedefined as the conscious awareness of body position and motion(Li et al., 2015). The research on kinesthetic sensitivity in childrenwith DCD is rather inconsistent (Coleman et al., 2001; Lord andHulme, 1987a) and some authors argue that they probably do notdisplay kinesthetic impairments (Vaivre-Douret, 2014). Some au-thors suggest for instance that when kinesthetic test are passivethey do not distinguish children with DCD from control (Piek andColeman-Carman, 1995). Most research in fact has relied on thekinesthetic sensitivity test (Laszlo and Bairstow, 1980). However,this test has several drawbacks: 1) it requires cross-modal trans-formation and motor processing and hence the two measures maybe confounded, 2) it has been criticized for its discriminative va-lidity and accuracy (e.g., Doyle et al., 1986). Recently, Li and col-leagues (2015) have administered a k'nesthetic test, successfullyused in children and patients with Parkinson's disease (Konczaket al., 2007; Pickett and Konczak, 2009). They tested 30 childrenwith DCD aged 6–11 year with 30 typically developing (TD) chil-dren. Children were blinded and passively sensed a motion of theirarm with different speeds. They were asked to detect as soon aspossible when they sensed the motion7. The authors conclude thatchildren with DCD, which were slower than TD children to pas-sively detect a motion of their arm, have a kinesthetic defect.However, if the deficit is simply kinesthetic, it is unclear why nointeraction effect appeared between groups and condition (speedof motion) although performance did interact with age). In fact,speed of motion is a factor that facilitates the kinesthetic detec-tion; hence, one could expect that this facilitation would be par-ticularly beneficial to children with DCD who show a reducedproprioceptive sensitivity, like younger children. Hence, to date, nounquestionable evidence suggests that children with DCD have

6 A third line of research in the neuropsychology of DCD pertains to attentionaldeficits. However, this topic will not be reviewed in the neuropsychology section ofthe present article.

7 To control for processing speed difference across groups, a visual control taskwas used: children were asked to touch the screen as soon as they saw the Ledappear. This reaction time was subtracted from their decision time in the kines-thetic task to perform movement detection time analysis.


kinesthetic defects.In the visual domain, on the contrary, children with DCD are

less proficient than controls; they fail to discriminate shape, area,slope, line, length, and size constancy (Caçola et al., 2014; Chenand Wu, 2013; Elbasan et al., 2012; Hulme et al., 1982, 1983;Schoemaker et al., 2001). Tsai and colleagues recently assessed thevisual perceptual skills of 170 children (aged 9–10 yrs old) withDCD using the Test of Visual-perceptual skills (Non-motor) Revised(TVPS-R (Gardner, 1982)). They showed that children with DCDwere significantly impaired in all sub-tests (i.e., visual dis-crimination, visual memory, visual-spatial relationships, visualform constancy, visual sequential memory, visual figure-groundand visual closure). However, the construct and predictive validityof the test has been repeatedly questioned (e.g., Brown, 2008).Interestingly, a recent meta-analysis showed that children withDCD are impaired in processing visual-spatial information, evenwhen no motor component is involved (Wilson et al., 2013).However, to date the precise mechanisms underlying these deficitsremain unknown.

Within visual processing two distinct streams are often dis-tinguished, the dorsal for action and the ventral for perception(Milner and Goodale, 2008). This segregation in terms of cognitiveprocessing has also been proposed to be useful for the character-ization of neurodevelopmental disorders. In fact, it has been pro-posed that for vision, the dorsal stream may be more sensitive andmore likely to be impaired in neurodevelopmental disorders (e.g.,Grinter et al., 2010). Following this line of research, O’Brien et al.(2002) have tested 8 children with DCD (aged 7–11 yrs. old).Children were asked to detect if the target appeared to the left orto the right. Please note that in one condition the target was dis-played in an incongruent motion direction while in another (formcoherence condition) as a pattern of concentric circles. The authorsprovided evidence that children with DCD detect global form co-herence with a higher percentage of dots moving in the oppositedirection than TD children. However, this detection threshold isnot higher for perceiving global motion coherence. Although theauthors interpret the results as reflecting a ventral stream im-pairment, more recent fMRI studies indicate that these tasks ac-tivate both the ventral and the dorsal pathways. For instance, theyboth involve the intraparietal sulcus (Braddick et al., 2000; Man-nion et al., 2013). Hence, to refine our understanding of the un-derlying mechanisms responsible for impaired visual-spatial pro-cessing impairment, future studies should test in a more sys-tematic way visual perception in children with DCD with tasksclearly segregating processing of dorsal from ventral stream.

Current knowledge on visual perception does not clearly in-dicate whether the observed deficit pertained to a low-level purelyvisual impairment or whether it can be qualified as a spatial deficit(non-modality specific). The hypothesis of spatial perception def-icits would require a more complete evaluation of spatial or-ientation in 3-D environments, using non-visual orientation tasks(not just visual perception) (e.g., Gomez et al., 2012). To ourknowledge such studies have not been conducted in children withDCD although impairments in navigational space have been re-ported in similar pathologies such as cerebral palsy (Belmontiet al., 2015; Petrarca et al., 2013).

3.2.1.2. Noise in the sensory and in the motor system: cause or con-sequence?. When we execute the same motor command re-peatedly, every trial is slightly different from the other. Thisvariability of the motor execution is attributed to unpredictablefluctuations at the neural, neuromuscular or environment level.Noise in general is an inherent characteristic of many systems andin particular in the motor system (Friston et al., 2010; Friston,2010). Smits-Engelman and Wilson (2013) have proposed thatchildren with DCD may have an excessive noise in the






sensorimotor system. Several studies have shown that the pro-duction of motor commands in children with DCD are both morevariable and less accurate than that of TD children (for a reviewsee, Smits-Engelsman and Wilson, 2013). Smits-Engelsman et al.,2008 showed that during isometric force production tasks chil-dren with DCD were able to produce an isometric force but weremore variable than TD control even of younger age.

Moreover, as reported in Wilson and colleagues' large meta-analyses (2013), comparison of performance on postural controland gait in children with DCD and TD children revealed large effectsizes. In particular, they showed that variability in sway is muchhigher in DCD.

However, sensory noise also contributes to variability in esti-mating internal states of the body (e.g., the position of your hand)and external states of the world (e.g. location of the cup on thetable. One solution is to identify the weight of each factor (motorand sensory noise and disentangle the intricate relationship be-tween motor and sensory interaction) in a longitudinal follow-upstudy. Until then, the hypothesis of the noise in the sensory systemmust remain hypothetical and await for further investigations.

As we will see in the next section, this noise may be responsiblefor preventing children with DCD from learning (implicitly) fromtheir own motor system.

3.2.1.3. Sensorimotor adaptation tasks: error signal used for learn-ing. Sensorimotor adaptation tasks have been used to understandhow we learn to adapt our motor parameters to the sensoryfeedback. In healthy participants, a useful approach is to in-vestigate how motor performance changes when the relationshipbetween the effector and the visual sensory feedback of themovement is altered (Yavari et al., 2013). These classical sensor-imotor experimental task usually involve prism adaptation (e.g.,Redding et al., 2005) or distortion of feedback using computerprograms or virtual reality (Wright, 2014). A sensorimotor adap-tation is divided into three phases: a) a baseline performancewhere normal feedback is provided (e.g., normal pointing task), b)a distorted learning phase where the visual or proprioceptivefeedback of the hand is changed (e.g., pointing with prisms on), c)a post-learning trial where the feedback is returned to normal(e.g., takes the prisms off and points.). A measure of adaptation isprovided by the difference between the baseline trials and thepost-learning trials. The neural underpinning of this process isproposed to rely on the cerebellum. In fact, current stimulation ofthe cerebellum was shown to increase the adaptation rate in areaching task (Galea et al., 2011).

Surprisingly, few studies have assessed this sensorimotoradaptation in children with DCD. Kagerer et al. (2004, 2006) havesubmitted 6–10 years old children with DCD to a visuomotoradaptation tasks and to a center-out drawing test. In the normalcondition, children with DCD were more variable and had lowerspatial accuracy in their drawing than TD children. However, whenexposed to a visual feedback distortion (drawing was rotated 45°from normal during 60 trials), no after-effects were observable inthe DCD group compared to the TD group. The authors suggestthat the noisier initial visuomotor representation of children withDCD did not allow them to take advantage of error signals fromsensory feedback. Similar results have been reported using prismadaptation tasks in small samples of children with DCD (Cantinet al., 2007; Zoia et al., 2005). In a follow-up study with a largersample, Kagerer and colleagues (2006) performed again the visualfeedback distortion task by presenting a drawing rotated 60° fromnormal (larger than in the previous study) and with 126 learningtrials (more than in the previous study). They observed that, al-though initial motor noise was larger in the baseline condition,when the discrepancy was large enough (60°), children with DCDwere able to adapt and to show an after-effect. However, this after-


effect on several movement parameters (root mean square error,normalized jerk, initial directional error, movement length) stillseem smaller compared to that of the TD children with a similarnumber of trials (please note that statistical test of intergroup ef-fects on the after effect are not reported). Nevertheless, such in-terpretation needs to be taken with caution since a replication ofthis result using both auditory and visual feedback failed to find astatistical difference in the after effect between DCD and controlchildren. In fact, when assessing 6 children with DCD (aged 9–11yrs old) they observed that only 2 out of 6 in the auditory feedbackcondition and only 1 out of 6 in the visual condition did not exhibitan after-effect at all (King et al., 2011). However, this study hasseveral significant drawbacks: first, the sample size is again verysmall (6 subjects) and interpretations of a null effect must awaitstudies with larger sample; second, after effects in the visualcondition occurred after 9 normal auditory trials which can reducethe amplitude of the aftereffect in control children only for in-stance if they adapt faster than DCD children.

Two provisional conclusions may be drawn from these results:first, children with DCD may need larger sensory discrepancy togenerate error signal used for adaptation than TD children whichmay explain previous failure to observe adaptation to visuomotordiscrepancy. Second, even when the sensorimotor discrepancy islarge enough to generate an error signal and an adaptation, therate of learning may be different across groups and among chil-dren with DCD. In other words, even if they are able to adapt, theiradaptation may be slower than TD children. Future studies shouldassess whether children with DCD are able to adapt at the samerate than TD children on larger samples and by varying thenumber of learning trials. It is possible that the learning rate isslower in children with DCD to compensate for the noisier motorcommand generated. In such case, providing sensory error feed-back may help children with DCD to increase their reliance onsensory error generation and this it may possibly increase theirlearning rate.

3.2.1.4. A movement representation deficit?. To find the cause ofDCD one of the most prominent hypothesis has focused on themotor control systems and suggest that children with DCD maysuffer from a deficit of the internal modeling (IMD) of the move-ment (for a systematic review see, Adams et al., 2014). Accordingto this hypothesis, children with DCD have a difficulty in internallymodeling the spatiotemporal parameters for prospective actions, adeficit of movement feedforward ability and predictive motorcontrol (Wilson et al., 2004). This hypothesis relies largely onneuro-computational models of motor control which capture thecomplexity of perceptual-motor system and the various operationsnecessary to maintain adaptive control over time (e.g., Blakemoreet al., 2002; Wolpert and Flanagan, 2001; Wolpert, 1997). Re-searchers have provided several lines of evidence in favor of thishypothesis that are reviewed below.

3.2.1.5. Efference copy and double-step paradigms. A study byKatschmarsky and colleagues (2001) assessed the ability of 10children with DCD aged 7–11 to perform a double-step saccadetask compared to 10 TD children. In each trial, the participant isrequired tofixate two dots, presentedone after another. The posi-tion of the second dot appears shortly after the initiation of thefirst saccade. The idea behind this task is that the position of thesecond dot and the related motor command to reach its positionmust be programmed on the basis of the motor command or ef-ference copy of the first saccade. In fact, the estimated final state ofthe first saccade is not yet available when the double-step saccadestarts, moreover, intersaccadic interval was not different acrossgroups suggesting that both groups spent as much time on thefirst target (See Fig. 2). They observed that children with DCD were





Fig. 2. Double-step saccade paradigm (Hallett and Lightstone, 1976) adapted from Katschmarsky et al., 2001. Red diodes are first fixated during a jittered time between 900and 1300 ms then two red diodes are lit for a total duration of 240 ms. Saccades starting before 240 ms are excluded; the targets were extinguished before any eyemovement took place. This allows creating a dissonance between the retinal coordinates of the stimulus at B and the motor coordinates of the saccade to it: B was flashed inthe right visual field but had to be acquired with a leftward eye movement. Ensembles of saccades with an inaccuracy greater than 15% are excluded. Children with DCD areless accurate only for the second saccade. FP: Fixation point; A and B first and second diode. (For interpretation of the references to color in this figure legend, the reader isreferred to the web version of this article.)


less accurate than control only on the second saccade. The resultssuggest that children with DCD are unable to use the efferencecopy of the first saccade to construct a spatial representation of thesecond target location in order to generate an accurate saccadetowards it. Internal forward modeling in that case allows antici-pating the sensory consequences of a given saccade in the pre-sence of slow sensorimotor feedback.

This study provides strong evidence in favor of efference copyimpairment but replications are necessary given several limita-tions: 1) the small number of participants in each group; 2) thelack of visually guided double saccades condition, to insure thatchildren with DCD are able to perform adequately such tasks8.Moreover, an alternative interpretation in terms of a general im-pairment in the ability to generate saccades and to remember atarget cannot be fully discarded. In fact, the existence of a datatrimming procedure9 showed that more than 30% of trials in thecontrol group and 42% in the DCD group were excluded as none ofthe target was accurately fixated. Hence, one alternative inter-pretation is that in several cases the exact location of the secondtarget is not correctly remembered. In fact, Tsai and colleagueshave shown that a delay interval of only 3 seconds with only oneposition is sufficient to impair the recognition of children withDCD (Tsai et al., 2012). Hence, in this study, the generation frommemory (rather than the recognition, which is known to be easier)of two position interleaved with a delay of 1 s is sufficient to reach

8 Impairments have been recently observed in smooth saccade pursuit (Robertet al., 2014).

9 Saccades ensembles in which both targets were not obtained using a saccadethat fell within the 15% accuracy were rejected.


the limits of the children's visuo-spatial working memory.Another line of evidence in favor of the internal IMD hypothesis

relies on the rapid online correction paradigms which also involvethe use of efference copy. Because efference copy must be usedduring online movements, it does not require maintaining visuo-spatial information in memory.

3.2.1.6. Conscious rapid online correction paradigm: error signal usedfor online adjustment. The double step reaching paradigm requiresa target-directed touch movement to one or several targets whichremain visible at all times. In the majority of the trials the targetdoes not change location but in a small number of trials the targetjumps shortly after the movement onset. In that case, the targetlocation is visible at all-time but in unexpected jump trials theparticipant needs to update its motor plan to accurately reach thetarget. It is currently thought that this form of control relies on theability of the motor system to use predictive control processes –

that is, to generate a predictive estimate of limb dynamics throughan efference copy and thus to integrate this estimate (or forwardmodel) in real time with sensory feedback (Desmurget and Graf-ton, 2000, 2003). It has been shown that in the case of a (virtual)posterior parietal cortex lesion, patients are unable to correct areach trajectory in response to such unexpected target perturba-tion (Desmurget et al., 1999; Gréa et al., 2002), which suggest thatthis region plays a crucial role in this computation.

Three studies have reported a rapid online control task usingvisual perturbation in 7–13 years old children with and withoutDCD (Hyde and Wilson, 2011a, 2011b; Plumb et al., 2008). Hydeand Wilson excluded children with ADHD (2011a, 2011b) in bothstudies. They reported that children with DCD made more errors





10 gesture directed toward an object.


and had longer movement time on jump trials than controls.Moreover, kinematic analysis showed that DCD patients weresignificantly slower to correct the trajectory of their reaching awayfrom the initial target on jump trials. Their deficits may reflectthree cognitive impairments: 1) an inability to generate andmonitor forward estimates of the limb position that specify therelative position of the hand with respect to the target; 2) an in-ability to integrate or compare the error signal after visual per-turbation with the ongoing motor command or 3) an impairedability to update motor commands.

These studies have examined motor control in the presence ofovert and conscious visual perturbation. However, the onlinecorrection of motor command without conscious awareness hasnot been investigated. It is possible that children with DCD canexhibit similar levels of automatic online motor control whencorrection is unconscious. Researchers have showed that duringreaching imperceptible visual change of location which happenduring saccadic gaze displacement (when vision is temporarysuppressed) induce automatic updates in the motor command(Desmurget et al., 2001; Prablanc and Martin, 1992). This deviationin the movement hands are known to occur early and smoothly. Infact, modifying slightly the target location during gaze shift isthought to simply increase an error that is already present in thesystem due to the initial motor command being computed on thebasis of peripheral visual signal. These corrections to the initialcommand would rely on a parieto-cerebellar network (Desmurgetet al., 2001). For children with DCD it is possible that if the locationchange occurred without conscious experience (i.e., subliminalcondition), children with DCD may be able to update their motorcommand. In this case, the question of the role of motor awarenessas a necessary component to produce optimal motor correctionneeds to be raised.

Future studies may focus on the impact of conscious and un-conscious motor processes in children with DCD as already shownin psychiatric (Fourneret and Jeannerod, 1998; Georgieff andJeannerod, 1998) and brain damages patients (Slachevsky et al.,2003). For instance, to date no studies have examined the pre-sence of a normal readiness potential in children with DCD (Libetet al., 1983; Libet, 1993). Readiness potential, an electro-physiological marker of motor preparation, is the recordable cer-ebral activity that precedes a freely voluntary act and which pre-cedes the reportable time of appearance of the subjective experi-ence of “wanting” to move. In adults, the onset of this cerebralactivity precedes by at least several hundred milliseconds the re-ported time of conscious intention to act. However, it has beenshown that patients with lesions in the parietal cortex are able toreport when they move but not when they intend to movewhereas patients with lesions in the cerebellum are perfectly ableto monitor their intention to move (Sirigu et al., 2004). The par-ietal cortex therefore seems a key region for action prediction. Ifpredictive coding in children with DCD is impaired one then ex-pect that these patients may not get access to their intention tomove although being still able to report when their movementoccurred.

3.3. Gesture representation

3.3.1. Imitation, pantomiming, tool use, meaningless gesturesOne approach to the inability to conceptualize the action rather

than an inability to produce the motor act per se has been taken byneuropsychologist studying apraxia. In fact, patients with apraxiaare known to exhibit specific dissociation patterns in the pro-duction of pantomime gestures, performance of meaningful ges-ture on command and use of tools or objects (Buxbaum et al.,2005; Buxbaum, 2001; Goldenberg, 2009; Ietswaart and Evans,2014; Osiurak, et al., 2011; Sirigu et al., 1995). Impairments in


patients with apraxia are thought to reflect a deficit in maintainingor storing the visuo-spatial and features of a gestureact (Dapratiand Sirigu, 2006; Goldenberg, 2009). Studies of apraxic patientshave led to models of action such as the “gesture engram hy-pothesis”, where the production of an action must follow the ac-tivation of the sensorimotor representation of this action (Bux-baum, 2014; Heilman et al., 1982; Liepmann, 1920). Lesions studiesof apraxic patients have repeatedly showed that the performanceof meaningful gestures to command and pantomime of tool useare particularly vulnerable to parietal lesions for instance (e.g.,Buxbaum et al., 2005).

Following these results, one may wonder whether childrenwith DCD having a deficit in representing actions, they should alsofail in praxic tasks and in particular in the gestural appraisal oftools and objects utlisation. Studies of gestures in children withDCD have mainly used validated test to assess praxic abilities(Albaret and Castelneau, 2007; Berges Lézine, 1965; Vaivre-Douret,2014). One important aspect of the praxis motor test is that per-formance seems to increase with age, although no studies havedeeply investigated this issue. Some studies which have directlycompared the production of adults apraxic and children with DCDdo not outline significant difference in the errors produced be-tween groups (Poole et al., 1997). However, the De Renzi, Pieczuroand Vignolo test (DPVT) of apraxia was used to include childrenwith dyspraxia; hence it is unclear if the same conclusions holdusing current criterion of DCD.

Other experimental studies have focused on the ability ofchildren with DCD to produce a transitive10 and intransitive ges-ture under verbal command or imitation. Hill (1998; Hill et al.,1998) assessed a group of 11 children with DCD aged 5–13 and agroup of 25 age-matched control. They observed that childrenwith DCD were always impaired on both transitive and intransitivegestures during imitation and on verbal command. Hence, neitherthe production nor the representation of the sensorimotor andvisual features of the movement is preserved (see also, Wilsonet al., 2001). Because the degree of impairment is greater for tooluse and for gestures performed on verbal command, a re-presentational impairment of the action rather than its productionappears more likely in patients with DCD.

Zoia and colleagues (2002) studied 35 children with DCD agedbetween 5 and 10 and compared them to 105 TD children. Chil-dren were asked to produce a gesture under different conditions:1) on verbal command 2) with the tool, 3) by pantomiming the useof the tool visually presented, 4) by imitating the gesture per-formed by the experimenter. This study was the first to report adescription of developmental changes related to gestural perfor-mance. The results indicate that the proportion of correct gestureperformed by children with DCD was lower than in the controlgroup and in all 4 conditions. However, in all conditions the groupeffect decreased with age, except in the verbal command conditionwhere in control children accuracy increased with age faster thanin children with DCD. These observations argue in favor of a coremotor representational deficit which may be the cause of theimpaired execution increasing with age. However, further long-itudinal studies will be necessary to assess this hypothesis. Pa-tients’ larger samples are necessary as the number of participantsby age band was very small in the above study. Using a largersample and a wider age band (46 children with DCD and 78 TDchildren aged 8–16 years old), Dewey and colleagues did not re-plicate these results. These authors found no gesture impairmentsin children with DCD compared to typically developing childrenwhen using a transitive gesture task on verbal command andimitation (Dewey et al., 2007) Therefore, no clear conclusions can





11 The praxis questionnaire added in the Wilson and colleagues (2001) studydoes not rule out this possibility as the questions refer to the relationship betweenbody parts and objects (“Imagine you are clicking a seatbelt in. Does your handmove towards the seat or toward the car window?”).


be raised from the available studies yet on whether children withDCD are impaired in transitive and intransitive gestures. Onepossibility is that children with DCD do not exhibit deficits ingesturing but only a sensorimotor maturational delay which couldexplain the contradictory findings across studies.

3.4. Efference copy and mental imagery

3.4.1. Motor imageryThe representation of movements has been analyzed more

closely using tasks that assess motor imagery (Caçola et al., 2014;Gabbard and Bobbio, 2011; Lewis et al., 2008; Maruff et al., 1999;Williams et al., 2013, 2006, 2008, 2004, 2001, 2002). Motor ima-gery is an active cognitive process during which the representa-tion of a specific action is internally reproduced in workingmemory without any overt motor output (Decety and Grèzes,1999; Sirigu et al., 1996, 1995). It involves motor simulation of amotor action and has been shown to allow someone to predict thetime needed to complete a movement. Mental re-enactement ofan effortful exercise causes the same vegetative changes as itsactual performance, implicating most of the regions that are activeduring overt movement execution (parietal, premotor cortices, thebasal ganglia and the cerebellum (Decety et al., 1989; Decety andJeannerod, 1995; Decety, 1996a, 1996b).

One set of evidence come from studies which have used themental rotation paradigm in 7–12 years old children with andwithout DCD (Deconinck et al., 2006; Williams et al., 2006, 2008,2004). Wilson and colleagues (2004) tested 10 years old childrenwith DCD on a handedness judgment task of single-hand images(Parsons, 1987). Hands were represented at angles varying be-tween 0° and 180° at 45° intervals in either direction. Typicallydeveloping children showed the expected trade-off between re-sponse time and angle of rotation. Although, response accuracydid not differ across groups, children with DCD showed a smallertradeoff, suggesting a greater reliance on visual imagery processthan on motor imagery. Since it cannot be ruled out that the taskcan be solved by using only visual imagery in both groups con-cluding that the process impaired in children with DCD is a gen-uine motor imagery is precluded, since a deficit in visual imageryor in visual working memory may also explain patients' perfor-mance. Therefore, Deconinck and colleagues (2006) investigatedthis possibility using a mental rotation paradigm with both handand letters as a stimuli presented in various orientations. Thehypothesis here was that children with DCD should only be im-paired on the hand rotation paradigm if the IMD hypothesis iscorrect. Not surprisingly, childrenwith DCD were slower and mademore errors than the TD group with both types of stimuli.Therefore, this study highlight the possibility that the workingmemory or the visual imagery component during motor simula-tion might be responsible for the altered performance of childrenwith DCD (e.g., Alloway and Temple, 2007). In contrast with thisfindings, the study by Williams and colleagues (2006) which usedalphanumeric stimuli and body parts with 7–11 years old childrenwith DCD showed no group difference in the alphanumeric con-dition. Group difference occurred with body parts when childrenwere explicitly instructed to rely on motor imagery. Overall, theresults using mental rotation of body parts and objects indicatethat children with DCD are not always selectively impaired withbody parts.

Alternatively, motor imagery of children with and without DCDaged 7–12 was also assessed (Williams et al., 2013) using achronometric visually guided pointing paradigm designed by Sir-igu et al. (1996, 1995). In this task, when asked to move rapidlyand accurately with the stylus from a starting position to a squarevisual target, the hand must decelerate more slowly when ithomes in on a small target than on a large one. Speed accuracy


tradeoff which is expressed in Fitts (1954), implies that totalmovement duration is inversely related to the logarithm of thetarget width. This relation also applies to simulated movementswhich are in normal individuals highly correlated with executedmovement times (Sirigu et al., 1996). Sirigu and colleagues (1996)have showed that using the visually guided pointing task (VGPT),in patients with parietal lesions, actual movement execution ismodulated by target size, but motor imagery is not. Using thesame paradigm, Maruff and colleagues (1999) showed that al-though children with DCD were slower to execute the movement,their movement times followed Fitts' law just like healthy parti-cipants. However, unlike controls imagined movement times didnot correlate with motor execution and did not conform to Fitts'law. Taken together these findings (Katschmarsky et al., 2001;Wilson et al., 2001) suggest that in children with DCD simulatedmovement impairments in Fitts’ law tasks provides strong evi-dence in favor of the IMD hypothesis.

In conclusion, studies of mental imagery and double-step sac-cade tasks point to an efference copy deficit, although an alter-native interpretation in terms of working memory deficit shouldalso be considered.

3.4.2. A body representation deficit?A question that remains open from these motor imagery stu-

dies is whether children with DCD can generate a static re-presentation of their hands or body parts (in that case). Movementrepresentation would be in fact preempted without this ability andthe motor imagery disturbance would be in this case reduced to abody schema disturbance. For instance, Sirigu and colleagues(1996) examined whether parietal patients were able to imaginewith eyes closed the palm or the back of one hand with the fingersup or down and to report the spatial position of the little fingerorthe thumb. This task can be performed correctly only if subjectsimagine the designated hand in the appropriate orientation fromtheir own perspective. However, no such control tasks were usedin the mental rotation or VGPT studies11. Therefore, it is possiblethat impairment of body knowledge and body rotation in childrenwith DCD may cause incapacity to mentally simulate handmovements as well.

The existence of brain areas specifically dedicated to the pro-cessing of body parts was initially shown by neuropsychologicalstudies in patients with parietal lesions showing selective im-pairments in naming body parts while being able to name parts ofinanimate objects (Ogden, 1985). On the basis of a case studypresenting a striking autotopagnosia, Sirigu and colleagues (1991)have proposed a model of multiple concurrent body knowledgerepresentations. They hypothesized that at least four kinds of re-presentation contribute to body knowledge. The first containssemantic and lexical information about body parts, such as names.These relations are in large parts propositional and linked to theverbal system. The second level defines the structural descriptionof the individual parts in the body (e.g., the nose is in the middle ofthe face), the proximity relationship among parts, and theboundaries that define each body part, likely associated to sensorysystems such as the kinesthetic and proprioceptive system. Thethird level contributes to the construction of spatial representationof the body but relies mostly on motor representations. Finally, thefourth level called emergent body schema reflect a rather dynamicview of the body image since it integrates posture and vestibularinformation (Sirigu et al., 1991). In this study, the patient couldname body parts without being able to localize them; she could






also identify functional attributes of body parts but not theirspatial layout. Finally, she presented contiguity errors in the lo-calization of body parts, suggesting a fuzzier knowledge of proxi-mity relations and boundary among body parts. Hence, an un-explored question pertains to the ability of children with DCD toacquire and retrieve these multiple body representations. If somestudies have shown that children with DCD fail to correctly pointfingers that have been touch on a (visually) presented hand imageor on their own hand (Elbasan et al., 2012), it is still currentlyunknown how impaired are each of these body representations.

To explore more thoroughly this question, paradigms whichuse body illusions such as the rubber hand illusion (e.g., Kammerset al., 2009; Ramakonar et al., 2011; Serino et al., 2013), the illusoryout-of-body experience (Blanke et al., 2002; Slater et al., 2010) orthe Pinocchio effect (Lackner and Levine, 1979) may help in un-derstanding the status of sensory-integration and multiple bodyimage representations in children with DCD.

As firm conclusions on mental imagery and efference copydisturbances cannot be made at this stage, we can conclude thatseveral studies have pointed toward a deficit in mental imagery.However, to precisely define the cognitive mechanisms underlyingthis impairment, we suggest that future studies using motorimagery tasks in children with DCD will need to systematicallyassess body representations but also the impact of visuo-spatialworking memory load on their performance. Moreover, as men-tioned by Gabbard and Bobbio (2011), instructions to rely onmotor imagery may be crucial in such tasks especially with chil-dren. The cognitive deficits observed in children with DCD hasallowed researchers to form hypothesis on the potential brainareas that may be dysfunctional in children with DCD (Zwickeret al., 2009). In the following section, we review these studieswhich have provided evidence in favor of dysfunction in severalbrain networks.

4. Brain bases of DCD

The currently available neuroimaging studies of DCD are still scarce(Peters et al., 2013). Only 7 fMRI studies clearly aimed at identifyingthe brain bases neurofunctional deficits in children with DCD.

Fig. 3. Foci of abnormal activity reported from previous neuroimaging studies of childrright cortical surface (Left) and on an inflated human average of right cortical surface (Rcompared to typically developing children (TD) (Kashiwagi et al., 2009; Zwicker et alcompared to TD (Debrabant et al., 2013; Zwicker et al., 2010); light blue is for rest-related2014); Black is for areas identified as producing and receiving abnormal functional conn2008). Several foci of greater activation seem to cluster around the intraparietal sulcusimage). Resting-state foci suggest abnormalities in frontal and sub-cortical area (lower leof the references to color in this figure legend, the reader is referred to the web version


4.1. Functional neuroimaging

Neuroimagery studies have recently allowed to support someof the most promising hypotheses formulated on the basis of theneuropsychological observations in children with DCD (See Fig. 3,Cantin et al., 2007; Ivry, 2003; Zwicker et al., 2009). Among thesestands the idea of an impaired bold signal activity in the cere-bellum, the parietal and in the basal ganglia.

The cerebellum has been proposed as a potential dysfunctionalarea in this disorder given its implication in motor coordination,postural control, execution and control of movements (Blakemoreand Sirigu, 2003; Ivry, 2003; Koziol et al., 2014). In children withDCD it was repeatedly observed an abnormal activation within thisarea during visuo-motor control and motor prediction tasks(Debrabant et al., 2013; Zwicker et al., 2010, 2011).

The parietal lobe was conjectured for its involvement in visual-spatial processing, and action prediction (Blakemore and Sirigu,2003; Bueti and Walsh, 2009; Culham and Valyear, 2006; Des-murget and Sirigu, 2012; Fontana et al., 2012; Sack, 2009) and wasfound dysfunctional in children with DCD tested across 6 task-related fMRI studies involving visuo-motor control, motor pre-diction and attentional tasks (Debrabant et al., 2013; Kashiwagiet al., 2009; Querne et al., 2008; Zwicker et al., 2010, 2011).

The basal ganglia12 was targeted for its role in movement in-itiation and in movement learning (Calabresi et al., 2014; Schultzet al., 2003). However, evidence remains scarce for an impairmentin these areas.

The frontal hypothesis is both emergent and strengthen by fMRIreports, since it has been repeatedly observed as dysfunctional intask-related fMRI studies (Fig. 3). In fact, forward model of motorcontrol would be generated by frontal motor areas (including theSupplementary Motor Area), (Moore et al., 2010; Wolpe et al., 2014).However, the foci of dysfunctional activity within the frontal regiondo not cluster in a specific area and do not robustly reflect a tendencytoward an over or underactivation in the DCD group.

Results involving the frontal and parietal regions may appeardivergent. It is known that fronto-parietal areas are involved instrategic attentional effects and effortful activities (Posner andDehaene, 1994). fMRI studies in DCD children reporting such ac-tivation always involved the realization of a task which was

en with Developmental coordination Disorder overlaid on a flat human average ofight) using Caret5. Red foci are for task-related overactivation in children with DCD., 2010, 2011); dark blue is for task related underactivation in children with DCDconnectivity abnormalities in DCD children compared to TD children (McLeod et al.,ections in DCD compared to TD children during an attentional task (Querne et al.,(upper right image), several foci are also diffused in the frontal area (lower right

ft and right image). Cerebellum activations are not reported here. (For interpretationof this article.)






impaired only in the DCD group but not in TD children (Debrabantet al., 2013; Zwicker et al., 2010, 2011; but see McLeod et al., 2014for frontal dysfunction during resting-state). To clarify their in-volvement in the deficit, future studies in children with DCDshould assess if these differences in fronto-parietal activation re-flects task difficulty or automatic compensation strategies.

Alternative hypothesis have suggested that DCD may reflect adisconnection syndrome of the corpus callosum due to its in-volvement in interhemispheric transfer of motor information(Sigmundsson, 2003; Van der et al., 2011). Langevin and colleagues(2014) recently performed a Diffusion Tensor Imaging (DTI) studyincluding children with DCD alone, ADHD alone and children withboth DCD and ADHD. When examining the corpus callosum ofchildren with DCD, they observed that the connectivity betweenthe superior /posterior parietal region of the corpus callosum andparietal brain regions was reduced, thus providing further supportto the parietal dysfunction hypothesis. Interestingly, this sector ofthe corpus callosum with reduced fibers also showed connectionswith both primary and somatosensory motor areas (Geffen et al.,1994). The score of fractional anisotropy of the superior-posteriorparietal region of the corpus callosum was significantly correlatedto the level of fine and gross motor performance suggesting astructure-function link. Additionally, the authors report that theleft lateral superior longitudinal fasciculus showed a reducedconnectivity coefficient. Although, the study involved a total of 85children only 9 children were diagnosed with DCD alone and thegroup-level was not matched for IQ. Zwicker and colleaguescompared seven children with DCD to nine TD children. Theyobserved a lower mean diffusivity of the corticospinal tract andthalamic radiation in children with DCD. The mean diffusivitymeasure of both tracts was also correlated to the MABC score:children with lower diffusivity scores showed higher scoring onthe MABC tests (Zwicker et al., 2012). Both DTI studies used verysmall samples and did not assess the same tracts, therefore, fur-ther studies are needed to confirm these observations with largersamples.

4.2. Electrophysiology and others

Other methodologies, such as electrophysiology, are also juststarting to provide insights on the probable etiology of the func-tional impairments.

To date, few studies used EEG in children with DCD and most ofthem have assessed the hypothesis of a visuospatial attentional orworking memory impairment (Tsai et al., 2012, 2014; Tsai et al.,2010; Wang et al., 2014). De Castelneau and colleagues assessedthe EEG coherence of 24 8-13 years-old children with DCD duringa finger tapping task. Compared to TD children, they observed anincrease of intrahemispheric coherence in fronto-central regionsin 8-9 year old DCD children which could reflect an increase ofmotor planning. They did not measure any difference in inter-hemispheric coherence (but see Tsai et al., 2009 for an inter-hemispheric ability measured on a P3) However, this methodologyseems still underused in children with DCD given its potentialinsights on the time course of motor predictive coding.

Recently, Langevin and colleagues (2015) have measured cor-tical thickness in a sample of 12 children diagnosed with DCD.They observed a significant reduction of the cortical thickness inparietal frontal and temporal lobes. These results may explain thepatterns of under and overactivation of parietal and frontal areasobserved in fMRI studies. Moreover, they suggest that the tem-poral areas may also play a significant role in the disorder even if

12 the striatum, including the caudate nucleus and putamen, the globus palli-dus, the substantia nigra, the nucleus accumbens, and the subthalamic nucleus.


these regions have not been initially involved. This observation oftemporal abnormalities is congruent with fMRI results (Debrabantet al., 2013) and is in line with previous observation of form co-herence processing impairment and impairments in gesture pro-duction on verbal command (O’Brien et al., 2002; Zoia et al., 2002).Therefore, better understanding of the etiology may emerge fromanatomo-physiological studies.

Future studies may continue in this direction, but we may alsosuggest that neurotransmission in children with DCD should befurther assessed. For instance no studies have been performed toinvestigate the role of the glutamatergic, dopaminergic and ser-otoninergic system despite we know that all of these neuromo-dulators have been involved in the regulation of the motor system(see Deng et al., 2014 for a similar detailed proposal ). In conclu-sions, multiple brain areas seem to be involved in the neurology ofDCD but future research may focus on the biological mechanismsresponsible for such atypical developments (genetic, neuro-transmission, development of tracts…).

5. Summary

The present review detailed and assessed the evidence ofseveral hypotheses for the core deficit of DCD that have beensynthesized in Fig. 4. We suggest that impairments in two keyprocesses in the movement circuits may be altered and have cas-cading effects on the movement circuits: the efference copy andthe sensory feedback to estimate actual body states.

First, children with DCD exhibit some degree of impairments invisual and visuo-spatial processing that can impair their actionand the sensory feedback estimation. However, the precise un-derlying mechanisms of these deficits remain unclear. We suggestthat the dorsal stream or perception for action weakness hy-pothesis should be further examined in these children.

Second, children with DCD adapt differently to sensory-motorremapping: they need a larger discrepancy between sensory andmotor signals to adapt and learn. It is possible that the motor andsensory system of children with DCD suffers from a higher degreeof noise. These fluctuations in turns may impair their ability tolearn (implicitly) through sensory-motor adaptation. Alternatively,their impairment might arise from a deficit to adapt to error sig-nals used for online and/or offline adjustments of action. This errorsignal arises from the comparison of sensory feedbacks and theefference copy. It is possible that children with DCD learn to remapmotor and sensory information based on this error signal at aslower rate than controls. This inability could be caused a) by anoisier or inefficient sensory feedback (in particular, visual or ki-nesthetic, related to hypothesis 1 and 2 ) or / and b) by an inabilityto build efference copy of motor plan.

Last, children with DCD fail to perform mental imagery tasks,double-step saccade paradigms, and rapid-online corrections.These results can all be explained by an inability to form an ap-propriate efference copy of their movement.

As such, it is possible that daily activities failed by children withDCD reflect the dysfunction of these cognitive sensori-motor com-ponents. For instance, handwriting difficulties observed in childrenwith DCD can be explained by an initial inability to take advantage ofthe sensory-feedback (visual and kinesthetic) from their own pro-duction during letter copying tasks for instance. In fact, handwritingacquisition is known to rely on sensori-motor components (e.g., Bloteand Hamstra-bletz, 1991; Kandel et al., 2000; Kandel and Perret,2015). To produce the letter automatically, without model for in-stance, more practice might thus be necessary. With practice, themotor representation of a letter might still remain fuzzier due toinaccurate feedback perception. Therefore, children with DCD mightstruggle to shift from a feedback control to a feedforward control of





Fig. 4. Adapted from (Blakemore et al., 2002). Model of the motor control system. In gray, the motor representation which is postulated to be available to consciousness, inblack, unavailable to consciousness in control individuals. In red, two key processes embedded in the circuits that are proposed to be dysfunctional in children with DCD.Efference copy was hypothesized using motor imagery, and double-step paradigms. Perception for action and sensory feedback is hypothesized on the basis of visualperception impairments and adaptation paradigms. Dotted green lines are systems which are supportive of the action and which have not been systematically assessed inchildren with DCD. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)


handwriting movements (Jolly et al., 2010; in normal development,Jolly and Gentaz, 2013; Meulenbroek and van Galen, 1988; Zesigeret al., 2000). Consequently, they might have to postpone lexical andspelling processes of writing to the end of the syllables or lettershandwriting, which could lead to the observed slowness in writing(Prunty et al., 2014)

Future studies should try however to clarify this hypothesissince their impairment might reflect a deficit in the efference copy,but also a deficit in the monitoring of the execution or in thecomparisons between the error signal due to the perturbation andthe efference copy of the initial motor command (See Fig. 4). Onealternative interpretation of the available data is that children withDCD always perceive a signal of error and tend to not rely anymoreon this error signal.

6. Conclusions

Among developmental disorders, DCD is one of the least stu-died and less understood one (Bishop, 2010). We hope that thisreview has made clear which progress in our scientific under-standing still need to be undertaken by future researchers. It isclear that to further our understanding of this disorder we willbenefit from a highly interdisciplinary approach including devel-opmental psychology, neuroscience, cognitive science, behavioral


and molecular genetics. The answer to some basic questions aboutthe disorder, particularly confined to a single level of analysis isstarting to provide a clearer picture. This work also can lay thefoundation for research that try to make links across levels ofanalysis and which might ultimately provide applied issues onearly identification and treatment.

Appendix A. Supplementary material

Supplementary data associated with this article can be found inthe online version at http://dx.doi.org/10.1016/j.neuropsychologia.2015.09.032.

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developmental coordination disorder: core sensori-motor deficits, neurobiology and etiology

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