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Perceptual and Motor Skills

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DOI: 10.1177/0031512517690607
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A Critical Review

Juliana B. Goulardins1, Juliana C. B. Marques1,


and Jorge A. De Oliveira1

Abstract
Attention deficit hyperactivity disorder (ADHD) is the most common neurobeha-
vioral disorder during childhood, affecting approximately 3% to 6% of school-aged
children; its cardinal symptoms of high activity, impulsivity, and behavioral distract-
ibility might be assumed to have close relationships to interferences with motor
skills. A separate body of literature attests to ways that motor problems can severely
impact children’s daily lives, as motor problems may occur in 30% to 50% of children
with ADHD. This article critically reviews research on motor impairment in children
with ADHD, notable differences in motor performance of individuals with ADHD
compared with age-matched controls, and possible neural underpinnings of this
impairment. We discuss the highly prevalent link between ADHD and developmental
coordination disorder (DCD) and the lack of a clear research consensus about
motor difficulties in ADHD. Despite increasing evidence and diagnostic classifications
that define DCD by motor impairment, the role of ADHD symptoms in DCD has
not been delineated. Similarly, while ADHD may predispose children to motor prob-
lems, it is unclear whether any such motor difficulties observed in this population are
inherent to ADHD or are mediated by comorbid DCD. Future research should
address the exact nature and long-term consequences of motor impairment in chil-
dren with ADHD and elucidate effective treatment strategies for these disorders
together and apart.

1
Laboratory of Motor Behavior, School of Physical Education and Sport, University of São Paulo, São Paulo,
Brazil
Corresponding Author:
Juliana B. Goulardins, Avenida Professor Melo de Moraes, 65, São Paulo, SP 05508-030, Brazil.
Email: jugoulardins@usp.br
2 Perceptual and Motor Skills 0(0)

Keywords
attention or distraction, child motor development, motor skills, attention deficit
hyperactivity disorder, developmental coordination disorder

Introduction
Behavioral disorders related to inattention and hyperactivity have been described
in the literature for many years and have received such different diagnostic labels
over time as, for example, ‘‘minimal brain damage,’’ ‘‘minimal brain dysfunc-
tion,’’ ‘‘hyperkinetic reaction of childhood,’’ and ‘‘hyperactivity’’ (Lange et al.,
2010). Currently, mental health versions of the major classification systems show
differences in the definition and diagnostic criteria of these problems (American
Psychiatric Association, 2013; World Health Organization, 1992). The
International Classification of Mental and Behavioral Disorders 10th revision
defines ‘‘Hyperkinetic Disorder’’ as the group of disorders characterized by early
onset, lack of persistence in tasks that require cognitive involvement, and a ten-
dency to move from one activity to another without finishing any, associated with
a disorganized, uncoordinated, and excessive global activity (World Health
Organization, 1992). The American Psychiatric Association’s Diagnostic and
Statistical Manual of Mental Disorders—5th Edition (DSM-5) uses the term,
Attention Deficit Hyperactivity Disorder (ADHD; American Psychiatric
Association, 2013); it is currently the most popular definition used within scien-
tific publications in the field, and it was used in this review as well.
According to the DSM-5, ADHD is classified as a neurodevelopmental dis-
order, characterized by difficulties in development that manifest early and influ-
ence personal, social, academic, or occupational functioning (American
Psychiatric Association, 2013). The main symptoms of ADHD are inattention,
hyperactivity, and impulsivity. These cardinal symptoms are manifested in an
excessive, persistent, and inappropriate pattern for chronological age, do not
occur in a single context, and cannot be attributed to another medical diagnosis
(American Psychiatric Association, 2013; Barkley, 2003). Inattention is the lim-
ited ability to sustain attention for the time required to perform or understand
certain tasks. Hyperactive–impulsive behavior is linked to a multidimensional
construct of inhibition (Barkley, 2003), in which hyperactivity is characterized
by an excessive motor or mental activity, and impulsivity is manifested by
thoughtless and sudden reactions. This set of symptoms leads to difficulties in
inhibiting behavior, with losses in planning and task interruption skills and with
features like low tolerance for waiting, high need of immediate reward, failure in
predicting the consequences, deficits in self-regulation, and the presence of fast
but inaccurate answers (Barkley, 1998; Barkley et al., 2001).
ADHD is not only the most common neuropsychiatric disorder in childhood
but also one of the most investigated conditions in children’s mental health
Goulardins et al. 3

(Lopez-Munoz et al., 2008), with estimated worldwide prevalence of 5.29%


(Polanczyk et al., 2007). It is more often observed in males than in females,
with rates ranging from 2:1 in general population samples to 10:1 in clinical
samples (Scahill & Schwab-Stone, 2000; Willcutt, 2012). Despite difficulties in
establishing definitive causal factors of ADHD, due to the heterogeneity of the
disorder (Sonuga-Barke, 2005), both genetic and environmental influences have
been proposed (Rohde & Halpern, 2004), and genetic influence is particularly
important since heritability is quite high, estimated at 76% (Faraone et al.,
2005). While many environmental risk factors associated with ADHD occur
early in development, the most important of these have biological influences
on brain development, such as complications during pregnancy or childbirth
(oxygen perfusion perinatal problems, toxemia, preeclampsia, fetal postmatur-
ity, birthing duration, fetal distress, and low birth weight) that may predispose
children to the disorder (Banerjee, Middleton, & Faraone, 2007; Kieling et al.,
2008; Rohde & Halpern, 2004). In addition, exposure to lead, smoking, and
alcohol have been linked to increased risk for ADHD (Banerjee et al., 2007).
Thus, while environmental factors have been judged to contribute 40% and
heritability 60% for ADHD disease development (Lehn et al., 2007) and
ADHD symptomatology may be a result of interactions between genes
and environment (Banerjee et al., 2007), the neurodevelopmental, biological
basis of ADHD has been clearly established.
Traditional subtypes of ADHD (predominantly inattentive, predominantly
hyperactive-impulsive, and combined; American Psychiatric Association, 2000)
have been downgraded to presentations in the DSM-5 (American Psychiatric
Association, 2013). This change is due to results of numerous studies reflecting
that symptom type and onset may vary according to the age at which the diag-
nosis is considered (Biederman, Mick, & Faraone, 2000; Dopfner et al., 2014;
Larsson et al., 2011; van Lier et al., 2007). The term presentation is different from
the meaning of ‘‘subtype,’’ in that the latter term refers to an invariable condi-
tion. Researchers have described a general decline in the severity of symptoms of
hyperactivity-impulsivity with increasing age (Larsson et al., 2011; van Lier
et al., 2007), whereas age relationships to symptoms of inattention are incon-
clusive. Inattentiveness symptom reduction (Biederman et al., 2000), stability
(Dopfner et al., 2014), and increase (Larsson et al., 2011) have all been reported.
Up to 70% of children diagnosed with ADHD in childhood continue to have
developmentally inappropriate levels of inattention and, to a lesser extent, symp-
toms of hyperactivity-impulsivity during adolescence and adulthood (Biederman
et al., 1998; Faraone, Biederman, & Monuteaux, 2002).
DSM V diagnostic criteria include the expectation that symptoms and con-
cerns must have appeared before 12 years of age. Thus, prominent clinical pres-
entation during childhood is a critical feature of the disorder (American
Psychiatric Association, 2013). The symptomatic triad is often observed after
the child enters school because it is in this period that these difficulties are most
4 Perceptual and Motor Skills 0(0)

likely to be perceived by teachers who are able to compare children of the same
age in the same environment (Poeta & Rosa Neto, 2004). Understanding the
symptoms within the context of the child’s life history is necessary for the iden-
tification of ADHD, as is a consideration of the duration, frequency, intensity,
and persistence of these symptoms in different contexts (Rohde &
Halpern, 2004).
The ADHD cardinal symptoms of high activity, impulsivity, and behavioral
distractibility might be assumed to have close relationships to interferences with
motor performance, such as impairment of fine motor skills, slow reaction time,
and difficulty with motor coordination (handwriting; Kaiser et al., 2015).
Children with ADHD can also be clumsy in performing motor skills (Pitcher,
Piek, & Hay, 2003; Watemberg et al., 2007). Indeed, motor problems can have a
severe impact on children’s daily lives, and occur in 30% to 50% of children with
ADHD (these percentages depend on the type of motor assessment, references,
and cutoff points used; Fliers et al., 2009; Gillberg et al., 2004; Goulardins
et al., 2013).
Research has shown specific motor difficulties in children with ADHD, such
as fine and gross motor skills (Pitcher et al., 2003), and there are established
associations between primary symptoms of ADHD and motor performance
(Kroes et al., 2002; Tseng et al., 2004). Results from these studies have generated
different hypotheses to explain the motor difficulties often seen in individuals
with ADHD. These hypotheses are divided along two lines: The first suggests
that motor difficulties may be attributed to the basic symptomatic triad and thus
arise from ADHD itself; and the second suggests that motor problems in ADHD
may be secondary to a comorbid developmental coordination disorder (DCD;
Kaiser et al., 2015), whose main features are difficulties in the acquisition and
execution of coordinated motor skills (American Psychiatric Association, 2013).
DCD is one of the most frequent comorbidities found in children with ADHD
(Kadesjo & Gillberg, 2001). The remainder of this critical review will focus on
research addressing these two perspectives.

Method of Review
Publications reviewed here were found through an Internet-based literature
search of studies within PubMed, Medline, and Scielo. In addition, literature
references within further relevant articles were explored. Our searches were not
limited to certain key words, as the terminology used in the reviewed topics
varied widely between studies, including such terms as attention disorder or
ADHD, motor skills, motor performance, motor behavior, motor problems,
motor difficulties, motor impairment, handwriting, DCD, dyspraxia, and so
forth. When publications on a topic were scarce, older relevant publications
were studied. The review begins with a discussion of the ADHD motor difficul-
ties attributed to ADHD symptoms, followed by studies of the relationship
Goulardins et al. 5

between ADHD and DCD. Clinical implications and further research in the area
are also presented.

ADHD Motor Impairment and the ADHD Symptom Triad


Motor hyperactivity is an essential aspect of the disorder, manifested by agita-
tion, restlessness, and unnecessary body movements (Zametkin & Ernst, 1999).
Several motor difficulties have been identified in these individuals, including
problems with gross motor skills (i.e., ball skills; Piek, Pitcher, & Hay, 1999),
fine motor skills in manual dexterity and bimanual coordination tasks (Piek
et al., 1999; Rommelse et al., 2007), balance (Mao et al., 2014), gait, and postural
control (Buderath et al., 2009; Papadopoulos et al., 2014). In addition, children
with ADHD have shown poor performance on tests with motor development
scales when compared with typically developing children (Goulardins et al.,
2013; Poeta & Rosa-Neto, 2007; Rosa Neto et al., 2015; Vidarte, Ezquerro, &
Giraldez, 2009).
Previous studies have suggested that inattention may influence motor skills
(Ghanizadeh, 2010; Klimkeit et al., 2005). For example, fine motor skills of
writing were predicted by the severity of symptoms of inattention
(Ghanizadeh, 2010). Fliers et al. (2008) investigated motor problems reported
by parents and teachers of 486 children with ADHD and 269 controls, and they
concluded that the difficulties in gross and fine motor skills found in about one
third of children with ADHD were all related to the symptoms of inattention,
not hyperactivity or impulsivity.
Moreover, Kaiser et al. (2015) proposed that degree of vigilance affects the
motor performance of children with ADHD, and may fluctuate in simple tasks
and stabilize at dual task activities. Another argument for the relationship
between attention deficits and motor problems is the improvement of motor
performance after medication (Bart et al., 2013; Kaiser et al., 2015). The use
of a single dose of methylphenidate, which is the drug of first choice for the
treatment of ADHD in many countries, has led to the improvement of motor
function in maintenance of posture and balance tests (Stray et al., 2009). Fine
motor difficulties, such as manual dexterity impairment and poor quality of
writing and drawing, also improved after use of methylphenidate, but residual
problems remained such that a group with treated ADHD performed worse than
a control group without ADHD (Flapper, Houwen, & Schoemaker, 2006). The
improvements observed after the use of stimulants in motivation, coordination,
visual-motor skill, and short-term learning in subjects with ADHD appear to be
due to improvement in attentional performance (Andrade & Scheuer, 2004)
because stimulant medication treating these symptoms primarily address the
ability to stay focused during the motor tasks (Kaiser et al., 2015).
Tseng et al. (2004) demonstrated that attention and impulse control are
important predictors of gross and fine motor skills in children with ADHD.
6 Perceptual and Motor Skills 0(0)

A lack of inhibition resulting from impulsivity is one of the main characteristics


of ADHD (Alderson, Rapport, & Kofler, 2007); it involves the ability to inhibit
the preparation of a response, to stop an in-progress response, and to manage
the interference. These abilities influence executive functions such as working
memory, self-regulation of emotions, motivation, arousal, internalization of
speech, and reconstitution. The disturbance of these executive functions may
then interfere with motor control (Kaiser et al., 2015). However, although the
results of many studies have suggested that impulsivity level may interfere with
motor control (Bachorowski & Newman, 1990; Lage et al., 2011; Lemke et al.,
2005), other research has shown a lower association between hyperactive-impul-
sive symptoms in ADHD and motor impairment, rather than attentional symp-
toms (Meyer & Sagvolden, 2006; Pitcher et al., 2003).
The hypotheses that relate motor difficulties to the core symptoms of ADHD
may be supported in part by morphometric and neuroimaging studies that
describe abnormalities in individuals with ADHD in brain regions linked to
motor function (Berquin et al., 1998; Goulardins et al., 2013; Makris et al.,
2007; Seidman et al., 2006; Valera et al., 2007). In this sense, abnormalities in
the cerebellum amply demonstrated in ADHD appear to have a crucial role
(Bendiksen et al., in press; Castellanos et al., 2002; Seidman et al., 2006;
Valera et al., 2007), since their functions have traditionally been associated
with motor control, coordination, and balance (Barlow, 2002). Castellanos
et al. (2002) examined volume changes in brain regions over time in individuals
with ADHD and found that volumetric abnormalities persist with age in total
and regional measures in the cortex and cerebellum. Berquin et al. (1998) found
a smaller total cerebral volume and lower volumes of the right globus pallidus,
the right frontal cerebellum, and frontal region in individuals with ADHD.
Furthermore, a nonprogressive loss of volume was noted in the superior cere-
bellar vermis in children with ADHD (Mackie et al., 2007).
Other researchers have verified a delay in brain maturation of individuals
with ADHD (Dopheide & Pliszka, 2009; McLaughlin et al., 2010; Shaw et al.,
2007), which may explain the delay in motor development and specific motor
skills (Goulardins et al., 2013; Rosa Neto et al., 2015). Shaw et al. (2007)
compared 223 children and adolescents with ADHD with 223 controls in a
neuroimaging study of cortical thickness. The results showed that in both
groups brain maturation progressed similarly, but among children with
ADHD, there was a delay in obtaining the peak of cortical thickness at
half of the cortical points studied. The delay was most prominent in the pre-
frontal region, particularly in the lateral prefrontal cortex. The majority of
structural abnormalities and hypoactivation detected in ADHD are located
in these regions, and are linked to cognitive functions such as ability to inhibit
thoughts and unwanted responses, executive control of attention, evalu-
ation of shared rewards, precise motor control, and working memory (Shaw
et al., 2007).
Goulardins et al. 7

Lage et al. (2011) suggested that motor performance does not only involve the
activation of motor responses but also other variables such as mental represen-
tation of activity, the individual’s relationship with the context and the joint
action of processes of attention, memory, decision making, and control over
preponderant responses. Thus, evidence suggests an overlap between the
neural circuits that support cognitive and motor functions (Piek, 2006).
Nevertheless, little research has been conducted on motor impairment as an
integral symptom of ADHD (Goulardins, Marques, & Casella, 2011).

Comorbidity Between ADHD and DCD


The relationship between ADHD and DCD has been recognized for several
decades (Hellgren et al., 1993), and the overlap between both disorders is esti-
mated at about 50% (Fliers et al., 2008; Gillberg et al., 2004; Magalhaes,
Missiuna, & Wong, 2006; Pitcher et al., 2003; Polatajko & Cantin, 2005;
Visser, 2003). DCD is defined as a severe impairment on learning and execution
of motor skills, considering the chronological age of the child and the oppor-
tunity to acquire and use the skills; the deficits interfere significantly and per-
sistently in activities of daily living, with impacts on academic productivity,
prevocational and vocational activities, leisure, and play. The symptoms
appear in the early stage of development and motor difficulties are not due to
neurological, sensorial, or intellectual problems (American Psychiatric
Association, 2013; Blank et al., 2012).
The prevalence of DCD in the general population may vary from 5% to 20%
in children, while 5% to 6% estimates are the most frequently described in the
literature (Blank et al., 2012; Gaines et al., 2008). Like ADHD, DCD is a dis-
order more common in boys than girls with ratios ranging from 2:1 to 7:1 (Blank
et al., 2012). Most individuals continue to present motor difficulties into adult-
hood (Sugden, 2006; Sugden, Kirby, & Dunford, 2008; Zoia et al., 2007), with
consequences involving social, psychological, and physical health problems
(Cousins & Smyth, 2003). Even though frequent, DCD is still underestimated
by health and education professionals (Blank et al., 2012).
The hypothesis that motor problems in ADHD are a consequence of DCD
comorbidity may also be based on neurological findings of affected skills in
children with DCD. For example, some studies have suggested a cerebellar dys-
function in individuals with DCD (Brookes, Nicolson, & Fawcett, 2007; Cantin
et al., 2007) as an explanation for problems with postural control and balance
(Fong, Tsang, & Ng, 2012; Jover et al., 2010) and fast and accurate control of
movement (O’Hare & Khalid, 2002). Other possible neural correlates underlying
the motor problems in DCD are associated with abnormalities in frontal, tem-
poral, and parietal regions (Peters, Maathuis, & Hadders-Algra, 2013).
Abnormal patterns of parietal activity have been found in individuals with
DCD for motor sequencing tasks (Kashiwagi et al., 2009; Zwicker et al., 2011).
8 Perceptual and Motor Skills 0(0)

However, few studies have examined changes in brain regions in well-defined


samples of children with both ADHD and DCD (Goulardins et al., 2015). Three
recent studies have focused on the alterations in brain regions in different groups
of children with ADHD only, DCD only, and ADHD or DCD (Langevin et al.,
2014; Langevin et al., 2015; McLeod et al., 2014). McLeod et al. (2014) found
abnormal connectivity in the primary motor cortex in ADHD, which works in
association with other motor areas to plan and execute movements, and insular
cortices whose functions include perception, motor control, self-awareness, cog-
nitive functioning, and interpersonal experience. Compared with children with
only DCD or ADHD, the group with both disorders showed greater functional
connectivity between the primary motor cortex and brain regions involved in
motor control (bilateral caudate, left premotor cortex, lower right frontal gyrus),
processing speech and prosody (superior and anterior bilateral temporal gyri),
sensorimotor processing (left postcentral gyrus, right parietal operculum cortex,
bilateral precuneus cortices, and angular gyrus), and attention and error detec-
tion (bilateral anterior cingulate cortices; McLeod et al., 2014), suggesting that
some connections between the primary motor cortex and processing areas can be
erroneous, such that greater involvement of these regions is necessary to plan
and successfully execute movement in children with ADHD or DCD (Zwicker
et al., 2010).
Langevin et al. (2014) found alterations in the corpus callosum, an area
that has also been implicated in motor difficulties and attention functioning.
Nevertheless, these abnormalities were regionally and functionally distinct
for each disorder. Abnormalities in frontal regions were found in children
with ADHD and abnormalities in the connections of white matter under-
lying the primary motor, and somatosensory cortices were exclusive to the
DCD; while children with ADHD and DCD demonstrated changes in both
calloused regions (Langevin et al., 2014). In addition, children with ADHD
and comorbidity with DCD showed more generalized reductions in cortical
thickness compared with participants with a single diagnosis of ADHD or
DCD, concentrated in the frontal, parietal, and temporal lobes, and was
correlated with attentional and motor performance measures (Langevin
et al., 2015). Therefore, recent evidence suggests that ADHD and DCD
do not share brain bases, and the co-occurrence of ADHD and DCD
may not just be a sum of both, but probably represents different neuro-
pathological and plasticity aspects (Goulardins et al., 2015; Langevin et al.,
2014; Langevin et al., 2015).
However, despite these initial neurologic findings and very extensive comor-
bidity between ADHD and DCD, it is still not clear what difficulties are intrinsic
to each disorder, since, in many studies, the presence of DCD was not investi-
gated in groups with ADHD (Langmaid et al., 2013) and vice-versa (Goulardins
et al., 2015). In a recent systematic review of impaired motor skills and motor
control in ADHD, there were found only six studies that investigated whether
Goulardins et al. 9

children with ADHD without medication met the diagnostic criteria for DCD
(Kaiser et al., 2015).
Furthermore, results from other studies have suggested that motor difficulties
in ADHD cannot be attributed exclusively to the comorbidity with DCD, since
even when individuals with ADHD do not have DCD, they may have less
prominent motor difficulties (Langmaid et al., 2013). Accordingly, the DSM-5
is controversial, as it suggests that motor difficulties that occur in ADHD are
due to distraction and impulsivity rather than to motor disability. However,
DSM-5 allows dual diagnosis when, after careful observation, the criteria for
both disorders are met (American Psychiatric Association, 2013). It is note-
worthy that although the relationship between ADHD and DCD is described
in the differential diagnosis section for DCD in the current edition of the DSM,
there is no description of motor difficulties in any of the sections describing
ADHD (Sergeant, Piek, & Oosterlaan, 2006).

Conclusions and Clinical Implications


There seems to be no agreement among researchers regarding motor impairment
in ADHD. Despite growing evidence that DCD is significantly associated with
motor difficulties, many studies did not take into account the role of ADHD
symptoms in this relationship. Also, although the symptoms of ADHD may
predispose children to motor problems, it is unclear whether motor difficulties
are inherent to ADHD or are mediated by the presence of DCD. Further
research is needed to clarify these aspects. Future studies should address the
exact nature and long-term consequences of motor impairment in children with
ADHD, and focus on development of effective assessment and treatment
strategies.
Motor skills are important, and problems with them during childhood may
significantly impact general learning and school success. For this reason, early
identification and intervention are important, not only to increase the likelihood
that these children will be successful academically and socially but also to pre-
vent secondary emotional complications related to feelings of frustration and
failure. Unfortunately, motor problems in ADHD are still a neglected area of
clinical attention. The inclusion of physical therapists, occupational therapists,
and professionals of physical education in the multidisciplinary team that directs
assistance to individuals with ADHD is essential. In addition, parents and tea-
chers should be advised to manage motor problems to mitigate their impacts,
especially in regard to self-esteem and quality of life.

Declaration of Conflicting Interests


The author(s) declared no potential conflicts of interest with respect to the research,
authorship, and/or publication of this article.
10 Perceptual and Motor Skills 0(0)

Funding
The author(s) disclosed receipt of the following financial support for the research, author-
ship, and/or publication of this article: Juliana B. Goulardins and Juliana C. B. Marques
have received grant or research support from Coordenação de Aperfeiçoamento de
Pessoal de Nı́vel Superior (CAPES), Brazil.

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Author Biographies
Juliana B. Goulardins, PhD, is physiotherapist and research collaborator at the Laboratory of Motor
Behavior, University of Sao Paulo.

Juliana C. B. Marques, Master, is physiotherapist and PhD student at School of Physical Education
and Sport, University of Sao Paulo.

Jorge A. De Oliveira, PhD, is Professor at School of Physical Education and Sport, University of Sao
Paulo.

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