Accepted Manuscript

Title: Wrist position sense acuity and its relation to motor

dysfunction in children with developmental coordination
disorder

Authors: Yu-Ting Tseng, Chia-Liang Tsai, Fu-Chen Chen,

Jürgen Konczak

PII: S0304-3940(18)30208-8
DOI: https://doi.org/10.1016/j.neulet.2018.03.031
Reference: NSL 33490

To appear in: Neuroscience Letters

Received date: 19-12-2017

Revised date: 14-3-2018
Accepted date: 16-3-2018

Please cite this article as: Yu-Ting Tseng, Chia-Liang Tsai, Fu-Chen Chen,
Jürgen Konczak, Wrist position sense acuity and its relation to motor
dysfunction in children with developmental coordination disorder, Neuroscience
Letters https://doi.org/10.1016/j.neulet.2018.03.031

This is a PDF file of an unedited manuscript that has been accepted for publication.
As a service to our customers we are providing this early version of the manuscript.
The manuscript will undergo copyediting, typesetting, and review of the resulting proof
before it is published in its final form. Please note that during the production process
errors may be discovered which could affect the content, and all legal disclaimers that
apply to the journal pertain.
 1

Wrist position sense acuity and its relation to motor dysfunction in children with
developmental coordination disorder

Running title: Proprioception in Developmental Coordination Disorder

YU-TING TSENG*a, CHIA-LIANG TSAIb,FU-CHEN CHENc, JÜRGEN KONCZAKa

PT
a
Human Sensorimotor Control Laboratory of School of Kinesiology, University of Minnesota,
1900 University Ave. SE, Minneapolis, MN 55455, Minneapolis, USA
b
Institute of Physical Education, Health & Leisure Studies, National Cheng Kung University,

RI
No.1, University Road, Tainan City, 701, Taiwan
c
Department of Physical Education, National Kaohsiung Normal University, No.116, Heping 1st
Rd., Lingya District, Kaohsiung City, 802, Kaohsiung, Taiwan

SC
U
*Corresponding author: Yu-Ting Tseng
Human Sensorimotor Control Laboratory
School of Kinesiology
University of Minnesota, USA.
N
A
1900 University Ave. SE
M

Minneapolis, MN 55455
E-mail address: tseng023@umn.edu
D

Abstract word count: 199

TE

Manuscript word count: 3869

(Total length limit: 5000)
EP

HIGHLIGHTS
 DCD is associated with an underlying deficit in proprioceptive acuity.
 Children with DCD show an increased position sense bias (elevated thresholds) during
CC

passive joint displacement.

 Children with DCD show a decrease in proprioceptive precision (increased response
variability) during active joint position matching movements.
A

 Elevated proprioceptive thresholds at the wrist are associated with decreased fine motor
and balance function.
 2

ABSTRACT

This study obtained objective measures of wrist position sense to verify that children with DCD
have proprioceptive deficits. In addition, it examined the relationship of wrist proprioceptive
impairment with fine motor and balance function. Twenty children with DCD and thirty typically
developing children (TD) aged 10-11 years old were recruited and screened using the Movement
Assessment Battery for Children (MABC-2). The DCD group had total MABC-2 score below 5th
percentile, and TD group was above 25th percentile. Wrist position sense was assessed under two

PT
conditions: 1) an ipsilateral wrist joint position matching requiring active movement to reproduce
a reference position, and 2) a psychophysical discrimination threshold testing, in which the wrist
joint was passively rotated. The results showed that, in comparison to TD controls, the DCD

RI
group showed an increased joint position error variability during active matching (p < 0.05) and
highly elevated mean position sense threshold for passive displacement (+71%; p < 0.001).
Position sense threshold data correlated significantly with manual dexterity (r = -0.4) and

SC
balance scores (r = -0.5). This study documents that DCD is associated with a proprioceptive
dysfunction of the wrist/hand complex, which likely contributes to the fine motor problems in
children with DCD.

U
ABBREVIATIONS
DCD - developmental coordination disorder
N
A
TD - typically developing children
JND - just noticeable difference threshold
M

PE - wrist joint position error

SDPE - standard deviation of wrist joint position error
D

Key words: DCD, fine motor function; position sense; psychophysical methods;
proprioception, childhood
TE
EP
CC
A
 3

1 INTRODUCTION
Developmental coordination disorder (DCD) is a highly prevalent neurodevelopmental
disorder characterized by uncoordinated movements and poor motor skill learning that
significantly interferes with a child’s activities of daily living and academic performance [1].
Estimates indicate that up to 6% of all school-age children present with DCD [1, 2]. Its etiology
is unknown, but neural correlates of DCD involve the cerebellum, basal ganglia, parietal and
frontal cortex [3, 4].
It is well established that proprioceptive afferents give rise to the awareness of body and limb

PT
position and motion and are crucial for movement control [5-7]. Previous research proposed that
the processing of proprioceptive signals is compromised in children with DCD and that
proprioceptive deficits underlie the motor problems in children with DCD [8-10]. However, at

RI
present, the empirical results on proprioceptive abnormalities in children with DCD are mixed
[9-12]. For example, some reports demonstrated that children with DCD had poorer
proprioceptive function when compared to TD children [9, 10, 13, 35], while other studies could

SC
not confirm that DCD is associated with proprioceptive dysfunction [11, 14-16]. The lack of
solid, unequivocal evidence is likely attributable to several factors: First, the type of available
instruments to test proprioception in children are not sufficiently sensitive and/or do not restrict

U
sensory information from other modalities. For example, researchers using the Kinaesthetic
Sensitivity Test [8] and the Kinaesthetic Acuity Test (KAT) [7] reported poor reliability and lack
N
of sensitivity [17, 18]. In addition, the KAT requires cross-modal transformation (vision and
proprioception). Thus, it does not allow determining the influence of proprioceptive sensory
A
information on kinaesthesia or position sense. Second, the employed proprioceptive assessment
protocols test different aspects of proprioception. They either passively displace a limb or they
M

require the child to make an active movement. For example, recent reports show that children
with DCD require a larger displacement of the forearm before they detect passive motion [10],
but arm position sense errors were normal during active joint position matching [11]. The
D

difference between assessing proprioceptive function using active or passive motion is not
trivial. Sensing the position of a passively displaced limb relies solely on sensory feedback from
TE

proprioceptive afferents, while matching a limb position using active motion also involves the
processing of internal predicted sensory feedback that is based on the efference copy of the
motor command [19, 20]. That is, the former minimizes the movement confounding effects and
reflects processes of afferent sensory feedback, while the latter reflects the function of
EP

somatosensory as well as sensorimotor integration and control processes [21].

The purpose of this study was to provide comprehensive, objective data on the extent of
proprioceptive impairment in children with DCD and to relate them to their observable motor
CC

deficits. We employed two well-established methods to measure proprioceptive acuity,

psychophysical discrimination threshold testing using passive joint displacement, and an active
movement joint position matching task. Employing both tasks allowed us to address the sensory
A

as well as the sensorimotor integration processing aspect of joint proprioception in DCD.

Because psychophysical discrimination threshold testing involves no voluntary movement,
perception of joint position relies solely on the processing of proprioceptive afferent information.
It can determine, if a primary somatosensory processing deficit is present. In contrast, the joint
position matching method requires voluntary, active movement of the observer. It examines a
possible deficit in sensorimotor integration that can arise from faulty processing of peripheral
proprioceptive feedback (external) or internal predicted sensory feedback.[20, 22]. We
specifically investigated position sense acuity, that is, the ability to discriminate between two
 4

limb positions. Perceptual acuity has two aspects: bias and precision [23]. Here, bias indicates
how close a sensed limb position corresponds to the true physical position of the wrist. For a true
response, there is no systematic error or bias. Precision represents the random error or the
agreement between independent repeated responses.
Showing that proprioceptive thresholds during passive motion are elevated in children with
DCD would support the notion that DCD is associated with an underlying primary
somatosensory deficit. Demonstrating impairments in joint position matching would imply that
mechanisms of sensorimotor integration are affected in children with DCD. Both, the

PT
psychophysical discrimination threshold testing and joint position matching method have been
successfully employed with typically developing children [23, 24], or children with neurological
disorders [25].

RI
2 METHOD

SC
2.1 Participants
Twenty children with DCD [M age: 10 years 4 months (SD: 3 months); 9 ♂, 11♀] and thirty
TD children [M age: 10 years 5 months (SD: 3 months); 14 ♂, 16♀] participated in the present

U
study. Children were recruited from two elementary schools in Kaohsiung, Taiwan. We followed
the Diagnostic and Statistical Manual of Mental Disorders (DSM-5) criteria. All children were
N
screened using Movement Assessment Battery for Children (MABC-2) [26] by certified physical
therapists and trained researchers. Children were considered to present with DCD, if their total
A
MABC-2 score fell below 56 (< 5th percentile of the norm population) (Criterion A). The TD
group included children who performed MABC- 2 score higher than 68 (> 25th percentile of the
M

norm population). Mean total MABC-2 score for the DCD group was 49.8 (SD: 7.0) and 80.9
(SD: 8.9) for the TD group. Teachers were asked to determine the motor coordination problems
using the MABC-2 Checklist (Criterion B), and to report, if the motor problems persistently
D

interfered with activities of daily living (Criterion C). Parents were asked to provide any relevant
medical information for identifying children with DCD (Criterion D). The exclusion criteria
TE

were the documented presence of neurological disorders (e.g., cerebral palsy, muscular atrophy),
behavioral problems (e.g., ADHD), current injury of or implanted medical devices in the upper
limbs, or an IQ below 85. All children completed a modified Edinburgh handedness inventory to
determine their dominant upper limb. Appropriate parental consent and child assent was obtained
EP

before data collection. The study was approved by the Institutional Review Board of National
Cheng Kung University Hospital in Taiwan.
2.2 Apparatus
CC

A custom-built, portable wrist bimanual manipulandum with one degree of freedom in the
horizontal plane was used to assess wrist position sense acuity (see Fig. 1A). Two optical
encoders (spatial resolution: 0.036°; U.S. Digital H6), housed at the rotating point of the lever
A

arms, recorded angular position of each hand at a sampling rate of 200 Hz. To allow for the
testing of distinct joint positions across the joint range of motion, the device has a pegboard with
holes in a semicircular arrangement. By inserting a metal pin, researchers can select a precise
standard position from 140 different positions across 0°-70° range of motion of the wrist in 0.5°
increments (see Fig. 1C).

-----Insert Figure 1 about here-----

 5

2.3 Procedure
The children sat in a quiet room and placed their dominant arm on the lever of the wrist
manipulandum. Chair height, lever arm length, and handle placement were adjusted to the
anthropometrics of each participant so that the approximate wrist joint axis directly aligned with
rotating axis of the optical encoder. Children kept their fingers relaxed in neutral position.
Children wore vision-occluding goggles during all tasks to ensure that visual information about
wrist position was not available (see Fig. 1B). All participants underwent two proprioceptive
assessments: 1) an ipsilateral joint position matching task [27], and 2) psychophysical

PT
discrimination threshold testing [21]. The order of the assessment was counterbalanced to
account for possible order effects. Before each assessment, children practiced for 3-5 minutes to
become familiar with the procedure and the device.

RI
For joint position matching, the experimenter slowly moved a child’s dominant hand from
the neutral joint position to a position of 20° wrist flexion (reference). This reference position
was held for 3 seconds. Afterwards the hand was moved back to the neutral position. The

SC
experimenter maintained an approximate movement speed of 20-25°/s to displace the child’s
hand. Then, the child reproduced the reference position by actively moving the same hand to a
position that she/he felt matched the previously experienced reference. The child could adjust the

U
position until satisfied with the match and then verbally indicated that the final matching position
was assumed. Five trials were performed taking approximately 5 minutes to complete.
N
For psychophysical discrimination threshold testing, a child’s dominant hand rested on the
manipulandum lever and was passively moved to two different positions: a reference position
A
(20° of wrist flexion), and a comparison position (20.5 – 40 °, in 0.5° increment). The two
positions were randomly presented. Each position was presented for 2 seconds. During each trial,
M

the velocity of the moved hand was maintained at a speed of 20-25°/s. After each trial, using a
two-alternative forced choice technique, children were asked to verbally judge which position
has larger amplitude (i.e., “which of the two positions was farther way, the first one or the
D

second one?”). Based on the participant’s verbal response, an adaptive algorithm (psi-marginal
method) generated the subsequent comparison stimulus pair to guarantee fast convergence
TE

towards the perceivable threshold within 20 trials [28, 29]. Testing took approximately 15
minutes.
2.4 Measurements
EP

Both assessments obtained a measure of position sense acuity referring to the smallest
difference in position that a participant could reliably discriminate. For each trial in the joint
position matching task, the signed constant angular error was computed as the difference
CC

between the matching and reference angular position. A positive error indicated overshooting of
the reference position (too much wrist flexion), while a negative value indicated undershooting
(not enough wrist flexio). Subsequently, we calculated position error (PE) as the mean of the
absolute angular error over the five test trials. PE indicates position sense bias or systematic error
A

(also referred to as absolute error). The respective standard deviation (SDPE) indicates position
sense precision or random error [23]. For the data obtained during psychophysical discrimination
threshold testing, a respective sensitivity function was obtained by fitting each child’s verbal
response data to a logistic Weibull function [28, 29]. Based on the obtained function, the just-
noticeable difference (JND) threshold was determined as the angular position at the 75% correct
response rate [21] (see Fig. 3). It represented a measure of position sense bias based on passive
motion.
 6

2.5 Statistical analysis

Initial statistical analysis using Levene’s and Kolmogorov-Smirnov tests determined that all
data met homogeneity and normality of variance criteria. To investigate differences between
children with DCD and TD children, independent t-tests were performed for PE, SDPE and JND.
To investigate the relationship between proprioceptive and motor function, Pearson product-
moment correlations were computed between proprioceptive variables (PE, SDPE and JND), and
the motor variables (MABC-2 manual dexterity score and balance score) for all children (TD and
DCD) and for children in each group (TD or DCD). The significant level was set to p < 0.05.

PT
3 RESULTS
3.1 Position sense acuity based on joint position matching

RI
We assessed the ability to proprioceptively perceive a wrist joint position and then to match
this experienced position by actively moving the hand to it. The mean PE was not significantly

SC
different between the DCD and TD group (t48 = 0.36, p = 0.72), indicating no systematic
difference in bias. However, analysis of SDPE revealed that children with DCD performed
significantly more variable (M: 2.12°, SD 1.03°) in their judgements when compared to their TD

U
peers (M: 1.48°, SD 0.74°) (t48 = 2.58, p < 0.05), indicating that perceptual precision was lower
in the DCD group (see Fig. 2 for PE and SDPE data). The computed effect size was medium to
large (Cohen’s d = 0.71).
N
3.2 Position sense acuity based on the psychophysical discrimination threshold
A
testing
We here assessed wrist joint position sense acuity based on passive joint rotation without
M

muscle activation. Figure 3A shows the respective sensitivity functions for both groups
indicating a larger bias for the DCD group with 13/20 (65%) children exhibiting thresholds
above the maximum of the TD group. As a group, DCD children had significantly elevated
D

position sense JND thresholds (M: 3.96°, SD: 1.74°) when compared to the TD group (M: 2.32°
SD:1.00°) (t48 = 4.23, p < 0.001; see Fig. 3B). The computed effect size was large to very large
TE

(Cohen’s d = 1.16). The mean JND threshold of the DCD group was increased by 71% with
respect to the TD group.
3.3 Relationship between wrist proprioception and motor function
EP

We examined to what extent position sense acuity correlated with motor ability as measured
by MABC-2 in children with and without DCD. First, we performed the correlation for the
combined children group and found that the MABC-2 manual dexterity score correlated
CC

significantly with JND thresholds (r = -0.40, p = 0.005), indicating that wrist proprioception was
linked to fine motor function (see Fig. 4). However, there was no significant correlation between
the manual dexterity score and PE (r = 0.05, p = 0.754) or SDPE (r = -0.17, p = 0.227). Second,
the MABC-2 aiming and catching task correlated significantly with SDPE (r = -0.29, p = 0.043),
A

but not with PE (r = -0.08, p = 0.605) or JND (r = -0.23, p = 0.118). Third, we examined the
relationship between lower limb motor function and wrist proprioception using the balance skill
score of MABC-2 as a measure of lower limb motor function. A significant negative correlation
was found between MABC-2 balance scores and JND thresholds (r = -0.50, p = 0.0001; see Fig.
4). The respective correlation between the balance score and SDPE was significant (r = -0.30, p
= 0.037), but not for PE (r = 0.01, p = 0.937).
 7

We then performed the same correlation analysis between measures of position sense acuity
and motor ability separately for each group to understand, if measures of proprioceptive acuity
predict motor ability within TD and DCD children. For DCD group, the results yielded no
significant correlation between proprioceptive measures and MABC-2 subscores (p’s > 0.05).
For TD group, only a significant negative correlation between MABC-2 balance scores and JND
thresholds (r = -0.40, p = 0.032).

-----Insert Figures 2, 3, 4 about here-----

PT
4 DISCUSSION
The present study investigated wrist position sense acuity in children with DCD. Given that

RI
upper limb function like manual dexterity is often poor in children with DCD, we sought to
understand, if wrist proprioception is systematically affected and how well proprioceptive status
may predict motor function in children with and without DCD. We employed two test protocols

SC
that utilized a newly designed wrist manipulandum device. One protocol tested “pure”
proprioceptive limb position sense, in which the wrist joint was passively moved and no
volitional movement of the child was required. The other required the child to actively match a

U
previously assumed joint position. The main results can be summarized as follows: First,
position sense acuity thresholds based on the passive displacement of the hand were highly
N
elevated in the DCD group with 65% of the children having thresholds above the maximum of
the control group. Second, active joint position matching showed no consistent increase in bias
A
or position error, but error variability was significantly higher in children with DCD when
compared to TD children. Third, elevated thresholds and greater SDPE of wrist position sense
M

correlated significantly with measures of upper and lower limb motor dysfunction in our sample
of children.
4.1 Wrist position sense acuity is reduced in DCD
D

At present, no simple, standardized protocol for proprioceptive assessment exists and

TE

consequently proprioceptive status is not routinely determined in children with DCD. This stands
in contrast to the long established notion that proprioceptive dysfunction may underlie the overt
motor deficits in DCD [8, 9, 12]. Our study provides objective evidence that limb position sense
is affected in children with DCD. The JND threshold of the DCD group was increased by 71%
EP

when compared to TD controls (see Fig. 3). This result complements recent work on passive
limb motion sense reporting that the time to detect forearm motion in 10-year-olds with DCD
was increased by 79% [10]. Extrapolating from our limited sample of 20 DCD children indicates
CC

that at the age of 10 years approximately 2/3 of the DCD population presents with reduced
proprioceptive acuity.
The pathomechanism that impairs proprioceptive function in DCD is poorly understood. At
A

present no distinct neural signature of DCD has been identified [3, 30, 31]. There is no evidence
of mechanoreceptor or peripheral nervous impairment to explain proprioceptive dysfunction in
DCD. Moreover, abnormal processes of sensorimotor integration or motor control in DCD
cannot account for the observed reduced proprioceptive acuity given that the proprioceptive
impairment was measurable in the absence of volitional movement. That is, the proprioceptive
deficit is not explainable as a confound of motor planning or motor execution problems. It is also
not explained by assuming that children with DCD were systematically hypertonic or that
involuntary muscle contractions consistently accompanied the passive displacement of the
 8

wrist/hand. While children with DCD may reveal abnormal muscle tone, hypotonia and not
hypertonia is more common [32]. Moreover, concentric muscle contractions during passive
movement shorten intrafusal spindle fibers, which would increase muscle spindle sensitivity.
However, heightened stretch sensitivity also improves perceptual acuity, which was not observed
in our cohort of children with DCD. Thus, the observed perceptual deficit rather points to an
abnormal sensory processing of proprioceptive signals. Similar proprioceptive acuity deficits are
observed in diseases affecting the cortico-basal ganglia-thalamo-cortical circuitry such as
dystonia and Parkinson’s disease (for reviews see [6], Konczak and Abbruzzese [33]). Impaired

PT
position sense judgments are not consistent with cerebellar damage. Although the cerebellum
receives massive proprioceptive input via the spinocerebellar tract, position sense judgments of
patients with cerebellar ataxia are normal [34]. This conclusion warrants a caveat. Abnormal

RI
perceptual thresholds do not imply that processes of sensorimotor integration and motor control
are unaffected or the cerebellum is not implicated in DCD. In fact, recent imaging evidence
suggests that cerebellar dysplasia can underlie DCD [4].

SC
4.2 Abnormal precision, but not bias during active joint position matching
Children with DCD did not show an elevated perceptual bias during the active joint position
matching task – a finding consistent with Adams et al. (2016). While the position error as a

U
measure of bias was not systematically increased, error variability was significantly higher in the
DCD cohort (see Fig. 2). This implies that perceptual precision or response repeatability is
N
affected in children with DCD. On a first glance, it seems surprising that proprioceptive bias is
abnormal for threshold, but not for position matching testing. However, the results are actually
A
consistent with a recent study on the typical development of forearm position sense that also
employed a joint position matching paradigm and showed that position sense development
M

during childhood is characterized by an age-related increase in precision (i.e. reduced random

error), not a decrease in bias [23]. That is, the proprioceptive development of children with DCD
follows a similar trajectory, but with respect to their TD cohort, children with DCD are
D

proprioceptively less precise or delayed [10].

Nevertheless, clinicians and researchers need to recognize that an active joint matching
TE

method does not test “pure” sensory function, but sensorimotor function. It does require an
action and consequently involves voluntary motor control networks. Volitional motor commands
involve cortico-cerebellar efference copy mechanisms used to generate predicted sensory
EP

feedback. With respect to typically developing children, previous research has shown that motor
commands add noise to such internal feedback and degrade haptic perception [22]. It is therefore
plausible that motor interference plays a role in the perceptual deficits in DCD, although we
currently lack solid empirical evidence to substantiate this claim.
CC

4.3 Relationship between proprioception and motor function

Children with DCD are known to have difficulties with fine motor skills such as hand writing
or drawing, and may exhibit balance problems. Given that a link between proprioceptive and
A

motor dysfunction in children with DCD has long been proposed, we examined to what extent
wrist proprioceptive acuity correlates with upper and lower limb motor measures. Our results
show that the MABC-2 manual dexterity score negatively correlates with proprioceptive JND
thresholds meaning that children with higher thresholds tend to have poorer fine motor control.
JND wrist thresholds also correlated significantly with the MABC-2 balance score, implying that
upper limb proprioceptive status can serve as a predictor of lower limb balance function. While
both of these findings confirm a link between the motor and sensory signs in children with and
 9

without DCD, the one needs to recognize that wrist position sense acuity predicts only about 16-
25% of the variance of the MABC-2 motor measures (see Fig. 4). Furthermore, when collapsed
data across DCD and TD group, the relationship between proprioceptive measures and MABC-2
motor scores was not significant. Possible explanations for this lack of a strong relationship are
twofold: First, the MABC-2 instrument does not target wrist movement specifically. Thus, one
may argue, it is surprising to find a significant correlation, at all. In other words, to expect a
higher correlation than found here, one likely needs to couple measures of wrist proprioceptive
acuity with distinct measures of wrist motor performance. Second, the neural networks involved

PT
in somatosensory processing overlap with sensorimotor networks, but they are not identical. That
is, one should not and cannot expect to see a very tight relationship between proprioceptive and
motor measures.

RI
5 LIMITATIONS OF THE STUDY AND FUTURE DIRECTIONS
Several limitations of this study need to be acknowledged. First, our sample of children with

SC
DCD was not a clinical sample, that is, a sample examined by neurologist for other neurological
deficits. However, we followed a protocol established in previous studies [11, 35] that screened
children using the MABC-2 test [26]. We considered children to present with DCD, if their total

U
MABC-2 score fell below the 5th percentile of the norm population. In addition, we asked parents
to share information on other diagnosed neurodevelopmental or neurological abnormalities.
N
Thus, while we cannot fully exclude the possibility that some of the children presented with
other neurological signs, it is highly unlikely that the documented proprioceptive deficits of our
A
DCD group are fully explained by other underlying neurological diseases known to affect
somatosensation such as peripheral neuropathy or cerebral palsy. Second, the experimental
M

protocol was limited as only one reference position (20° wrist flexion) was tested. It would have
been desirable, but logistically not possible, to examine position sense acuity at several joint
positions, mapping the complete wrist joint workspace. Third, in the joint position matching task,
D

only five trials were collected for each child. While we found that proprioceptive precision
degrades during active matching in children with DCD, we could not confirm differences in bias.
TE

We cannot exclude the possibility that additional trials per participant would have yielded
significant differences in bias.
EP

6 CONCLUSION
This study documents that DCD is associated with proprioceptive dysfunction of the
wrist/hand complex, which likely contributes to the fine motor problems in children with DCD.
CC

The fact that low proprioceptive acuity of the wrist negatively correlates with MABC-2 balance
scores, and recent research reporting that elbow and wrist joint proprioception can be impaired in
DCD [35] supports the notion that proprioceptive dysfunction in children with DCD is probably
generalized in nature.
A

ACKNOWLEDGEMENT
We sincerely thank the students for their participation and the administration of the two schools
for accommodating the data collection. This study was funded through a research grant from the
Center for Translational Sensory Science at the University of Minnesota to YT, through research
development funds of JK, and through research funds from CT and FC.
 10

References

[1] American Psychiatric Association, Diagnostic and statistical manual of mental disorders:
DSM V. 2013, Washington, DC: American Psychiatric Association.
[2] Lingam, R., et al., Prevalence of developmental coordination disorder using the DSM-IV at 7
years of age: a UK population-based study. Pediatrics. 123 (2009) e693-700.
[3] Biotteau, M., et al., Neural signature of DCD: A critical review of MRI neuroimaging
studies. Front Neurol, 7 (2016) 227.

PT
[4] Mariën, P., et al., Developmental coordination disorder: disruption of the cerebello-cerebral
network evidenced by SPECT. Cerebellum. 9 (2010) 405-410.
[5] Hillier, S., M. Immink, and D. Thewlis, Assessing Proprioception A Systematic Review of

RI
Possibilities. Neurorehabil Neural Repair. 29 (2015) 933-949.
[6] Konczak, J., et al., Proprioception and motor control in Parkinson's disease. J Mot Behav. 41
(2009) 543-552.

SC
[7] Livesey, D.J. and N.A. Parkes, Testing kinaesthetic acuity in preschool children. Australian
Journal of Psychology. 47 (1995) 160-163.
[8] Bairstow, P.J. and J.I. Laszlo, Kinaesthetic sensitivity to passive movements and its
relationship to motor development and motor control. Dev Med Child Neurol. 23 (1981)

U
606-16.
[9] Coleman, R., J.P. Piek, and D.J. Livesey, A longitudinal study of motor ability and
N
kinaesthetic acuity in young children at risk of developmental coordination disorder.
Hum Mov Sci. 20 (2001) 95-110.
A
[10] Li, K.-Y., et al., Kinesthetic deficit in children with developmental coordination disorder.
Res Dev Disabil. 38 (2015) 125-133.
M

[11] Adams, I.L., et al., Action planning and position sense in children with Developmental
Coordination Disorder. Hum Mov Sci. 46 (2016) 196-208.
[12] Smyth, M.M. and U.C. Mason, Use of proprioception in normal and clumsy children. Dev
D

Med Child Neurol. 40 (1998) 672-681.

[13] Pick, J.P. and R. Coleman‐Carman, Kinaesthetic sensitivity and motor performance of
TE

children with developmental coordination disorder. Dev Med Child Neurol. 37 (1995)
976-984.
[14] Smyth, M.M. and U.C. Mason, Planning and execution of action in children with and
EP

without developmental coordination disorder. Journal of Child Psychology and Psychiatr.

38 (1997) 1023-1037.
[15] Hoare, D. and D. Larkin, Kinaesthetic abilities of clumsy children. Dev Med Child Neurol.
CC

33 (1991) 671-678.
[16] Lord, R. and C. Hulme, Kinaesthetic sensitivity of normal and clumsy children. Dev Med
Child Neurol. 29 (1987) 720-725.
[17] Visser, J. and R. Geuze, Kinaesthetic acuity in adolescent boys: a longitudinal study. Dev
A

Med Child Neurol. 42 (2000) 93-96.

[18] Doyle, A., J. Elliott, and K. Connolly, Measurement of kinaesthetic sensitivity. Dev Med
Child Neurol. 28 (1986) 188-193.
[19] Sciutti, A., et al., Predicted sensory feedback derived from motor commands does not
improve haptic sensitivity. Exp Brain Res. 200 (2010) 259-267.
[20] Konczak, J., et al., Parkinson’s disease accelerates age-related decline in haptic perception
by altering somatosensory integration. Brain. 135 (2012) 3371-3379.
 11

[21] Elangovan, N., A. Herrmann, and J. Konczak, Assessing proprioceptive function: evaluating
joint position matching methods against psychophysical thresholds. Phys Ther. 94 (2014)
553-561.
[22] Gori, M., et al., Motor commands in children interfere with their haptic perception of
objects. Exp Brain Res. 223 (2012) 149-157.
[23] Holst-Wolf, J.M., I.-L. Yeh, and J. Konczak, Development of proprioceptive acuity in
typically developing children: normative data on forearm position sense. Front Hum
Neurosci, 10 (2016) 1-8.

PT
[24] Marini, F., et al., Robot-aided developmental assessment of wrist proprioception in children.
J Neuroeng Rehabil. 14 (2017) 3.
[25] Goble, D.J., E.A. Hurvitz, and S.H. Brown, Deficits in the ability to use proprioceptive

RI
feedback in children with hemiplegic cerebral palsy. Int J Rehabil Res. 32 (2009) 267-
269.
[26] Henderson, S.E., Sugden, D.A., Barnett, A, Movement assessment battery for children -

SC
Second edition (Movement ABC-2). 2007: Pearson.
[27] Goble, D.J., Proprioceptive acuity assessment via joint position matching: from basic
science to general practice. Phys Ther. 90 (2010) 1176-1184.
[28] Kingdom, F. and N. Prins, Psychophysics: A practical introduction. 2010, Amsterdam:

U
Elsevier.
[29] Prins, N., The psi-marginal adaptive method: How to give nuisance parameters the attention
N
they deserve (no more, no less). J Vis. 13 (2013) 1-10.
[30] Brown-Lum, M. and J.G. Zwicker, Brain imaging increases our understanding of
A
developmental coordination disorder: a review of literature and future directions. Curr
Dev Disord Rep. 2 (2015) 131-140.
M

[31] Peters, L.H., C.G. Maathuis, and M. Hadders‐Algra, Neural correlates of developmental
coordination disorder. Dev Med Child Neuro. 55 (2013) 59-64.
[32] Hadders-Algra, M., Developmental coordination disorder: is clumsy motor behavior caused
D

by a lesion of the brain at early age? Neural Plast. 10 (2003) 39-50.

[33] Konczak, J. and G. Abbruzzese, Focal dystonia in musicians: linking motor symptoms to
TE

somatosensory dysfunction. Front Hum Neurosci. 7 (2013) 1-10.

[34] Maschke, M., et al., Dysfunction of the basal ganglia, but not the cerebellum, impairs
kinaesthesia. Brain. 126 (2003) 2312-22.
EP

[35] Tseng, Y.T., Tsai, C.L., Chen, F.C., Konczak, J., Position sense dysfunction affects
proximal and distal arm joints in children with developmental coordination disorder. J
Mot Behav. 2017 Dec 27: p. 1-10.
CC
A
 12

FIGURE CAPTIONS
Figure 1: Experimental device. A) A wrist bimanual manipulandum was used for both the
position sense matching and psychophysical discrimination threshold testing. Adjustable handles
and movable base panels allowed to accommodate for differences in hand size and shoulder
width. B) Experimental setup with a child seated in front of the manipulandum. Here, the
researcher passively moved the child’s dominant, right hand and he then actively reproduced this
position with the same hand. The red lines depict starting neutral position of 0° and the reference
position at 20° wrist flexion. C) A pegboard base panel housed under the lever arm allowed to

PT
insert a metal pin into a hole to mark a distinct reference position.

RI
SC
U
N
A
M
D
TE
EP
CC
A
 13

Figure 2: Mean position sense bias (PE) and precision (SDPE) for both groups in the joint
position matching task. Error bars indicate one standard deviation.\

PT
RI
SC
U
N
A
M
D
TE
EP
CC
A
 14

Figure 3: Position sense JND thresholds. The upper panel depicts the psychophysical sensitivity
functions for both groups. The angular difference at the 75% correct response level represents
the JND threshold. Note that the curve for DCD children is shifted to the right giving rise to a
higher threshold. The lower panel shows the respective mean and standard deviation of the
individual subject JND thresholds for each group.

PT
RI
SC
U
N
A
M
D
TE
EP
CC
A
 15

Figure 4: Correlation between proprioceptive acuity and fine motor and lower limb motor
function. Each data point coordinates represent the individual JND threshold and the respective
MABC-2 score. Fine motor function is indicated by the MABC-2 manual dexterity score, lower
limb motor function score by the MABC-2 balance score.

PT
RI
SC
U
N
A
M
D
TE
EP
CC
A