You are on page 1of 5

Physical Therapy in Sport 14 (2013) 105e109

Contents lists available at SciVerse ScienceDirect

Physical Therapy in Sport


journal homepage: www.elsevier.com/ptsp

Original research

Timing perception and motor coordination on rope jumping in children with


attention deficit hyperactivity disorder
Ying-Yi Chen a, Lih-Jiun Liaw b, Jing-Min Liang a, Wei-Tso Hung a, Lan-Yuen Guo a, Wen-Lan Wu a, *
a
Department of Sports Medicine, Kaohsiung Medical University, 100, Shih-Chuan 1st Rd., Kaohsiung City, 80708, Taiwan
b
Department of Physical Therapy, Kaohsiung Medical University, Taiwan

a r t i c l e i n f o a b s t r a c t

Article history: Objectives: To evaluate timing perception ability and motor coordination in children with ADHD
Received 14 June 2011 (Attention Deficit Hyperactivity Disorder) while rope jumping at different rates.
Received in revised form Design and setting: Rope jumping at (1) a constant tempo of 100 for 15 s (RJ-C) and (2) two randomly
22 February 2012
permutated tempos (80, 100, or 120) for 15 s (RJ-V).
Accepted 6 March 2012
Main Outcome Measures: The “timing variation while jumping”, “timing variation while whirling”, and
“hand-foot deviation time” in each rope jumping cycle were recorded, to assess the time estimation
Keywords:
ability.
Attention-deficit/hyperactivity disorder
(ADHD)
Participants: 10 children with ADHD (9.65  1.27 years) and 10 children without ADHD (9.93  1.54
Timing years) were recruited.
Rope jumping Results: The ADHD group showed greater variation in time between the foot jumping and the rope
whirling tasks. Also, the median value of hand-foot deviation time was greater in the ADHD group
(3.34 ms) than in the control group (1.75 ms). In RJ-V, the control group was able to modify their pace
and respond to the target speed in the post-phase, while the ADHD group could not.
Conclusion: Impaired timing perception leads to less accurate performance during rope jumping for
ADHD children. The findings also reveal that poor hand-foot coordination results in poor control of
simultaneous movements of the upper and lower limbs during rope jumping.
Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction (Harrington, Haaland, & Hermanowicz, 1998). Previous studies have


indicated that children with ADHD have perceptual deficits in the
Time perception is the ability to estimate periods of time of clock component, such as in time production and reproduction,
coming events. Processing of timing in shorter intervals is based on which further influences their performance on motor timing tasks
skilled movements and cerebellar mechanisms without cognitive (Barkley, Murphy, & Bush, 2001; Van Meel, Oosterlaan, Heslenfeld,
control, whereas, in longer intervals, it is associated with attention & Sergeant, 2005; Yang et al., 2007).
and working memory (Lewis & Miall, 2003a,b; Rammsayer, 1999). When rope jumping, it is necessary to coordinate the upper and
Previous studies have indicated that processing of precise timing lower body to maintain balance and rhythm. Rope jumping can
tasks and longer timing intervals are associated with the cere- enhance the precise coordination of multiple muscle groups, which
bellum and basal ganglia (Ivry & Keele, 1989; Ivry & Spencer, 2004; is why it is used widely in athletic training programs (Lee, 2010).
Mangels, Ivry, & Shimizu, 1998). The network of right hemispheric Rope jumping combines the angular momentum of the rope and
frontocerebellar time discrimination has also been shown to be vertical displacement of the body (Pitreli & O’Shea, 1986). Also, rope
involved in timing tasks (Harrington, Haaland, & Knight, 1998; jumping involves upper and lower synchrony (hand-foot coordi-
Smith, Taylor, Lidzba, & Rubia, 2003). nation) where positioning and timing is critical (Pitreli & O’Shea,
The output of motor timing consists of two components: a clock 1986). The ability of time reproduction makes it possible to
component, which reflects time keeper intervals, and a motor reproduce specified time periods with great precision (Toplak,
delay component, which reflects motor implementation delay Dockstader, & Tannock, 2006). Rope jumping skill involves good
perception of time reproduction. However, poor motor timing
performance has been found in children with ADHD. It seems that
* Corresponding author. Tel.: þ886 7 3121101x2646; fax: þ886 7 3138359.
E-mail address: wenlanwu@kmu.edu.tw (W.-L. Wu).
timing abnormalities have been related to impulsiveness, a core

1466-853X/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ptsp.2012.03.012
106 Y.-Y. Chen et al. / Physical Therapy in Sport 14 (2013) 105e109

clinical symptom of ADHD (Rubia, 2002; Rubia, Halari, Christakou, by CD player. Each participant was allowed to take a rest during this
& Taylor, 2009). It has been found that children with ADHD study. Muscle fatigue was not an issue.
show less activity in regions including the prefrontal and precentral Firstly, subjects were required to jump the rope at a constant
gyri, basal ganglia, cerebellum, inferior parietal lobule, superior tempo of 100 for 15 s (RJ-C). After 10 min rest, they were asked to
temporal gyri, and insula, which are associated with sensorimotor jump at variable speeds, consisting of the tempos of 80e100,
timing (Valera et al., 2010). Thus, they have demonstrated deficits 80e120, 100e80, 100e120, 120e80, and 120e100, for 15 s (RJ-V),
in time perception including shorter reproductions and greater respectively, in a random order. Each participant was allowed to
reproduction errors than healthy children (Barkley et al., 2001). take a 3 min rest between these 6 trials. Under RJ-V, the tempo was
ADHD children have been shown to be impaired at maintaining changed at around the 6the7th second during each trial. The tempo
a chosen tapping rhythm synchronously and in responding to of sound for each trial had been recorded before the experiment
organize their motor output (Rubia, Taylor, Taylor, & Sergeant, and was played continuously by CD player. Participants were
1999). Children with ADHD showed poor ability to plan events instructed to do their best to follow the tempo and were required to
which are separated by time (Barkley, 1997). Also, children with jump inside the edges of the force platform. Each subject was
ADHD have problems executing motor output (Pennington & instructed to finish 2 trials on RJ-C and only 1 trial on each RJ-V task
Ozonoff, 1996) and they exhibit slow output on automatic pro- to achieve a total of three acceleration trials and three deceleration
cessing tasks (Carte, Nigg, & Hinshaw, 1996). It has been suggested trials. If a subject tripped on the rope and failed on the task, then
that children with ADHD have difficulty adjusting their speed to they were asked to do more trials. The number of failures was
motor tasks with external cues (Carte et al., 1996). recorded.
Much evidence exists to suggest that children with ADHD have
impairments in fine motor timing when executing finger tapping 2.4. Data analysis
tasks. However, few studies have focussed on gross motor timing.
Through clinical observation, it was found that children with ADHD The recurrent period of jumping (foot jumping cycle) was defined
showed poor performance when rope jumping. It has been sug- as the time span from when the ground reaction force first excee-
gested that problems with timing perception and motor coordi- ded 10 N until the next time the ground reaction force exceeded
nation might be the reason. Thus, in this study, a series of rope 10 N, and so on. Similarly, the period of the rope cycle (rope whirling
jumping tasks involving different rope jumping rates was designed cycle) was defined by the rope marker reaching the lowest point
to evaluate the timing perception ability and motor coordination of and contacting ground. The “timing variation in jumping” and
ADHD children. “timing variation in whirling” were calculated as the absolute value
of the difference between 60 and the foot jumping cycle or rope
2. Methods whirling cycle, respectively; multiplied by the reciprocal of the
tempo. The timing variation is the inconsistency between the
2.1. Subjects manipulation of time by the performer and the expected manipu-
lation of time for the task, the symptom of which is either an
Five boys and five girls, with a mean age of 9.65  1.27 years, extended performance time or a shortened one compared with the
diagnosed as ADHD by a local hospital and without other combined expected time. Moreover, we subtracted the timing variation in
syndromes, were recruited in this study. Ten age-matched non- whirling from the timing variation in jumping and found the
ADHD children (4 boys, mean age 9.93  1.54 years), without ADHD absolute value to define the “hand-foot deviation time”.
symptoms or other neuromuscular symptoms, were recruited from In the RJ-C task, two trials were analyzed. Each trial of the RJ-C
local schools as the control group. Rope jumping was already a part task was analyzed from 4 to 9 s. In the RJ-V task, 6 different tasks
of the physical education curriculum at the time of data collection. were analyzed. Moreover, each trial of the RJ-V tasks was separated
Informed consent, approved by the university ethical review into three phases, which were selected as pre-phase (4e5 s), mid-
committee, was obtained from parents prior to involvement in the phase (6e7 s), and post-phase (8e9 s). Finally, the mean values for
study. hand-foot deviation time, timing variation in foot jumping, and
timing variation in rope whirling from all the available rope
2.2. Material jumping cycles of the RJ-C and RJ-V tasks were recorded.

A force plate (Kistler Instrument Corp, Winterhur, Switzerland) 2.5. Statistical analysis
with the sample rate of 1000 Hz was used to record the flight
timing of rope jumping. A six-camera motion capture system A non-parametric test (Mann Whitney U test) was used to assess
(Qualisys Motion capture Systems, Qualisys AB, Sweden), with the time difference between the ADHD group and the control group
a sample rate of 100 Hz, was used to capture rope movement using for RJ-C and RJ-V from 4 to 9 s. Also, a Mann Whitney U test was
a reflective label attached to the distal end of the rope. Further- used to assess the difference between successful trials and failed
more, the rhythm, as controlled by a metronome, was recorded by trials for RJ-C. The statistical significance for paired comparisons
a CD player for use as our target signal before the test. between each phase was calculated using Wilcoxon Signed-Rank
test method. All analyses were performed using SPSS 17.0 soft-
2.3. Procedure ware (SPSS Inc., USA). Results were considered statistically signifi-
cant when the p-value was less than 0.05.
A reflective label was stuck to the distal end and on the middle
of the rope in order to record the trajectory of the rope. Two 3. Results
reflective markers were stuck on each side of the third metatarsal
head to help judge the flight phase and landing phase during rope Fig. 1(a) displays the median value of hand-foot deviation time
jumping. Subsequently, participants were asked to warm up by from 4 to 9 s across the groups for the RJ-C task. The median value
doing rope jumping for at least 15 s before the formal rope jumping of hand-foot deviation time was greater in the ADHD group
test; they then practiced three cycles at each tempo; 80, 100 and (3.34 ms), compared to the control group (1.75 ms) (p<.01, Table 1).
120. The sounds at the various tempi were played during the task Moreover, no falls were found in the control group, but some
Y.-Y. Chen et al. / Physical Therapy in Sport 14 (2013) 105e109 107

ADHD-participants fell during the RJ-C task. The median value of


a hand-foot deviation time was greater in falling trials (7.77 ms) than
successful trials (3.34 ms) in the ADHD group (p<.05, Table 1).
Fig. 1(b) displays the median of hand-foot deviation time from 4 to
9 s across the groups in the RJ-V task. Also, we found a significant
difference in hand-foot deviation time between groups on the RJ-V
task (p<.01, Table 1). The median value of hand-foot deviation time
was greater in the ADHD group (4.89 ms) than in the control group
(2.93 ms, p<.01, Table 1). Furthermore, each trial of RJ-V tasks was
separated into three phases, including pre-phase (4e5 s), mid-
phase (6e7 s), and post-phase (8e9 s), to examine their timing
variation in foot jumping and timing variation in rope whirling in
different phases. Fig. 2 shows performance in foot jumping and
rope whirling across the groups in the three phases. It was found
that the ADHD group presented greater variation time in both the
foot jumping and rope whirling cycle than did the control group.
Further, Wilcoxon Signed-Rank test for paired comparisons
between the timing variations in each phase were performed
(Table 2). In the control group, the timing variation in foot jumping in
the mid-phase was 12.99 ms (Table 1) greater than it was in the pre-
b phase (4.39 ms, Table 1) (p<.05, Table 2). Also, in the ADHD group,
significantly greater timing variations in foot jumping were found in
the mid-phase (15.13 ms) and post-phase (15.35 ms) than in the pre-
phase (4.15 ms) (p<.05 in mid-phase; p<.05 in post-phase, respec-
tively, Table 2). In the control group, the timing variation in rope
whirling in the mid-phase was higher than in the pre-phase (p<.05,
Table 2). In the ADHD group, the timing variations in rope whirling in
the mid-phase (18.21 ms) and post-phase (12.78 ms) were signifi-
cantly greater than in the pre-phase (6.00 ms) (p<.05 in mid-phase;
p<.01 in post-phase, respectively, Table 2).

4. Discussion

In this study, the ADHD group demonstrated greater timing


variation in both RJ-C and RJ-V tasks (Table 1). Moreover, it is
interesting to note that the ADHD group showed greater variation
time in the RJ-V task than in the RJ-C task. This suggests that control
Fig. 1. (a) The interquartile range and median of hand-foot deviation time measured group subjects could follow the given rate with less timing vari-
for each group in the task of RJ-C. (b) The interquartile range and median of hand-foot ability when processing rope jumping; while the ADHD group
deviation time measured for each group in the task of RJ-V. could not. It also suggests that when conditions changed, the
symptoms of ADHD interfered with motor timing performance.
Previous studies have shown that greater variability in motor
Table 1 timing is obvious in children with ADHD (Pitcher, Piek, & Barrett,
Descriptive statistics for hand-foot deviation time (ms), timing variation in foot 2002; Rommelse et al., 2008; Rubia et al., 1999). Through func-
jumping (ms), and timing variation in rope whirling (ms) across group, and the tional magnetic resonance imaging, individuals with ADHD have
statistical significance of the hand-foot deviation time (ms) between groups and
between success trials and falling trials (median with interquartile range in
parentheses).

ADHD Control p-value


Hand-foot coordination
Hand-foot deviation time (ms)
RJ-C (40 e90 ) Success trails 3.34 (4.33/1.33) 1.75 (2.78/1.13) .005**
Failing trails 7.77 (12.13/5.86) N/A
p-value .028* e
RJ-V (40 e90 ) 4.89 (8.63/3.73) 2.93 (3.33/2.51) .003**

Foot jumping cycle


Timing variation in foot jumping (ms)
Pre-phase (40 e50 ) 4.15 (21.33/2.75) 4.39 (17.00/2.33)
Mid-phase (60 e70 ) 15.13 (32.75/11.11) 12.99 (17.64/7.00)
Post-phase (80 e90 ) 15.35 (25.43/6.11) 9.22 (11.56/4.38)

Rope whirling cycle


Timing variation in rope whirling (ms)
Pre-phase (40 e50 ) 6.00 (22.17/4.47) 6.30 (15.78/4.04)
Mid-phase (60 e70 ) 18.21 (27.58/12.11) 13.77 (17.89/6.75)
Post-phase (80 e90 ) 12.78 (24.71/8.11) 9.74 (11.17/3.94)

N/A denotes no falling trial; e denotes no p-value. Fig. 2. The median value of timing variation in foot jumping and rope whirling across
*Denotes p-value < 0.05; **denotes p-value < 0.01. groups in the pre, mid and post-phase in the task of RJ-V.
108 Y.-Y. Chen et al. / Physical Therapy in Sport 14 (2013) 105e109

Table 2 movements. ADHD-participants showed a big drop in overall


The pairwise comparison across the median value on timing variation in foot performance on the RJ-C task and on the RJ-V task with a higher hand-
jumping and timing variation in rope whirling, respectively.
foot deviation time. Simultaneously, the ADHD individuals tripped up
p-value more than the others. No control group subject failed on any of the
ADHD (n ¼ 10) Control (n ¼ 10) tasks. The experimental results showed that there was greater hand-
Timing variation in Pre-phase Mid-phase .015* .017* foot deviation time (7.77 ms, Table 1) in falling trials. This may suggest
foot jumping Post-phase .015* .074 that values of hand-foot deviation time closer to zero represent
Timing variation in Pre-phase Mid-phase .015* .009** jumpers who manifest synchronous activation of upper and lower
rope whirling Post-phase .008** .203
extremities during rope jumping. Better performance in rope jump-
*Denotes p-value < 0.05; **denotes p-value < 0.01. ing leads to good ability in motor coordination. Therefore, this
suggests that ADHD individuals were poor in controlling simulta-
been shown to have less activity in the prefrontal region, basal neous movements of the upper and lower limbs when facing high
ganglia, and cerebellum, which are associated with sensorimotor quality motor coordination tasks. Further study, testing other coor-
timing, resulting in wild variability in timing mechanisms (Valera dination tasks is suggested to understand with greater confidence the
et al., 2010). Previous studies have used tapping tasks to measure overall breakdown in hand-foot coordination in ADHD.
the variability of motor output in response to an external cue (Kalff There were some limitations to this study. Rope jumping is
et al., 2005; Rommelse et al., 2008). Children with ADHD displayed a gross motor performance task, combining upper and lower limbs.
impairments in duration discrimination on timing tasks (Toplak, A child’s ability to perform this motor skill depends on a number of
Rucklidge, Hetherington, John, & Tannock, 2003; Yang et al., 2007); factors, including muscle strength, coordination, flexibility, range of
therefore, poor timing performance causes them to show slower motion, cardiopulmonary endurance, and so on. Muscle strength
responses and more variability in processing sequential tapping variations in different school-age children may be an issue that
tasks (Kalff et al., 2005; Pitcher et al., 2002; Rommelse et al., 2008). influences their performance. Therefore, further studies are sug-
The findings of this study reveal that the ADHD group showed gested to investigate each participant’s muscle strength and then
greater timing variation on the RJ-C and RJ-V than did the control observe their performance in coordination tests. In this study, this
group, which means less accurate performance when emulating the factor was excluded by asking each participant to do rope jumping
target signal. The impaired timing perception in ADHD children 15 s before this study in order to observe their ability on rope
indeed causes less accurate performance during rope jumping. jumping. If they could not complete it, they were considered to
The RJ-V task was separated into three phases: pre- (4e5 s), mid have weak muscle strength and endurance and were excluded from
(6e7 s), and post- (8e9 s), to observe subjects’ adaptations in each this study. Leaving aside the muscle strength problem, and taking
phase. After the rate changed, timing variation in foot jumping and all other experiential elements to be the same, the performance
timing variation in rope whirling in the post-phase did not differ criterion set up in this study may serve as a reliable diagnostic
from those in the pre-phase in the control group (p ¼ .07 in foot marker for this complex challenge of observing the precision of
jumping; p ¼ .20 in rope whirling, Table 2). This indicates that the internal timing perception in conjunction with motor coordination
foot jumping and rope whirling performances were the same in ability. Moreover, cordless jump rope may be useful to construct
pre-phase and post-phase. This suggests that control group a simple task to compare rope jumping with and without rope to
subjects had the ability to adapt quickly to a given rate and dis- observe gross motor coordination skill.
played decreased timing variability in the post-phase. However, in
the ADHD group, the performance in foot jumping and rope 5. Conclusion
whirling in the post-phase still showed significant difference
compared to the pre-phase (p ¼ .02 in foot jumping; p ¼ .01 in rope The findings suggest that abnormalities in motor coordination
whirling, respectively, Table 2). This indicates that performance in and motor timing perception are present in ADHD children during
the pre-phase differs from that in the post-phase, without showing rope jumping. Longer hand-foot deviation time indicated poor rope
significant decline in timing variation in the post-phase, either in jumping performance. The findings reveal that the ADHD group
foot jumping or in rope whirling. This finding indicates that chil- had greater hand-foot deviation time in both RJ-C and RJ-V tasks.
dren with ADHD were impaired in time perception and reproduc- Due to the poor timing perception and motor coordination, most
tion, compared to children without ADHD. children with ADHD could not carry out tasks as well as children
In the task with longer time intervals (over 1 s); subjects relied without ADHD. Further studies could focus on specific training of
on attention and cognitive process (Nenadic et al., 2003). However, time perception skill as well as motor coordination for children
handling of short intervals (milliseconds) may be more related to with ADHD to improve their rope jumping skill.
an internal timing mechanism (Ivry, 1996). A previous study has
demonstrated that participants anticipated the following tone Conflict of interest
when the interval was less than 3-sec, and then tapped synchro- None declared.
nously with or before the tone, rather than hearing it (Mates,
Müller, Radil, & Pöppel, 1994). In this study, jumping intervals of Ethical approval
less than 1 s decreased the confounding influence from cognitive Informed consent, approved by the university ethical review
process. Excluding inferences from cognitive process, external cues committee, was obtained from parents prior to involvement in the
likes rope swing in a school yard jump rope, were not considered study.
relevant in this study. Thus, the poor performance on rope jumping
in this study was more related to ADHD children’s abilities with Funding
regard to time perception. None declared.
Previous research has also suggested that children with ADHD
have motor coordination deficiency in postural adjustment (Jucaite, Acknowledgments
Fernell, Forssberg, & Hadders-Algra, 2003), which also has a nega-
tive impact on daily life (Fliers et al., 2008). In this study, rope jumpers This work was supported by the National Science Council,
needed more skill for coordination of upper and lower limb Taiwan (NSC 97-2320-B-037-004-MY3). We are grateful to Mi-Chia
Y.-Y. Chen et al. / Physical Therapy in Sport 14 (2013) 105e109 109

Ma for providing the statistical consulting services from the Nenadic, I., Gaser, C., Volz, H. P., Rammsayer, T., Hager, F., & Sauer, H. (2003). Pro-
cessing of temporal information and the basal ganglia: new evidence from
Statistics Consulting Center, National Cheng Kung University.
fMRI. Experimental Brain Research, 148, 238e246.
Pennington, B. F., & Ozonoff, S. (1996). Executive functions and developmental
psychopathology. Journal of Child Psychology and Psychiatry and Allied Disci-
plines, 37, 51e87.
References Pitcher, T. M., Piek, J. P., & Barrett, N. C. (2002). Timing and force control in boys with
attention deficit hyperactivity disorder: subtype differences and the effect of
Barkley, R. A. (1997). Behavioral inhibition, sustained attention, and executive comorbid developmental coordination disorder. Human Movement Science, 21,
functions: constructing a unifying theory of ADHD. Psychological Bulletin, 121, 919e945.
65e94. Pitreli, J., & O’Shea, P. (1986). Sports performance series: rope jumping: the
Barkley, R. A., Murphy, K. R., & Bush, T. (2001). Time perception and reproduction in biomechanics, techniques of and application to athletic conditioning. Strength &
young adults with attention deficit hyperactivity disorder. Neuropsychology, 15, Conditioning Journal, 8, 5e13.
351e360. Rammsayer, T. H. (1999). Neuropharmacological evidence for different timing
Carte, E. T., Nigg, J. T., & Hinshaw, S. P. (1996). Neuropsychological functioning, mechanisms in humans. Quarterly Journal of Experimental Psychology B,
motor speed, and language processing in boys with and without ADHD. Journal Comparative and Physiological Psychology, 52, 273e286.
of Abnormal Child Psychology, 24, 481e498. Rommelse, N. N., Altink, M. E., Oosterlaan, J., Beem, L., Buschgens, C. J., Buitelaar, J.,
Fliers, E., Rommelse, N., Vermeulen, S. H., Altink, M., Buschgens, C. J., Faraone, S. V., et al. (2008). Speed, variability, and timing of motor output in ADHD: which
et al. (2008). Motor coordination problems in children and adolescents with measures are useful for endophenotypic research? Behavior Genetics, 38,
ADHD rated by parents and teachers: effects of age and gender. Journal of Neural 121e132.
Transmission, 115, 211e220. Rubia, K. (2002). The dynamic approach to neurodevelopmental psychiatric disor-
Harrington, D. L., Haaland, K. Y., & Hermanowicz, N. (1998). Temporal processing in ders: use of fMRI combined with neuropsychology to elucidate the dynamics of
the basal ganglia. Neuropsychology, 12, 3e12. psychiatric disorders, exemplified in ADHD and schizophrenia. Behavioural
Harrington, D. L., Haaland, K. Y., & Knight, R. T. (1998). Cortical networks underlying Brain Research, 130, 47e56.
mechanisms of time perception. Journal of Neuroscience, 18, 1085e1095. Rubia, K., Halari, R., Christakou, A., & Taylor, E. (2009). Impulsiveness as a timing
Ivry, R. B. (1996). The representation of temporal information in perception and disturbance: neurocognitive abnormalities in attention-deficit hyperactivity
motor control. Current Opinion in Neurobiology, 6, 851e857. disorder during temporal processes and normalization with methylphenidate.
Ivry, R. B., & Keele, S. W. (1989). Timing functions of the cerebellum. Journal of Philosophical Transactions of the Royal Society of London Series B: Biological
Cognitive Neuroscience, 1, 136e152. Sciences, 364, 1919e1931.
Ivry, R. B., & Spencer, R. M. (2004). The neural representation of time. Current Rubia, K., Taylor, A., Taylor, E., & Sergeant, J. A. (1999). Synchronization, anticipation,
Opinion in Neurobiology, 14, 225e232. and consistency in motor timing of children with dimensionally defined atten-
Jucaite, A., Fernell, E., Forssberg, H., & Hadders-Algra, M. (2003). Deficient coordi- tion deficit hyperactivity behaviour. Perceptual and Motor Skills, 89, 1237e1258.
nation of associated postural adjustments during a lifting task in children with Smith, A., Taylor, E., Lidzba, K., & Rubia, K. (2003). A right hemispheric frontocer-
neurodevelopmental disorders. Developmental Medicine and Child Neurology, 45, ebellar network for time discrimination of several hundreds of milliseconds.
731e742. NeuroImage, 20, 344e350.
Kalff, A. C., De Sonneville, L. M., Hurks, P. P., Hendriksen, J. G., Kroes, M., Feron, F. J., Toplak, M. E., Dockstader, C., & Tannock, R. (2006). Temporal information processing
et al. (2005). Speed, speed variability, and accuracy of information processing in in ADHD: findings to date and new methods. Journal of Neuroscience Methods,
5 to 6-year-old children at risk of ADHD. Journal of the International Neuro- 151, 15e29.
psychological Society, 11, 173e183. Toplak, M. E., Rucklidge, J. J., Hetherington, R., John, S. C., & Tannock, R. (2003). Time
Lee, B. (2010). Jump rope training (2nd ed.). Champaign, IL: Human Kinetics. perception deficits in attention-deficit/hyperactivity disorder and comorbid
Lewis, P. A., & Miall, R. C. (2003a). Brain activation patterns during measurement of reading difficulties in child and adolescent samples. Journal of Child Psychology
sub- and supra-second intervals. Neuropsychologia, 41, 1583e1592. and Psychiatry and Allied Disciplines, 44, 888e903.
Lewis, P. A., & Miall, R. C. (2003b). Distinct systems for automatic and cognitively Valera, E. M., Spencer, R. M., Zeffiro, T. A., Makris, N., Spencer, T. J., Faraone, S. V.,
controlled time measurement: evidence from neuroimaging. Current Opinion in et al. (2010). Neural substrates of impaired sensorimotor timing in adult
Neurobiology, 13, 250e255. attention-deficit/hyperactivity disorder. Biological Psychiatry, 68, 359e367.
Mangels, J. A., Ivry, R. B., & Shimizu, N. (1998). Dissociable contributions of the Van Meel, C. S., Oosterlaan, J., Heslenfeld, D. J., & Sergeant, J. A. (2005). Motivational
prefrontal and neocerebellar cortex to time perception. Brain Research Cognitive effects on motor timing in attention-deficit/hyperactivity disorder. Journal of the
Brain Research, 7, 15e39. American Academy of Child and Adolescent Psychiatry, 44, 451e460.
Mates, J., Müller, U., Radil, T., & Pöppel, E. (1994). Temporal integration in sensori- Yang, B., Chan, R. C., Zou, X., Jing, J., Mai, J., & Li, J. (2007). Time perception deficit in
motor synchronization. Journal of Cognitive Neuroscience, 6, 332e340. children with ADHD. Brain Research, 1170, 90e96.

You might also like