Abnormal rhythmic
hyperactivity disorder (ADHD), manifested by restlessness, fid-
motor response in
children with
attention-deficit–
hyperactivity disorder
Hilla Ben-Pazi* MD;
Varda Gross-Tsur MD, Neuropediatric Unit, Shaare Zedek
Medical Center;
Hagai Bergman MD PhD, Department of Physiology, The
Hebrew University–Hadassah Medical School;
Ruth S Shalev MD, Neuropediatric Unit, Shaare Zedek
Medical Center, Jerusalem, Israel.
*Correspondence to first author at Neuropediatric Unit, Shaare
Zedeck Medical Center, PO 3235, Jerusalem 91031, Israel.
E-mail: shmaryaho@hotmail.com
Children with attention-deficit–hyperactivity disorder
(ADHD) have difficulties with motor control, inhibition of
motor responses, motor flexibility, and motor preparedness.
We proposed that motor abnormalities in ADHD might result,
at least in part, from an abnormal neuronal oscillatory
mechanism necessary for motor temporal regulation. The aim
of this study was to assess pacing in children with ADHD, by
testing for rhythmic abnormalities of motor activity using a
tapping test. Twenty-seven children (21 males, six females; aged
6 to 14 years 6 months; mean age 11 years 4 months, SD 2 years
2 months) diagnosed with ADHD according to DSM-IV clinical
criteria, and 33 controls (25 males, eight females; aged 6 to 14
years 6 months; mean 11 years 1 month, SD 2 years 2 months),
underwent a finger-tapping test requiring rhythmic responses to
frequencies from 1 to 6Hz. All participants who were treated on
a daily basis with methylphenidate (n=22) were medication-
free on the day of the test. Most of the children with ADHD
responded at a constant rate regardless of stimulus frequency, a
phenomenon only seen in a small number of the controls. This
specific error pattern, also seen in Parkinson’s disease, has been
attributed to an abnormal oscillatory mechanism mediated by
dopaminergic fronto-striatal circuitry, which might also be
pathophysiologically relevant for ADHD.
Developmental Medicine & Child Neurology 2003, 45: 743–745 743
Motor hyperactivity is a striking feature of attention-deficit–
getiness, and unnecessary gross motor movements (Zametkin
and Ernst 1999). Whereas much research has been devoted to
the neurophysiology of attention, the underpinnings of the
motor impairment in ADHD have been relatively neglected
(Barkley 1997). Accumulating evidence points to abnormali-
ties in the dopaminergic system and participating cortico-stri-
atal-thalamic neural loops (Aylward et al. 1996) reminiscent
of that in Parkinson’s disease (Bergman and Deuschl 2002).
Although ADHD and Parkinson’s disease differ in aetiology,
age, and clinical signs, it might be possible to use experimental
motor paradigms from patients with Parkinson’s disease to
study motor phenomena in ADHD. Patients with Parkinson’s
disease participating in a repetitive motor task, such as finger
tapping, can accjurately produce low frequencies, but with
higher-frequency stimuli they respond faster than the exter-
nal cue, i.e. getting ‘ahead of themselves’ (Nakamura et al.
1978). This ‘hastened’, voluntary response, termed ‘hasten-
ing phenomenon’, falls within the tremor frequency band of
Parkinson’s disease and by extrapolation is considered to
result from a central oscillatory mechanism (Logigian et al.
1991). The commonalities between the two disorders led us
to suggest that an abnormal neuronal oscillatory mechanism
might also have a role in the motor abnormalities of ADHD.
The object of this study was to explore whether children with
ADHD also demonstrate hastening phenomenon.
Method
PARTICIPANTS
We examined two groups of children, both attending the reg-
ular school system in a suburban neighbourhood. The group
with ADHD consisted of 27 children (21 males, six females)
aged from 6 to 14 years 6 months old (mean age 11 years 4
months, SD 2 years 2 months) from the Neuropediatric Unit at
Shaare Zedek Medical Center, Israel, diagnosed with ADHD by
an experienced pediatric neurologist according to DSM-IV
clinical criteria (Diagnostic and Statistical Manual of Mental
Disorders; American Psychiatric Association 1994) and stan-
dard behavioural questionnaires (Conners Abbreviated Rating
Scale [Goyette et al. 1978] and Child Behavioral Checklist
[Achenbach et al. 1991]), and who consented to participate.
The second group consisted of 33 control participants
matched for age (mean age 11 years 1 month, SD 2 years 2
months) and sex (25 males, eight females) drawn from a regu-
lar elementary school, without attention or hyperactivity
problems according to their teachers. The 22 children with
ADHD treated with methylphenidate on a regular basis were
free of medication for at least 24 hours before the tapping
test. Children with a significant hearing and visual impair-
ment or other neurological disorder were excluded before
testing. We explained the experimental procedure to the
children and parents, and informed consent was received.
The study was approved by the Internal Review Board of the
Shaare Zedek Medical Center.
TESTING PROCEDURE
Each child was seated comfortably in front of a laptop comput-
er in a quiet room. The child was asked to tap on the space bar
immediately after the simultaneously computer-generated
visual and auditory stimuli appeared. The combined use of
simultaneous visual and auditory stimuli was to help the child
to stay on task during the testing session. The stimuli appeared
at the following frequencies: 1, 2, 2.5, 3, 3.5, 4, 5, and 6Hz
(stimuli per second). The visual stimulus was a 2cm black
diamond and the auditory stimulus was a 35dB bleep, both
lasting 50ms. Forty stimuli were presented for each frequen-
cy; there was a 3-second interval between frequencies. The
testing session lasted 7 minutes. Because most of the chil-
dren, both controls and those with ADHD, failed to follow
the 6Hz stimuli, it was excluded from the analysis.
RECORDING ANALYSIS
We used customized programmes written in Matlab (Matworks,
Beltsville, MD, USA) previously employed for analysis of the fin-
ger-tapping responses in patients with Parkinson’s disease and
in adults without disabilities (Elazary et al. 2003).
Hastening phenomenon was described as a fast and con-
stant response frequency, but previous studies did not
provide a quantitative measure of this phenomenon. We
defined hastening phenomenon operationally according to
the following criteria. (1) Recurrent mistakes: median tap-
ping frequency faster or slower by 0.5Hz than the stimulus
frequency on at least 2 of the 10 frequencies. (2) Rapid
response: at least one of the median tapping frequencies
more than 0.5Hz above the requested stimulus. To deter-
mine whether the tapping responses were faster or slower
than that of the stimulus frequency, we subtracted the num-
ber of fast mistakes from the number of slow mistakes, divid-
ed by the total number of responses and multiplied by 100.
A positive percentage value indicated an overall tapping rate
faster than the stimulus frequency. (3) Constant response:
linear regression slope of the median mistaken frequencies
hovering around zero (less than 0.5) instead of an expected
slope of one.
Statistical difference between the groups was determined by
using χ2 test, t-test, ANOVA, and linear and logistic regression.
Results
Children with ADHD had difficulty modulating their response
rate in accordance with the frequency of the stimulus (Fig.
1c, d) unlike the controls, who changed their responses in tan-
dem with the stimulus (Fig. 1a, b). Children with ADHD tended
to tap faster than the stimulus presentation, thereby ‘getting
ahead of themselves’. Fifteen of the 27 children with ADHD ful-
filled all three criteria for hastening phenomenon, in compari-
son with 2 of the 33 controls (p<0.05). The hastened frequency
hovered between 2.8 and 4.7Hz (mean 3.8Hz, SD 0.6Hz).
(1) Recurrent mistakes: children with ADHD who demon-
strated hastening phenomenon (n=15) made errors on 2 to 7
of the 10 stimulus frequencies (mean 3.9Hz, SD 1.3Hz), in
comparison with 0 to 4 (mean 0.5Hz, SD 1.1Hz) of the controls
(p<0.05). (2) Rapid response: all children with hastening phe-
nomenon had a rapid response. Tapping responses of children
with ADHD were faster than those of controls, i.e. 8.9% (SD
23.3%) in comparison with –6.7% (SD 32%) respectively
(p<0.05); this effect could be attributed to the 15 children with
hastening phenomenon (mean 20.7%, SD 17%). The remain-
ing 12 children with ADHD responded similarly to controls
(ADHD mean –5.7%, SD 22.4%; controls mean –6.7%, SD 32%;
p=0.92). (3) Constant response: the slope of median errors by
frequency was horizontal (range 0.15 to 0.38; mean 0.1, SD
0.2) demonstrating a response frequency that was, for the most
part, constant regardless of the stimulus (Fig. 2).
We found a significant inverse correlation between age and
fast tapping responses for children with ADHD (r2=0.53,
p<0.05), a correlation not found among the controls (p=0.36).
There was no correlation between hastening phenomenon and
sex or handedness.
Discussion
More than half of the children with ADHD demonstrated a
response pattern that was constant and faster than the input

a b
Figure 1: Recording of tapping
Stimulus Adequate median response
Tapping response
test to frequencies in control
6 5
Output frequency (Hz)

and child with ADHD.

5 Tapping tested from 1 to 6Hz
Frequency (Hz)

4
4 in ascending and descending
3 order. (a) In control child,
3
2 response rate of finger-
2 tapping pattern (dots)
1 1 follows pace of the stimulus
(line). (b) When output is
0
100 200 0 1 2 3 4 5 plotted against input
Time (s) Input frequency (Hz) frequency, control child
c d demonstrated adequate
median response (squares),
Adequate median response
matching requested
6 5
Output frequency (Hz)

Errors frequencies, and slope

5
Frequency (Hz)

4 approaches 1. (c) For the child

4 with ADHD, however, there is
3 typical fixed frequency of
3
2 response rate (dots)
2 unrelated to input stimulus
1 1 (line). (d) Most tapping
responses defined as errors
0
100 200 0 1 2 3 4 5 (triangles), with an error
Time (s) Input frequency (Hz) slope approaching 0.

744 Developmental Medicine & Child Neurology 2003, 45: 743–745

frequency. This untoward ‘hastened’ voluntary response,
termed hastening phenomenon, has been documented in
patients with Parkinson’s disease and might reflect an underly-
ing oscillatory pathology in subcortical circuits (Logigian et al.
1991). The hastened response that we found in ADHD is, in our
opinion, a manifestation of motor abnormalities in ADHD and
is indicative of neither impulsivity nor an inability to follow
the task because it occurred in a distinct, constant, and rapid-
ly paced manner. Hastening phenomena were associated
with younger children in the ADHD group but not the controls,
suggesting that it is not a variant of normal development.
Rubia et al. (1999) found that boys with ADHD tapped sig-
nificantly faster at 2.5Hz but not at lower frequencies. They
concluded that their data could not support the hypothesis
of an accelerated internal pacemaker responsible for their
fast response style (Rubia et al. 1999). In our participants,
tapping abnormalities were also uncommon at frequencies
lower than 2Hz and were elicited mainly at higher frequen-
cies. We would argue that children with ADHD can follow
slow rhythmic stimuli but at higher frequencies their volun-
tary motor response is influenced by a dysfunctional central
oscillatory mechanism. Another abnormal oscillatory pat-
tern has been shown by Mann et al. (1972), who found that
children with ADHD have abnormal EEG theta activity (4 to
7.5Hz) in the frontal lobes: a frequency that, interestingly, is
within the same range as in this study.
Can a putative mechanism of abnormal oscillatory activity
be reconciled with the evidence of inhibitory deficits in ADHD?
(Barkley 1997, Moll et al. 2000). If there is indeed decreased
cortical neuronal inhibition in ADHD (Barkley 1997, Moll
et al. 2000), this could release underlying primitive oscilla-
tory mechanisms between the cortex and the basal ganglia.
Alternatively, abnormal subcortical oscillatory pathways might
produce a repetitive stimulus that can secondarily reduce
intracortical inhibition, as occurs in Parkinson’s disease
(Bergman and Deuschl 2002). Regardless of the precise phys-
iological mechanism, neuronal oscillations pulsating at a
Control
ADHD
15
Number of children
10
5 implications. Pediatr Neurol 8: 30–36.
–0.1 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9
Slope
Figure 2: Error slopes of controls and children with ADHD.
Histograms represent slopes of responses of control group
(white) and children with ADHD (black). Note that slopes of
controls cluster around 1, indicating an accurate response.
Children with ADHD had bimodal distribution of slopes.
Those with fixed response peaked at 0, whereas those with an
accurate response peaked at 1.
fixed frequency can affect voluntary repetitive motor activity.
There is evidence for the role of central pattern generators in
the execution of rhythmic voluntary movements (Cohen et al.
1988). Even the higher cortical function of writing is rhyth-
mic, with a clear preferred frequency (Kunesch et al. 1989). A
delineation of the underlying oscillatory mechanisms involved
in voluntary movements in children with ADHD might, there-
fore, lead to a better comprehension of the motor abnormali-
ties inherent in this disorder, with diagnositic and therapeutic
implications.
DOI: 10.1017/S0012162203001385
Accepted for publication 18th July 2003.
Acknowledgements
We thank Mrs Tamar Etzioni, principal, and the teachers and students
of Tzora Elementary School for their cooperation and participation;
and Gilad Fernandens for statistical analysis. This study was
supported in part by a grant from the Joshua Family Foundation, and
the National Institute of Psychobiology in Israel, founded by the
Charles E Smith Family.
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Abnormal Rhythmic Motor Response and ADHD Hilla Ben-Pazi et al. 745