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neuromotor deficits in
ADHD
J Steger PhD, Laboratory for Biomechanics, Eidgenssiche
Technische Hochschule (ETH) Zurich;
K Imhof PhD;
E Coutts lic phil;
R Gundelfinger MD;
H-Ch Steinhausen MD PhD;
D Brandeis*PhD, Department of Child and Adolescent
Psychiatry, University of Zurich, Switzerland.
*Correspondence to last author at Department of Child and
Adolescent Psychiatry, University of Zurich,
Neumnsterallee 9/ Postfach, CH-8032 Zrich, Switzerland.
E-mail: brandeis@kjpd.unizh.ch
172
Attention-deficithyperactivity disorder (ADHD) is characterized by developmentally inappropriate attention, overactivity, and impulsivity, but several lines of evidence suggest
that children with ADHD also have motor deficits. Some
research suggests that the overlap between ADHD and motor
deficits is close to 50% and therefore high enough to warrant a
separate diagnostic category (deficit in attention, motor control, and perception DAMP; Gillberg 1995) while other
research suggests that motor processing is typically unaffected
in ADHD (Leung and Connolly 1998). Such large discrepancies are likely to result from addressing different populations,
and from differences in the assessment and conceptualization
of motor deficits, ADHD, and their combination.
Motor deficits in ADHD have been assessed in a wide
range of tests. In the neuromotor assessment battery of
Denckla and Rudel (1978), the speed of pure motor functions is strongly represented. The time needed for repetitive
simple movements or movement sequences in the different
tasks, is measured for finger, hand, and foot. Denckla and
Rudel (1978), Carte and colleagues (1996), and Schuerholz
and coworkers (1997) all used these tasks to examine children with ADHD with a mean age below 10 years. Denckla
and Rudel (1978) reported that slowing of gross movements
(i.e. heeltoe taps) differentiated the ADHD and control
groups most accurately while Carte and colleagues (1996)
found that hand and foot movements were significantly
slower in children with ADHD. Both Denckla and Rudel
(1978) and Carte and colleagues (1996) showed that neuromotor parameters contributed significantly to group discrimination between children with ADHD and control
children. Schuerholz and colleagues (1997) reported that
even though children with ADHD showed no overall slowing of finger movements, they had a larger time discrepancy
between simple and patterned movements, and performed
fewer tasks within the age-appropriate speed limits than
children with Tourette syndrome. More subtle motor
deficits which affect movement quality rather than speed are
also found in ADHD. These include motor overflow, i.e.
involuntary associated movements such as mirror movements
(Denckla and Rudel 1978). Motor overflow also appears to correlate with inattentiveness in normally developing school-age
children (Waber et al. 1985, Lazarus and Todor 1991).
More complex tests of fine motor skills based on handwriting, manual dexterity, ball skills, and balance have also
indicated deficits in children with ADHD. However these
tests tend to measure both pure motor as well as visuomotor
or higher cognitive functions, similar to neuropsychological
frontal-lobe tests such as copying a complex design or maze
tracing. Compared to control children, children with ADHD
were found to have impaired handwriting skills (McMahon
and Greenberg 1977, Barkley 1990), poorer fine visuomotor
ability (Whitmont and Clark 1996), and poorer performance
in visuomotor frontal-lobe tests (review in Barkley et al.
1992). In addition, different types of motor deficits appear
to characterize different ADHD subgroups (Piek et al. 1999).
Children of the inattentive subtype of ADHD had significantly
poorer manual dexterity skills, whereas children of the combined subtype experienced greater difficulty with balance.
Direct experimental manipulation of premotor processing
via low or irregular event rate (Chee et al. 1989, van der Meere
et al. 1992, Fldnyi et al. 2000) or via stimulusresponse
incompatibility (van der Meere et al. 1989) have also revealed
Method
PARTICIPANTS
Age
Sex (F/M)
IQ
CBCL attention problems
(T-scores)
Comorbidity (nr children)
Multiple comorbidities
Single comorbidity
ODD
CD
Phobias
ADHD
n=22
Full group
Control
n=20
10.93
3/19
98.67
66.13
10.55
3/17
105.56
43.10
4
10
11
2
5
ADHD
n=14
Subgroup
Control
n=14
>0.3
<0.05
<0.0001
10.54
0/14
101.43
64.31
10.78
0/14
104.10
43.11
>0.3
<0.0001
2
8
7
1
4
>0.5
CBCL, Child Behavior Checklist; ODD, Oppositional defiant disorder; CD, Conduct disorder.
NEUROMOTOR ASSESSMENT
10 (N)
Right hand
Left hand
0 ms
800 ms
200 ms
Force (N)
Right hand
Left hand
Time
0s
1.65 s
3.3 s
4.95 s
Figure 1: Selected stimuli (not drawn to scale) and force-pulse analysis in reaction-time test. Pulses in force curves for left
(bottom) and right (top) hand reflect correct responses for this arbitrary stimulus sequence. Inset: black line indicates,
correct; dashed small lines indicate incorrect; and dashed multipeak lines indicate imperfect right-hand responses to right
unilateral target. (a), parameters force-onset latency, (b) time from force onset to force peak, (c) peak force.
174
peak force had to be higher than 0.5 N (grey box in Fig. 1).
In addition to the traditional error types (omission and
commission errors, side errors, unilateral responses in the
bilateral condition, and bilateral responses in unilateral conditions), several imperfect but correct responses were coded
and analysed. These were: (1) trials with force-onset latencies shorter than 200 ms or longer than 800 ms, (2) trials with
mirror movements (correct but additional response pulses
below 0.5 N with the incorrect hand, see Fig. 1), (3) trials
with multiple force peaks (see Fig. 1), and (4) trials with
poor synchronization of bilateral responses (defined as
force-onset latency differences of more than 60 ms ). These
imperfect responses were not included in the total error
count in order to maintain compatibility with previous error
analyses. All errors were transformed into percentages and
time measures were log transformed (base 10).
DATA ANALYSIS
Results
Table I shows that the mean IQ was lower for children with
ADHD than for control children whereas the analysis of the
subgroups (n=14 for each group, males only) showed no
significant IQ differences. According to the CBCL, children
with ADHD had significantly higher attention-problem scores
than control children. No significant age differences between
the ADHD and control children were found.
NEUROMOTOR ASSESSMENT
The multivariate analysis of the neuromotor measures indicated that whether children with ADHD needed more time to
complete movements than control children depended on the
extremity (group extremity, F[2,37]=3.77, p<0.05). Posthoc analysis of this interaction indicated that the additional
time needed to complete finger compared to hand movements was increased in the ADHD group (group extremity,
F[1,38]=7.27, p<0.01), but none of the three extremities
revealed slowing when tested individually except for a trend
for slower finger movements (F[1,38]=3.22, p=0.08).
Univariate analysis also showed no significant group differences (see Table II) and only a trend for slower sequential finger movements in the ADHD group (F[1,38]=2.89, p=0.1).
A main effect of extremity (F[2,37]=4.96, p<0.05) indicated that finger and foot movements were slower than
hand movements. Patterned movements were slower than
simple movements (8.41 versus 5.84 seconds, F[1,38]=10.44,
p<0.01). In addition, the covariate age significantly affected
the time to complete movements, F[1,38]=8.00, p<0.01).
The negative correlations between age and time to complete
finger (r=0.260, p=0.048), hand (r=0.436, p=0.002), and
foot (r=0.318, p=0.02) movements indicated that younger
children were slower with all extremities. No significant
resutls were obtained for the covariate IQ.
REACTION -TIME TEST
Finger
Repetition
Sequention
Hand
Pat
Pronationsupination
Foot
Toe taps
Heeltoe
ADHD (n=22)
Controls (n=20)
5.85 (1.28)
10.37 (2.47)
5.68 (1.10)
8.87 (2.06)
4.84 (1.13)
7.00 (1.30)
5.07 (1.09)
6.88 (1.29)
7.20 (2.19)
9.23 (3.17)
6.39 (1.25)
8.10 (2.25)
Control (n=20)
Unilateral
Bilateral
421.7 (70.8)c
110.3 (26.7)c
228.8 (52.3)a
15.5 (9.0)a
445.2 (85.5)a
109.3 (27.1)a
221.6 (49.0)a
12.0 (10.0)a
415.2 (72.6)
84.2 (13.0)
197.7 (39.2)
6.8 ( 3.0)
439.9 (68.2)
85.5 (15.4)
188.1 (42.5)
2.7 (2.3)
13.0 (11.7)a
18.0 (11.3)c
4.5 (10.1)c
12.1 (7.7)b
6.9 (6.1)a
3.2 (3.5)a
1.0 (2.0)a
7.4 (5.3)d
3.8 (3.6)d
6.6 (15.3)d
17.4 (13.1)d
3.8 (10.4)d
5.5 (6.9)c
19.0 (9.2)c
2.5 (3.3)c
2.8 (5.2)dd
10.7 (5.0)d
5.3 (3.3)
8.2 (4.7)
0.8 (1.6)
6.5 (3.7)
2.2 (2.1)
2.0 (3.9)
0.6 (0.9)
3.9 (3.4)
2.9 (2.1)
0.8 (1.1)
4.7 (4.2)
0.3 (0.8)
1.7 (3.3)
8.8 (5.9)
0.6 (1.2)
0.5 (1.0)
5.5 (3.5)
176
Clark (1996). Whereas additional analyses confined to children younger than 10 or to children with severe ADHD failed
to reveal neuromotor deficits for finger or foot movements
alone, the small samples (n<10) available for these analyses
do not allow firm conclusions.
REACTION-TIME TEST
Table IV: Evaluation of best predictor of reaction-time test for diagnostic status
Method
Enter
Enter
Enter
IQ
Enter
Enter
Variables
Parameter estimates
Standard error
Overall classification %
Variability
IQ
Total errors
IQ
Synchronicity
0.1822
Multiple peaks
IQ
Biuni
IQ
0.1046
0.1019
55.0279
0.1526
45.1713
5.9702
14.6179
0.0634
37.0397
0.1755
8.0232
3.8771
7.7888
3.9819
8.3961
0.8334
9.3773
1.7476
9.0808
7.4096
1.1103
0.9032
7.912E+23
0.8585
4.146E+19
0.015
2.230E+06
0.9386
1.219E+16
0.8390
0.005
0.049
0.005
0.046
0.004
85.71
83.33
80.95
0.002
0.186
0.003
0.007
78.57
73.81
Multiple peaks, responses with multiple peaks; Biuni, bilateral responses in unilateral conditions; Synchronicity, synchronicity of bilateral
responses.
Forward
Backward
Entry/removal
probability
Variables
Parameter
estimates
Standard error
ratio
Adjusted odds
Overall
classification %
0.05/0.1
Movement
Variability
time
IQ
Variability
Movement
time
IQ
Variability
Movement
time
IQ
Variability
Movement
time
IQ
Variability
Movement
time
IQ
0.1046
8.0232
1.1103
0.0919
0.005
85.71
0.1019
0.0917
0.4620
3.8771
6.1202
2.5943
0.9032
1.0960
1.5872
0.05
0.0134
0.1072
88.10
0.0951
0.1046
3.0749
8.0232
0.9093
1.1103
0.0795
0.005
0.0919
85.71
0.1019
0.1046
3.8771
8.0232
0.9032
1.1103
0.05
0.005
0.0919
85.71
0.1019
0.0972
0.6229
3.8771
8.7194
7.0179
0.9032
1.1021
1.8644
0.05
0.0031
0.0081
80.95
69.05
0.0957
5.2194
0.9087
0.0223
64.29
0.05/0.1
Forward
0.05/0.06
Backward
0.05/0.06
Enter
Enter
0.05/0.1
0.05/0.1
Enter
0.05/0.1
Variability, overall variability of reaction time test; Movement time, increased time to complete finger movements compared to hand
movements (group extremity, neuromotor variables).
178
studies; omission errors are typically prominent only in vigilance tests with low-response probability.
Taken together, continuous-force measurements during
the reaction-time test revealed both specific motor and attentional deficits in children with ADHD but no clear age effects
and no general motor slowing. This finding is consistent with
recent event-related potential findings during the same test,
which indicate that both premotor and attentional brain
activity is reduced in boys with ADHD despite normal latencies (Steger et al. 2000). The neuromotor assessment also
indicated no general motor slowing in children with ADHD,
but instead resulted in clear age effects. Both modes of testing thus indicated that children with ADHD have no general
motor slowing but specific deficits which differ from those
characterizing younger children.
Correlating neuromotor with reaction-time parameters
provided further insight into the determinants of movement
speed during the neuromotor assessment. Finger movement
time correlated with force-onset latency during correct
responding (r=0.387, p=0.011) but not with the latency
between force onset and peak or with error rate in the reaction-time test. This suggests that the time needed to complete finger movements primarily varies with force-onset
latencies and is relatively unaffected by movement time and
errors of movement or sequencing in this child population.
GROUP PREDICTION
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