Increased Variability in Finger Position Occurs Throughout Overarm
Throws Made by Cerebellar and Unskilled Subjects
D. TIMMANN, R. CITRON, S. WATTS, AND J. HORE
Department of Physiology, University of Western Ontario, London, Ontario N6A 5C1, Canada
Received 18 January 2001; accepted in final form 14 August 2001
INTRODUCTION
A current proposal is that that the cerebellum is the site of
internal models of arm dynamics for learned movements (Kawato 1996; Wolpert et al. 1998). Internal models are hypothetical neural representations that enable predictive (anticipatory)
commands to be generated which compensate for movement
Address reprint requests to J. Hore (E-mail: [email protected]).
2690
related loads. One reason for implicating the cerebellum in
anticipatory control of arm dynamics is that patients with
cerebellar lesions show disorders in control of force. However,
relatively few studies have investigated force control in skilled
movements in cerebellar patients, and for those that have, some
inconsistencies exist. For example, for the case of the fingers,
Holmes (1917) reported that acute cerebellar patients showed
longer rise times to peak force and lower levels of maximum
pinch forces. However, more recent studies on chronic cerebellar patients have shown that the maximum level of force
produced in the precision (pinch) grip is unaffected by the
cerebellar lesion (Mai et al. 1988; Müller and Dichgans
1994a,b). Furthermore, in a drawer-pulling task, cerebellar
patients actually showed an increase in grip force compared
with controls (Serrien and Wiesendanger 1999). These studies
agree with Holmes that deficits occur when patients perform
tasks in which there is a force change. For example, patients
showed a slowness in making fast alternating changes between
two levels of isometric force and deficits in isometric force
tracking (Mai et al. 1988) and a reduced ability to increase the
rate of isometric pinch force when adapting to heavy loads
(Müller and Dichgans 1994a).
One task where precise and rapid change of finger force is
required is gripping and releasing a ball in an overarm throw.
We have previously shown that during the period of ball
release in a throw, as the hand accelerates forward and downward, a back force occurs from the ball on the fingers (Hore et
al. 1999). In the preceding paper (Hore et al. 2001), we show
that skilled throwers keep finger amplitude relatively constant
for throws with balls of different weights by estimating the
magnitude of the back forces and generating fast force changes
in finger muscles throughout the throw to oppose them. If the
cerebellum is the site of internal models of hand dynamics for
learned movements, then it would be expected that patients
with lesions of the cerebellum would have disorders in their
ability to correctly predict back forces from the ball on the
fingers and in their ability to produce the appropriate force
change.
The overall aim was to test the ability of cerebellar patients
to predict and produce the appropriate levels and rate of change
of finger forces in an overarm throw, which is an example of a
skilled multijoint movement. However, it was considered that
it was not practical in cerebellar patients to measure force on
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0022-3077/01 $5.00 Copyright © 2001 The American Physiological Society
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Timmann, D., R. Citron, S. Watts, and J. Hore. Increased variability in finger position occurs throughout overarm throws made by
cerebellar and unskilled subjects. J Neurophysiol 86: 2690 –2702,
2001. We investigated the ability of cerebellar patients and unskilled
subjects to control finger grip position and the amplitude of finger
opening during a multijoint overarm throw. This situation is of interest
because the appropriate finger control requires predicting the magnitude of back forces from the ball on the finger throughout the throw
and generating the appropriate level and rate of change of finger flexor
torque to oppose the back force. Cerebellar patients, matched controls,
and unskilled subjects threw tennis balls and tennis-sized balls of
different weights. In all cases angular positions of five arm segments
in three dimension were recorded at 1,000 Hz with the search-coil
technique as subjects threw from a seated position. When the hand
was stationary, cerebellar patients showed a normal ability to grip the
ball and open the fingers and drop the ball. In contrast, in overarm
throws where a back force occurred on the fingers, cerebellar patients
showed an abnormally large variability in amplitude of the change in
finger position when gripping, in amplitude of finger opening, and in
amplitude of the change in finger position 10 ms after ball release.
This was not due to more trial-to-trial variation in throwing speed.
When throwing balls of increasing weights, both controls and cerebellar patients had increasing finger flexions after ball release that
indicated that, on average, both scaled finger force in proportion to
ball weight during the throw. Unlike skilled controls, cerebellar patients showed a small (⬍20°) increase in the amplitude of finger
opening with balls of increasing weight. However, neither the increase
in variability of finger position nor the increase in finger amplitude
with balls of increasing weight were unique cerebellar signs because
both were observed to various degrees in unskilled throwers. It is
concluded that in the absence of either normal cerebellar function or
skill, the central neural activity that controls finger opening in throwing can increase finger flexor force to oppose an increase in back force
from heavier balls and can open the fingers but cannot control finger
force or finger opening precisely and consistently from throw to
throw. These results fit with the idea that cerebellar disorders are
greater in multijoint than single-joint movements because control of
force is more complicated. They are also consistent with the hypothesis that the cerebellum produces skill in movement by reducing
variability in the timing and force of muscle contractions.
FINGER POSITIONS IN THROWING
TABLE
compare the ability of unskilled subjects to control finger
position throughout a throw with that of skilled subjects and
cerebellar patients.
METHODS
Subjects
Data were analyzed in detail from experiments performed on nine
right-handed cerebellar patients, nine controls, and six unskilled
throwers and from previously published experiments (Hore et al.
1999) on six skilled throwers. Additional experiments with force
transducers taped to the fingers were performed on four unskilled
throwers. The experiments were approved by the local ethics committee, and all subjects and patients gave informed consent. Patient
information is given in Table 1. In brief, five patients had right-sided
surgical lesions that affected the region of the cerebellar nuclei, one a
right-sided cerebellar infarction (superior cerebellar artery) and three
diffuse cerebellar cortical atrophy. In all cases, the extent of the lesion
was confirmed by magnetic resonance imaging (MRI) or computerized tomography (CT) scans. All patients had a full neurological
examination at the time of the experiments. These 9 cerebellar patients
were selected from a total of 16 cerebellar patients who performed the
experiment. Data from seven patients was excluded from the final
analysis either because they showed significant signs of brain stem
damage or polyneuropathy on clinical examination (4 patients) or
because they showed no evidence that the cerebellar lesion had
affected the fingers (3 patients). Disorder of the fingers was assessed
in two ways. First, patients and controls were asked to make fast and
accurate small amplitude finger extensions to a target ⬃10° away (cf.
Hore et al. 1991). Patients were excluded if they did not show
hypermetria compared with controls. On average, controls overshot
1. Patient information
Ataxia
Disorders
Length of
Illness, yr
Patient
Age/Sex
Lesion
MRI Findings
Ol
15/M
Hv
11/F
Ls
33/F
Surgical defect of midline
structures including the right
deep cerebellar nuclei
Surgical defect of midline
structures including the right
deep cerebellar nuclei
Extended surgical defect of the
right cerebellar hemisphere
including the deep cerebellar
nuclei
Hs
28/M
Cerebellar
astrocytoma
removed 1992
Cerebellar
astrocytoma
removed 1996
Aneurysm of the
right PICA
clipped 1990;
Right cerebellar
cyst removed
1991
Infarction of the
right SCA 1989
Dv
18/F
Cerebellar
astrocytoma
removed 1989
Sc
26/M
Vn
44/F
Cerebellar
astrocytoma
removed 1976
ADCA III
Hn
Pr
53/M
61/M
SCA-6
ADCA III
Ischemic defect of the superior
parts of the right cerebellar
hemisphere including the
deep nuclei
Surgical defect of the right
cerebellar hemisphere
including the deep cerebellar
nuclei
Extended surgical defect of
midline structures and right
cerebellar hemisphere
Pancerebellar atrophy, most
pronounced inferior vermis
Pancerebellar atrophy
Pancerebellar atrophy
Upper
Limb
Lower
Limb
Stance/
Gait
Speech
Oculomotor
5
6/36
2/16
3/34
0/8
0/6
1
12/36
4/16
6/34
0/8
4/6
6
5/36
1/16
4/34
0/8
3/6
7
7/36
2/16
3/34
2/8
0/6
9
5/36
0/16
2/34
0/8
1/6
20
3/36
0/16
0/34
0/8
0/6
⬎30
12/36
4/16
14/34
3/8
3/6
15
⬎25
17/36
16/36
6/16
5/16
24/34
22/34
5/8
5/8
6/6
3/6
Patient information, radiological findings and scaling of cerebellar symptoms according to the International Cooperative Ataxia Rating Scale (Trouillas et al.
1997). MRI, magnetic resonance imaging; SCA, superior cerebellar artery; SCA-6, spinocerebellar ataxia type 6; PICA, posterior inferior cerebellar artery;
ADCA III, autosomal dominant ataxia type III.
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the fingers directly with force transducers taped to the fingers
as was done with skilled throwers (Hore et al. 2001). This was
because this technique requires that the ball should roll directly
over the transducer—any deviation to the side results in a
decreased force being recorded. These transducers also result
in the subjects having decreased tactile information, i.e., they
cannot clearly feel the middle finger gripping the ball. While
these were not problems for skilled throwers, it was felt that
they could result in spurious results in the cerebellar patients,
e.g., a decrease in measurement of force could result either
because of a real decrease in force of grip by the middle finger
or because the ball was not perfectly centered on the middle
finger. An alternative way to gain information about finger
force is to record finger position with respect to the hand. For
example, once the ball has left the hand, finger position (i.e.,
the amplitude of the finger flexion flick that occurs immediately after ball release) is directly related to the magnitude of
force recorded on the distal phalanx before ball release (Hore
et al. 2001). Consequently, in the present study, we measured
finger position with respect to the hand with the search-coil
technique (at 1,000 Hz) that records angular position at high
resolution and causes no impediment to gripping. The specific
objective of the present experiments was to investigate the
ability of cerebellar patients to control finger position throughout an overarm throw. Because not all patients were skilled
throwers before the lesion, it was necessary to test controls
who were unskilled to various degrees. In the process, it
became clear that unskilled throwers showed similar deficits to
the cerebellar patients. Therefore a second objective was to
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D. TIMMANN, R. CITRON, S. WATTS, AND J. HORE
General procedures
All subjects threw from a sitting position because some patients
could not stand for long periods. Subjects were instructed to throw
tennis-sized balls with an overarm motion (using shoulder adduction)
at a central target which was located at eye level on a vertical target
grid of numbered 6-cm squares 3 m away. Each throw was scored for
accuracy by an experimenter calling out the square that was hit. The
time of final ball release from the fingertip was defined by a number
of criteria including: 1) the time the ball rolled off a small, lightweight microswitch (distal trigger) attached to the distal phalanx of
the middle finger, 2) the moment of a deflection or peak in finger
extension, or horizontal finger motion all with respect to the hand
(these motions result from reactive forces associated with the ball
TABLE
leaving the hand), and 3) the duration of finger opening to ball release
(for throws of the same speed this time is fixed because there is a fixed
time for the ball to roll along the finger). The small number of throws
not satisfying at least two of these criteria were omitted. All patients
and controls were instructed to throw 40 tennis balls (55 g weight, 65
mm diam) accurately at a medium speed. In addition, six of the
cerebellar patients (Ol, Hv, Dv, Vn, Hn, and Pr), six controls, and six
very unskilled throwers made an additional 40 throws with a light
plastic ball that had a hard surface (14 g, 70 mm) and 40 throws with
a heavy tennis ball filled with concrete (196 g, 65 mm). Balls were
thrown in the order of 20 tennis balls, 20 light balls, and 20 heavy
balls, and the sequence was repeated. In all cases, subjects were
instructed to center the ball on the middle finger so that during release
it rolled along that finger. This grip position was monitored throughout the experiment.
As previously, arm segment orientations were measured with the
use of a modification of Robinson’s (1963) magnetic-field search-coil
technique (Tweed et al. 1990). Arm movements were sampled at
1,000 Hz by means of a pair of orthogonal search coils taped to four
arm segments and the distal phalanx of the middle finger. A reference
arm position was recorded where the upper arm was held horizontal
and the forearm and fingers were held vertical. Calculations were
performed to obtain rotations of the distal phalanx with respect to the
hand.
RESULTS
Force on the fingers changes during an overarm throw
In the preceding paper (Hore et al. 2001), we show how
force on the fingers changes throughout an overarm throw in
skilled throwers. The essential findings are summarized in Fig.
1. Figure 1A shows a diagrammatic representation of the three
middle finger phalanges and hand during the forward throw,
which began ⬃150 ms before final ball release (time 0). A
force transducer on the distal phalanx is represented (䡲). Figure
1B shows average force records from the distal phalanx for 10
throws made with balls of 14, 55, 196, and 360 g weight; and
Fig. 1C shows the average angular positions of the distal
phalanx of the finger with respect to the hand (finger extension)
for the same throws. Early in the forward throw (⫺100 ms), the
hand grips the ball with a force proportional to ball weight
(Fig. 1B). Between ⫺60 and ⫺30 ms (Fig. 1A), the finger starts
to extend (open), and there is a decrease in force applied to the
ball (Fig. 1B); between ⫺30 and ⫺10 ms, the ball rolls up the
finger and the force on the distal phalanx increases and then
2. Timing windows for ball release
Control
Cerebellar
Unskilled
Skilled
Subject
Sex
Window, ms
Subject
Sex
Window, ms
Subject
Sex
Window, ms
Subject
Sex
Window, ms
Mi
Rn
Tm
Kp
An
Bs
Sh
Jn
Wt
Mean
M
F
F
M
F
M
F
M
M
11
16
27
9
16
7
21
10
11
14
Ol
Hv
Ls
Hs
Dv
Sc
Vn
Hn
Pr
Mean
M
F
F
M
F
M
F
M
M
98
82
97
22
20
28
46
39
23
51
Lt
Kt
Ab
Tn
Ss
Ml
M
F
F
F
F
M
22
17
31
19
58
14
Cc
De
Co
Ak
Jn
Nv
M
M
M
M
M
M
9
7
7
6
5
6
27
Mean
Mean
7
Timing windows for ball release (ms) for ⬃40 throws made with tennis balls. Time of ball release was measured with respect to the point in the throw when
the hand was vertical in space. The standard deviation was multiplied by 3.92 to give the range of variability for 95% of the throws. Means for each group are
also shown. M, male; F, female.
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the target slightly (mean amplitude of total movement was 15°),
whereas the included patients showed hypermetria (mean amplitude,
39°) followed in some cases by a damped intention tremor. Second,
finger disorder was assessed by the size of the timing window for ball
release. As before (e.g., Hore et al. 1995; Timmann et al. 1999), we
defined variability in timing of ball release (timing windows) in terms
of the standard deviation (SD) about the mean time of ball release
with respect to the moment in the throw when the hand was vertical
in space (the timing window for 95% of the throws was calculated by
multiplying the SD by 3.92). Patients were excluded if they had
shorter timing windows for 40 throws with the tennis ball than their
matched controls (Table 2). Previous results from our laboratory have
shown that average timing windows for normal subjects are ⬃5 ms for
very accurate male competitive ball players, 9 –10 ms for male recreational ball players, 15 ms for female recreational ball players,
15–30 ms for unskilled female throwers, and 55 ms for cerebellar
patients (cf. Hore et al. 1995, 1996a,b; Timmann et al. 1999).
Control subjects were chosen to match cerebellar patients with
respect to the estimated skill of the patient at throwing before the
cerebellar lesion, their sex, and their approximate age. Subjects and
patients rated their prelesion throwing ability on a score from 1 to 5
(1, very bad; 2, bad; 3, reasonable; 4, good; 5, very good thrower). Six
of the cerebellar patients were from Germany, and their self-assessed
throwing ability before the lesion was verified by asking them how far
they threw in the standardized test for athletic ability given every year
to German school children. In addition, further information was
obtained by asking all subjects how often in a series of throws they
felt they would hit our 6 cm target which was located 3 m away (in the
case of the patients, how accurate they felt they were before the
lesion). Unskilled subjects were selected on the basis of being selfassessed “bad or very bad” throwers and having never played recreational sports involving throwing. Four of the six unskilled throwers
were female and one (subject Lt) was a 70-yr-old male.
FINGER POSITIONS IN THROWING
2693
phalanx), two results were the same. First, the force on the
distal and middle phalanges increased in proportion to ball
weight. Figure 2, A and B, shows that mean forces with the
heavy ball (196 g, thick lines) were greater than those for the
tennis ball (55 g, medium lines), which in turn, were greater
than those with the light ball (14 g, thin lines). Second, on
average, the amplitude of the finger flexion 10 ms after the
moment of ball release (dashed line; Fig. 2C) was proportional
to the peak force on the distal phalanx prior to ball release (Fig.
2A). Figure 2D shows this relation in plots of the means ⫾ SD
for each parameter for each of the three balls of different
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FIG. 1. Finger forces and finger positions during the forward component of
overarm throws made by a skilled thrower. A: diagrammatic representation of
the angular positions of the 3 finger phalanges of the middle finger and the
hand. Times are with respect to ball release (time 0). ■, force transducer on
distal phalanx. B: mean forces recorded on the distal phalanx for 10 throws
each with balls of 14, 55, 196, and 360 g weight. C: mean angular positions of
distal phalanx of middle finger with respect to hand for the same throws;
subject De.
peaks, and between ⫺10 and 0 ms, the ball rolls off the
transducer and is released from the fingertip. These records
show three findings that have been reported previously for
skilled recreational ball players (Hore et al. 1999, 2001): for
throws of similar speeds, the force on the finger throughout the
throw is proportional to ball weight (Fig. 1B); the amplitude of
finger opening (from the baseline to the moment of ball release) does not increase with balls of increasing weights and in
some subjects may actually decrease (Fig. 1C); and the amplitude of the finger flexion (Fig. 1C) that begins at the moment
of ball release (time 0) is proportional to the peak force on the
distal phalanx (Fig. 1B). This latter finding presumably occurs
because the sudden release of the ball from the fingertip leaves
the finger flexor torque unopposed and the larger flexor torques
with the heavier balls produce larger finger flexions. In summary, these records illustrate that skilled throwers adjust the
level and rate of change of finger force throughout a throw and
that this is associated with a finger extension amplitude that
does not increase with balls of increasing weight.
However, not all cerebellar patients were skilled throwers
before the lesion. To verify that the preceding relations between finger force and finger position also apply for unskilled
subjects, we asked four unskilled throwers to throw the 14-,
55-, and 196-g balls when force transducers were taped to the
distal and middle phalanges of the middle finger. Figure 2,
A–C, shows averages of 30 throws aligned on the moment of
ball release (time 0) for one unskilled subject. Although this
subject threw at a slower speed and had a different pattern of
force on the distal phalanx than previously found for skilled
throwers (because she gripped the ball with only the middle
J Neurophysiol • VOL
FIG. 2. Finger forces and finger positions for throws made by an unskilled
thrower. A: mean force recorded on distal phalange for 30 throws made with
each ball of 14-, 55-, and 196-g weight. B: mean force on middle phalanx. C:
mean angular position of distal phalanx with respect to the hand for same
throws. Traces have been aligned vertically (as well as horizontally) to be at
the same finger position at ball release. D: relation for each ball for same
throws between mean amplitude and SD of finger flexion 10 ms after ball
release from the fingertip and mean peak force and SD on distal phalanx before
ball release; subject Sh.
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D. TIMMANN, R. CITRON, S. WATTS, AND J. HORE
weights. A similar increase in force on the distal and middle
phalanges and increase in finger flexion for the heavier balls
was found in one other unskilled subject, but in the other two
unskilled subjects, the force on the distal phalanx was highly
variable from throw to throw, presumably because the ball did
not consistently roll over the force transducer on the distal
phalanx. Nevertheless, the fact that in these two latter subjects
the middle finger was not pushed back into extreme extension
with the heavy ball (i.e., their finger extensions were similar to
those in Fig. 2C) indicates that they were also scaling finger
force to ball weight. This point will be taken up in a later
section.
Cerebellar patients show greater variability in amplitude of
finger opening when throwing
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FIG. 3. Variability of finger opening in a cerebellar patient when throwing
but not when opening the hand to drop a ball. In all cases, traces are 10
superimposed records of angular position of the distal phalanx of the middle
finger with respect to the hand. A: finger opening aligned on end of movement
when a control subject (Mi) and cerebellar patient (Ol) opened the hand and
dropped a tennis ball. For all 20 ball drops, mean finger extension amplitudes
were 94 ⫾ 8.3° (mean ⫾ SD) for the control and 136 ⫾ 6.3° for the cerebellar
patient. The difference in amplitude occurred because the cerebellar patient’s
finger grip position on the ball was more flexed. B: finger opening for same
subjects aligned on ball release (time 0) for throws made at a medium speed
with a tennis ball. C: finger opening for same throws aligned to be at the same
finger position at ball release.
was larger for the cerebellar patient. In agreement, unpaired
t-test revealed a significant group difference (P ⫽ 0.023). Thus
cerebellar patients show a greater variability in the amplitude
of finger opening.
Could this variability in finger amplitude be due to more
trial-to-trial variability in throwing speed? We used hand angular velocity at ball release as a measure of throwing speed
because many throws made by cerebellar patients missed the
target and ball speed could not be calculated (from flight time
to target impact). The mean throwing speed for patients
(1,586°/s) was lower than that for controls (2,440°/s; P ⫽
0.016; unpaired t-test). However, the variability of throwing
speed, although larger for the cerebellar group (mean 204°/s)
than the control group (mean 144°/s), was not significantly
different (P ⫽ 0.203). In keeping with this, only one cerebellar
patient (Sc) showed a relation between finger amplitude and
throwing speed (R2 ⫽ 0.24) that could have resulted from
increased variability in throwing speed compared with their
matched control. In short, considering all patients, the increased variability in finger amplitude was not due to more
trial-to-trial variation in throwing speed.
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We now consider whether cerebellar patients can control
these levels and changes in finger force throughout an overarm
throw to produce a consistent finger grip and consistent amplitude of finger opening. As a starting point, we examined the
ability of patients to open the fingers when no backforce due to
arm movement was applied to the fingers. This was achieved
by instructing the controls and patients to hold the hand stationary at about the position in a throw where the ball was
released, to grip the ball as if throwing, and to open the hand
fully and drop the ball. Figure 3A shows for 10 trials that both
control (Mi) and cerebellar patient (Ol) opened the fingers
smoothly and consistently from trial to trial. No cerebellar
patient showed any abnormality such as hypometria or tremor
of the fingers in this task. The likely reason that finger extension was constant in amplitude from trial to trial in both control
and cerebellar subjects was that the movement started from one
fixed position (finger grip on the ball) and finished at another
(fingers fully open) and did not require active braking because
of the effect of passive visco-elastic forces.
In contrast, when both the control and cerebellar patient
threw a 55-g tennis ball, which is a situation where back force
from the ball has to be controlled (Figs. 1 and 2), major
differences were found in finger opening. Figure 3B shows that
for 10 throws aligned on the time of ball release, angular finger
position with respect to the hand in the control subject was
similar from throw to throw but was highly variable in the
cerebellar patient. One obvious difference was the greater
variability in amplitude of finger opening in the cerebellar
patient (from onset of finger extension to ball release). To
examine finger opening in detail, the mean amplitude of finger
extension and its SD was measured for 40 throws made with a
tennis ball in all cerebellar patients and their controls. The
amplitude of finger extension was measured from when finger
extension velocity crossed a low threshold (200°/s) to the
moment of ball release (time 0; Fig. 4). This threshold was
chosen because it gave a reliable measure of the onset of finger
opening. Mean finger extension amplitudes and SDs for the
patients and matched controls, which are in equivalent positions across the page, are shown in Fig. 5. Although there was
a tendency for mean finger amplitude to be larger in the
cerebellar group (i.e., in 7 of the 9 pairs finger amplitude was
larger for the cerebellar patients), this did not reach statistical
significance (P ⫽ 0.103; unpaired t-test). However, a more
striking result can be seen when considering variability of
finger amplitude as measured by the SD: for each pair the SD
FINGER POSITIONS IN THROWING
2695
of the fingers at the ⫺100 ms point. Figure 6A (top) shows that
100 ms after the fixed 200-ms point, cerebellar patients on
average had finger grip positions slightly more toward extension than the controls. However, a more striking difference can
be seen in Fig. 6A (bottom), i.e., variability in the amplitude of
the change in finger grip position (as measured by the SD) was
larger in the cerebellar group (P ⫽ 0.014; unpaired t-test). Only
one patient (Hs) showed a relation between the change in finger
FIG. 4. Diagram illustrating how 3 parameters of finger position were
measured during a throw. Trace is angular position of the distal phalanx of the
middle finger with respect to the hand before and after ball release (time 0);
control subject Mi.
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Cerebellar patients have more variable amplitudes of finger
movement before and after finger opening
Inspection of Fig. 3B reveals further differences between the
finger position records from the control subject and cerebellar
patient. A second difference is that there is an increase in
variability from throw to throw in the change in finger position
when gripping in the cerebellar patient. That is, for each throw
before the onset of finger opening (i.e., the period between
⫺200 and ⫺100 ms in Fig. 3B), the control shows a fairly
constant finger position for each throw as the hand grips the
ball, whereas the cerebellar subject shows fluctuations in finger
position. This often consisted of a drift toward extension, but in
some cases, there was extension followed by flexion. Inspection of traces over a long time course showed that this flexion
movement was not a rhythmic tremor. No patient showed
cerebellar tremor of the fingers when gripping the ball. The
amplitude of the change in finger grip position for each throw
was measured as shown in Fig. 4. A fixed finger position was
taken 200 ms before ball release (⫺200 ms), and the amplitude
of finger position with respect to this position (i.e., change in
grip position) was measured 100 ms later (⫺100 ms). For this
single throw from control subject Mi, there was a slight flexion
FIG.
5. Means and standard deviations of the amplitude of finger extension
for 40 throws made with a tennis ball. Data from controls and their matched
cerebellar patients are in equivalent positions going from left to right.
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FIG. 6. Means and SD of the amplitude of the change in finger grip position
(A) and amplitude of finger movement 10 ms after ball release (B). Amplitudes
measured as shown in Fig. 4 for 40 throws made with a tennis ball in cerebellar
patients and their matched controls.
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D. TIMMANN, R. CITRON, S. WATTS, AND J. HORE
Evidence that cerebellar patients can scale finger force for
balls of different weight
The preceding results demonstrate that cerebellar patients
have more variable changes in finger positions throughout a
throw than controls. The likely explanation is that this resulted
from disordered control of finger force. Considering that
throws with balls of different weights require development of
different finger force (Figs. 1B, and 2, A and B), the question
arose whether cerebellar patients can scale the appropriate
level of finger force for throws with the different balls. To
answer this question, we instructed six cerebellar patients and
their controls to make 40 throws with each of the 14-, 55-, and
196-g balls. We determined their ability to scale finger force by
means of an indirect approach based on previous results (Hore
et al. 2001), which showed that the amplitude of the finger
flexion that occurred after ball release is proportional to the
force on the fingers before ball release, e.g., Figs. 1, B and C,
and 2D. Records of finger position for 20 throws made with
each of the three balls are shown in Fig. 7A aligned on the time
of ball release for a cerebellar patient (Hv) and her control
(Rn). For each of the three balls, the patient, as before, showed
more variable changes in grip position for each throw, more
variable amplitudes of finger opening to ball release, and more
variable changes in finger position after ball release. For the
first throw with a different ball (e.g., heavy after light), the
amplitude of finger extension was no different from that in
subsequent throws with the same ball. Figure 7B shows averages of finger position for all 40 throws for each ball aligned on
ball release and aligned vertically so that finger positions were
at the same point at ball release. For both the control and
cerebellar patient, there was, on average, a flexion proportional
to ball weight with the heavy ball having the largest flexion.
This was determined quantitatively (as shown in Fig. 4) by
J Neurophysiol • VOL
FIG. 7. Angular finger position during throws made with balls of 3 different
weights. A: superimposed traces of angular position of the distal phalanx of the
middle finger with respect to the hand for 20 throws made with the light balls
(14 g), tennis balls (55 g), and heavy balls (196 g). Traces aligned on ball
release; control (Rn); cerebellar patient (Hv). B: average of 40 throws made
with each ball aligned on the same angular finger position at ball release. - - -,
10 ms after ball release.
measuring finger position 10 ms after ball release (Fig. 7B,
- - -). The height of the bars in Fig. 8A represents mean finger
position at this 10-ms point with respect to finger position at
ball release (0°). When going from the light ball to the tennis
ball to the heavy ball (䊐 to o to ■), although there is variability
in absolute finger position, all controls and all cerebellar patients show a progression to greater flexion (or less extension)
for the heavy ball. Accordingly, a repeated-measures ANOVA
(with ball weight as repeated measure) revealed a significant
effect of ball weight (P ⬍ 0.001), but no significant difference
between patient and control groups (P ⫽ 0.77) and no significant ball weight ⫻ group interaction (P ⫽ 0.35). In view of the
finding that the amplitude of finger flexion 10 ms after ball
release is proportional to the force on the distal phalanx before
ball release in skilled subjects (Hore et al. 2001) and in unskilled subjects (Fig. 2), we take this as evidence that, on
average, both control subjects and cerebellar patients scaled
finger force in proportion to ball weight.
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grip position and throwing speed (R2 ⫽ 0.21), but he had a
lower variability in throwing speed than the matched control.
A third difference between the cerebellar patients and controls occurred in the finger positions after release of the ball
from the fingertip. Figure 3B shows that following ball release
(0 time) for all throws in the control, the finger flexed slightly
then extended. In contrast, in the cerebellar patient, after the
moment of ball release, the finger flexed in some throws and
extended in others. This difference is seen more clearly in Fig.
3C in which the finger position records have been aligned
vertically (as well as horizontally) to be at the same finger
position at the time of ball release. At any time after ball
release, finger position is more variable in the cerebellar patient. This was determined quantitatively as shown in Fig. 4 by
measuring for each throw the amplitude of finger movement
after ball release, i.e., the amplitude difference of finger
position 10 ms after ball release with respect to finger
position at ball release. A value of 10 ms was chosen
because in control subjects (e.g., Figs. 4 and 7B), it was the
optimal time for measuring finger flexion before the rebound
of the finger toward extension. Figure 6B (bottom) shows
that the variability (SD) of the amplitude of finger movement 10 ms after ball release was larger in the cerebellar
group (P ⫽ 0.024; unpaired t-test). Again, this could not be
explained by increased variability in throwing speed in the
cerebellar patients.
FINGER POSITIONS IN THROWING
2697
Variability of finger position in unskilled throwers
Because cerebellar patients were of variable throwing ability
before the lesion and because controls were matched in part on
the basis of this prelesion throwing ability, it resulted that
controls were also of variable throwing ability. We noticed that
for some finger position parameters, variability (as measured
by the SD), was higher for the unskilled controls compared
with the skilled controls. For example, in Fig. 5B, the SDs of
the amplitude of finger extension were larger for Mi, Rn, and
Tm, who were relatively unskilled throwers, than they were for
Kp, Bs, and Jn, who were relatively skilled. This raised the
question of whether unskilled throwers, who did not have a
cerebellar lesion, would show variability in finger position
parameters equivalent to that observed for the cerebellar patients. To answer this question, the same experiment of throwing balls of three different weights was performed by six
further subjects who were selected on the basis of their self
assessment that they were unskilled (bad or very bad) throwers.
Four subjects were 20- to 35-yr-old females (Kt, Ab, Tn, and
Ss), one was a 22-yr-old male (Ml), and one was a 70-yr-old
male (Lt). Of particular interest was subject Ss, a 24-yr-old
female dental student who had passed the dental aptitude test
for finger dexterity and who claimed to have almost no previous throwing experience.
In the very unskilled subject Ss, finger position varied in
a similar way from throw to throw as found for the cerebellar patients. Figure 9 shows angular position of the distal
phalanx with respect to the hand for 20 throws made with
the heavy ball by a control subject (Mi), the very unskilled
subject (Ss), and a cerebellar patient (Ol). Compared to the
control, both the very unskilled subject and the cerebellar
J Neurophysiol • VOL
patient show more variable finger grip positions during each
throw, more variable amplitudes of finger extension, and
more variable finger movements after ball release than the
control.
The mean amplitudes and SDs of finger opening (extension) for 40 throws made with the balls of different weight
are shown in Fig. 10 for the controls, cerebellar patients and
unskilled throwers (light ball, 䊐; tennis ball, o; heavy tennis
ball, ■). One similarity between unskilled subjects and
cerebellar patients was that both showed an increase in
finger extension amplitude with an increase in ball weight.
Regression analysis showed that such an increase was found
in five of the six cerebellar patients (not in Hn) and in six of
the six unskilled throwers. In contrast, most of the controls
did not show a statistically significant increase (Mi, An, and
Wt), and Jn showed a decrease. This fits with previous
studies on skilled subjects that have shown no change or a
decrease in the amplitude of finger extension with balls of
increasing weight (Hore et al. 1999, 2001). Although control subjects Rn and Sh both showed an increase, this could
have been because they were unskilled subjects. Like controls and cerebellar patients, all unskilled subjects also
showed a finger flexion flick after ball release that was
proportional to ball weight (e.g., Fig. 2, C and D).
As far as variability of finger extension amplitude is
concerned, Fig. 10 shows that unskilled subjects Ss and Ab
had larger SDs than any of the controls. Considering groups,
SDs were larger for the cerebellar patient group than the
control group for all three balls (P ⫽ 0.008, repeatedmeasures ANOVA) and were larger for the unskilled than
the control group. However, in the latter case this did not
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FIG. 8. Mean finger positions 10 ms after ball release are flexed in proportion to ball weight for both controls and cerebellar
patients. A: mean finger angular positions with respect to the hand 10 ms after ball release for 40 throws plotted with respect to
a baseline of 20° flexion from finger position at ball release (0°). B: SDs for amplitudes of finger positions 10 ms after ball release
with respect to finger positions at ball release (measured as shown in Fig. 4).
2698
D. TIMMANN, R. CITRON, S. WATTS, AND J. HORE
DISCUSSION
Indirect evidence for deficits in force production in
cerebellar patients
FIG. 9. Very unskilled throwers show a similar increase in variability in
finger angular position throughout the throw as found in cerebellar patients.
Traces are superimposed records of angular position of the distal phalanx of
the middle finger with respect to the hand aligned on ball release for 20 throws
made with the heavy ball by a control subject (Mi), a very unskilled thrower
(Ss), and a cerebellar patient (Ol).
reach statistical significance. The likely reason was that the
control group also contained a number of relatively unskilled throwers. In fact, only two throwers in the control
group were recreational ball players (Jn and Wt).
To investigate this further, we examined the variability in
finger extension amplitude for each of the balls of different
weights for four groups: the same three as before (Fig. 10)
and a new group of six skilled male recreational ball players
from a previous study (Hore et al. 1999). The bar heights in
Fig. 11, which give the mean value of the SD of finger
extension for throws with a particular ball made by the six
subjects in each group, show that there was a progressive
increase in variability of finger extension amplitude for all
three balls in the order of skilled, control, unskilled, and
cerebellar. In keeping with this, repeated-measures ANOVA
showed a group difference between cerebellar and skilled
(P ⫽ 0.001) and between unskilled and skilled (P ⫽ 0.043).
In summary, unskilled throwers to various extents showed
the same increased variability in finger position throughout
and after the throw and the same increased amplitudes of
finger extension for balls of increasing weights as found for
the cerebellar patients.
J Neurophysiol • VOL
FIG. 10. Means and standard deviations of finger extension amplitude for
40 throws made with balls of 3 different weights by control, cerebellar, and
unskilled subjects.
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Cerebellar patients perform different finger opening tasks
with different degrees of disorder. For example, when asked to
make small-amplitude finger flexions fast and accurately, cerebellar patients showed marked hypermetria followed by intention tremor (Hore et al. 1991). This was confirmed for small
amplitude finger extensions in the present study (METHODS).
However, the same patients were able to open the stationary
hand to drop the ball with no obvious disorder (Fig. 3A). And
when throwing, rather than marked hypermetria, patients
showed increased variability in the amplitude of finger opening
(Fig. 5). The likely explanation for the differences in performance in the different tasks is that the control of force and
braking are different. Whereas fast small movements require
early onset of antagonist muscle activity to brake the movement, which cannot be generated by cerebellar patients (Hore
FINGER POSITIONS IN THROWING
FIG. 11. Mean variability of finger extension amplitude for different groups
of throwers. Each bar was obtained by determining the mean and SD of the
amplitude of finger extension for 40 throws made by each of 6 subjects then
determining the mean of the SDs.
J Neurophysiol • VOL
tween throws, which would have determined differences in
initial (static) finger configurations, we measured the amplitude
of the dynamic change in finger position when gripping during
each throw and averaged this across throws. This measure of
dynamic change should not be greatly affected by different
initial finger configurations. Furthermore, variability in the
middle finger configuration would not affect the ball rolling
along the finger (Fig. 1A) and therefore would not cause the
increased variability in finger amplitude or in finger flexion
after ball release.
Although as a group cerebellar patients showed evidence of
disordered control of the fingers, the degree of this disorder
varied from patient to patient. In general, it appeared that the
degenerative patients (Vn, Hn, and Pr) showed less disorder
than patients with surgical or ischemic lesions, which affected
the cerebellar nuclei. It was somewhat surprising that the two
male degenerative patients (Hn and Pr), who had severe disorders in their posture and gait and who had abnormalities in
braking fast small-amplitude finger movements (METHODS),
showed a relatively small increase in variability in finger
extension amplitude when throwing balls of different weights
(Fig. 10). This may reflect a relatively small affect of the lesion
on the control of the fingers (which would fit to some extent
with the relatively small timing windows of 39 and 23 ms
shown in Table 2) or it may have something to do with the fact
that they were both good throwers before the lesion.
The question arises whether these findings of disordered
finger control in cerebellar patients are related to the classic
cerebellar signs of asthenia (decrease in force in voluntary
movements) and hypotonia (decreased resistance to passive
muscle stretch) (Holmes 1917, 1922; Luciani 1915). Although
we did not directly measure muscle strength and muscle tone
and therefore cannot make definitive conclusions, the evidence
does not support this possibility. First, these classic disorders
are only prominent in acute cerebellar patients and we studied
chronic patients. In chronic patients, Mai et al. (1988) found no
decrease in maximum force developed by the fingers. Second,
cerebellar patients do not have to be hypotonic to show disorders in movement. Although hypotonia was originally believed
to be a cause of cerebellar movement disorders (Holmes 1922),
more recent work has failed to find any relation between
hypotonia and arm ataxia and tremor (Growdon et al. 1967),
gait ataxia in cats (Gorassini et al. 1993), and arm dysmetria in
monkeys (Flament and Hore 1986). And third, unskilled subjects who were not weak or hypotonic showed the same finding
as the patients of variable finger positions and a small increase
in the amplitude of finger opening with balls of increasing
weight. In summary, the evidence suggests that the increased
variability in finger position throughout an overarm throw in
cerebellar patients is due to variable control of finger force and
not to weakness or hypotonia. This finding complements previous results where we have shown that cerebellar patients
have increased variability in the timing of finger opening in this
same task (Timmann et al. 1999).
Cerebellar involvement in prediction and production of force
A likely possibility is that increased variability in the production of finger force and in the timing of finger opening in
cerebellar patients arises from disorder in the central commands to the fingers during a throw. Although most studies
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et al. 1991), hand opening in the ball drop task is presumably
braked in large part by visco-elastic forces. In contrast, in
throwing, accurate finger opening requires prediction of the
back force from the ball on the finger based on motions at other
joints, generation of the appropriate magnitude and rate of
change of net finger flexor torque (grip force) to oppose the
changing back force, and extension of the fingers while still
applying the net finger flexor torque.
Indirect evidence indicates that the increased variability in
finger position throughout the throw in cerebellar patients was
caused by increased variability in finger forces. One piece of
evidence comes from the finding that finger position shortly
after ball release from the fingertip was more variable in the
cerebellar patients (Figs. 3C, 6B, 7, 8B, and 9). We previously
found in skilled throwers that the peak amplitude of the finger
flexion (flick) that occurs immediately after ball release is
directly proportional to the peak force on the distal phalanx
prior to ball release (Hore et al. 2001). The same relation was
found in some unskilled subjects in averages from throws made
with the 14-, 55-, and 196-g balls (Fig. 2). It is therefore likely
that the finger flexion that occurs after ball release in cerebellar
patients and that on average is proportional to ball weight (Fig.
8A), also reflects the magnitude of net finger flexor torque prior
to ball release. If this is the case, then the increased variability
in finger position after ball release in cerebellar patients reflects
increased variability in finger flexor force prior to ball release.
Furthermore, because the amplitude of finger extension (to ball
release) reflects the sum of all the forces acting on the finger,
the increased variability in the amplitude of finger extension in
cerebellar patients (Fig. 5) presumably reflects the same increased variability in these forces. Overall this finding in
throwing of increased variability in finger position fits with the
view of Thach et al. (1992) that cerebellar disorders are larger
in multijoint than in single-joint movements because control of
force is more complicated.
Could some other factor explain the increased variability in
finger position throughout the throw? Although cerebellar patients were instructed to center the ball on the middle finger, it
is possible that they had more variable middle finger configurations when gripping the ball. This could result in variable
finger positions for the same overall grip force during each
throw, which could have contributed to the larger variability in
baseline finger grip positions (Figs. 3B, 7A, and 9). However,
rather than measuring the differences in baseline levels be-
2699
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D. TIMMANN, R. CITRON, S. WATTS, AND J. HORE
J Neurophysiol • VOL
myographic activity in response to both an increase in mass on
the limb (Manto et al. 1994) and to an increase in movement
amplitude (Hore et al. 1991). These findings bear some resemblance to those of Timmann and Horak (1997), who studied
postural responses to perturbations of stance. They found that
cerebellar patients could predict perturbation amplitudes based
on prior experience, but they could not use this prediction to
modify precisely the gain of responses. Taken together, these
findings indicate that cerebellar patients retain considerable
ability to scale force to the expected load, i.e., to predict and
generate appropriate force levels, though this ability is disordered. Whether this residual ability results from function of
intact areas of the cerebellum or from other extra-cerebellar
motor areas remains unclear.
Increased variability is associated with lack of skill and with
cerebellar lesions
The most striking result in the present study was increased
variability in the changes in finger position throughout the
throw in both the unskilled throwers and the cerebellar patients. For the unskilled throwers, this fits with previous studies
that have shown that an increase in skill is associated with a
decrease in variability of hand trajectories. For example, an
increase in skill as a result of practice produced more consistent trajectories in a dart throwing task (Higgins and Spaeth
1972), in elbow movements in humans (Darling and Cooke
1987), and in an arm aiming task in monkeys (Georgopolous et
al. 1981). As far as timing is concerned, we have previously
found that lack of skill results in an increase in timing windows
for finger opening and ball release. For example, male recreational ball players had timing windows for ball release of 9 ms
when throwing with their skilled (dominant) arm and 22 ms
when throwing with their unskilled (nondominant) arm (Hore
et al. 1996b). Similarly, in the present study mean timing
windows were 7 ms for skilled subjects and 27 ms for unskilled
subjects (Table 2).
For cerebellar patients and monkeys with lesions of the
cerebellum, increased trial-to-trial variability in movement appears to be a cardinal sign of their disorder. Such variability
has been observed in saccades where the trial-to-trial variability affects both amplitude and direction (e.g., Robinson 1995;
Robinson et al. 1993; Takagi et al. 1998). Similarly, for arm
movements, Holmes (1922) described disorders and variability
in their direction, range and rate. In agreement, recent studies
of multijoint arm movements in cerebellar patients have found
increased trial-to-trial variability in hand trajectories in throwing (Becker et al. 1990; Timmann et al. 1999, 2000) in reaching (Becker et al. 1991; Day et al. 1998), and in a pointing task
(Bastian et al. 1996) and increased variability in the timing of
finger opening in throwing (Timmann et al. 1999, 2000).
At first sight the results shown in Figs. 9 –11 might be
interpreted to suggest that in throwing, finger control in unskilled subjects and patients with a cerebellar lesion is equivalent. But this view would not be correct because cerebellar
patients had larger timing windows (Table 2) and were considerably less accurate on the target. Furthermore, it is important to emphasize that we did not study patients with a nonfunctioning cerebellum. Rather the present patients had mild to
medium cerebellar disorders (Table 1), which could be associated with the retention of considerable cerebellar function.
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have interpreted the disorder in hand and arm movements in
cerebellar patients as loss of predictive programming (Brooks
and Thach 1981), the precise cause of the central deficit is still
unclear. This is because loss of predictive programming could
result from loss of the ability to predict movement dynamics
per se or from loss of the ability to generate precise movement
commands for the production of phasic force. As yet there is no
consensus as to the relative importance of each of these mechanisms. One situation that has been studied in detail is control
of interaction torques in fast multijoint reaching movements.
There is agreement that cerebellar patients show disorder in
control of these torques, which then contributes to cerebellar
arm ataxia (Bastian et al. 1996; Topka et al. 1998). However,
there is controversy as to whether this results from an inability
to predict and compensate for interaction torques (Bastian et al.
2000) or from an inability to generate sufficient levels of phasic
muscle torque (Boose et al. 1999; Topka et al. 1998).
For throwing, some results can be interpreted as being
consistent with the proposal that cerebellar patients have lost
the ability to generate precise movement commands for the
production of phasic force. For example, the finding that five of
the six cerebellar patients showed a tendency for larger finger
amplitudes with balls of increasing weight could be explained
as being due to loss of the ability of the fingers to generate a
large-amplitude, fast-changing flexor force. This would fit with
previous observations of deficits in finger control in cerebellar
patients. It has previously been shown that patients have
slowed speed in a repetitive isometric task involving the fingers
(Mai et al. 1988), slowed development of finger grip force
(Müller and Dichgans 1994b), and a reduced ability to adapt to
heavy loads by increasing the peak pinch force rate (Müller and
Dichgans 1994a). According to this scheme, the same finding
in unskilled subjects of increased finger amplitudes with
heavier balls would be due to the subjects failure to have
learned the skill of producing large, fast-changing finger flexor
torques. Alternatively, the increase in finger amplitude in patients and unskilled subjects could simply have been caused by
a small passive movement at the distal interphalangeal joint
with the heavier balls that was due to a failure to stiffen this
joint properly as the ball rolled along the finger.
The present results indicate that patients had neither lost all
of their ability to predict force nor to produce it. Two pieces of
evidence indicate that patients, at least to some extent, were
able to scale up finger flexor forces for the heavier balls. First,
although back forces were 14 times larger for the heavy 196-g
ball compared with the light 14-g ball (for the same hand
acceleration), the fingers were not pushed back into extreme
extension in throws with the heavy ball. Second, on average,
cerebellar patients (like controls) had larger finger flexions
after ball release for balls of heavier weights (Fig. 8A). Given
that the amplitude of finger flexion 10 ms after ball release is
proportional to peak force on the finger before ball release in
skilled subjects (Hore et al. 2001) and in unskilled subjects
(Fig. 2), this result suggests that in cerebellar patients finger
force was on average scaled up for the heavy balls.
This ability of cerebellar patients to scale up finger force to
some extent to the expected load agrees with other findings.
For example, Müller and Dichgans (1994a) found that cerebellar patients were able to scale their pinch force levels to
different loads in the 1- to 8-N range. Furthermore, in singlejoint movements, cerebellar patients increased agonist electro-
FINGER POSITIONS IN THROWING
Similarly, for the unskilled subjects, the cerebellum presumably contributed significantly to the control of their motions
even if they were less accurate than those of skilled subjects. If
one assumes that precise control of the fingers in throwing
depends on the development of skill, which in turn depends on
the cerebellum, it is not surprising that the performance of
patients with various sized cerebellar lesions overlaps that of
unskilled subjects with various degrees of skill.
Models of cerebellar function
We thank L. van Cleeff for technical assistance. R. Citron performed and
analyzed some experiments as part of her fourth year Honors Physiology thesis
requirement.
J Neurophysiol • VOL
This work was supported by Canadian Medical Research Council Grant MT
14695 and Deutsche Forschungsgemeinschaft Grants DFG Ti 239/3-1 and
DFG Ti 239/4-1.
REFERENCES
BASTIAN AJ, MARTIN TA, KEATING JG, AND THACH WT. Cerebellar ataxia:
abnormal control of interaction torques across multiple joints. J Neurophysiol 76: 492–509, 1996.
BASTIAN AJ, ZACKOWSKI KM, AND THACH WT. Cerebellar ataxia: torque
deficiency or torque mismatch between joints? J Neurophysiol 83: 3019 –
3030, 2000.
BECKER WJ, KUNESCH E, AND FREUND H-J. Coordination of a multi-joint
movement in normal humans and in patients with cerebellar dysfunction.
Can J Neurol Sci 17: 264 –274, 1990.
BECKER WJ, MORRICE BL, CLARK AW, AND LEE RG. Multi-joint reaching
movements and eye-hand tracking in cerebellar incoordination: investigation of a patient with complete loss of Purkinje cells. Can J Neurol Sci 18:
476 – 487, 1991.
BOOSE A, DICHGANS J, AND TOPKE H. Deficits in phasic muscle force generation explain insufficient compensation for interaction torque in cerebellar
patients. Neurosci Lett 261: 53–56, 1999.
BROOKS VB AND THACH WT. Cerebellar control of posture and movement. In:
Handbook of Physiology. The Nervous System. Motor Control. Bethesda,
MD: Am. Physiol. Soc., 1981, sect 1, vol. II, p. 877–946.
DARLING WG AND COOKE JD. Changes in the variability of movement trajectories with practise. J Mot Behav 19: 291–309, 1987.
DAY BL, THOMPSON PD, HARDING AE, AND MARSDEN CD. Influence of vision
on upper limb reaching movements in patients with cerebellar ataxia. Brain
121: 357–372, 1998.
FLAMENT D AND HORE J. Movement and electromygraphic disorders associated
with cerebellar dysmetria. J Neurophysiol 55: 1221–1233, 1986.
FLANAGAN JR AND WING AM. The role of internal models in motion planning
and control: evidence from grip force adjustments during movements of
hand-held loads. J Neurosci 17: 1519 –1528, 1997.
GROWDON JH, CHAMBERS HW, AND LIU CN. An experimental study of cerebellar dyskinesia in the rhesus monkey. Brain 90: 603– 632, 1967.
GORASSINI M, PROCHAZKA A, AND TAYLOR JL. Cerebellar ataxia and muscle
spindle sensitivity. J Neurophysiol 70: 1853–1862, 1993.
GEORGOPOLOUS AP, KALASKA JF, AND MASSEY JT. Spatial trajectories and
reaction times of aimed movements: effects of practice, uncertainty, and
change in target location. J Neurophysiol 46: 725–743, 1981.
HIGGINS JR AND SPAETH RK. Relationship between consistency of movement
and environmental condition. Quest 17: 61– 69, 1972.
HOLMES G. The symptoms of acute cerebellar injuries due to gunshot injuries.
Brain 40: 461–535, 1917.
HOLMES G. The Croonian lectures on the clinical symptoms of cerebellar
disease and their interpretation. Lancet 100: 1231–1237, 1922.
HORE J, WATTS S, LESCHUK M, AND MACDOUGALL A. Control of finger grip
forces in overarm throws made by skilled throwers. J Neurophysiol 86:
2678 –2689, 2001.
HORE J, WATTS S, MARTIN J, AND MILLER B. Timing of finger opening and ball
release in fast and accurate overarm throws. Exp Brain Res 103: 277–286,
1995.
HORE J, WATTS S, AND TWEED D. Errors in the control of joint rotations
associated with inaccuracies in overarm throws. J Neurophysiol 75: 1013–
1025, 1996a.
HORE J, WATTS S, AND TWEED D. Prediction and compensation by an internal
model for back forces during finger opening in an overarm throw. J Neurophysiol 82: 1187–1197, 1999.
HORE J, WATTS S, TWEED D, AND MILLER B. Overarm throws with the
nondominant arm: kinematics of accuracy. J Neurophysiol 76: 3693–3704,
1996b.
HORE J, WILD B, AND DIENER HC. Cerebellar dysmetria at the elbow, wrist and
fingers. J Neurophysiol 65: 563–571, 1991.
JOHANSSON RS AND WESTLING G. Coordinated isometric muscle commands
adequately and erroneously programmed for the weight during lifting task
with precision grip. Exp Brain Res 71: 59 –71, 1988a.
JOHANSSON RS AND WESTLING G. Programmed and triggered actions to rapid
load changes during precision grip. Exp Brain Res 71: 72– 86, 1988b.
KAWATO M. Learning internal models of the motor apparatus. In: The Acquisition of Motor Behavior in Vertebrates, edited byBloedel JR, Ebner TJ, and
Wise SP. Cambridge, MA: MIT Press, 1996, p. 409 – 430.
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Can these results be explained by current theories of cerebellar function? A recent extension of the concept that the
cerebellum operates in part by predictive programming is that
the cerebellum is the site of internal models of the motor
apparatus and load (Kawato 1996; Wolpert et al. 1998). Considerable experimental evidence has been found to support the
idea that skilled hand movements are controlled by such internal models (e.g., Flanagan and Wing 1997; Hore et al. 1999;
Johansson and Westling 1988a,b; Laquaniti and Maioli
1989a,b). The cerebellum is implicated because of its adaptive
capability (synaptic plasticity), its broad range of sensory inputs, and the properties of its circuitry, which it is argued,
possess a capacity to approximate complex dynamics (Kawato
1996). The present results are consistent with this proposal in
so far as they show loss of accurate and precise feedforward
control. Beyond this, the proposal has not yet been developed
so that it accounts for the retention in cerebellar patients of
some predictive ability and the increased variability in their
movement kinematics.
In contrast, a recent model of the function of the cerebellum
in the control of saccades has been proposed which accounts
for increased variability with cerebellar lesions (Quaia et al.
1999). In this model, the cerebellum accounts for both the
accuracy and consistency (lack of variability) of saccades. This
cerebellar contribution occurs during each saccade to compensate for both the characteristics of the occulomotor plant and
the variability present in the rest of the saccadic system during
the preparation and execution of the movement. Presumably
the cerebellum is playing a similar, but more complex, role in
arm movements.
In conclusion, the present study has demonstrated that, in a
multijoint arm movement where generation of the appropriate
finger force is based on prediction of the back force from the
ball and production of the appropriate finger flexor torque, both
cerebellar patients and unskilled subjects show the same deficits to various degrees: both can predict and scale force to some
extent to the expected load, but both have an abnormally large
variability from throw to throw in the amplitude of the finger
position changes that occur throughout each throw. This presumably reflects increased variability in the control of finger
force that depends in turn on the degree of cerebellar dysfunction and the degree of lack of skill. This result is consistent
with the hypothesis that an essential role of the cerebellum is
to achieve skill in movements by reducing variability in both
timing and force of muscle contractions.
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D. TIMMANN, R. CITRON, S. WATTS, AND J. HORE
J Neurophysiol • VOL
TAKAGI M, ZEE DS, AND TAMARGO RJ. Effects of lesions of the oculomotor
vermis on eye movements in primate: saccades. J Neurophysiol 80: 1911–
1931, 1998.
THACH WT, GOODKIN HP, AND KEATING JG. The cerebellum and the adaptive
coordination of movement. Annu Rev Neurosci 15: 403– 442, 1992.
TIMMANN D, WATTS S, AND HORE J. Failure of cerebellar patients to time finger
opening precisely causes ball high-low inaccuracy in overarm throws.
J Neurophysiol 82: 103–114, 1999.
TIMMANN D, WATTS S, AND HORE J. Causes of left-right ball inaccuracy in
overarm throws made by cerebellar patients. Exp Brain Res 130: 441– 452,
2000.
TIMMANN D AND HORAK FB. Prediction and set-dependent scaling of early
postural responses in cerebellar patients. Brain 120: 327–337, 1997.
TOPKA H, KONCZAK J, SCHNEIDER K, BOOSE A, AND DICHGANS J. Multijoint
arm movements in cerebellar ataxia. Abnormal control of movement dynamics. Exp Brain Res 119: 493–503, 1998.
TROUILLAS P, TAKAYANAGI T, HALLETT M, CURRIER RD, SUBRAMONY SH,
WESSEL K, BRYER A, DIENER HC, MASSAQUOI S, GOMEZ CM, COUTINHO P,
BEN HAMIDA M, CAMPANELLA G, FILLA A, SCHUT L, TIMMANN D, HONNORAT J, NIGHOGHOSSIAN N, AND MANYAM B. International cooperative
ataxia rating scale for pharmacological assessment of the cerebellar syndrome. J Neurol Sci 145: 205–211, 1997.
TWEED D, CADERA W, AND VILIS T. Computing three-dimensional eye position
quaternions and eye velocity from search coil signals. Vision Res 30:
97–110, 1990.
WOLPERT DM, MIALL RC, AND KAWATO M. Internal models in the cerebellum. Trends Cognit Sci 2: 338 –347, 1998.
86 • DECEMBER 2001 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.5 on June 16, 2017
LACQUANITI F AND MAIOLI C. The role of preparation in tuning anticipatory and
reflex responses during catching. J Neurosci 9: 134 –148, 1989a.
LACQUANITI F AND MAIOLI C. Adaptation to suppression of visual information
during catching. J Neurosci 9: 149 –159, 1989b.
LUCIANI L. The hindbrain. In: Human Physiology, Muscular and Nervous
System, edited by Welby FA. London: Macmillan, 1915, vol. 3, p. 467.
MAI N, BOLSINGER P, AVARELLO M, DIENER HC, AND DICHGANS J. Control of
isometric finger force in patients with cerebellar disease. Brain 111: 973–
998, 1988.
MANTO M, GODAUX E, AND JACQUY J. Cerebellar hypermetria is larger when
the inertial load is artificially increased. Ann Neurol 35: 45–52, 1994.
MÜLLER F AND DICHGANS J. Dyscoordination of pinch and lift forces during
grasp in patients with cerebellar lesions. Exp Brain Res 101: 485– 492,
1994a.
MÜLLER F AND DICHGANS J. Impairments of precision grip in two patients with
acute unilateral cerebellar lesions: a simple parametric test for clinical use.
Neuropsychologia 32: 265–269, 1994b.
QUAIA C, LEFÈVRE P, AND OPTICAN LM. Model of the control of saccades by
superior colliculus and cerebellum. J Neurophysiol 82: 999 –1018, 1999.
ROBINSON DA. A method of measuring eye movement using a scleral search
coil in a magnetic field. IEEE Trans Biomed Eng 10: 137–145, 1963.
ROBINSON FR. Role of the cerebellum in movement control and adaptation.
Curr Opin Neurobiol 5: 755–762, 1995.
ROBINSON FR, STRAUBE A, AND FUCHS AF. Role of the caudal fastigial nucleus
in saccade generation. II. Effects of muscimol inactivation. J Neurophysiol
70: 1741–1758, 1993.
SERRIEN DJ AND WIESENDANGER M. Grip-load force coordination in cerebellar
patients. Exp Brain Res 128: 76 – 80, 1999.