Brain (1996), 119, 281-293
Interj oint coordination during pointing movements
is disrupted in spastic hemiparesis
Mindy F. Levin
Centre de Recherche, lnstitut de Riadaptation de Montreal,
fccole de Riadaptation, Universite de Montreal, Montreal,
Canada
Correspondence to: Dr Mindy F. Levin, Centre de
Recherche, lnstitut de Riadaptation de Montrial, 6300 av.
Darlington, Montreal, Quebec, Canada H3S 2J4
Summary
Approaches to the rehabilitation of movement in spastic
hemiparetic patients depend on knowledge of the underlying
mechanisms of movement deficits. The goals of this study
were to characterize end-point trajectories and interjoint
coordination of arm pointing movements to different targets
on a horizontal planar surface and to correlate disruptions
in motor control in the affected arm of hemiparetic subjects
with the level of spasticity and the degree of functional
impairment measured clinically. Arm movements were studied
in six normal and 10 hemiparetic subjects. Data from the
affected arms of hemiparetic subjects were compared with
those from their non-affected arms and to data from the arms
of normal subjects. Subjects were seated in front of a
horizontal surface adjusted to the height of the sternal notch
with the trunk stabilized. They made planar arm reaching^
movements (20 and 40 cm) to four different targets located
directly in front of them and in the ipsilateral and
contralateral workspace. Kinematic data from the finger,
wrist, elbow and shoulder were recorded with a threedimensional optical tracking system. Results showed that
movement amplitudes were lower and movement times were
significantly prolonged in the affected arms. Although
trajectories were marked by deviations from smooth straight
lines and characterized by increased dispersion and
segmentation, even those subjects with the most severe
spasticity could reach into all parts of the workspace with
both their affected and non-affected arms. This indicated that
movement planning in terms of extrapersonal space was
unaffected in these subjects. On the other hand, the interjoint
coordination of movements made into or out of the typical
extensor or flexor synergies was equally disrupted. These
findings suggest a bi-level control organization of pointing
movements in both normal and hemiparetic subjects: the
level of trajectory planning in extrapersonal space and the
level specifying interjoint coordination according to the
trajectory plan. Deficits in motor performance in stroke
patients may be associated with problems at the second
control level. This implies some strategies for the rehabilitation of stroke patients with motor disorders. Treatment
aimed at improving arm function should be oriented toward
restoring the normal sensorimotor relationships between the
joints. We also found that while clinical spasticity scores
were correlated with some aspects of motor performance, they
provided little information about the movement deficit itself.
Keywords: motor control; stroke; spasticity; pointing movement; synergies
Introduction
Bilateral or unilateral hemispheric damage results in deficits
in the ability of these patients to make smooth and accurate
visually guided arm movements in external space (Riddoch,
1935; Fisk and Goodale, 1988). Deficits in the coordinated
use of the limb are most evident in the limb contralateral to
the side of unilateral damage (Levine et al., 1978; Trombly,
1992) and occur together with spasticity, muscle weakness
(Bourbonnais and Vanden Noven, 1989; Wiesendanger, 1990)
and stereotypic movement patterns or synergies (Brunnstrom,
1970; Bobath, 1990). The recovery of motor function after
a stroke typically follows characteristic stages (Brunnstrom,
1970). Early stages are marked by the appearance of spasticity
© Oxford University Press 1996
and the development of stereotypic movement patterns, while
isolated joint movements are compromised. In the upper
limb, the flexor synergy consists of forearm supination and
elbow flexion associated with shoulder flexion, abduction
and external rotation. The extensor synergy is characterized
by pronation and elbow extension combined with shoulder
extension, adduction and internal rotation. In later stages of
the recovery from stroke, spasticity declines and the patient
is able to make movements out of synergy (i.e. elbow
extension combined with shoulder flexion). Still later, isolated
joint control returns.
Goal-directed movements with the affected limb in
282
M. F. Levin
hemiparetic subjects are characterized by decreased movement speed, smoothness and coordination, and abnormal
patterns of muscle activation (Hammond et al., 1988;
Gowland et al, 1992; Trombly, 1992) which have been
attributed, in part, to peripheral factors. Deficits in voluntary
control of movement together with the presence of spasticity
have been associated, in particular, with disorders in the
organization of segmental reflex activity (e.g. Corcos et al.,
1986; Powers et al., 1988; Levin and Feldman, 1994).
However, enhanced reflex activity may not be the sole
contributor to the movement deficit. Indeed, at least in
children with cerebral palsy, disorders in muscle activation
may be predominantly related to abnormalities in the
coordination of descending inputs to motoneurons of different
muscles since movement remained disrupted after spasticity
was reduced or eliminated by dorsal rhizotomy (Giuliani,
1991).
To date, the control and production of multi-joint functional
arm movements in hemiparetic subjects has received little
attention although numerous studies have documented
trajectory formation and interjoint coordination in normal
subjects (Lacquaniti, 1992; Flanagan et al., 1993; for review,
see Jeannerod, 1988). In normal subjects, certain elements in
reaching and grasping display invariant behaviours suggesting
key principles in motor control. For example, movement
trajectories involving more than one joint tend to be straight,
smooth and have bell-shaped velocity profiles (Hogan and
Flash, 1987). In addition, peak velocities and accelerations
are generally scaled to movement distance (Gordon et al.,
1994). Some authors have suggested that this implies that
the extent of hand movement may be programmed in advance
of the movement (Gordon et al., 1994) while others presume
that scaling may simply be a consequence of the specification
of the rate and duration of the shift in the equilibrium
configuration of the arm end-point (Flanagan et al., 1993;
Feldman and Levin, 1995). Reaching movement is believed
to be planned in a hand (Georgopoulos et al., 1981; Flash
and Hogan, 1985; Flanagan et al., 1993; Gordon et al.,
1994) or alternatively, a shoulder-centred coordinate system
(Soechting and Flanders, 1989a, b).
The analysis of end-point trajectories and interjoint
coordination during pointing movements may be helpful in
the understanding of the nature of movement deficits in
patients with CNS lesions (Kelso and Tuller, 1981; Flanders
et al., 1992). The generation of movement trajectories and
interjoint coordination may be associated with functionally
different heterarchical levels of motor control. This
subdivision may be illustrated by the ability of subjects
to produce the same trajectory using different interjoint
coordinations (Bernstein, 1967). Several hypotheses suggest
that interjoint coordination is achieved by organizing the
motor apparatus into coordinative structures specifically
oriented to achieve the goal (Gurfinkel et al, 1971; Kugler
et al., 1980). In addition, deficits in single-joint control
may also influence motor performance by disruption of the
linkages required for the construction of a coordinative
structure.
We sought to determination the level at which motor
control is disrupted in stroke patients. The goals of this study
were: (i) to compare end-point trajectories and interjoint
coordination of arm pointing movements to different targets
on a horizontal planar surface between the affected side of
spastic hemiparetic subjects, their non-affected sides and the
arms of an age-matched normal control group; and (ii) to
correlate disruptions in motor control in the affected arm of
hemiparetic subjects with the level of spasticity and the
degree of functional impairment measured clinically. Our
results may help in the development of more effective
approaches to the rehabilitation of these patients. Some of
the results of this study have been published in abstract form
(Levin et al, 1993).
Material and methods
Subjects
Ten hemiparetic and six age/sex-matched normal subjects
participated in these studies which were approved of by the
hospital Ethics committee according to the declaration of
Helsinki. They were informed of the experimental procedures
and gave their written consent. Hemiparetic subjects were
included if they (i) had sustained a single cerebro-vascular
accident leading to upper limb paresis, as documented by
their medical history and confirmed by appropriate medical
tests (computer-assisted tomography scan, nuclear magnetic
resonance); (ii) had no other neurological disorders; (iii) were
able to understand simple commands (no receptive aphasia);
and (iv) had spasticity in the elbow flexors but preserved
some control of isolated muscles in the upper limb. Subjects
were excluded from the study if they had left-sided neglect,
perceptuomotor or visual field deficits, apraxia, shoulder
subluxation or pain in the upper limb. Normal subjects were
excluded if they had a medical history of (i) pain or (ii)
previous orthopaedic or neurological problems affecting the
shoulder, elbow or wrist.
Research protocol
Pointing arm movements were recorded in a single testing
session for all subjects. Prior to the recording, hemiparetic
subjects were also tested clinically by an experienced
physiotherapist to assess spasticity (modified Ashworth scale)
and sensorimotor function (Fugl-Meyer scale, see below).
The physiological testing sessions were run by an investigator
who was unaware of the results of the clinical tests.
Clinical assessments
Spasticity was assessed with the subject in the sitting position
using two commonly used measurements, (i) Biceps tendon
jerks were scored on a five-point scale ranging from no
Interjoint coordination in hemiparesis
283
Tkble 1 Demographic data and clinical scores for hemiparetic subjects
Subject
Age/sex
Site*
Side of
hemiparesis
Years
after onset
Spasticity
score (\2)r
Fugl-Meyer
score (66)
1
2
3
4
5
6
7
8
9
10
38/M
58/F
54/F
487M
32/M
47/M
42/M
63/F
52/M
51/M
ICS
ICS
ppcs
Right
Left
Right
Left
Right
Left
3.0
1.0
7.2
3.5
2.5
2.7
0.8
0.5
4.0
0.8
8
7
7
8
6
6
5
4
3
3
32
19
49
30
55
57
65
66
50*
65
ppc
FP"
ICS
FP0-5
IC5
ICS
pcs
Right
Right
Left
Left
*F = frontal; P = parietal; IC = internal capsule; c = cortical lesion; s = sub-cortical lesion. ^Spasticity score: 0-6 mild, 7-9 moderate,
10-12 severe.^Test incomplete: score out of 58.
response (0) to a maximally hyperactive response (4). (ii)
Resistance to full-range passive elbow extension at a moderate
speed were scored on a modified five-point Ashworth Scale
(Ashworth, 1964). Using this scale, zero corresponded to
normal tone, 2 corresponded to a slight increase in tone,
giving a 'catch' when the limb was moved, 4 equalled a
more marked increase in tone but the limb was still easy to
move, 6 was given if there was a considerable increase in
tone making passive movement of the limb difficult and an
8 corresponded to the limb being rigidly fixed in flexion or
extension. The scores were doubly weighted since resistance
to passive movement most closely represents tone (Berardelli
et al., 1983). These two scores were then summed to provide
a composite index of spasticity representing both phasic and
tonic responses of the spastic muscles. Based on previous
clinical experience, the computed scores ranging from 0 to
6, 7 to 9 and 10 to 12 correspond to mild, moderate and
severe spasticity, respectively. The full version of this scale
(including wrist clonus) has been used in previous studies
of spastic hemiparetic subjects and has demonstrated both
reliability and responsiveness (Levin and Hui-Chan, 1992).
The second clinical evaluation was the measurement of
residual motor function of the upper limb using the FuglMeyer scale (Fugl-Meyer et al., 1975). This scale allows
assessment of the ability of the subject to make isolated
movements within and out of pathological synergy patterns.
In addition, it allows assessment of sensory function, reflexes,
hand function and coordination. A maximum score of 66
corresponds to normal function.
Demographic data for all 10 hemiparetic subjects are
shown in Table 1 as well as clinical spasticity and motor
function scores. Their mean age was 48.5±9.3 years and the
majority were male. All subjects had sustained a unilateral
stroke {see Table 1 for locations of lesions). In nine out of
the 10 subjects studied, the CNS lesion involved sub-cortical
structures (Table 1). Four of these subjects also had a cortical
lesion. Only one subject (Subject 4) had a cortical lesion
only. Half the subjects had clinical signs of spasticity and
weakness on the left side while the other half had signs on
the right side of the hemicorps. Levels of spasticity ranged
Target positions
for reaching movements
Ipsilateral
Contralateral
Fig. 1 Diagram of the target positions (black circles) for reaching
movements made on a horizontal surface. The starting position
(small stippled circle) was located in the midline of the body.
from 3 (mild) to 11 (severe) out of a possible total score of
12. For the motor function scores, only one subject had a
score of 19 indicating a severe motor deficit (gross motor
function only) while the others ranged from 30 to 66 (gross
and some fine motor function).
Planar arm pointing movements
Subjects were seated in front of a height-adjustable table
inlaid with light-emitting diodes distributed as in Fig. 1.
Movements started from the midline of the body at a distance
of -15 cm from the chest. In the initial position, the shoulder
was abducted 45°, the elbow was flexed 45° and the forearm
was pronated so that the hand rested on the table. The near
and far targets were placed in a sagittal direction 200 and
400 mm, respectively, away from the initial position. The
ipsilateral and contralateral targets were placed 200 mm
lateral to the near target in the ipsilateral and contralateral
284
M. F. Levin
workspace, respectively. We purposely arranged the targets
in different parts of the workspace so that reaching them
required different combinations of joint movement in and
outside of stereotyped synergy patterns (Brunnstrom, 1970).
Moving towards the ipsilateral target required an out-ofsynergy movement which consisted of a combination of
shoulder horizontal abduction (extension) with elbow
extension if the subject intended to produce a straight line
trajectory or a single-joint elbow movement if he intended
to produce a curved trajectory. Movements to the other
three targets required a combination of shoulder horizontal
adduction (flexion) and elbow extension. While subjects
could make use of the extensor synergy to reach the
contralateral target, reaching the near and far targets required
a combination of flexor and extensor synergies in order to
direct the arm forward. Three of the targets were located in
the near field of the workspace and the far target was located
in the far field which required the greatest excursion of
both joints.
The timing and sequencing of target illumination were
controlled by a computer programme. Movements of the
shoulder and wrist were unconstrained while trunk movement
was limited but not completely blocked by strapping both
shoulder girdles to the high back support of the chair. In
addition, to standardize the position of the wrist and hand,
hemiparetic subjects wore a splint which held the wrist in
the neutral position and the fingers in slight flexion. A trial
consisted of a continuous self-paced movement made with
the forearm in pronation, by sliding the hand on the table
from the starting position to the target and back to the starting
position. Subjects performed 10 movements to each target in
a randomized block sequence (i.e. 10 movements to the near
target, 10 movements to the far target, etc.). Vision of the
moving arm was permitted. Experiments were repeated for
the affected and non-affected arms of the hemiparetic subjects
and for the right arm of normal subjects.
Data acquisition and analysis
Wrist, elbow and shoulder positions were recorded in three
dimensions with the Optotrak motion analysis system by
infrared light emitting diodes positioned on the tip of the
third finger and over bony landmarks of the wrist (head of
the ulna), elbow (lateral epicondyle) and shoulder (ipsilateral
and contralateral acromions). Personal computers were used
to collect kinematic data and control the timing of target
light emitting diodes.
Wrist, elbow and shoulder positions were recorded at a
sampling rate of 400 Hz and digitally low-pass filtered at
12 Hz using a fourth-order zero phase-lag Butterworth filter
(Ackroyd, 1973). Joint angles were computed from the
filtered position data as the angles between the corresponding
vectors joining the infrared light emitting diodes. Velocities
were obtained by numerically differentiating the filtered
position data using a second-order, least-squares method. The
velocity data was also digitally low-pass filtered as for the
position data.
All data records were analysed from individual trials which
were displayed on an interactive video programme and then
means and SDs were calculated. Kinematic variables were
analysed in terms of movement times, movement distances
and paths of the trajectories in terms of curvatures and
directions. Movement times from the initial position to the
target and from the target backward to the initial position
were calculated from the movement onset to movement
offset defined as the time at which the velocity of the
shoulder surpassed or returned to 10% of the peak velocity,
respectively. These were calculated separately for each
direction. After aligning traces from single trials according to
movement onsets, movement trajectories were reconstructed
from x and v data from the tip of the third finger and angle/
angle diagrams relating the movement of the elbow to the
shoulder joint were plotted.
The curvature of the trajectory was estimated by the
deviation of the trajectory from an ideal straight line. The
deviation was defined as the length (in millimetres) of a
segment (d) drawn perpendicular from the point of maximum
deflection of the trajectory from the segment (b) joining the
beginning and end-points of the trajectory. This deflection
was calculated by a computer algorithm. We also calculated
the variance of d as a measure of dispersion of the trajectories.
Interjoint coordination was analysed by calculating the
slopes and the correlation coefficients of the linear regression
equations between the shoulder and elbow joint excursions
for movements made to the far and ipsilateral targets.
Data from non-affected and affected limbs of the same
subjects were compared using two-way repeated measures
ANOVAs and multiple comparisons post hoc tests. For the
analysis of the deflections in the normal subjects, one-way
repeated measures ANOVAs were used for each subject.
Non-parametric statistics were used when normality and
variance requirements were not met (Fleiss, 1986). Student's
t tests or Mann-Whitney rank sums statistics were used for
comparisons between the slopes of the regression lines for
normal and affected sides of the same subjects. For the
hemiparetic arms, kinematic variables were correlated with
clinical scores of spasticity and residual motor function using
Pearson Product Moment statistics. Significance levels of
P < 0.05 were used for all statistical comparisons.
Results
End-point trajectories made to all targets and angle/angle
plots for movements made to the contralateral, far and
ipsilateral targets are compared in Fig. 2 for the affected
(left) and non-affected (right) arm of one hemiparetic subject
with severe spasticity.
For movements made to each target by the non-affected
arm in this subject (n = 10, right panel), the trajectories
and interjoint coordinations were smooth and continuous,
illustrated by the almost linear relationship between the elbow
Interjoint coordination in hemiparesis
End-point trajectory
Affected arm
Non-affected arm
520
E
0
x(mm)
520
Interjoint coordination
120
(B)
Contra
(C)
Far
(D)
Ipd
CD
120
Shoulder angle (degrees)
Fig. 2 End-point trajectories (A) in spatial coordinates and
interjoint coordination (B-D) in angular coordinates for the
affected left arm (left panels) and the non-affected arm (right
panels) for a hemiparetic subject with severe spasticity. All
diagrams show movements made from the starting position to the
target positions only. Trajectories are shown in A for movements
made to the contralateral (contra), far, near and ipsilateral (ipsi)
targets. Interjoint coordination (elbow versus shoulder angle
diagrams) for the movements in A are shown for the contralateral
(B), far (C) and ipsilateral (D) targets. Angular diagrams for die
near target (not shown) were similar to those for the far target
shown in C.
and shoulder joint excursions. For different targets, the degree
of excursion in the shoulder joint varied from maximal for the
contralateral target (Fig. 2B, right panel) to no involvement in
this subject for the ipsilateral target (Fig. 2D, right panel). In
contrast, on her affected side, this subject could not produce
a smooth trajectory nor a smooth coordination between these
two joints for the contralateral and far targets (Fig. 2, left
285
panel) illustrated by segmentation of the movement. The
same was true for the near target (not shown). The subject
whose data is illustrated in Fig. 2 had the most difficulty
making movements to the contralateral and far targets.
Segmentation was most obvious for the movement to the
contralateral target (Fig. 2B, left panel) in which she produced
a combined elbow/shoulder movement followed by an
isolated elbow extension movement. Movements to the far
and ipsilateral targets were achieved predominantly by the
elbow joint. However, for the far target, there was nonsystematic involvement of the shoulder joint (Fig. 2C, left
panel). Although for the ipsilateral target, the shoulder
excursion was small, there was a strict linear relationship
between elbow and shoulder joint excursions (Fig. 2D, left
panel) in contrast to the non-affected arm in which the
shoulder joint was motionless. Finally, movement distances
and joint excursions were decreased in the affected compared
with the non-affected arm for the contralateral and far targets
(Fig. 2A, B and C, cf. right and left panels).
To illustrate that the differences observed in our data for
the left and right arms of hemiparetic subjects could be
explained by laterality, data from only the right arms in three
different subjects for a movement made to and from the far
target are compared in Fig. 3. Data from a normal arm is
shown in the left panel while that from non-affected and
affected right arms are shown in the middle and right panels,
respectively. In normal and non-affected arms of hemiparetic
subjects, movements were smooth and characterized by bellshaped velocity profiles for each component of the movement
to and from the target (Fig. 3C). The change in elbow and
shoulder angles was related by a linear function (Fig. 3B)
and the peak velocities for elbow and shoulder movements
were synchronous (Fig. 3C).
The right panels in Fig. 3A-C show data from an
hemiparetic subject with severe spasticity in whom the
interjoint coordination to the far target was disrupted. This
subject was unable to coordinate the elbow and shoulder
joint excursions (cf. middle panel, Fig. 3B). Instead, he
produced the movement primarily with the elbow joint
combined with small medio-lateral movements of the trunk
(not illustrated). Similar to the movements illustrated in
Fig. 2, the target was reached by a series of sequential
movements characterized by multiple lateral directional
changes (Fig. 3A, right panel). This subject was also not able
to reach the velocity of joint movement typical of normal or
non-affected arms (Fig. 3C, right panel). Movements made
by the hemiparetic arms were segmented and the velocity
profiles were skewed and disrupted (Fig. 3, right panel). In
the example shown, despite the occurrence of multiple peaks
indicative of short bursts of unsustained movement and
episodes of acceleration, the pattern of the velocity profile
for the elbow was generally preserved while that of the
shoulder was disorganized. Movements made backwards
from the target were, just as slow as those made towards the
target. Thus, both of the subjects shown in Figs 2 and 3
286
M. F. Levin
(A) End-point trajectory
\
Horizontal displacement (mm)
(B) Interjoint coordination
1*0
£
Contra
Far
Near
Ipsi
Fig. 4 Histograms of the mean (+SD) variance of the deflection,
d (see inset), of the trajectories for the non-affected (closed bars)
and the affected (open bars) arms of all hemiparetic subjects. The
variance was high for all targets except the ipsilateral target for
the hemiparetic arms.
Shoulder angle (degrees)
(C) Elbow velocity
60°/. I
similarly characterized by smooth bell-shaped symmetrical
profiles. Peak velocities were also not different in these two
groups of subjects. Thus, the kinematic characteristics of
movements made by the arm ipsilateral to the side of the
hemispheric lesion were used as the control for test
movements made by the affected arm.
1000 oa
Fig. 3 End-point trajectories (A), their corresponding interjoint
coordination (B) and velocity profiles for the elbow and shoulder
joints (C) for single movements made to and from the far target
by the right arms of three different subjects: normal control (left
panel), non-affected arm of a hemiparetic subject (middle panel)
and the affected arm of a hemiparetic subject (right panel).
Arrows in A and B indicate the direction of the movement.
demonstrated that they were unable to produce the elbow/
shoulder coordination required for reaching the far target.
In order to be able to compare data from the non-affected
arms of hemiparetic subjects to their affected arms, the
parameters to be compared should not differ from those of
normal arms. Some characteristics of movement have been
reported to be different from those in normal subjects
(see Fisk and Goodale, 1988; Mattingley et al., 1994). To
determine whether or not this was the case in the present
study, we compared movement times, velocity profiles, joint
angle coordinations and trajectories of movements made by
the arm on the non-affected side with those of age-matched
normal subjects. Our comparison showed (see Fig. 3) that
trajectories and interjoint coordinations were similar in the
two groups of subjects. Movement times were also
comparable (see Fig. 6). For example, the mean movement
time to the far target for the normal subjects was 1085 ± 139
ms and for the non-affected arm of the hemiparetic subjects
was 1168± 219 ms. Although the peak velocity of the
movement illustrated in Fig. 3 for the non-affected arm was
less than that of the normal arm, the velocity profiles were
Movement trajectories
Movement trajectories were analysed in terms of their
deflection from a straight line and their dispersions.
Deflections (d) of the trajectory from a straight line for
movements requiring the coordination of two joints were of
the same order of magnitude for the affected and non-affected
arms of hemiparetic subjects except for the sub-group of
subjects (n = 4) with the most severe spasticity. For example,
the mean deflections for movements made to the near target
were 14.13±8.47 mm for the non-affected arms compared
with 19.30±9.29 mm for the affected arms. For the
contralateral target, corresponding values were 19.33± 13.79
and 31.85 ±30.79, respectively. The large variability in the
hemiparetic arms for movements made to this target was due
to extremely wide deflections in the subjects with the most
severe spasticity (e.g. Subject 1,102.43 mm) while deflections
in the rest of the group ranged from 8.48 to 37.24 mm.
The dispersion of each set of trajectories was evaluated
by examining the variance of the deflection (d). Dispersions
were significantly larger for movements made by the affected
arm compared with the non-affected arm for each subject
(two-way repeated measures ANOVA) but grouped data for
each target was not significant due to the large variability
(Fig. 4). In contrast, comparison of the dispersions for
movements made to the ipsilateral target to those for the
three other targets revealed a significant decrease for this
target. This might be expected if the subjects made a singlejoint movement on the hemiparetic side as was done on the
non-affected side. However, as was obvious from the angle/
Interjoint coordination in hemiparesis
287
Table 2 Movement distance (b), the deviation of the trajectory (d), movement times and individual joint excursions for all
hemiparetic subjects for movements made to the far target
Total
distance
(b, mm)
Total
deviation
(d, mm)
Total
movement
time (ms)
Outward
movement
time (ms)
Backward
movement
time (ms)
Elbow
excursion
(°)
Shoulder
excursion
386.13
281.83
345.12
273.79
392.99
390.08
414.83
394.40
400.70
391.95
29.53
81.81
21.10
40.41
37.36
27.80
35.36
15.38
17.40
13.22
3703.81
6375.81
4846.07
3822.58
2137.10
2247.10
888.06
1056.85
1379.03
1916.13
1607.45
4390.33
2269.60
2715.05
1054.52
980.01
408.71
489.51
791.29
864.19
2156.35
1985.49
2576.47
1107.53
1130.65
1267.09
479.36
567.34
587.74
1051.93
67.26
46.84
75.10
53.77
74.35
69.80
68.16
64.37
73.86
59.08
10.85
8.68
17.30
9.56
28.78
21.42
22.04
24.24
18.42
23.74
367.18
50.32
31.94
19.93
2837.25*
1796.94
1557.07*
1246.73
1291.00*
720.93
65.26*
9.41
18.50*
6.86
Non-affected side
1
408.68
2
371.86
3
400.99
4
405.37
5
396.78
6
423.89
7
411.29
9
407.52
18.52
54.64
10.44
14.00
30.91
16.52
32.04
9.78
1238.06
1143.87
1227.74
1300.64
1301.94
959.34
744.52
1430.65
633.23
519.03
598.71
631.29
618.69
408.38
363.23
682.90
604.84
624.84
629.03
669.35
683.24
550.96
381.29
747.74
82.95
80.49
81.80
93.23
71.37
82.30
77.28
71.38
25.80
32.37
25.50
38.27
24.83
21.80
27.19
27.49
403.30
15.00
23.36
15.21
1168.35*
219.24
556.93*
115.76
611.41*
109.70
80.10*
7.06
27.91*
5.14
Subject
Affected side
1
2
3
4
5
6
7
8
9
10
X
SD
X
SD
(°)
Subjects are numbered according to Table 1 and arranged in decreasing order of spasticity. Note that there are no data for the nonaffected side of Subjects 8 and 10. *Differences significant (P < 0.05) between groups.
angle data (see Fig. 2D, left panel), subjects tended to make
coordinated elbow/shoulder movements which could not be
classified as being part of either the flexor or extensor synergy.
Movement extent and timing
Nine of the 10 subjects could extend their arms in the sagittal
plane to the near target (200 mm) but only six of the 10
could accurately reach the far target (400 mm in front of the
sternum). The remaining four subjects undershot the far
target by distances ranging from 20 to 126 mm. The mean
movement distances for the near target were 203.69±8.20
mm for the non-affected arms compared with 198.84±8.87
mm for the affected arms of hemiparetic subjects while those
to the far target were 4O3.30± 15.00 mm and 367.18±50.32
mm, respectively (Table 2). In general, the movement distance
deficit was more striking in those subjects with more severe
spasticity. Analysis of the contributions of the individual
elbow and shoulder joints to the total arm excursion (Fig. 5)
revealed no decrease in the hemiparetic arms (open bars)
compared with normal (hatched bars) and non-affected arms
(filled bars) for the near and ipsilateral targets. However, the
total joint excursions for both the elbow and shoulder
joints were significantly decreased for the hemiparetic arms
compared with normal and non-affected arms for reaches
made to targets located in the far (see also Table 2) and
contralateral workspace.
Movement times to air targets were longer for the affected
arms (Fig. 6, top panel) compared with the non-affected arms
of the hemiparetic patients (Fig. 6, middle panel) or to normal
arms (Fig. 6, bottom panel). For example, for movements to
the near target, the mean total movement time for the affected
arms of the hemiparetic subjects was significantly longer
(1867 ± 1094 ms) than for their non-affected arms (1062 ± 224
ms, P < 0.05). Peak velocities were lower and times to peak
velocities were similarly prolonged for movements made to
all targets. For example, for the outbound movement to the
contralateral target, the mean peak velocity of the hemiparetic
arm of six subjects was 649.95 ±246.61 mm/s compared with
1008.37±338.5 mm/s for the non-hemiparetic arm. The
difference in movement times was also reflected in the
prolongation of the time to peak velocity for this target
(415.53± 106.15 ms compared with 276.78±77.67 ms,
respectively).
Movements towards three of the four targets (near, far
and contralateral) required the coordinated activation of the
horizontal flexors of the shoulder and the elbow extensors.
This represented, for the near and far targets, a movement
M. F. Levin
288
Joint excursions
Contra Far Near
made outside of the usual extensor arm synergy (shoulder
adduction and internal rotation with elbow extension;
Brunnstrom, 1970). In addition, for all targets, the outward
movement was made primarily with the weak extensor
muscles as agonists opposed by the spastic flexor muscles.
In an attempt to determine if the increase in movement time
was due to a differential prolongation of the outward or the
backward component of the movement, these times were
analysed separately and the results are also summarized in
Fig. 6. The durations of movements made outward to (open
bars) and backward from (hatched bars) each target for
normal (bottom panel), non-affected (middle panel) and most
affected arms (upper panel) were not statistically different
although each phase of the movement was significantly
longer in hemiparetic compared with normal arms (repeated
measures ANOVA, P < 0.001).
Ipai
Fig. 5 Histograms of mean (+SD) excursions of the elbow (top
panel) and shoulder (bottom panel) joints for normal control
(hatched bars), non-affected (closed bars) and affected (open bars)
arms. Asterisks indicate significant differences (P < 0.05)
between the affected and non-affected arms.
Affected
arms
Lis
m
Non-affected arms
4 S
CD
s
ra
CD
O
rfl
s
2
Normal arms
*
•
a •
Contra
Far
Near
Ipsi
Fig. 6 Comparison of mean (+SD) movement times for
movements made to and from the target (filled bars) and for those
made from the starting position to the target (open bars) and from
the target back to the starting position (hatched bars) for both
arms of all subjects. Asterisks indicate significant differences
(P < 0.05) between times for the affected arms compared with
the non-affected arms.
Interjoint coordination
For movements made to the far and contralateral targets, the
elbow and shoulder joint excursions were very highly coupled
in normal arms and in non-affected arms of hemiparetic
subjects. For example, correlation coefficients ranged from
0.993 to 0.998 for the contralateral and from 0.986 to 0.998
for the far target in the non-affected arms of hemiparetic
subjects. In contrast, hemiparetic arms showed a marked and
significant decrease in elbow/shoulder correlation for both
targets. For hemiparetic arms, values ranged from 0.131 to
0.998 for the far and from 0.878 to 0.997 for the contralateral
target. The higher correlation between shoulder and elbow
joint excursions for the contralateral target may have been
due to the fact that this target was so placed as to require a
movement essentially made within the extensor synergy.
However, in spite of the high correlation, the relationship
was still significantly decreased in the affected compared
with the non-affected arms in seven out of the eight subjects
in whom recordings were made from both arms (P < 0.05).
As expected, in normal and non-affected arms, elbow and
shoulder joint excursions were not so highly correlated for
movements made to the ipsilateral target (mean = 0.722,
range 0.527-0.925). However, the reverse was true on the
affected side of stroke patients (mean = 0.855, range 0.7030.963) again demonstrating the tendency for these subjects
to use a movement synergy to reach this target.
Interjoint coordination for movements made to and from
the far and ipsilateral targets was assessed by examining the
slope of the regression between the elbow and shoulder
joints. A slope of one would indicate that both joints
contributed equally to the task while a very high or low slope
would indicate that the movement involved predominantly the
elbow or the shoulder joint, respectively. Movements made
to the far and contralateral targets were characterized by the
greatest amounts of segmentation especially in the subjects
with moderate and severe spasticity as shown in Figs 2 and
3. For movements made to the far target, the slope of the
regression was significantly higher than normal (4.40±2.43
Interjoint coordination in hemiparesis
289
interjoint coordination measures correlated more significantly
with the degree of motor impairment as measured by the
Fugl-Meyer test than with spasticity scores.
Discussion
Fig. 7 Correlations between clinical spasticity scores and FuglMeyer motor function scores (A), movement (mvt) times (B) and
movement distances (C) for reaches made to the contralateral
(contra, squares) and far (filled circles) targets with the affected
arm.
compared with 2.66±0.22, respectively) indicating that
subjects used a different elbow/shoulder coordination from
normal in this area of the workspace. In contrast, movements
made to the ipsilateral target were characterized by lower than
normal slopes between elbow and shoulder joint excursions
(4.67±2.03 for affected compared with 9.40±5.00 for nonaffected arms of the same subjects) indicating that a
movement synergy was employed by these subjects to reach
the target when a predominantly single-joint movement
was required.
Correlations with clinical spasticity scores
Correlations between the level of spasticity and clinical
and objective motor function scores were calculated for
movements made to the far and contralateral targets. Subjects
with mild spasticity had normal or slightly less than normal
Fugl-Meyer scores. As the level of spasticity increased, the
clinical motor function scores decreased. The correlation
(r = -0.795, P < 0.02) is shown in Fig. 7A.
The level of clinical spasticity was also significantly
correlated with movement time to both targets (Fig. 7B,
P < 0.05) and with movement distance to the contralateral
target (Fig. 7C, P < 0.05; Table 3). Significant correlations
were also found between spasticity scores and various
parameters of the movement made to the far target (Table 3).
A general finding was that the objective trajectory and
In this study we have documented that, at least for stroke
patients having no perceptuomotor problems (apraxia, leftsided neglect), movement disruption occurs at the level of
interjoint coordination and is not linked to pathological
movement synergies. Several lines of evidence support this
conclusion. First, trajectories of movements made to all but
the ipsilateral target were characterized by segmentation,
marked deflections from a straight line and a large degree of
dispersion. This was equally obvious for movements made
within the extensor synergy (the contralateral target) and
outside of pathological synergies (near and far targets). In
contrast, for the ipsilateral target, also placed so as to require
an out-of-synergy movement, the trajectories appeared more
normal in shape and were less dispersed. Secondly, the
normal tight interjoint coordination between the elbow and
shoulder joints for movements made to the targets in the
sagittal and contralateral workspace was decreased in
hemiparetic subjects and the decrease was much more evident
in those subjects with the most severe spasticity. For the
ipsilateral target, the higher than normal correlation between
the elbow and shoulder joints supports the suggestion that
these subjects used a coordinated movement instead of a
single-joint movement to reach this target. Therefore, the
movement deficits in our subjects, although generally related
to the degree of clinical motor deficit were not strictly related
to pathological movement synergies.
The disruption in interjoint coordination was the predominant finding in our study. This has been indirectly
implied by others based on the description of abnormal
trajectories of pointing movements in hemiparetic subjects
in previous studies (Lough et al., 1984; Trombly, 1992). The
target locations used in our study imposed task constraints
requiring distinct interjoint coordinations. Our data showed
that movements involving muscles activated in the extensor
synergy (contralateral target) were no less impaired than
those made out of any particular synergy (ipsilateral target).
If the motor control deficit were related to trajectory
planning in extrapersonal space, then differential disruptions
would be evident in movements made by the affected arm
to different parts of the workspace. In addition, movement
deficits would be seen in movements made by the non-affected
arm. Indeed, several authors have reported hypometria in
eye (Butter et al., 1988) and ipsilateral arm movements
(Meador et al., 1988; Flanders et al., 1992) in stroke patients
with left-sided attentional deficits. However, in our sample
of subjects with no problems of neglect, movements made
with the unaffected arm were essentially normal and all
subjects, even those with the most severe motor impairment
were able to make movements with the affected limb in all
parts of the workspace studied. These data complement and
290
M. F. Levin
Table 3 Correlations between clinical scores (spasticity and Fugl-Meyer) and objective measures of motor function for the
affected arm of hemiparetic subjects
Movement
time
Movement
distance
Shoulder
excursion
xly
correlation
Sho/elb
correlation
Far target
Spasticity
F-M
0.814*
-0.811*
-0.602
0.690
-0.688+
0.898*
-0.775+
0.702*
0.448
-0.709*
Contralateral target
Spasticity
F-M
0.713*
-0.691*
-0.702*
0.755+
-0.524
0.809*
-0.439
0.617*
-0.091
-0.353
F-M = Fugl-Meyer, sho/elb = shoulder/elbow. *P < 0.005; */» < 0.02; *P < 0.05.
extend those of Fisk and Goodale (1988) for the unimpaired
limb and Trombly (1992) for the impaired limb of subjects
with left hemiparesis.
Movements in the affected arm were hypometric for targets
located in both the far and contralateral workspace. Although
deficits in the ability to reach the target may have been due
to biomechanical restrictions in joint excursions due to muscle
or joint contracture, our subjects were initially screened for
this possibility and had no range of motion limitations. Thus,
the decrease in movement amplitude could be attributed to
a disruption of interjoint coordination leading to a limitation
in the active range of both joints and not due to range of
motion deficits per se in individual joints.
The deficit in interjoint coordination as well as the decrease
in the speed of movement may also partly be explained by
biomechanical factors. Changes in mechanical properties of
muscle (Dietz et al., 1991) including a redistribution in the
proportions of Type I and II motor units (Hufschmidt and
Mauritz, 1985; Jakobsson et al., 1992) may contribute to the
slowness of movement due to an increased passive muscle
tension to stretch of the spastic agonist during the outbound
movement in our reaching task but would not explain why
the return movement was equally prolonged (Fig. 6). On the
other hand, recent studies have documented that decreased
recruitment of agonist motor units rather than abnormally
high antagonist cocontraction predominates in hemiparetic
subjects making functional (Gowland et al., 1992), isotonic
(el-Abd et al., 1993; Fellows et al., \994b) and isometric
(Fellows et al., 1994a) movements with the impaired upper
limb. Muscle weakness has been reported in both spastic
elbow flexor and non-spastic elbow extensor muscles.
The inability to activate agonists adequately may explain
the increased movement time in our subjects. Whether
abnormally high antagonist cocontraction may have
contributed to the movement speed deficit was not
investigated in the present study but increasing evidence
against this possibility has been reported for the upper limb
(Gowland et al, 1992; Fellows et al., 1994a, b). Further
analysis of this behaviour would necessitate an examination of
the muscular activity associated with coordinated movement.
Although it was evident that even the most severely
affected hemiparetic patient could reach into all parts of
the workspace, these movements were much slower and
segmented than normal. Movement segmentation appeared
to be due to a deficit in a smooth interjoint coordination
between elbow and shoulder joints so that movements
appeared jerky and saccadic. Trombly (1992) has suggested
that this occurs due to the subjects' need to learn how to
integrate new 'abnormal' proprioceptive feedback from the
impaired limb and further proposes that the increase in
movement time may be related to the use of vision to guide
the extension of the limb into extrapersonal space. We suggest
that, in stroke, the fundamental impairment is not in the
ability of the subject to plan movement in terms of control
variables specifying trajectory parameters in an extrapersonal
frame of reference (Feldman and Levin, 1995), rather it is
in the ability of the nervous system to transform these control
variables into meaningful functional variables governing the
spatiotemporal interaction between the joints. The level at
which movement is planned and controlled is unknown and,
most probably, these functions are distributed throughout
cortical and subcortical areas. The parietal cortex may be
involved in the coordination of attention with goal-directed
movements as well as in the production of the movement itself
(Georgopoulos, 1990; Goodale and Milner, 1992; Kalaska and
Crammond, 1992). For example, in non-impaired animals
and humans, the activity of single cells in both motor and
parietal cortices is selectively tuned to the direction of a
goal-directed movement (Georgopoulos, 1990; Kalaska and
Crammond, 1992). It has been suggested that the parietal
cortex may form part of the central control mechanism coding
the location of the target and the trajectory of the limb as
well as the kinematic parameters of limb movement (Kalaska,
1991) during goal-directed movement. In addition, the
supplementary motor area and the premotor cortex have also
been implicated based on findings of disturbances in visually
guided reaching following lesions to these areas in monkeys
(Haaxma and Kuypers, 1974; LaMotte and Acuna, 1978).
On the other hand, studies in patients with subcortical
and cortico-reticulospinal pathway lesions suggest that these
pathways are sufficient to provide control of trunk and limb
postures and movements, except for fine finger movement
which is served by the ipsilateral uncrossed corticospinal
tract (Liu and Chambers, 1964; Freund, 1987). Thus, lesions
Interjoint coordination in hemiparesis
in both cortical and subcortical structures may lead to
impairments in goal-directed reaching. In our study, half of
our subjects had subcortical and the other half, cortical or
cortico-subcortical lesions (Table 1). The fact that most of
the lesions involved sub-cortical brain structures may explain
why our hemiparetic subjects, as a group, showed similar
types of motor deficits. It would be interesting to correlate
the site of the lesion with the deficit in motor control.
Unfortunately, this study was not designed to do so for
several reasons. First, the subjects studied had chronic motor
deficits ranging in time since cerebro-vascular accident from
0.5 to 7.2 years (Table 1). It is likely that quite a bit of
recovery and compensation could occur in this space of time
making the relationship of location of the lesion to the motor
deficit unclear. Such correlations would be better made by
examining sensorimotor deficits in acute cases. Secondly, we
did not examine specific motor tasks that would be more
closely related to the location of the lesion such as fine hand
function versus gross motor control of the proximal arm
joints. We studied a relatively gross motor task that did not
require a high level of end-point precision. Within the limits
of our study, the location of the lesion did not correlate with
either the degree of clinical impairment nor with the level
of incoordination. Our findings do suggest that regardless of
the location of the lesion, following a stroke, the nervous
system may not be able to determine the optimal set of
relationships between muscles and segments to perform a
smooth coordinated movement. This may occur due to the
inability of the nervous system to use proprioceptive feedback
from the moving limbs or due to the use of altered
proprioceptive feedback from hyperactive reflex pathways in
the limb.
Our data implies that there is a bi-level organization for
the control of pointing movements. One level plans the
trajectory of the movement while the other specifies the
interjoint coordination necessary to accomplish the movement. The two levels are requisite elements for the production
of goal-directed movements. Disruptions at either level results
in movement deficits as indicated by studies in patients with
problems of neglect (Fisk and Goodale, 1988; Mattingley
et al., 1994) and in patients with purely motor problems
(Trombly, 1992).
Clinical implications
Clinical motor function scores were only significantly
correlated with four objective measures of the movement
deficit: movement time, movement distance, shoulder
excursion and the shape of the trajectory while the clinical
spasticity score was only consistently related to the movement
time. Clinical scores could be useful in describing the
movement deficit globally as expressed in terms of movement
time or movement distance. While both of these are important
clinical descriptors for characterizing the results of therapeutic
interventions in stroke rehabilitation, they provide little
information about the movement deficit itself. Thus, a
291
measure of interjoint coordination such as the one described
here may be of more clinical benefit.
Our findings imply that treatment aimed at improving
arm function should be oriented at restoring the normal
sensorimotor relationships between the joints. In this respect,
even non-specific sensory stimulation may accomplish this
goal. For example, techniques such as reflex inhibiting
postures (Bobath, 1990) and transcutaneous electrical nerve
stimulation (Levin and Hui-Chan, 1992) have been found to
reduce, at least temporarily, spasticity in stroke patients.
Following repeated applications of transcutaneous electrical
nerve stimulation in spastic hemiparetic subjects, a decrease
in spasticity in the triceps-surae muscles was accompanied
by an immediate decrease in cocontraction and a concomitant
increase in ankle dorsiflexion (Levin and Hui-Chan, 1992).
The mechanism for this restoration of motor control is
unknown but it may have been related to a decrease in
abnormal afferent activity from the spastic muscles. Once
tone has been decreased, patients should practice coordinated
movements with increasing difficulty and speed. Current
research also supports the notion that, contrary to the
traditional belief that muscle strengthening would only serve
to augment spasticity and abnormal postural relationships, if
administered at the appropriate time, specific strengthening
of agonist muscles may be of benefit to the re-education of
movement (Colebatch et al, 1986; Gowland et al., 1992).
Acknowledgements
I wish to thank my colleague, Dr Anatol Feldman for valuable
comments on the manuscript, Jolande Jurrius and Claudine
Lamoth for some of the data collection under the direction
of Dr Onno G. Meijer (Free University of Amsterdam) and
Melissa Horowitz for assistance in data compilation and
analysis. This project was supported by the Fonds de
Recherche en Sant6 du Quebec, the Roseau de recherche en
readaptation de Montreal et de l'Ouest du Quebec and the
Universit6 de Montreal.
References
Ackroyd MH. Digital filters. London: Butterworths, 1973.
Ashworth B. Preliminary trial of carisoprodal in multiple sclerosis.
Practitioner 1964; 192: 540-2.
Berardelli A, Sabra AF, Hallett M, Berenberg W, Simon SR. Stretch
reflexes of triceps surae in patients with upper motor neuron
syndromes. Neurol Neurosurg Psychiatry 1983; 46: 54-60.
Bernstein NA. The co-ordination and regulation of movements.
Oxford: Pergamon, 1967.
Bobath B. Adult hemiplegia. Evaluation and treatment. 3rd ed.
Oxford: Heinemann Medical, 1990.
Bourbonnais D, Vanden Noven S. Weakness in patients with
hemiparesis. [Review]. Am J Occup Ther 1989; 43: 313-19.
292
M. F. Levin
Brunnstrom S. Movement therapy in hemiplegia. A
neurophysiological approach. New York: Harper & Row, 1970.
reaction times of aimed movements: effects of practice, uncertainty,
and change in target location. J Neurophysiol 1981; 46: 725-43.
Butter CM, Rapcsak S, Watson RT, Heilman KM. Changes in
sensory inattention, directional motor neglect and 'release' of the
fixation reflex following a unilateral frontal lesion: a case report.
Neuropsychologia 1988; 26: 533-45.
Giuliani CA. Dorsal rhizotomy for children with cerebral palsy:
support for concepts of motor control. [Review]. Phys Ther 1991;
71: 248-59.
Colebatch JG, Gandevia SC, Spira PJ. Voluntary muscle strength
in hemiparesis: distribution of weakness at the elbow. J Neurol
Neurosurg Psychiatry 1986; 49: 1019-24.
Corcos DM, Gottlieb GL, Penn RD, Myklebust B, Agarwal GC.
Movement deficits caused by hyper-excitable stretch reflexes in
spastic humans. Brain 1986; 109: 1043-58.
Dietz V, Trippel M, Berger W. Reflex activity and muscle tone
during elbow movements in patients with spastic paresis. Ann
Neurol 1991; 30: 767-79.
el-Abd MA, Ibrahim IK, Dietz V. Impaired activation pattern in
antagonistic elbow muscles of patients with spastic hemiparesis:
contribution to movement disorder. Electromyogr Clin Neurophysiol
1993; 33: 247-55.
Goodale MA, Milner AD. Separate visual pathways for perception
and action. [Review]. Trends Neurosci 1992; 15: 20-5.
Gordon J, Ghilardi MF, Ghez C. Accuracy of planar reaching
movements. I. Independence of direction and extent variability. Exp
Brain Res 1994; 99: 97-111.
Gowland C, deBruin H, Basmajian JV, Plews N, Burcea I. Agonist
and antagonist activity during voluntary upper-limb movement in
patients with stroke [see comments]. Phys Ther 1992; 72: 624-33.
Comment in: Phys Ther 1993; 73: 402-3.
Gurfinkel VS, Kots YA, Paltsev El, Feldman AG. The compensation
of respiratory disturbances of the erect posture of man as an example
of the organization of interarticular interaction. In: Gelfand IM,
editor. Models of the structural-functional organization of certain
biological systems. Cambridge: MIT Press, 1971: 310-21.
Feldman AG, Levin MF. Positional frames of reference. Origin and
use. Behav Brain Sci 1995; 18: 723-804.
Haaxma R, Kuypers HGJM. Role of occipito-frontal cortico-cortical
connections in visual guidance of relatively independent hand and
finger movements in rhesus monkeys. Brain Res 1974; 71: 361-6.
Fellows SJ, Kaus C, Ross HF, Thilmann AF. Agonist and antagonist
EMG activation during isometric torque development at the elbow
in spastic hemiparesis. Electroencephalogr Clin Neurophysiol 1994a;
93: 106-12.
Hammond MC, Kraft GH, Fitts SS. Recruitment and termination
of electromyographic activity in the hemiparetic forearm. Arch Phys
Med Rehabil 1988; 69: 106-10.
Fellows SJ, Kaus C, Thilmann AF. Voluntary movement at the
elbow in spastic hemiparesis. Ann Neurol 1994b; 36: 397^107.
Fisk JD, Goodale MA. The effects of unilateral brain damage on
visually guided reaching: hemispheric differences in the nature of
the deficit. Exp Brain Res 1988; 72: 425-35.
Flanagan RJ, Ostry DJ, Feldman AG. Control of trajectory
modifications in target-directed reaching. J Mot Behav 1993; 25:
175-92.
Flanders M.Tillery SIH, Soechting JF. Early stages in a sensorimotor
transformation. Behav Brain Sci 1992; 15: 309-62.
Hogan N, Flash T. Moving gracefully: quantitative theories of motor
coordination. Trends Neurosci 1987; 10: 170-4.
Hufschmidt A, Mauritz K-H. Chronic transformation of muscle in
spasticity: a peripheral contribution to increased tone. J Neurol
Neurosurg Psychiatry 1985; 48: 676-85.
Jakobsson F, Grimby L, Edstrom L. Motoneuron activity and muscle
fibre type composition in hemiparesis. Scand J Rehabil Med 1992;
24: 115-19.
Jeannerod M. The neural and behavioural organization of goaldirected movements. Oxford: Clarendon, 1988.
Flash T, Hogan N. The coordination of arm movements: an
experimentally confirmed mathematical model. J Neurosci 1985; 5:
1688-703.
Kalaska JF. Parietal cortex area 5: a neuronal representation of
movement kinematics for kinaesthetic perception and movement
control? In: Paillard J, editor. Brain and space. Oxford: Oxford
University Press, 1991: 133-46.
Fleiss JL. The design and analysis of clinical experiments. New
York: Wiley, 1986.
Kalaska JF, Crammond DJ. Cerebral cortical mechanisms of reaching
movements. [Review]. Science 1992; 255: 1517-23.
Freund HJ. Abnormalities of motor behavior after cortical lesions
in humans. In: Mountcastle VB, Plum F, editors. Handbook of
physiology, Sect. 1, Vol. 5, Pt. 2. Bethesda (MD): American
Physiological Society, 1987: 763-810.
Kelso JAS, Tuller B. Toward a theory of apractic syndromes. Brain
Lang 1981; 12: 224-7.
Fugl-Meyer AR, JaiiskO L, Leyman I, Olsson S, Steglind S. The
post-stroke hemiplegic patient. I. A method for evaluation of
physical performance. Scand J Rehabil Med 1975; 7: 13-31.
Georgopoulos AP. Neurophysiology of reaching. In: Jeannerod M,
editor. Attention and performance XIII: motor representation and
control. Hillsdale (NT): Lawrence Eribaum, 1990: 227-63.
Georgopoulos AP, Kalaska JF, Massey JT. Spatial trajectories and
Kugler PN, Kelso JAS, Turvey MT. On the concept of coordinative
structures as dissipative structures. I. Theoretical lines of
convergence. In: Stelmach GE, Requin J, editors. Tutorials in motor
behavior. Amsterdam: North-Holland, 1980: 3-47.
Lacquaniti F. Automatic control of limb movement and posture.
[Review]. Curr Opin Neurobiol 1992; 2: 807-14.
LaMotte RH, Acuna C. Defects in accuracy of reaching after
removal of posterior parietal cortex in monkeys. Brain Res 1978;
139: 309-26.
Interjoint coordination in hemiparesis
Levin MF, Feldman AG. The role of stretch reflex threshold
regulation in normal and impaired motor control. Brain Res 1994;
657: 23-30.
Levin MF, Hui-Chan CW. Relief of hemiparetic spasticity by TENS
is associated with improvement in reflex and voluntary motor
functions. Electroencephalogr Clin Neurophysiol 1992; 85: 131^*2.
Levin MF, Horowitz M, Jurrius J, Lamothe C, Feldman AG.
Trajectory formation and interjoint coordination of drawing
movements in normal and hemiparetic subjects [abstract]. Soc
Neurosci Abstr 1993; 19: 990.
Levine DN, Kaufman KJ, Mohr JP. Inaccurate reaching associated
with a superior parietal lobe tumor. Neurology 1978; 28: 555-61.
Liu CN, Chambers WW. An experimental study of the corticospinal system in the monkey (Macaca mulatta): the spinal pathways
and preterminal distribution of degenerating fibers following discrete
lesions of the pre- and postcentral gyri and bulbar pyramid. J Comp
Neurol 1964; 123: 257-83.
293
Meador KJ, Loring DW, Baron MS, Rogers OL, Kimpel TG.
Hemispatial-limb hypometria. Int J Neurosci 1988; 42: 71-5.
Powers RK, Marder-Meyer J, Rymer WZ. Quantitative relations
between hypertonia and stretch reflex threshold in spastic
hemiparesis. Ann Neurol 1988; 23: 115-24.
Riddoch G. Visual disorientation in homonymous half-fields. Brain
1935; 58: 376-82.
Soechting JF, Flanders M. Errors in pointing are due to
approximations in sensorimotor transformations. J Neurophysiol
1989a; 62: 595-608.
Soechting JF, Flanders M. Sensorimotor representations for pointing
to targets in three-dimensional space. J Neurophysiol 1989b; 62:
582-94.
Trombly CA. Deficits of reaching in subjects with left hemiparesis:
a pilot study. Am J Occup Ther 1992; 46: 887-97.
Lough S, Wing AM, Fraser C, Jenner JR. Measurement of recovery
of function in the hemiparetic upper limb following stroke: a
preliminary report. Hum Mov Sci 1984; 3: 247-56.
Wiesendanger M. Weakness and the upper motoneurone syndrome:
a critical pathophysiological appraisal. In: Berardelli A, Benecke
R, editors. Motor disturbances n. London: Academic Press, 1990:
319-31.
Mattingley JB, Bradshaw JL, Bradshaw JA, Nettleton NC. Residual
rightward attentional bias after apparent recovery from right
hemisphere damage: implications for a multicomponent model of
neglect. J Neurol Neurosurg Psychiatry 1994; 57: 597-604.
Received December 29, 1994. Revised July 20, 1995.
Accepted August 23, 1995