Download Differential Impairment of Individuated Finger Movements in

J Neurophysiol 90: 1160 –1170, 2003;
10.1152/jn.00130.2003.
Differential Impairment of Individuated Finger Movements in Humans After
Damage to the Motor Cortex or the Corticospinal Tract
Catherine E. Lang1,2 and Marc H. Schieber1– 4
1
Departments of Neurology, 2Neurobiology and Anatomy, and 3Physical Medicine and Rehabilitation, University of Rochester School of
Medicine and Dentistry, and the 4Brain Injury Rehabilitation Program, St. Mary’s Hospital, Rochester, New York 14642
Submitted 10 February 2003; accepted in final form 24 March 2003
The motor cortex and the corticospinal tract are crucial for
the control of relatively independent finger movements (Porter
and Lemon 1993). Lawrence and Kuypers (1968a) observed
that after permanent lesions to the corticospinal tract, monkeys
recovered the ability to use the upper limb when walking and
climbing, but were left with an inability to move the fingers
independently when retrieving food morsels and grooming.
These early observations have been extended using more quantitative techniques, such as force recordings and electromyography (Hepp-Reymond and Wiesendanger 1972; Hepp-Reymond et al. 1974). More recently, similar deficits in fine finger
movements have been produced temporarily by reversible inactivation of small portions of the primary motor cortical hand
representation (Brochier et al. 1999; Kubota 1996; Schieber
and Poliakov 1998).
How relatively selective lesions of the motor cortex or
corticospinal tract affect the independence of finger movements in humans has not been examined in detail, for two
reasons. First, many studies of hand control after lesions to the
motor system have used heterogeneous patients with relatively
nonspecific lesions, and with a wide range of motor and nonmotor abnormalities (Carroll 1965; Wade et al. 1983). Pure
motor hemiparesis, a relatively homogeneous clinical syndrome, is characterized by paresis on one side of the body
without sensory, cognitive, or language disturbance (Fisher and
Curry 1964; Fisher 1979, 1982). This syndrome most frequently results from relatively isolated ischemic lesions affecting the corticospinal tract unilaterally in the basis pontis or in
the posterior limb of the internal capsule. Here, we investigated
how lesions relatively restricted to the motor cortex or corticospinal tract affect independent finger movements by studying
people with pure motor hemiparesis.
Second, in reports where lesions have been restricted to the
motor cortex or corticospinal tract, the capacity to move each
finger independently has not been measured quantitatively.
Most case reports provide only descriptive observations of
finger strength or finger movements (Aguilar 1969; Back and
Mrowka 2000; Kim et al. 2002; Lee et al. 1998; Phan et al.
2000; Ropper et al. 1979; Schieber 1999; Tereo et al. 1993).
Fries and colleagues used a standardized clinical test of arm
function (Fries et al. 1993), which provided a global score of
arm and hand function but could not provide quantitative
information about the fingers (Lincoln and Leadbitter 1979).
Here, we used kinematic analyses to quantify the independence
of each finger.
We questioned whether damage to the motor cortex or
corticospinal tract would impair the ability to move each finger
to the same degree or would affect some fingers more than
others. Although we expected that the independence of the
thumb would be the most affected given its relative cortical
magnification compared with the other fingers (Penfield and
Boldrey 1937; Penfield and Rasmussen 1950; Woolsey et al.
1952), our results showed the opposite. In our subjects with
residual pure motor hemiparesis, the independence of the
thumb was normal; the independence of the index finger was
slightly impaired, while the independence of the middle, ring,
and little fingers was substantially impaired.
Address for reprint requests: C. E. Lang, University of Rochester Medical
Center, 601 Elmwood Ave., Box 603, Rochester, NY 14642 (E-mail:
[email protected]).
The costs of publication of this article were defrayed in part by the payment
of page charges. The article must therefore be hereby marked ‘‘advertisement’’
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
INTRODUCTION
1160
0022-3077/03 $5.00 Copyright © 2003 The American Physiological Society
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
Lang, Catherine E. and Marc H. Schieber. Differential impairment
of individuated finger movements in humans after damage to the
motor cortex or the corticospinal tract. J Neurophysiol 90:
1160 –1170, 2003; 10.1152/jn.00130.2003. The purpose of this
study was to quantify the long-term loss of independent finger movements in humans with lesions relatively restricted to motor cortex or
corticospinal tract. We questioned whether damage to the motor
cortex or corticospinal tract would permanently affect the ability to
move each finger to the same degree or would affect some fingers
more than others. People with pure motor hemiparesis due to ischemic
cerebrovascular accident were used as our experimental sample. Pure
motor hemiparetic and control subjects were tested for their ability to
make cyclic flexion/extension movements of each finger independently. We recorded their finger joint motion using an instrumented
glove. The fingers of control subjects and of the unaffected hands
(ipsilateral to the lesion) of hemiparetic subjects moved relatively
independently. The fingers of the affected hands (contralateral to the
lesion) of hemiparetic subjects were differentially impaired in their
ability to make independent finger movements. The independence of
the thumb was normal; the independence of the index finger was
slightly impaired, while the independence of the middle, ring, and
little fingers was substantially impaired. The differential long-term
effects of motor cortical or corticospinal damage on finger independence may result from rehabilitative training emphasizing tasks requiring independent thumb and index movements, and from a greater
ability of the spared components of the neuromuscular system to
control the thumb independently compared with the other four fingers.
DIFFERENTIAL FINGER MOVEMENT IMPAIRMENT AFTER STROKE
METHODS
Subjects
TABLE
affected hands of the hemiparetic group (see Table 1 for individual
affected hemiparetic values). Although the z-scores appear to indicate
severe impairment in some of the affected hands of hemiparetic
subjects (Table 1), all subjects completed all the items on the test, and
therefore, the high z-scores mainly reflect the increased time taken for
task completion.
In addition, four of our hemiparetic subjects (H-01, H-05, H-06,
H-07, see Table 1) were evaluated with the upper extremity FuglMeyer scale (Fugl-Meyer et al. 1975). The Fugl-Meyer is a clinical
rating scale that tests tendon reflexes and voluntary movements in and
out of synergistic limb postures. Possible scores range from 0 to 66,
where 66 means there was no observable deficit. Fugl-Meyer scores
for these four subjects ranged from 64/66 (H-01) to 35/66 (H-07L).
Arm function as measured by the Fugl-Meyer test was highly correlated with hand function as measured by the Jebsen Test (Pearson
correlation ⫽ ⫺0.986, P ⫽ 0.015). For example, H-01 had a Jebsen
z-score of 1.8 and a Fugl-Meyer score of 64/66. Likewise, H-07L had
a Jebsen z-score of 24.6 and a Fugl-Meyer score of 35/66. For
subsequent analyses examining relationships between function and
finger independence, we used the Jebsen Test because we felt it was
a better tool for evaluating the typical use of the hand.
Experimental procedures
To probe the function of the motor cortex and corticospinal tract in
our subjects, we tested their ability to make individuated finger
movements (i.e., their ability to move each finger while keeping the
other fingers still). If possible, subjects with pure motor hemiparesis
were tested on both the affected side, contralateral to lesion, and the
unaffected side, ipsilateral to lesion. Two hemiparetic subjects were
tested only on the affected side, H-01 (time constraints) and H-06
(MRI report of old lacune). For subject H-07 (bilateral internal capsule lesions), both sides were tested and both sets of data were
included in the affected group. Control subjects were tested on one
side only, except for one who was tested on both sides as a match for
H-07. In sum, we evaluated 8 affected hands (6 right, 2 left), 4
unaffected hands (1 right, 3 left), and 10 control hands (6 right, 4 left).
All of our control subjects and five of seven hemiparetic subjects
reported being right-handed. Because previous work has shown that
the ability to independently produce finger movements or finger forces
is not different in the dominant versus nondominant hand (Hagar-Ross
and Schieber 2000; Reilly and Hammond 2000), data from right and
left hands were pooled for all analyses.
Subjects were seated with the elbow and forearm on a table. The
forearm was positioned in neutral pronation/supination and the wrist
was positioned in approximately 15° extension. Figure 2A shows a
schematic of the forearm and wrist supported and stabilized with a
vacuum cast (VersaForm, Sammons Preston Inc., Bolingbrook, IL).
Subjects wore a right- or left-handed instrumented glove (Cyber-
1. Characteristics of subjects with pure motor hemiparesis
Subject
Age
Gender
Lesion Locationa
Time Since
Stroke
H-01
H-02
H-03
H-04
H-05
H-06
H-07L
H-07R
70
72
66
55
71
65
49
49
M
F
M
M
M
M
F
F
L precentral gyrusc
L corona radiata, descending fibers
L basis pontis
L basis pontis
R basis pontise
L internal capsule, posterior limbf
L internal capsule, posterior limb
R internal capsule, genu
34 months
29 months
7 months
2 months
21 months
25 months
2 months
19 months
Initial Hemiparesis in:
Face,
Face,
Face,
Face,
Face,
Face,
Face,
Face,
arm,
arm,
arm,
arm,
arm,
arm,
arm,
arm,
hand
hand,
hand,
hand,
hand,
hand,
hand,
hand,
leg
leg
leg
leg
leg
leg
leg
Residual
Hemiparesis in:
Hand
Arm, hand
Arm, hand,
Arm, hand,
Arm, hand
Arm, hand,
Arm, hand,
Arm, hand
leg
leg
leg
leg
Jebsen Test z-Scoreb
1.8 ⫾ 0.7 (FM ⫽ 64/66)d
11.0 ⫾ 1.4
2.1 ⫾ 0.9
22.0 ⫾ 8.8
2.3 ⫾ 0.8 (FM ⫽ 58/66)d
15.9 ⫾ 3.8 (FM ⫽ 45/66)d
24.6 ⫾ 7.0 (FM ⫽ 35/66)d
3.4 ⫾ 1.0
Values are means ⫾ SE. L, left; R, right. a See Fig. 1 for magnetic resonance images for each subject. b z-Score compared to age-, gender-, and hand
dominant-appropriate means on the Jebsen Test of Hand Function; higher scores reflect increased time to complete test items (see text for details). c Extends into
white matter beneath. d Fugl-Meyer Upper Extremity scale was used to evaluate 4 hemiparetic subjects, normal arm function ⫽ 66. e Extends up into pontine
tegmentum. f Extends into white matter above and into the posterior of the putamen.
J Neurophysiol • VOL
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
Seven subjects with pure motor hemiparesis (age range 49 –72 yr,
Table 1) and nine neurologically intact, control subjects (age range
19 –52 yr) participated in this study. The study protocol was approved
by the Research Subjects Review Board of the University of Rochester Medical Center, Rochester, NY. Informed consent was obtained
from all subjects prior to participation.
Figure 1 shows the magnetic resonance image (MRI) that best
illustrates the lesion that produced pure motor hemiparesis in each
subject. Our sample consisted of five subjects with classic lesions (2
with unilateral lesions of the basis pontis and 3 with lesions in the
posterior limb of the internal capsule) and findings of contralateral
hemiparesis in the face, arm, and leg. We also included subjects with
isolated lesions in the genu of the internal capsule (H-07R), in the
corona radiata adjacent to the lateral ventricle (H-02), and in the
precentral gyrus (H-01). Clinically, these three subjects presented
with pure motor hemiparesis affecting the contralateral face, arm, and
leg, except for H-01 (lesion to the precentral gyrus), who had only
face and arm weakness. The MRI for H-06 showed signal changes
consistent with old, asymptomatic lacunes in both the left and the right
putamen in addition to the internal capsule lesion responsible for the
hemiparesis. Another subject, H-07, had bilateral internal capsule
lesions that occurred 17 mo apart. The lesion on the left side was in
the middle portion of the posterior limb of the internal capsule. The
lesion on the right side was in the genu of the internal capsule.
Hemiparetic subjects underwent a clinical neurological examination to rule out sensory impairments and involvement of other motor
system structures. As part of this examination, we evaluated light
touch sensation of the hand using a five-filament mini-set (Semmes
Weinstein, North Coast Medical, Campbell, CA) and evaluated kinesthesia of the wrist and fingers. Potential subjects with sensory or
cognitive loss or movement disorders suggesting involvement of other
motor structures were excluded from participation. At the time of
testing, the hemiparetic subjects reported substantial recovery compared with the severity of their initial symptoms. Mild residual paresis
persisted in most subjects, as indicated in Table 1.
Functionally, all hemiparetic subjects could use a precision grip to
hold a pen with the affected hand and could walk short distances with
an assistive device. For five of eight subjects, hand function remained
impaired as measured by the Jebsen Test of Hand Function (Jebsen et
al. 1969), a standardized clinical test measuring timed performance on
seven items that simulate common activities. The seven test items are
as follows: 1) writing a sentence; 2) turning index cards; 3) picking up
small objects; 4) using a spoon; 5) stacking checkers; 6) lifting light
food cans; and 7) lifting heavy food cans. The mean Jebsen z-score
was 1.6 ⫾ 0.2 (SE) for the control group, 3.53 ⫾ 0.94 for the
unaffected hands of the hemiparetic group, and 10.4 ⫾ 3.3 for the
1161
1162
C. E. LANG AND M. H. SCHIEBER
Data analysis
Off-line, glove data were low-pass filtered at 6 Hz. We used data
from 14 of the 22 glove sensors: metacarpophalangeal (MCP), proximal interphalangeal (PIP), and distal interphalangeal (DIP) sensors
for the index, middle, and ring fingers (9 sensors), MCP and PIP for
the little finger (2 sensors), and MCP, PIP, and opposition sensors for
the thumb (3 sensors). The thumb opposition sensor best captured the
movement about the carpometacarpal (CMC) joint in the flexion/
extension plane of the thumb phalanges. Sensor data were transformed
FIG. 1. Magnetic resonance images (MRIs) illustrating lesions in subjects
with pure motor hemiparesis. Each lesion (white) is emphasized by a surrounding black circle. Images are presented such that the left side of the brain
appears on the right side of the page. Axial, flair images, obtained at initial
presentation of symptoms, are shown for all hemiparetic subjects except H-04,
for whom an axial, diffusion-weighted image is shown. Lesion locations were
as follows. H-01: left precentral gyrus extending into white matter beneath;
H-02: left corona radiata, descending fibers adjacent to the lateral ventricle;
H-03: left basis pontis; H-04: left basis pontis; H-05: right basis pontis,
extending into the pontine tegmentum above; H-06: left internal capsule,
posterior limb, extending into white matter above and into the posterior
putamen anteriorly, also note a small fluid filled cyst in the left putamen, just
anterior to the new lesion, consistent with an old lacune; H-07L: left internal
capsule, posterior limb; H-07R: right internal capsule, genu.
Glove, Virtual Technologies, Palo Alto, CA). Prior to testing, glove
sensor output and goniometric joint measurements were obtained in
standard positions to calibrate the glove sensors for each tested hand
(Hager-Ross and Schieber 2000). Glove sensor output was linearly
related to joint position for all sensors except the little finger distal
J Neurophysiol • VOL
FIG. 2. A: schematic of testing position. B: definitions of joint angles and
(X, Y) coordinate frames for the 4 fingers. For the thumb, joint angles are
defined in the same manner and the carpometacarpal (CMC) joint is defined as
(0, 0).
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
interphalangeal (DIP) sensor. Our calibrations indicated that the little
finger DIP sensor data did not accurately reflect movement of the little
finger DIP joint; thus data from this sensor were not used. Spike2
software and a Micro 1401 interface (Cambridge Electronic Design,
Cambridge, UK) were used to collect glove data, with each sensor
sampled at 78 Hz.
Subjects were asked to make cyclic flexion-extension movements
of one finger at a time. We instructed them to move one finger, at a
“comfortable pace,” through a “comfortable range of motion,” and to
keep the other fingers still. In general, the noninstructed fingers tended
to remain in a relaxed, flexed posture during motion of an instructed
finger. The hand was in full view of the subject at all times so they
were able to see the movements of the instructed and noninstructed
fingers. Subjects practiced each movement prior to recording trials to
be sure that they understood the task and the instructions. All subjects
reported an awareness of movement in the noninstructed fingers when
it occurred. After practicing an instructed movement, a 10-s trial was
recorded. We recorded two consecutive trials for each instructed
finger. The order of instructed fingers was varied between subjects.
DIFFERENTIAL FINGER MOVEMENT IMPAIRMENT AFTER STROKE
冋冉冘
n
II j ⫽ 1 ⫺
册冒
兩Dij兩⫺1
i⫽1
共n⫺1)
where IIj is the individuation index the jth finger, Dij is the normalized
path distance of the ith finger during the jth instructed movement, and
n is the number of fingers (here n ⫽ 5). One is subtracted from the
sum of the normalized path distances in the numerator and from n in
the denominator to remove the normalized path distance of the instructed finger itself. The individuation index will be close to 1 for an
ideally individuated movement in which the instructed finger moves
with no movement of noninstructed fingers and closer to 0 the more
noninstructed finger movement occurs simultaneously with instructed
finger movement.
The stationarity index is a measure of how well a finger is able to
remain motionless, when it is not the instructed finger. The stationarity index was calculated as 1 minus the average normalized path
distance of that finger whenever it was the noninstructed finger, or
冋冉冘 册冒
m
SI i ⫽ 1 ⫺
兩Dij兩 ⫺ 1
共m ⫺ 1兲
j⫽1
where SIi is the stationarity index for the ith finger during the m
instructed movements. One is subtracted from the sum of the normalJ Neurophysiol • VOL
ized path distances in the numerator and from m in the denominator to
remove the normalized path distance of the ith finger when it was
instructed. The stationarity index will be close to 1 for a finger that
remains stationary whenever it is the noninstructed finger and closer
to 0 the more the finger moves when it is a noninstructed finger.
We compared individuation indices and stationarity indices using
3 ⫻ 5 analyses of variance (ANOVAs) to look for differences between groups (control, affected hand, nonaffected hand) and between
fingers (thumb, index, middle, ring, and little). All statistical tests
were performed using Prism (GraphPad Software, San Diego, CA)
and significance levels were set at P ⬍ 0.05. When significant effects
were found in the ANOVAs, means were evaluated using t-test, with
Bonferroni error corrections for multiple comparisons. Additionally,
we looked for relationships between function of the hand (as measured by the Jebsen Test of Hand Function z-score) and the independence of each finger (as measured by the individuation index) using
Spearman rank correlation coefficients. All of the analyses on the
individuation index data yielded the same statistical results and inferences as the analyses on the stationarity index data. We therefore
present only the individuation index data in RESULTS.
Two other kinematic variables were also investigated. First, to test
whether differences in indices could be explained by rate of movement, we calculated and compared movement frequency for each
finger during its instructed movement. Second, to test whether differences in indices could be explained by range of movement, we
calculated and compared maximum joint excursions for each finger
during its instructed movement. These variables were compared using
ANOVAs.
RESULTS
We tested 8 affected hands, 4 unaffected hands, and 10
control hands. MRIs (Fig. 1) illustrate the lesions of the motor
cortex or corticospinal tract that caused paresis in the affected
hands. Sensory testing revealed that no hands (in any group)
had deficits in the modalities of light touch or kinesthesia.
Clinical neurological testing showed that the affected hand/side
of the hemiparetic subjects exhibited signs consistent with
motor cortical or corticospinal tract damage (e.g., hyperreflexia, residual weakness on one side of the body) and did not
exhibit signs (e.g., ataxia, tremor), suggesting involvement of
other motor structures.
Fingers of the affected hands of hemiparetic subjects moved
less independently than fingers of control hands and of unaffected hands. Figure 3 shows plots of joint position versus time
for a control hand, and the affected and unaffected hands of a
hemiparetic subject (H-03) during a single trial of instructed
ring finger movement. All three hands showed movement of
the instructed ring finger, as expected. The affected hand
(middle column) showed greater movement of the noninstructed fingers (thumb, index, middle, and little) compared
with the control and unaffected hands.
Figure 4 shows plots of fingertip position and the corresponding normalized path distance for the unaffected (Fig. 4A)
and affected hand (Fig. 4B) of a hemiparetic subject (H-02)
during single trials of instructed movement of each finger.
Fingertip position is shown on the left and normalized path
distance is shown on the right for each hand. The top row
shows instructed thumb movement, followed by the instructed
movements of the index, middle, ring, and little (bottom)
fingers in descending order. Movement of the fingertips are
color-coded similar to a rainbow, such that red ⫽ thumb,
orange ⫽ index, yellow ⫽ middle, green ⫽ ring, and blue ⫽
little. Horizontal bars in each plot of normalized path distance
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
into joint angles, using the offset and gain values for each sensor for
each subject as derived from calibration procedures. We defined the
finger joint angles such that 0° at each joint was a straight finger;
positive numbers indicated flexion (curled finger), and negative numbers indicated hyperextension (Fig. 2B). Finger segment lengths (measured from hand tracings) and joint angles were used to calculate
fingertip position in the flexion/extension plane of each finger. Fingertip position was defined such that the origin of the x- and y-axes
was at the center of the MCP joint for each of the four fingers (Fig.
2B) and at the CMC joint for the thumb.
Our laboratory has previously used relative motion slopes to quantify the movement of the noninstructed fingers compared with the
instructed fingers (Hagar-Ross and Schieber 2000; Schieber 1991).
This methodology works well when the relative motion between a pair
of fingers is linear (i.e., when plotting the motion of one finger vs. the
motion of the other finger, the result is a straight line). For the
majority of finger pairs in the current data, the relative motion between a pair of fingers was best described by a nonlinear function.
This may be due to the fact that our subjects were moving through
greater excursions at each joint compared with monkeys (Schieber
1991) and compared with previously studied normal human subjects
(Hagar-Ross and Schieber 2000). At larger joint excursions, biomechanical coupling between the digits may have a greater effect on the
linearity of the motion between pairs of digits and on the independence of finger movements.
Therefore to determine the relative motion of instructed versus
noninstructed fingers, we used the normalized path distance. We
defined the average path distance as the total distance a fingertip
traveled during the 10-s trial divided by the number of completed
cycles, where one cycle was considered flexion and extension of the
finger (Fig. 2B). The average path distance was calculated for each
fingertip during each 10-s trial. The average path distance values were
normalized by dividing the values by the average path distance of that
finger when it was the instructed finger. Thus the normalized path
distance equals 1 when a finger is the instructed finger and is usually
⬍1 when it is a noninstructed finger. We then used the normalized
path distances to derive two indices to quantify finger independence,
the individuation index and the stationarity index (Schieber 1991).
The individuation index is a measure of how well a finger is able to
move independently (i.e., without the other fingers moving). The
individuation index was calculated as 1 minus the average normalized
path distances of the noninstructed fingers, or
1163
1164
C. E. LANG AND M. H. SCHIEBER
are ordered: thumb (top), index, middle, ring, and little (bottom). The instructed finger always has a normalized path
distance of 1 (see METHODS). The unaffected hand (Fig. 4A)
showed little movement of the noninstructed fingers. For example, during instructed middle finger movement in the unaffected hand (middle row of Fig. 4A), the normalized path
distances of the noninstructed thumb, index, ring, and little
fingers are all ⬍0.1. The small amount of movement in the
noninstructed fingers in Fig. 4A was similar to that in our
control subjects and to data from previously reported normal
subjects (Hagar-Ross and Schieber 2000). In comparison, the
affected hand (Fig. 4B) showed substantial movement of the
noninstructed fingers, particularly during the instructed movements of the middle, ring, and little fingers. This can be seen in
the traces of fingertip position and in the normalized path
distance plots. For example, during instructed middle finger
movement in the affected hand (middle row of Fig. 4B), the
normalized path distance of the ring finger was also equal to 1,
indicating that the ring finger moved as much during instructed
middle finger movements as it did during instructed ring finger
movements.
An ideally independent finger would move without any
accompanying motion of the other fingers. We used the individuation index to quantify the degree to which the noninstructed fingers moved when they were supposed to be still (see
METHODS). The individuation index will be 1 for an instructed
finger that moves alone and will be closer to 0 the more the
J Neurophysiol • VOL
noninstructed fingers move. Figure 5A shows the individuation
indices for hemiparetic subject H-02. The unaffected hand had
individuation indices around 0.9. On the affected hand, the
thumb had an individuation index of 0.907, but the index,
middle, ring, and little fingers had individuation indices that
were much lower, 0.706, 0.593, 0.447, and 0.639, respectively.
This subject illustrates a finding typical of the affected hands:
the individuation index of the thumb was normal, and the
individuation index of the index finger was slightly below
normal, while the individuation indices for the middle, ring,
and little fingers were substantially below normal.
Figure 5B shows group individuation indices (mean ⫾ SE)
for each finger. The control group and the unaffected group had
mean individuation indices around 0.9, indicating that the
fingers on these hands moved almost independently. The individuation indices of the affected hands were normal for the
thumb but were substantially lower in the more ulnar fingers,
indicating that the noninstructed fingers moved more during
instructed movement of the more ulnar fingers. A 3 ⫻ 5
(group ⫻ finger) ANOVA revealed a significant group ⫻
finger interaction (P ⬍ 0.0001). Post-hoc testing showed no
differences existed between the control and unaffected groups
or between their fingers (P ⬎ 0.05). The affected group had
individuation indices for the thumb that were not significantly
different from the control and unaffected groups (P ⫽ 0.831).
The affected group individuation indices for the index, middle,
ring, and little fingers were significantly lower than the control
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
FIG. 3. Single trials of joint position vs. time for a control (left), and the affected (middle), and unaffected hand (right) of a
hemiparetic subject (H-03). The ring finger was instructed to move during these 3 trials. Joint traces from the thumb are on top,
followed by the index, middle, ring, and little (bottom) fingers in descending order. The thick line shows metacarpophalangeal
(MCP) movement; the thin line shows proximal interphalangeal (PIP) movement, and the dotted line shows distal interphalangeal
(DIP) movement. For the thumb, the dotted line shows CMC movement. Although little finger DIP data were not used in our
analysis (see METHODS), we show little finger DIP motion here because the little finger DIP sensor accurately transduced DIP
movement in these 3 hands, due to the size of the hands and the fit of the instrumented glove.
DIFFERENTIAL FINGER MOVEMENT IMPAIRMENT AFTER STROKE
1165
and unaffected groups (Pindex ⫽ 0.017, Pmiddle ⫽ 0.003, Pring ⫽
0.0002, Plittle ⫽ 0.0001).
The finding of relatively normal individuation of the thumb
compared with the other four fingers was consistent across
hemiparetic subjects. Individuation indices for each affected
hand and means for each group are provided in Table 2. The
thumb moved relatively independently for the subject with
damage to the motor cortex (H-01) and for subjects with
damage to the corticospinal tract in the internal capsule (e.g.,
H-06) or in the pons (e.g., H-04). An interesting observation in
our data was that hemiparetic subject H-07R, who had damage
to the genu of the internal capsule, also had relatively normal
independence of the thumb and pronounced deficits in the other
four fingers.
The individuation index data show that damage relatively
restricted to the motor cortex or to the corticospinal tract
impaired the ability to make independent finger movements.
The affected fingers were not uniformly impaired, however.
The independence of the thumb was normal, and the indepenJ Neurophysiol • VOL
dence of the index finger was slightly impaired, while the
independence of the middle, ring, and little fingers was the
most impaired.
Relationships between finger independence and function
We next asked whether the ability to make individuated
finger movements was related to function. Subjects that had
greater functional deficits (higher Jebsen z-scores) were generally the same subjects that moved their fingers less independently. We therefore used nonparametric Spearman rank-order
correlations to look for relationships, in the entire data set,
between finger independence, as measured by the individuation
index, and hand function, as measured by the Jebsen Test of
Hand Function (see METHODS). Our data indicated that hand
function was related to finger independence. Spearman r values
between the Jebsen z-score and the individuation index for
each finger were ⫺0.528 for the thumb (P ⫽ 0.012), ⫺0.516
for the index finger (P ⫽ 0.014), ⫺0.431 for the middle finger
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
FIG. 4. Single trials of fingertip position and normalized path distance for instructed movements of each finger for the unaffected
(A) and affected hand of a hemiparetic subject (H-02). Fingertip position (cm) is shown on the left and normalized path distance
is shown on the right for each hand. The top row shows instructed thumb movement, followed by the instructed movements of the
index, middle, ring, and little (bottom) fingers. Movement of the fingertips are color-coded similar to a rainbow, such that red ⫽
thumb, orange ⫽ index, yellow ⫽ middle, green ⫽ ring, and blue ⫽ little. Horizontal bars in each plot of normalized path distance
are ordered: thumb (top), index, middle, ring, little (bottom).
1166
C. E. LANG AND M. H. SCHIEBER
expected because the Jebsen test items require wrist, forearm,
elbow, and shoulder control as well as finger control.
Frequency and range of movement
(P ⫽ 0.045), ⫺0.538 for the ring finger (P ⫽ 0.010), and
⫺0.507 for the little finger (P ⫽ 0.016). Note that the relationships are negative because a lower Jebsen z-score signifies
better hand function. The r values show small-to-moderate
correlations, indicating that other variables, in addition to finger independence, would be needed to accurately describe
hand function. The fact that other variables are needed is
TABLE
2. Individuation indices for each affected hand and means for each group
Subject
H-01
H-02
H-03
H-04
H-05
H-06
H-07L
H-07R
Group
Affected (n ⫽ 8)
Control (n ⫽ 10)
Unaffected (n ⫽ 4)
Thumb
Index
Middle
Ring
Little
0.851
0.907
0.837
0.899
0.798
0.847
0.914
0.849
0.886
0.706
0.666
0.875
0.797
0.683
0.812
0.738
0.623
0.593
0.619
0.753
0.694
0.339
0.702
0.331
0.668
0.447
0.663
0.727
0.641
0.567
0.405
0.735
0.688
0.639
0.830
0.693
0.708
0.667
0.630
0.697
0.862 ⫾ 0.015
0.936 ⫾ 0.010
0.851 ⫾ 0.042
0.770 ⫾ 0.030
0.888 ⫾ 0.023
0.880 ⫾ 0.023
0.582 ⫾ 0.057
0.882 ⫾ 0.017
0.839 ⫾ 0.027
0.607 ⫾ 0.044
0.892 ⫾ 0.016
0.890 ⫾ 0.020
0.694 ⫾ 0.022
0.896 ⫾ 0.016
0.879 ⫾ 0.019
Values are means ⫾ SE.
J Neurophysiol • VOL
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
FIG. 5. A: individuation indices for each finger for the affected (filled
triangles) and unaffected (filled circles) hand of the same hemiparetic subject
(H-02) shown in Fig. 4. Each data point is the mean of 2 trials. B: individuation
indices for each finger for the control (open circles), affected (filled triangles),
and unaffected (filled circles) groups. Each data point is the group mean ⫾ SE.
Our subjects were told to move the instructed finger “at a
comfortable pace, through a comfortable range” (see METHODS).
During practice of each movement prior to a recording, subjects had the opportunity to experience different movement
frequencies and different ranges of joint motion that they felt
would best meet the requirements of the task (i.e., “move one
finger, while keeping the others still”). Thus each subject’s data
presumably reflect their best ability to make individuated
movements at each finger. Because we tested only the selfselected movement frequencies and joint excursions, we are
unable to determine whether the pattern of differential deficits
and the magnitude of these deficits would be the same at other
movement frequencies or other joint excursions. We did, however, examine the self-selected frequencies and joint excursions to see if they could account, in part, for our results.
To exclude the possibility that self-selected movement frequency could account for some of the impairments in independent finger movement seen in our affected hands, we compared
movement frequencies between fingers and between groups.
Figure 6A shows movement frequencies (mean ⫾ SE) for each
group. Instructed fingers were moved cyclically back and forth
at a rate of approximately 0.7 Hz. Within each group, the range
of frequencies was large. Frequencies ranged from 0.21 to 1.21
Hz in the control group, 0.32 to 1.24 Hz in the unaffected
group, and 0.21 to 2.74 Hz in the affected group. Although the
movement frequencies chosen by our subjects appear rather
slow, the fingers moved through ⬎50% of the available range
at each joint and average joint speeds were well within the
typical ranges used during functional tasks of the hand and
fingers in normal subjects (C. E. Lang, unpublished observations). Interestingly, most of the variance in self-selected frequency could be attributed to differences between subjects
(⬎70%), while only a small portion (12%) could be attributed
to differences within subjects (i.e., within the five fingers of
one hand). Thus subjects in all three groups appeared to select
a particular frequency and move each finger near that frequency.
The self-selected movement frequencies were not significantly different among the five fingers and three groups (P ⬎
DIFFERENTIAL FINGER MOVEMENT IMPAIRMENT AFTER STROKE
1167
DISCUSSION
FIG. 6. A: movement frequencies for instructed movement of each finger. B:
joint excursions for instructed movement of each finger. Data points are group
means ⫾ SE. The control group is shown with open circle; the affected group is
shown with filled triangles, and the unaffected group is shown with filled circles.
0.05) nor did we find any relationship between self-selected
frequencies and finger individuation indices in the affected
group (Spearman rank-order correlations, thumb ⫽ ⫺0.095,
index ⫽ 0.276, middle ⫽ ⫺0.429, ring ⫽ 0.323, and little ⫽
J Neurophysiol • VOL
Asking subjects to move each finger by itself, we probed a
crucial function of the motor cortex and corticospinal tract. Our
results were obtained from subjects who reported substantial
recovery from their initial hemiparesis and who were tested
several months to several years after the lesion occurred.
Independent finger movements were differentially impaired in
humans with lesions relatively restricted to the motor cortex or
corticospinal tract. In the affected hands, the independence of
the thumb was normal, and the independence of the index
finger was slightly impaired, while the independence of the
middle, ring, and little fingers was substantially impaired.
The lesions in our hemiparetic subjects all disrupted the wellknown pathway of the corticospinal system; lesions were located
in the motor cortex itself, in the corona radiata adjacent to the
posterior body of the lateral ventricle, in the internal capsule, or in
the basis pontis. Although we found no clinical signs of involvement of other structures, lesions in the present subjects may have
included subclinical damage to additional pathways. For example,
unilateral lesions in the basis pontis may have damaged portions
of the pontine nuclei. Likewise, lesions in the internal capsule may
have damaged thalamocortical fibers. Nevertheless, the observed
pattern of impairments was consistent across subjects. We infer
that the differential pattern of impairments in finger independence
resulted predominately from damage to the motor cortex or the
corticospinal tract. The differential deficits in our hemiparetic
subjects presumably reflect corticospinal function for which
spared components of the neuromuscular system could not compensate. We therefore consider several factors that might have
contributed to the normal independence of the thumb and the
diminished independence of the more ulnar fingers: 1) structural
independence, 2) incomplete lesions, and 3) recovery of function.
Possible explanations for the normal independence
of the thumb
The normal independence of the thumb may be partially explained by the architecture of the hand and forearm. The thumb is
the most structurally independent digit. All the muscles which
move the thumb act on no other digits, while each of the other four
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
0.276, all P values ⬎0.05). We conclude that movement frequency could not account for the differences in individuation
indices described above.
We also considered the possibility that the self-selected range
through which the instructed fingers moved could account for
some of the impairments seen in our affected hands. Figure 6B
shows joint excursions (mean ⫾ SE) during instructed finger
movement for each group. Joint excursions of the instructed
fingers were not significantly different among the three groups
(P ⬎ 0.05). The plots in Fig. 6B illustrate that the most excursion
typically occurred at the PIP joint of each finger (approximately
85°), followed by the MCP joint (approximately 55°), and then the
DIP joint (approximately 20°). The thumb shows a slightly different pattern with similar excursions occurring at the MCP and IP
joints (approximately 55°), and a smaller excursion occurring at
the CMC joint (approximately 30°). Thus these data indicate that
the impairments in independent finger movements in the affected
hands cannot be explained by differences in self-selected joint
excursions.
1168
C. E. LANG AND M. H. SCHIEBER
J Neurophysiol • VOL
immediate days and weeks after the lesion occurs, then somatopically complete, but partial tissue damage might account
for the deficits observed here.
Rehabilitation, plasticity, and compensation might explain
the differential impairments
Clinical observations suggest that patients with pure motor
hemiparesis typically have uniform involvement of all the
fingers in the affected hand in the first hours and days after
their stroke (M. H. Schieber, unpublished observations). Although longitudinal quantitative data on the recovery of finger
independence are not available on the present subjects, we
consider the possibility that the thumb recovered independence
more than the other fingers. All of our hemiparetic subjects
received extensive rehabilitation services after their stroke.
After stroke, rehabilitative training of the upper extremity
generally focuses on functional use of the hand and fingers.
Common tasks such as picking small objects off the table,
buttoning a shirt, or writing require more independent control
of the thumb and index finger than of the middle, ring, and little
fingers. Thus the differential impairments we observed may be
explained in part by practice-induced recovery during the rehabilitation process that emphasized tasks requiring independent movements of the index finger and thumb. Repetition of
tasks requiring independent thumb and index finger movements could lead to plastic changes in the primary motor
cortex, compensation by other descending pathways, and/or
compensation by nonprimary cortical motor areas.
Task-specific training (Nudo et al. 1996a), ischemic lesions
(Nudo and Milliken 1996), and ischemic lesions plus taskspecific training (Nudo et al. 1996b) all induce plastic changes
in the primary motor cortex hand and forearm representation in
nonhuman primates. In humans with hemiparesis due to corticospinal tract lesions, primary motor cortex activation is preserved and the magnitude of activation is similar to healthy
control subjects (Cramer et al. 2002). Our hemiparetic subjects
had sufficient time and task-specific training after their injuries
for plastic changes to occur in the hand and forearm representation of the primary motor cortex. If rehabilitative training
emphasized independent thumb and index finger movements,
the thumb and index finger representation in the primary motor
cortex might have expanded at the expense of the representations of the more ulnar fingers.
If the crossed corticospinal tract were destroyed completely,
how might plastic reorganization in the primary motor cortex
contribute to recovery of function? Descending pathways other
than the crossed corticospinal tract may provide alternate
routes for motor commands to reach the spinal cord (Fries et al.
1991; Kuypers 1987; Woolsey et al. 1972). An intact ipsilateral
corticospinal tract may contribute to functional recovery after
stroke (Cao et al. 1998; Fisher 1992), although ipsilateral axons
are likely to exert more control over proximal rather than distal
musculature (Colebatch and Gandavia 1989; Kuypers and
Brinkman 1970). The rubrospinal tract and the reticulospinal
tract, which both receive input from the motor cortex, also have
been implicated in recovery of function after pyramidal tract
lesions in nonhuman primates (Belhaj-Saif and Cheney 2000;
Kuypers 1982; Lawrence and Kuypers 1968a,b). Although the
extent of the rubrospinal tract and its relative importance in
humans remain unclear (Nathan and Smith 1982), we cannot
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
fingers is moved, in large part, by multitendoned muscles (i.e.,
flexor digitorum profundus, flexor digitorum superficialis, and
extensor digitorum communis). Physiologic and anatomical evidence in humans suggest that these multitendoned muscles may
not be fully compartmentalized to exert force on just one finger at
a time (Kilbreath and Gandevia 1994; Kilbreath et al. 2002; Reilly
and Schieber 2001, 2002; Segal et al. 2002). Biomechanically, the
finger web space and the connections between tendons (e.g.,
juncturae tendinum of the extensor tendons) place greater restrictions on independent movement of the index, middle, ring, and
little fingers than of the thumb (Austin et al. 1989; Gonzalez et al.
1997; Von Schroeder et al. 1990; Von Schroeder and Botte 1993).
Thus due to the architecture of the hand itself, any surviving
neural control may be able to move the thumb more independently than the other digits.
Given that the motor cortex and corticospinal tract are believed
to have a greater influence on the thumb than on the other fingers
(Penfield and Boldrey 1937; Penfield and Rasmussen 1950;
Woolsey et al. 1952), we did not expect the independence of the
thumb to be normal in patients recovering from pure motor
hemiparesis. The possibility exists that the normal independence
of the thumb was due to incomplete lesions of the hand representation in the motor cortex or the corticospinal tract. Incomplete
lesions can take the two following forms: 1) the tissue affected by
the lesion was destroyed completely, but the lesion failed to affect
the entire hand representation; or 2) the tissue affected by the
lesion included the entire hand representation but the lesion damaged the tissue only partially.
In the first scenario, a portion of the hand representation in the
motor cortex or corticospinal tract might have been completely
destroyed, but that destroyed portion did not contain all the
neurons or axons controlling the thumb. One hemiparetic subject
(H-01) had a lesion relatively restricted to the hand knob of the
motor cortex (Yousry et al. 1997). He initially had paresis of the
face and hand, with only mild paresis of the arm. We cannot rule
out the possibility that his lesion permanently damaged the portion
of the motor cortex representing the more ulnar digits and spared
the portion representing more radial digits, as has been reported
previously (Kim et al. 2002; Phan et al. 2000; Schieber 1999;
Takahashi et al. 2002). Involvement of the face makes this possibility unlikely, however, because the thumb representation
would be expected to lie between the representation of the more
ulnar fingers and the representation of the face. For the other seven
hands affected by subcortical lesions, hemiparesis uniformly involved the face, arm, and leg, making selective sparing of axons
controlling the thumb quite unlikely. Thus lesions that completely
destroyed the affected tissue while sparing the representation of
the thumb are unlikely to account for the differential impairments
observed here.
In the second scenario, the entire hand representation in the
motor cortex or corticospinal tract might have been damaged,
but the damage would have been only partial. If the thumb
normally has a greater representation in the motor cortex and
the corticospinal tract compared with the other four fingers,
then partial damage would spare more neurons and/or axons
controlling the thumb. Although we find it unlikely that such
partial damage would yield the same consistent pattern of
differential impairments across our hemiparetic subjects, we do
not have data to exclude this possibility. Future studies can test
this possibility by measuring finger independence shortly after
lesions occur. If the independence of the thumb is normal in the
DIFFERENTIAL FINGER MOVEMENT IMPAIRMENT AFTER STROKE
J Neurophysiol • VOL
The authors thank K. T. Reilly for helpful suggestions throughout this
project.
DISCLOSURES
This work was supported by National Institute of Neurological Disorders
and Stroke Grants F32 NS-44584 and R01 NS-27686.
REFERENCES
Aguilar MJ. Recovery of motor function after unilateral infarction of the basis
pontis. Am J Phys Med 48: 279 –288, 1969.
Austin GJ, Leslie BM, and Ruby LK. Variations of the flexor digitorum
superficialis of the small finger. J Hand Surg [Am] 14: 262–267, 1989.
Axer H and Keyserlingk DG. Mapping of fiber orientation in human internal
capsule by means of polarized light and confocal scanning laser microscopy.
J Neurosci Methods 94: 165–175, 2000.
Back T and Mrowka M. Infarction of the “hand knob” area. Neurology 57:
1143, 2000.
Belhaj-Saif A and Cheney PD. Plasticity in the distribution of the red nucleus
output to forearm muscles after unilateral lesions of the pyramidal tract.
J Neurophysiol 83: 3147–3153, 2000.
Brochier T, Boudreau M-J, Pare M, and Smith AM. The effects of muscimol inactivation of small regions of motor and somatosensory cortex on
independent finger movements and force control in the precision grip. Exp
Brain Res 128: 31– 40, 1999.
Cao Y, D’Olhaberriague L, Vikingstad EM, Levine SR, and Welch KMA.
Pilot study of functional MRI to assess cerebral activation of motor function
after poststroke hemiparesis. Stroke 29: 112–122, 1998.
Carroll D. Hand function in hemiplegia. J Chronic Dis 18: 493–500, 1965.
Colebatch JG and Gandavia SC. The distribution of muscular weakness in
upper motor neuron lesions affecting the arm. Brain 112: 749 –763, 1989.
Cramer SC, Mark A, Barquist K, Nhan H, Stegbauer KC, Price R, Bell K,
Odderson IR, Esselman P, and Maravilla KR. Motor cortex activation is
preserved in patients with chronic hemiplegic stroke. Ann Neurol 52: 607–
616, 2002.
Dum RP and Strick PL. Spinal cord terminations of the medial wall motor
areas in Macaque monkeys. J Neurosci 16: 6513– 6525, 1996.
Ehrsson HH, Kuhtz-Buschbeck JP, and Forssberg H. Brain regions controlling non-synergistic versus synergistic movement of the digits: a functional magnetic resonance imaging study. J Neurosci 22: 5074 –5080, 2002.
Fisher CM. Capsular infarcts: the underlying vascular lesions. Arch Neurol
36: 65–73, 1979.
Fisher CM. Lacunar strokes and infarcts: a review. Neurology 32: 871– 876,
1982.
Fisher CM. Concerning the mechanism of recovery in stroke hemiplegia. Can
J Neurol Sci 19: 57– 63, 1992.
Fisher CM and Curry HB. Pure motor hemiplegia. Trans Am Neurol Assoc
89: 94 –97, 1964.
Fries W, Danek A, Scheidtmann K, and Hamburger C. Motor recovery
following capsular stroke: role of descending pathways from multiple motor
areas. Brain 116: 369 –382, 1993.
Fries W, Danek A, and Witt TN. Motor responses after transcranial electrical
stimulation of cerebral hemispheres with a degenerated pyramidal tract. Ann
Neurol 29: 646 – 650, 1991.
Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, and Steglind S. The
post-stroke hemiplegic patient. I. A method for evaluation of physical
performance. Scand J Rehab Med 7: 13–31, 1975.
Gonzalez MH, Whittum J, Kogan M, and Weinzweg N. Variations of the
flexor digitorum superficialis tendon of the little finger. J Hand Surg [Br] 22:
277–280, 1997.
Hager-Ross CK and Schieber MH. Quantifying the independence of human
finger movements: comparisons of digits, hands, and movement frequencies.
J Neurosci 20: 8542– 8550, 2000.
Hepp-Reymond M-C, Trouche E, and Wiesendanger M. Effects of unilateral and bilateral pyramidotomy on a conditioned rapid precision grip in
monkeys (Macaca fascicularis). Exp Brain Res 21: 519 –527, 1974.
Hepp-Reymond M-C and Wiesendanger M. Unilateral pyramidotomy in
monkeys: effect on force and speed of a conditioned precision grip. Brain
Res 36: 117–131, 1972.
Jebsen RH, Taylor N, Trieschman RB, Trotter MJ, and Howard LA. An
objective and standardized test of hand function. Arch Phys Med Rehabil 50:
313–319, 1969.
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
rule out contributions from this pathway. The reticulospinal
tract appears to descend at least to the thoracic spinal cord in
man (Nathan et al. 1996) and has been hypothesized to assist,
along with the ipsilateral corticospinal tract, in the recovery of
function after partial cordotomy (Nathan and Smith 1973) and
capsular stroke (Fries et al. 1991). If these alternate descending
tracts do contribute to recovery of function in humans, then the
present results suggest that more independent control of the
thumb and index fingers than of the more ulnar digits may be
achieved over these pathways.
Besides the primary motor cortex, nonprimary cortical motor areas may also contribute to recovery of hand function.
Premotor, supplementary, and cingulate motor areas contain
representations of the hand and forearm, are interconnected
with the primary motor cortex, and send corticofugal projections to subcortical centers, including the spinal cord (see, for
review, Passingham 1997; Picard and Strick 2001; Rizzolatti et
al. 1998). Although it has not been documented in neurophysiological studies, the possibility exists that the thumb might
have a greater representation than the other digits in these
areas, as it does in the primary motor cortex. When the thumb
is moved independently of the other fingers, premotor, supplementary motor, and cingulate motor areas are more active than
when the thumb is moved synergistically with the other fingers,
as shown in a recent imaging study (Ehrsson et al. 2002). Other
imaging studies indicate that premotor and supplementary motor areas may be more active during finger movements in
hemiparetic subjects compared with control subjects (Seitz et
al. 1998; Weiller et al. 1992, 1993). Neurons in nonprimary
cortical motor areas are more frequently related to bilateral
movements than neurons in the primary motor cortex (Tanji et
al. 1988) and thus may be able to exert control via an intact
ipsilateral corticospinal tract. Additionally, axons from the
nonprimary cortical motor areas project to the contralateral
spinal cord via a more anterior route through the internal
capsule compared with the primary motor cortex axons (Axer
and Keyserlink 2000; Fries et al. 1993; Morecraft et al. 2002)
and these more anterior axons may have been spared in some
of our hemiparetic subjects. Our subject with damage to the
genu of the internal capsule (H-07R) had finger impairments
that were similar to other hemiparetic subjects. This case
supports the idea that nonprimary cortical motor areas also play
a role in the control of independent finger movements. Although the functional significance of the spinal connections
from the nonprimary cortical motor areas is still controversial
(Dum and Strick 1996; Maier et al. 2002; Rouiller et al. 1996),
these areas may have contributed to the differential impairments in finger independence seen here.
In sum, our results show that independent finger movements
were differentially impaired in humans with substantial recovery from motor cortical or corticospinal tract damage. The
independence of the thumb was normal, and the independence
of the index finger was slightly impaired, while the independence of the middle, ring, and little fingers was substantially
impaired. We hypothesize that the differential impairments
remaining after damage to the motor cortex or corticospinal
tract may result from rehabilitative training emphasizing tasks
requiring independent thumb and index movements, and from
a greater ability of the spared components of the neuromuscular system to control the thumb independently compared with
the other four fingers.
1169
1170
C. E. LANG AND M. H. SCHIEBER
J Neurophysiol • VOL
Reilly KT and Schieber MH. Prog No. 938.3. Electromyographic activity of
functional subdivisions in human multitendoned finger muscles. Abstract
Viewer and Itinerary Planner. Washington, DC: Soc Neurosci CD-ROM,
2001.
Reilly KT and Schieber MH. Prog No. 768.17. The functional distribution of
force by motor units in the human FDP. Abstract Viewer and Itinerary
Planner. Washington, DC: Soc Neurosci CD-ROM, 2002.
Rizzolatti G, Luppino G, and Matelli M. The organization of the cortical
motor system: new concepts. Electroencephalogr Clin Neurophysiol 106:
283–296, 1998.
Ropper AH, Fisher CM, and Kleinman GM. Pyramidal infarction in the
medulla: a cause of pure motor hemiplegia sparing the face. Neurology 29:
91–95, 1979.
Rouiller EM, Moret V, Tanne J, and Boussaoud D. Evidence for direct
connections between the hand region of the supplementary motor area and
cervical motoneurons in the Macaque monkey. Eur J Neurosci 8: 1055–
1059, 1996.
Schieber MH. Individuated finger movements of Rhesus monkeys: a means of
quantifying the independence of the digits. J Neurophysiol 65: 1381–1391,
1991.
Schieber MH. Somatotopic gradients in the distributed organization of the
human primary motor cortex hand area: evidence from small infarcts. Exp
Brain Res 128: 139 –148, 1999.
Schieber MH. Constraints on somatotopic organization in the primary motor
cortex. J Neurophysiol 86: 2125–2143, 2001.
Schieber MH and Poliakov AV. Partial inactivation of the primary motor
cortex hand area: effects on individuated finger movements. J Neurosci 18:
9038 –9054, 1998.
Segal RL, Catlin PA, Krauss EW, Merick KA, and Robilotto JB. Anatomical partitioning of three human forearm muscles. Cells Tissues Organs 170:
183–197, 2002.
Seitz RJ, Hoflich P, Binkofski F, Tellmann L, Herzog H, and Freund H-J.
Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch Neurol 55: 1081–1088, 1998.
Takahashi N, Kawamura M, and Araki S. Isolated hand palsy due to cortical
infarction: localization of the motor hand area. Neurology 58: 1412–1414,
2002.
Tanji J, Okano K, and Sato KC. Neuronal activity in cortical motor areas
related to ipsilateral, contralateral, and bilateral digit movements of the
monkey. J Neurophysiol 60: 325–343, 1988.
Tereo Y, Hayashi H, Kanda T, and Tanabe H. Discrete cortical infarction
with prominent impairment of thumb flexion. Stroke 24: 2118 –2120, 1993.
Von Schroeder HP and Botte MJ. The functional significance of the long
extensors and juncturae tendinum in finger extension. J Hand Surg [Am] 18:
641– 647, 1993.
Von Schroeder HP, Botte MJ, and Gellman H. Anatomy of the juncturae
tendinum of the hand. J Hand Surg [Am] 15: 595– 602, 1990.
Wade DT, Langton-Hewer R, Wood VA, Skilbeck CE, and Ismail HM.
The hemiplegic arm after stroke: measurement and recovery. J Neurol
Neurosurg Psychiatry 46: 521–524, 1983.
Weiller C, Chollet F, Friston KJ, Wise RJS, and Frackowiak RSJ. Functional reorganization of the brain in recovery from striatocapsular infarction
in man. Ann Neurol 31: 463– 472, 1992.
Weiller C, Ramsay SC, Wise RJS, Friston KJ, and Frackowiak RSJ.
Individual patterns of functional reorganization in the human cerebral cortex
after capsular infarction. Ann Neurol 33: 181–189, 1993.
Woolsey CN, Gorska T, Wetzel A, Erickson TC, Earls FJ, and Allman
JM. Complete unilateral section of the pyramidal tract at the medullary level
in the Macaca mulatta. Brain Res 40: 119 –123, 1972.
Woolsey CN, Settlage PH, Meyer DR, Sencer W, Hamuy TP, and Travis
AM. Patterns of localization in precentral and “supplementary” motor areas
and their relation to the concept of a premotor area. Res Publ Assoc Res Nerv
Ment Dis 30: 238 –264, 1952.
Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud D, Buettner A,
and Winkler P. Localization of the motor hand area to a knob on the
precentral gyrus: a new landmark. Brain 120: 141–157, 1997.
90 • AUGUST 2003 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.4 on August 12, 2017
Kilbreath SL and Gandevia SC. Limited independent flexion of the thumb
and fingers in human subjects. J Physiol 479: 487– 497, 1994.
Kilbreath SL, Gorman RB, Raymond J, and Gandevia SC. Distribution of
the forces produced by motor unit activity in the human flexor digitorum
profundus. J Physiol 543: 289 –296, 2002.
Kim JS, Chung JP, and Ha SW. Isolated weakness of index finger due to
small cortical infarction. Neurology 58: 985–986, 2002.
Kubota K. Motor cortical muscimol injection disrupts forelimb movement in
freely moving monkeys. Neuroreport 7: 2379 –2384, 1996.
Kuypers HGJM. A new look at the organization of the motor system. Prog
Brain Res 57: 381– 403, 1982.
Kuypers HGJM. Some aspects of the organization of the output of the motor
cortex. In: Motor Areas of the Cerebral Cortex, edited by Bock G, O’Conner
M, and Marsh J. Sussex, UK: John Wiley, 1987.
Kuypers HGJM and Brinkman J. Precentral projections to different parts of
the spinal intermediate zone in the rhesus monkey. Brain Res 24: 29 – 48,
1970.
Lawrence DG and Kuypers HGJM. The functional organization of the motor
system in the monkey. I. The effects of bilateral pyramidal lesions. Brain 19:
1–14, 1968a.
Lawrence DG and Kuypers HGJM. The functional organization of the motor
system in the monkey. II. The effects of lesions of the descending brain-stem
pathways. Brain 15–36, 1968b.
Lee PH, Han SW, and Heo JH. Isolated weakness of the fingers in cortical
infarction. Neurology 50: 823– 824, 1998.
Lincoln N and Leadbitter D. Assessment of motor function in stroke patients.
Physiotherapy 65: 48 –51, 1979.
Maier MA, Armand J, Kirkwood PA, Yang H-W, Davis JN, and Lemon
RN. Differences in the corticospinal projection from primary motor cortex
and supplementary motor area to Macaque upper limb motoneurons: an
anatomical and electrophysiological study. Cereb Cortex 12: 281–296,
2002.
Morecraft RJ, Herrick JL, Stilwell-Morecraft KS, Louie JL, Schroeder
CM, Ottenbacher JG, and Schoolfield MW. Localization of arm representation in the corona radiata and internal capsule in the non-human
primate. Brain 125: 176 –198, 2002.
Nathan PW and Smith MC. Effects of two unilateral cordotomies on the
motility of the lower limbs. Brain 96: 471– 494, 1973.
Nathan PW and Smith MC. The rubrospinal and central tegmental tracts in
man. Brain 105: 223–269, 1982.
Nathan PW, Smith M, and Deacon P. Vestibulospinal, reticulospinal and
descending propriospinal nerve fibres in man. Brain 119: 1809 –1833, 1996.
Nudo RJ and Milliken GW. Reorganization of movement representations in
primary motor cortex following focal ischemic infarcts in adult squirrel
monkeys. J Neurophysiol 75: 2144 –2149, 1996.
Nudo RJ, Milliken GW, Jenkins WM, and Merzenich MM. Use-dependent
alterations of movement representations in primary motor cortex of adult
squirrel monkeys. J Neurosci 16: 785– 807, 1996a.
Nudo RJ, Wise BM, SiFuentes F, and Milliken GW. Neural substrates for
the effects of rehabilitative training on motor recovery after ischemic infarct.
Science 272: 1791–1794, 1996b.
Passingham R. Functional organization of the motor system. In: Human Brain
Function, edited by Frackowiak RSJ, Friston KJ, Frith CD, and Dolan RJ.
San Diego: Academic Press, 1997.
Penfield W and Boldrey E. Somatic motor and sensory representation in the
cerebral cortex of man as studied by electrical stimulation. Brain 37:
389 – 443, 1937.
Penfield W and Rasmussen T. The Cerebral Cortex of Man. New York:
MacMillan, 1950.
Phan TG, Evans BA, and Huston J. Pseudoulnar palsy from a small infarct
of the precentral knob. Neurology 54: 2185, 2000.
Picard N and Strick PL. Imaging the premotor areas. Curr Opin Neurobiol
11: 663– 672, 2001.
Porter R and Lemon R. Corticospinal Function and Voluntary Movement.
New York: Oxford Univ. Press, 1993.
Reilly KT and Hammond GR. Independence of force production by digits of
the human hand. Neurosci Lett 290: 53– 65, 2000.