 |
INTRODUCTION |
The purpose of this study was to
characterize motor patterns at the wrist during three-joint reaching
movements in order to determine the general rules for coordination of
the distal joint with its proximal joints. During planar reaching
movements, the wrist joint appears to move very little (Cruse et
al. 1993
; Dean and Bruwer 1994
). In order for
motion at a joint to be minimal during a multijoint movement, muscle
activities and torques at a joint must resist inertial effects arising
from motion of adjacent joints. This has been demonstrated for
movements in which subjects are instructed to actively keep one joint
immobile in shoulder-elbow (Almeida et al. 1995
;
Gribble and Ostry 1999
) and elbow-wrist movements
(Latash et al. 1995
). Evidence from one study
(Koshland and Hasan 1994
) suggests that this may
also occur at the wrist during three-joint reaching movements when no
instructions were given about joint motion. Reaches to targets in two
directions were examined in this previous study and initial muscle
activities were qualitatively appropriate to counteract inertial
effects resulting from motion at proximal joints but torques were not computed. Although wrist muscle activities have been described for a
range of directions of isometric 3-D forces (Delp et al. 1996
) and 3-D wrist movements (Hoffman and Strick
1999
), wrist muscle activities and torques have not yet been
quantified across a range of planar directions of three-joint arm
movements. This study tested the hypothesis that wrist muscle
activities and torques would consistently resist proximal inertial
effects such as to minimize wrist motion for all reaches. Given that
muscle activities, torques, and excursions at the shoulder and elbow
joints are known to vary across direction (Flanders
1991
; Flanders et al. 1996
; Gottlieb et
al. 1997
; Karst and Hasan 1991
), it would be
expected that wrist muscle activities and torques would also vary
systematically across directions to resist the proximal inertial effects.
A second question addressed the pattern of wrist muscle activities.
Wrist muscles have been shown to be coactive when resisting a changing
load (Milner and Cloutier 1998
; Milner et al.
1995
) but shown to be reciprocal during reaches to two
directions (Koshland and Hasan 1994
). We tested the
hypothesis that wrist muscles would be consistently activated in a
reciprocal pattern for reaches across directions and in this manner
they would be similar to proximal muscle patterns, suggesting similar
rules at the three joints of the arm. To test the robustness of the
wrist muscle pattern, inertial effects from proximal joints were
blocked by immobilizing the wrist joint. We predicted that the
reciprocal pattern would not be altered at first because the response
to changes in inertial effects seems to require several trials, as shown with experiments with perturbed dynamic effects (Sainburg et al. 1999
; Shadmehr and Mussa-Ivaldi 1994
).
After several trials of reaching with the wrist immobilized, however,
we predicted that the wrist muscles would no longer be activated
because a previous study showed that wrist muscles eventually became
quiescent when the wrist was splinted for volitional elbow movements
and perturbations of the forearm (Koshland et al. 1991
).
Results confirmed that wrist muscle torques consistently dampened
proximal inertial effects across directions. Muscle activities were
reciprocal and were not altered with wrist immobilization, even after
many trials. The findings suggest that the nervous systems selects
wrist muscles as part of a plan for the arm. Some of the results have
been reported in abstract form (Koshland et al. 1995
)
 |
METHODS |
Subjects, apparatus, and protocols
Four subjects (2 males and 2 females, 64-77 kg) performed
point-to-point arm movements to targets in the horizontal plane (Fig.
1A). Subjects gave informed
consent and procedures were approved by the Human Subject Committee and
were in accordance with the ethical standards enclosed in the
Declaration of Helsinki. The apparatus and procedures have been
described in detail (Koshland et al. 1999
). Subjects sat
in front of a table with the dominant right arm supported by a
mechanical apparatus which rolled on the table. The apparatus allowed
only horizontal flexion and extension at the shoulder, elbow, and wrist
joints but no finger movement. An orthoplast splint held the forearm in
supination and the hand in a vertical position with the fingers
maintained in a slightly flexed posture and the index finger visible.
The same initial configuration of the arm was used by a subject to
reach to each of 12 equidistant targets (20 cm distance) at 30°
intervals (Fig. 1). Subjects started with the wrist in neutral position
and were instructed to make one quick movement without instructions
regarding wrist motion or hand path. Six movements were performed to
each target, totaling 72 movements for each subject. In another
experiment performed on a different day, the double hinge joint in the
apparatus underlying the wrist joint was locked, restricting movement
to the shoulder and elbow joints, and the same protocol was repeated (72 trials).

View larger version (28K):
[in this window]
[in a new window]
|
Fig. 1.
Data for 2 representative trials from the same subject are shown.
A and D: schematic figure of subject demonstrates
direction of movement. Excursions, from distal to most proximal joint,
are shown below, followed by muscle activities in B and
E and torques at each joint in C and
F. Upward deflections indicate flexion or flexor muscle
activities and torques whereas downward deflections indicate extension
or extensor muscle activities and torques. Vertical calibration bars
for excursions indicate scaling of degrees. Muscle activities are
scaled the same in B and E, except shoulder
muscles in E are 10 times larger than in B.
Muscle abbreviations are: pectoralis major (PEC), posterior deltoid
(PDL), biceps brachii (BIC), triceps (TRI), flexors of wrist and
fingers (FWF), and extensors of wrist and fingers (EWF). Time of onset
of movement (10% of peak velocity) and of peak fingertip velocity are
indicated by arrows on time axis.
|
|
Kinematics and kinetics
Reflective markers were placed at locations along the right arm
of the subject (index finger, wrist, elbow, and shoulder) and on the
left shoulder. Movements were videotaped (120 Hz, 2 subjects; 60 Hz, 2 subjects) and digitized (Peak Performance Technologies). Angular
displacements of the shoulder, elbow, and wrist joints were filtered
using a fourth order critically damped filter at a 5-Hz cutoff.
Equations of motion, adapted from Sainburg (Ghez and Sainburg
1995
; Sainburg et al. 1995
) to include the wrist joint, were used to calculate the generalized muscle and interaction torques at each of the three joints (see APPENDIX). The
calculated muscle and interaction torques were plotted for each trial.
The magnitude of the first peak in muscle torque was determined, along with the magnitude of interaction torque at the same time. These initial values were averaged for each direction and subject. Because shoulder and elbow muscle torques have been described in previous studies (Buneo et al. 1995
; Gottlieb et al.
1997
), the comparison of wrist to elbow torques was emphasized
in this study to highlight similarities/differences between distal and
proximal joint torques.
Electromyographic activity
Bipolar surface electrodes were used to record electromyographic
(EMG) activity of six muscles, generally a flexor and extensor at each
joint. These included the following: pectoralis major (clavicular
portion), posterior deltoid, biceps brachii, the lateral head of the
triceps, the flexors of the wrist and fingers (FWF), and extensors of
the wrist and fingers (EWF). The electrodes for the FWF (1 cm diam, 2 cm interelectrode distance) were placed on the forearm overlying the
flexor carpi radialis and flexor digitorum superficialis muscles (see
Koshland and Hasan 1994
). The electrodes for the EWF
were placed on the forearm overlying the extensor digitorum muscle. EMG
signals were initially processed by preamplifiers (1000 × gain,
band-pass of 10-2,500 Hz) and later rectified and smoothed (RMS, 4-ms
window, Datapac-Run Technologies). Onsets of muscle activities were
determined as the time when the EMG activity of a muscle exceeded a
value 5 × SD of its EMG during the first 100 ms after the go
signal when the arm was at rest. Computer-derived onsets were verified
by visual inspection. In addition, integrated area for the first 50 ms
after the onset (Q50) was calculated (Gottlieb et al.
1996
). The integrated area (Q50) was normalized to the largest
value obtained during an experiment. A repeated measures analysis of
variance (ANOVA; P = 0.05) was used to compare subject
averages between wrist conditions (wrist free, wrist immobilized).
 |
RESULTS |
Individual movements
During an individual movement in which the wrist was free to move,
the wrist joint typically showed little overall excursion, often
1-5°. Although the excursion was minimal, the wrist joint frequently
experienced 1-2 joint reversals during the movement. This is most
obvious for the movement to 90° in Fig. 1D for which overall wrist excursion was only 1° despite the fact that the wrist
initially flexed 3° and extended 4°. In contrast, the excursions at
the shoulder and elbow joints were typically monotonic. Even when
excursions were minimal at a proximal joint such as the shoulder in
Fig. 1A (4°), reversals did not occur.
The general pattern of EMG activities at the wrist joint was similar to
the pattern at the shoulder and elbow joints (Fig. 1, B and
E). Wrist muscles became active at the same time as proximal muscle activities, which occurred before the start of any joint motion.
In addition, an initial reciprocal pattern was apparent at each joint.
For example, wrist extensors were initially activated followed by wrist
flexors in the movement to 300° (Fig. 1B), whereas the
opposite sequence occurred for the movement to 90° (Fig.
1D). Later in the movement, both wrist muscle groups tended
to remain active, resulting in coactivation.
The relationship of muscle to interaction torque differed among the
joints. At the wrist the muscle torque mirrored the interaction torque
throughout a movement (Fig. 1, C and F). Wrist
muscle torque was at each moment nearly equal in magnitude but in the
opposite direction (opposite sign) to that of the interaction torque at the wrist. In contrast, the torques at the shoulder and elbow showed
various relationships but never a perfect mirror image. For example in
Fig. 1C, muscle and interaction torques at the elbow and
shoulder joints were in the same direction for most of the movement.
Even when muscle and interaction torques were in opposite directions,
as in Fig. 1F, magnitudes were not equal and elbow and
shoulder muscle torques were two and three times interaction torque, respectively.
Across directions
KINEMATICS/KINETICS.
The pattern at the wrist was consistent for movements
across directions. The wrist joint moved little during reaching
movements to any of the 12 directions, except for 2 directions (120°
and 270°) for which excursions reached 8-16° during individual
trials for 2/4 subjects (Fig.
2A). Peak initial muscle
torques at the wrist gradually changed across direction in a
cosine-like tuning (Fig. 2B). Initial interaction torques
across directions were equal in magnitude but of opposite sign to those
of the muscle torque. Although instructed to make one quick movement,
subjects typically varied speed from trial to trial. Nonetheless,
subjects showed a similar variation across directions that was
approximately ±0.25 m/s for each subject. The slowest subject had an
average speed of 1.0 m/s and lower magnitudes of interaction torques
(triangular symbols in Fig. 2B). The quickest subject had an
average speed of 1.5 m/s and the largest magnitudes of interaction
torques (circular symbols in Fig. 2B). Regardless of the
differences in speed, correlations of wrist muscle torque to wrist
interaction torque resulted in Pearson r values of
0.99 to
1.0 for individual subjects (Fig. 2C).

View larger version (37K):
[in this window]
[in a new window]
|
Fig. 2.
Contrasting kinematics and kinetics at wrist vs. elbow joints across
target directions. A and D: averaged joint
excursions (n = 6) for each subject. B and
E: similarly averaged values for first peak in muscle torque
and interaction torque (at the same time as peak muscle torque).
C and F: scatterplots in which the data points of
muscle and interaction torque for each trial are plotted against each
other.
|
|
Magnitudes of the wrist muscle and interaction torque were relatively
small in this study, ranging from 0.05-0.3 Nm, one-tenth of the
magnitude of elbow torques. Larger torques have been reported for
vertical elbow-wrist movements with large wrist excursions, in the
range of 0.5-1.0 Nm (Cooke and Virji-Babul 1995
;
Virji-Babul and Cooke 1995
). To determine if the wrist
interaction torques of this study were indeed significant in causing
motion at the wrist, we estimated the kinematic effect from unopposed
interaction torques at the wrist. Using the equation A × T2/2I (where
A = average interaction torque up to the first zero crossing, T = time to the first zero crossing, and
I = moment of inertia of the hand at the wrist), wrist
motion increased to an average of 27 ± 13° (SD). For
directions with large interaction torques (e.g., 90 and 270°),
excursion increased up to 40-50° and even for directions with small
interaction torques (e.g., 180 and 330°), excursions increased by
2-22°. These excursions reflect estimates for the first phase of the
biphasic interaction torque profile, unopposed by muscle torque. Given
that the torque profile is typically symmetrical, the wrist would move
an equal amount in the opposite direction during the second phase of
the biphasic torque. In general, the estimates suggest that even though wrist torques were low in magnitude, interaction torques were sufficient to cause substantial movement at the wrist, and wrist muscle
torques were sufficient to minimize the wrist motion.
The relationship of kinematics and kinetics across directions at the
elbow joint were quite different from the wrist joint. Similar to
previous reports (Buneo et al. 1995
; Gottlieb et
al. 1997
), elbow joint excursions varied in a smooth
progression across direction (Fig. 2D) and peak elbow muscle
torques gradually changed across direction (Fig. 2E). The
interaction torques, however, were not equal and opposite to muscle
torques across directions. Interaction torque for a number of
directions had the same sign as the elbow muscle torque (120, 150, and
270-300°). The largest interaction torque did not occur at the same
direction with the largest and opposite peak muscle torque.
Correlations of elbow muscle torque with elbow interaction torque were
weak and ranged from
0.34 to 0.54 among subjects (Fig.
2F). These findings suggest that for many directions, elbow
muscle torques either augmented or partially resisted interaction torques.
MUSCLE ACTIVITIES.
To counteract interaction effects at the wrist, one
strategy may have been to cocontract wrist muscles to stiffen the
joint. As shown for individual trials in Fig. 1, B and
E, reciprocal activation of wrist muscles typically occurred
at the initiation of movement, with little cocontraction. Onsets of
wrist and elbow muscles across directions are compared in Fig.
3, A-D. Wrist and elbow
flexors muscles were activated first for movements to targets located
medial to the arm (~0-180°), whereas wrist and elbow extensors initiated movements to targets that were lateral to the arm
(~210-330°). Onsets of muscles at the three joints often followed
a proximal to distal sequence from shoulder to wrist (40% of trials).
However, in 42% of all trials the wrist and elbow muscles switched
order of onsets. Differences in onsets between flexor/extensor muscles at each joint were computed as a measure of initial cocontraction (Fig.
3, E and F). The time between flexor-extensor
onsets gradually shifted across direction in a similar manner for both
the wrist and elbow joints. Although differences in onsets at the wrist did not reach as large values as at the elbow, the differences were
substantial between 30-119 ms, except two directions (30 and 90°)
for which the differences were small (20 ms). If initial coactivity
were a strategy to deal with interaction effects, one would predict
that the difference in onset would covary with the magnitude of
interaction torque in which the least difference in onset (greatest
cocontraction) should occur at the direction with the largest
interaction torque. However, the correlation between differences in
onset and interaction torques was weak at the wrist (
0.52), similar
to a weak correlation at the elbow (
0.37).

View larger version (31K):
[in this window]
[in a new window]
|
Fig. 3.
Similarities of electromyographic (EMG) data for movements with
wrist-free-to-move vs. wrist immobilized are shown. Each data point in
this figure represents values averaged for the 4 subjects (6 trials/subject). : averaged values when wrist was free
to move. : averaged values when wrist joint was
immobilized in a neutral position. Vertical lines indicate SE.
A-D: onsets of wrist and elbow muscles referenced to onset
of movement (10% of peak fingertip velocity), indicated by 0 on
y axis. Initial cocontraction, measured as difference in
onset between flexor and extensor bursts, is shown for wrist
(E) and elbow (F). Integrated areas over 1st 50 ms of each EMG burst, normalized to largest value recorded, are shown
for wrist (G and I) and elbow (H and
J) muscles.
|
|
The most surprising results occurred in the other experiment in which
the same subjects performed the reaching movements again but this time
with the wrist joint mechanically locked in a neutral position. Speeds
of these two-joint movements with the wrist immobilized were similar to
speeds with the wrist free and peak velocity averaged at 1.6 ± 0.8 m/s. It was remarkable that wrist muscle activities persisted in
these experiments with the wrist immobilized for all 72 trials from
each subject. Indeed, muscle activities in general were not altered, as
shown in Fig. 3. Differences in onsets between flexors and extensors at
the three joints did not change and no statistically significant
differences were noted between the wrist free and wrist immobilized
conditions (Fig. 3, A-F, shoulder not illustrated).
Comparison of the integrated areas (Q50) demonstrated that initial
amplitudes of EMG were also not altered with wrist immobilization, and
no significant differences were found for any of the muscles (Fig. 3,
G-J, shoulder not illustrated).
 |
DISCUSSION |
This study demonstrated that wrist motion was consistently
restricted because wrist muscle torques matched interaction torques for
movements to all directions. An alternative could have occurred in
which the wrist moved substantially for some or many directions and
therefore muscle torque would not always match proximal interaction effects. It is possible for the wrist to move during reaching (Dean and Bruwer 1994
; Koshland et al.
1994
), so the fact that the wrist consistently did not move in
this study reflects a choice by the nervous system, similar to the
choice of a relatively straight hand path toward a target
(Morasso 1981
; Wadman et al. 1980
;
Wolpert et al. 1995
). The choice to minimize wrist
motion infers that the nervous system must select wrist muscles to
resist proximal inertial effects, and unlike proximal muscles, the
wrist muscles must completely dampen inertial effects. This
coordination may be important for functional use of the hand because
the inertial effects of the proximal segments would be less apt to
disturb finger movement (Werremeyer and Cole 1997
).
Wrist muscle activities and torques, however, remain to be examined in
a task in which grasping is combined with reaching.
A similar pattern of wrist muscle torques that counteracted interaction
torques has been demonstrated for other multijoint arm tasks in the
vertical plane. These included instructed elbow-wrist movements
(Virji-Babul and Cooke 1995
) and cyclical elbow-wrist movements, both bidirectional and unidirectional patterns
(Dounskaia et al. 1998
). In these cases, the matching
was not perfect and wrist motion occurred. Interestingly, when cats
reached in the vertical plane to retrieve food from a well, wrist
muscle torques counteracted interaction torques during the phases of
the reach, but a perfect matching of muscle to interaction torque
occurred during the last phase (Ghez et al. 1996
).
Moreover, the final wrist joint angle remained constant for reaches at
different heights, whereas wrist muscle torques increased with
increased interaction torques for the different heights much like
results of this study in which muscle torques increased with increased
interaction torques at different directions. No case of reaching has
been described in which wrist muscle torques assisted interaction
torques. The role of wrist muscles during a reaching task may then be
to counteract proximal inertial effects. Depending on the requirements
of the task for wrist motion or lack of motion, inertial effects are partially or completely dampened.
The wrist joint showed similar features to the proximal joints,
suggesting that the wrist joint is included in a plan for the arm as a
whole. Initial muscle activities at all joints began before limb
displacement for movements to every direction, expanding earlier
results for movements to two directions (Koshland and Hasan
1994
). Moreover, muscles at each joint were consistently activated in an initial reciprocal pattern, similar to previous reports
for shoulder-elbow (Flanders 1991
; Flanders et
al. 1996
; Karst and Hasan 1991
; Wadman
1980
) or elbow-wrist movements (Latash et al.
1997
; Virji-Babul and Cooke 1995
). Wrist muscle
torques varied in a cosine-like manner across direction, as previously reported for shoulder and elbow muscle torques (Buneo et al.
1995
; Gottlieb et al. 1997
). Moreover, onsets
between flexor-extensor muscles and initial EMG amplitude at each joint
gradually shifted across direction (Fig. 3), similar to other reports
of changes in amplitudes and onsets of shoulder and elbow muscles
across direction in the horizontal or vertical plane (Flanders
1991
; Flanders et al. 1996
; Karst and
Hasan 1991
; Wadman 1980
). From the numerous
similarities, the inertially coupled motions of flexion/extension at
the three joints of the arm would seem to be generally controlled as a unit.
One explanation for the coupling among joints is that it results from
biarticular muscles (Sergio and Ostry 1995
; van
Bolhuis et al. 1998
). Most wrist muscles cross the elbow joint
and may contribute to torque at the elbow. However, moment arms and the cross sectional area of wrist muscles are relatively small compared with elbow muscles and therefore they do not contribute a large portion
to the resulting active elbow muscle torque (Amis et al. 1979
; Ann et al. 1981
; Loren et al.
1996
). For a few wrist muscles the moment arm can even switch
directions; for example, the moment arm of extensor digitorum changed
from extensor to flexor at extended elbow angles. Nonetheless, it
appears that the choice and amplitude modulation (AM) of wrist
muscles closely followed the choice and modulation of elbow muscles
across direction as shown in Fig. 3. In addition, wrist muscle torque
profiles closely followed elbow muscle torque profiles (Koshland
et al. 1999
) despite differences of interaction torques (Fig.
2, B and E). In this manner, the similar
modulation at the wrist and elbow joints suggests that control of the
two joints are linked, probably neurally and anatomically. A separate
and parallel control of the wrist may arise when inertially uncoupled
motions, such as pronation and supination, are important for
orientation of the hand (Desmurget et al. 1996
;
Garvin et al. 1997
; Lacquaniti and Soechting
1982
; Sergio and Ostry 1995
; Soechting
and Flanders 1993
).
In this study, the initial muscle activities were not altered when the
wrist joint was immobilized. These findings could be explained by the
fact that the initial configuration of the arm and the minimal wrist
excursion did not change with wrist free or immobilized; however, it
would also be expected that the muscles would become quiescent when
they are no longer needed to keep the joint still. In contrast to
previous reports of adaptations after several repeated trials
(Sainburg et al. 1999
; Shadmehr and Mussa-Ivaldi
1994
), wrist muscle activities did not adapt after many
repeated trials of this study. This suggests that the pattern of wrist
muscles may reflect a plan of central origin which is in anticipation
of inertial effects that would occur under normal circumstances. It is
interesting that a pattern of initial reciprocal activation persisted
at the wrist, suggesting that the nervous system's strategy to resist
inertial effects was not to increase joint stiffness by initial
cocontraction of muscles. The initial reciprocal activation
characterized in this study seems typical because other studies report
similar differences in agonist/antagonist onsets (60-100 ms) for
proximal muscles during reaching movements (Wadman et al.
1980
) and for wrist muscles during instructed elbow-wrist
movements (Latash et al. 1995
) and 3-D wrist movements
(Hoffman and Strick 1999
; Mustard and Lee 1987
). The tendency for coactivity in wrist muscles observed
later in the movement of this study has also been reported in
elbow-wrist movements and 3-D movements (Hoffman and Strick
1999
; Latash et al. 1995
). Alternatively,
subjects have used cocontraction to stiffen the wrist against an
unstable load (Milner and Cloutier 1998
; Milner
et al. 1995
), but they could not reach maximal stiffness and
EMG levels when told to cocontract. Speculating from these single-joint
cases, cocontraction may not be the optimal strategy to limit wrist
joint motion during a multijoint reaching movement, and hence
cocontraction of initial muscle activities was not observed in this
study. Given the robustness of the muscle patterns at the three joints
and their modulation across direction under unrestrained conditions,
the neural system does not appear to reduce the three-joint arm to a
simpler two-joint control system, despite its kinematic appearance.
SYMBOLS:
I |
= |
inertia; r = distance to center of mass from proximal joint |
I |
= |
length; m = mass |
1 |
= |
mh · rh2 |
2 |
= |
mf · rf2 |
3 |
= |
ma · ra2 |
1 |
= |
mh · rh · la |
2 |
= |
mh · rh · lf |
3 |
= |
mh · rh |
4 |
= |
mh · Ih · la |
5 |
= |
mh · rf · la |
6 |
= |
mh · lf2 |
7 |
= |
mh · lf + mf
· rf |
8 |
= |
mf · la2 |
9 |
= |
mh · la2 |
10 |
= |
ma · ra + mf
· Ia + mh · Ia |
SUBSCRIPTS:
a |
= |
upper arm |
f |
= |
forearm |
h |
= |
hand |
s |
= |
shoulder |
e |
= |
elbow |
w |
= |
wrist |
The authors thank Dr. A. Fuglevand and anonymous reviewers for
critical reading of the manuscript.
This work was partially supported by National Institute of Neurological
Disorders and Stroke Grant NS-07309.
Present address of J. C. Galloway: Dept. of Physical Therapy,
University of Delaware, Newark, DE 19716.
Address for reprint requests: G. F. Koshland, Dept. of Physiology,
Arizona Health Sciences Center, University of Arizona, Tucson AZ
85724-0001.
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.