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Basic elements of arm postural control

analyzed by unloading. Exp. Brain Res. 164:22541
ARTICLE in EXPERIMENTAL BRAIN RESEARCH AUGUST 2005
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Exp Brain Res (2005) 164: 225241

DOI 10.1007/s00221-005-2245-6

R ES E AR C H A RT I C L E

Philippe S. Archambault Pavel Mihaltchev

Mindy F. Levin Anatol G. Feldman

Basic elements of arm postural control analyzed by unloading

Received: 15 September 2004 / Accepted: 23 November 2004 / Published online: 27 April 2005

Springer-Verlag 2005

Abstract To address the question of how arm posture is

controlled, we analyzed shoulderelbow unloading responses in the horizontal plane for dierent directions of
the initial load. The initial load, produced by a doublejoint manipulandum, was suddenly diminished to 1of 12
randomly presented levels (60 to
10% of the initial
load; in 6 out of 12 cases the nal load direction varied
by 20). Subjects were instructed not to intervene in
response to unloading. Neither the unloading onset nor
the nal load level was predictable and we assumed that
the responses to rapid unloading were involuntary.
Unloading elicited a smooth hand movement characterized by a bell-shaped velocity prole. The changes in
hand position, joint angles, and joint torques generally
increased with greater amounts of unloading. For each
direction of the initial load, tonic electromyographic
activity of the shoulder and elbow muscles also changed,
depending on the amount of unloading. The shoulder
and elbow joint torques before and after unloading were
a function of the dierence between the actual conguration of the arm and its referent conguration (R)
P. S. Archambault A. G. Feldman
Centre de Recherche en Sciences Neurologiques,
Universite de Montreal, Montreal,
Quebec, H3S 2J4, Canada
P. Mihaltchev M. F. Levin
Ecole de Readaptation,
Universite de Montreal,
Montreal, Quebec,
H3S 2J4, Canada
M. F. Levin A. G. Feldman
CRIR, Institut de Readaptation de Montreal,
Universite de Montreal, Montreal,
Quebec, H3S 2J4, Canada
P. S. Archambault (&)
Dipartimento di Fisiologia Umana e Farmacologia,
Universita` di Roma La Sapienza,
Piazzale Aldo Moro 5,
00185 Rome, Italy
E-mail: philippe.archambault@uniroma1.it
Tel.: +39-06-49910772
Fax: +39-06-49910942

described by the angles at which each joint torque was

zero. The R conguration changed depending on the
direction of the initial load. Our electromyographic data
imply that these changes result from a central modication of muscle activation thresholds. The nervous
system may thus control the R conguration in a taskspecic way by leaving it unchanged to generate involuntary responses to unloading or modifying it to
accommodate a new load direction at the same initial
position. It is concluded that the R conguration is a
major variable in both intentional and involuntary
control of posture.
Keywords Unloading Shoulder Elbow Postural
control Equilibrium-point hypothesis

Introduction
A basic objective of research in motor control is to
understand how the nervous system, and the musculoskeletal apparatus and aerent feedback, controls posture in the presence of changing external forces. Postural
regulation includes adaptive reactions to sudden alterations in the load. In particular, in response to rapid
unloading, the forearm moves to another position, with
the tonic electromyographic (EMG) activity of agonist
muscles decreasing and that of antagonists increasing so
that a lower net joint torque is generated to balance the
remaining load torque at the new position (Asatryan
and Feldman 1965; Dufosse et al. 1985). Unloading responses are generally considered to be postural reactions
mostly devoid of voluntary corrections, and thus
resulting from the action of short- and long-latency reexes when constant values of reex parameters (for
example thresholds and gains) are maintained by the
central nervous system (Crago et al. 1976; Feldman and
Levin 1995; Latash 1994).
In previous studies it has been shown that the change
in elbow angle was augmented with increasing amounts

226

of unloading, thus producing a monotonic torqueangle

characteristic (Asatryan and Feldman 1965; Levin and
Dimov 1997). For a given characteristic, tonic EMG
signals of agonists and antagonists disappeared or appeared, respectively, at specic elbow angles called the
activation threshold angles. Unloading from dierent
initial elbow angles yielded similar characteristics but
shifted along the angular axis so that the threshold angles were dierent for dierent characteristics (Asatryan
and Feldman 1965; Levin and Dimov 1997; Fig. 1A).
This implies that the voluntary movements necessary to
reach the various initial positions before unloading were
associated with a resetting of the muscle activation
thresholds by neural control levels. In contrast, to provide the involuntary EMG, force and kinematic responses to unloading, control levels maintained

Fig. 1 Invariant torqueangle characteristics (ICs) for single-joint

and two-joint systems (theoretical schemes). In (A), an IC (thick
solid curve) for a single joint is the sum of ICs (dotted curves) of two
opposing muscles groups, one of which starts generating active
torques at threshold angle k1and the other group at threshold angle
k2. R represents the referent joint angle at which the net joint
torque is 0. The nervous system produces movement by shifting R
to R, thus setting another IC for that joint (thick dashed curve). In
(B), two ICs (surfaces) of a two-joint system are shown. Each joint
torque is a function of both joint angles. The referent conguration
of the arm (circle) is the combination of joint angles at which all
joint torques are zero

invariant values of muscle activation thresholds.

Accordingly, the measured torqueangle relationships
were called invariant characteristics (ICs) of the joint.
Families of ICs have been recorded in humans for the
elbow, knee, wrist, and jaw (Feldman 1966, 1979; Ostry
et al. 1997). Similar families of characteristics, each
identied by specic values of exor and extensor activation thresholds, have been recorded for dierent
muscles in decerebrated cats (Feldman and Orlovsky
1972; Matthews 1959).
These empirical ndings underlie the k model for
motor control, a version of the equilibrium-point (EP)
hypothesis (Feldman and Levin 1995). According to this
model, the nervous system would produce intentional
movements by modifying muscle activation thresholds
(k). Consistent with this hypothesis is the observation
that descending systems in the cat have the capacity to
shift muscle activation thresholds (Feldman and Orlovsky 1972; Nichols and Steeves 1986). With each resetting
of the activation thresholds the systems previous position appears as a deviation from the newly specied
threshold position. The same neuromuscular mechanisms that produce EMG signals and forces in response
to deviations from the previous position will produce
EMG signals and forces that oppose deviations from a
newly specied position and thus will move the appropriate body segments to it. In other words, by modifying
muscle activation thresholds, control levels force the
posture-stabilizing mechanisms to generate EMG
activity and muscle forces required for the transition to a
new posture. In this sense, posture and movement stem
from a single process.
To our knowledge, no attempt has been made to
characterize unloading responses and record joint torque characteristics in a system with more than one degree of freedom, although in modeling of double-joint
arm movements the notion that the nervous system may
control posture and movement by changing muscle
activation thresholds, and thus shifting double-joint ICs,
has been used (Flanagan et al. 1993; Gribble et al. 1998).
Indirectly, the presence of ICs is supported by a study of
the eects of perturbations of static arm postures
(Shadmehr et al. 1993). It is necessary to directly verify
whether or not the results of the analysis of single-joint
unloading movements can be extended to the doublejoint system. To meet this objective, we used a doublejoint manipulandum to specify and change an external
load and to determine, by the unloading method, ICs for
the shoulderelbow system of the arm. In the single-joint
case, the relationship between joint torque and angle is
monotonic (Asatryan and Feldman 1965; St-Onge et al.
1997). We expected that the same would be valid in the
double-joint case. However, because of the presence of
double-joint muscles and inter-muscular reexes (Lacquaniti and Soechting 1986; Nichols 1989), torque at
either the shoulder or the elbow would depend on both
joint angles. Therefore, the IC of each joint should
represent a surface relating torque to the two joint angles (Fig. 1B).

227

The k model provides a theoretical background from

which an additional prediction may be made. To balance
initial loads acting in dierent directions but at the same
initial arm position, the nervous system should specify
dierent double-joint ICs that should be separated from
each other in angular coordinates and possibly dier in
terms of slopes. Therefore, by comparing dierent ICs,
one can nd parameters that remain invariant during
involuntary responses to unloading but are changed by
descending neural levels when subjects produce an
intentional action to accommodate a new load direction
at the initial position. Thus as in the case of single-joint
experiments (Asatryan and Feldman 1965), the present
analysis in the double-joint arm may help to identify
intrinsic variables that are directly specied by the nervous system both in voluntary and involuntary control
of posture. Specically, such a variable may represent a
referent (R) conguration of the arm (Feldman and
Levin 1995). In the absence of co-activation of opposing
muscle groups, it is the conguration at which all muscles of the arm reach their individual recruitment
thresholds (Feldman and Levin 1995). This conguration is thus described by the set of threshold angles (one
threshold angle for each degree of freedom of the arm).
Because of the threshold nature of the R conguration,
the activity of each arm muscle will depend on the
deviation of the actual conguration of the arm from the
R conguration. In other words, the dierence between
these congurations is a global factor inuencing all arm
muscles, regardless of their biomechanical function. In
the presence of muscle co-activation, the R conguration
may be operationally dened as the conguration at
which arm muscles generate active forces that together
produce net zero torques. The R conguration is modied by the nervous system to elicit movement or, if the
movement is mechanically prevented, to ensure isometric torque generation.
Thus, the objectives of this study were:
to characterize responses of the double-joint arm to
dierent changes in the load; and
to test the validity of the R concept by verifying that a
dierent R conguration is specied when subjects are
required to produce an intentional motor actionto
accommodate a change in the load condition at the
same initial position of the arm.

Methods
The procedure was approved by the local ethics committee. Eleven right-handed subjects (7 men, 4 women;
mean ageSD: 4612 years) without any known neurological disorders participated in the experiment after
having provided their informed consent. Two of the
subjects had participated in earlier single-joint unloading
experiments and were familiar with the objectives of the
study. Their results did not dier from those in the other
subjects.

Experimental set-up
Subjects were seated in a high-backed chair and grasped
the handle of a custom built double-joint manipulandum. The height of the chair was adjusted so that the
manipulandums handle was at the level of the shoulder
and the subjects arm moved in the horizontal plane.
Subjects were strapped to the chair in order to limit
movement of the trunk. Their wrist and hand were stabilized using a wrist splint attached to the manipulandums handle. Arm movement was thus restrained to
elbow and shoulder excursions in the horizontal plane.
Torque could be produced independently at each
joint of the manipulandum through two torque motors
(maximum torque 60 N m, or approximately 165 N at
the level of the manipulandums handle for the conguration used in this experiment).
The manipulandum had a non-negligible mass that, if
not compensated, could elicit a tendency of subjects to
voluntarily modify unloading responses. A software
procedure was developed to reduce the eect of rotational inertia on movement. Specically, positive feedback was introduced in the torque output, based on the
instantaneous acceleration (recorded using accelerometers) and on the moment of inertia of each axis of the
manipulandum. The feedback factor was selected, by
trial and error, to reduce inertia without introducing
oscillations. The moment of inertia was measured
experimentally for each segment of the manipulandum
by applying a torque pulse of known value and measuring the angular velocity. This measurement was repeated after the introduction of the inertia-correcting
feedback. The eective moment of inertia was reduced
from 0.209 to 0.120 kg m2 (reduction of 62%) for the
proximal limb of the manipulandum, and from 0.038 to
0.031 kg m2 (reduction of 18%) for the distal limb.
Software for control of the experiment was developed
in Labview (version 5.1, National Instruments, Texas,
USA).
Task
The general task was for subjects to bring and to
maintain the handle of the manipulandum at a specied
initial position while balancing an external load that was
subsequently reduced or removed. To achieve this,
subjects viewed a cursor on a computer screen, corresponding to the position of the handle in the horizontal
two-dimensional workspace. They were instructed to
bring the cursor to an initial target (0.5 cm red dot),
which in external space corresponded to a point located
30 cm in front of the sternum (mean initial elbow exion
angle: 1017; shoulder exion angle: 5711). As the
hand approached the target, an elastic load in one of ve
directions was generated by the torque motors. The load
resistance appeared at a distance of 10 cm from the
target and attained its maximum value when the hand
reached the target. This combination of position and

228

external load at the target constituted the initial condition. After a random 24 s delay, the load was suddenly
diminished and the cursor on the screen disappeared.
Subjects were instructed not to correct their arm
movement when provoked by the change in load. They
then had to hold the new arm position until the end of
the trial (3 s). The paradigm involved unloading only,
because sudden loading has been observed to cause
stretching of initially active muscles and the triggering of
protective reactions such as co-activation of antagonist
and antagonist muscles, possibly to prevent damage to
contractile bers (Feldman 1979; Feldman and Levin
1995; see also Discussion section).
To measure multiple torqueangle relationships, the
direction of the initial load was set so that subjects either
had to pull (0) or push (165) against it (Figs. 2A, B).
We chose to use a load direction of 165 for pushing,
because for 180 pilot studies had shown that some
unloading conditions caused the subjects arm to hit the
body. Subjects performed all the unloading trials rst for
the 0 load, then for the 165 load. The 0 load was
somewhat easier to handle and it was more convenient
for subjects to start the experiment with this load. In
addition, 3 of the 11 subjects returned for a second
session in which three dierent initial directions of force
were used. These directions were selected so that they
were equally spaced between 0 and 165 (e.g., at 41,
82.5 and 124). The magnitude of the load at the initial
target corresponded to 30% of each subjects maximum
voluntary force, measured before the experiment for the
pushing and pulling directions. By specifying dierent
initial load directions we implicitly induced subjects to
produce dierent intentional actions to bring the hand
to the same position before unloading while compensating for dierent loads. In terms of the k model, subjects were forced to change parameters of their ICs to
accommodate the dierent initial conditions.
We used a large number of unloading conditions to
better characterize the torqueangle surfaces resulting
from unloading. For each of the initial loads there were
12 unloading conditions. Six of these involved a change
of magnitude of the load while maintaining its initial
direction (unloading to 60, 40, 20, 10, 0, and
10% of
the initial value). For the other six conditions, both the
magnitude and direction of the load were changed in
randomly selected trials (unloading to 40, 20, and
10%
of the initial value with a 20 change in direction
relative to the direction of the initial load). Blocks of 12
trials were used in which each of the 12 nal load conditions was presented once, in a random order to discourage anticipatory behavior of the subject. This was
repeated six times, using a dierent ordering of the
unloading conditions within each block (72 trials for
each initial load).
For two subjects, additional experimental conditions
were used. Unloading from the initial 0 or 165 loads
was produced with and without changes in the direction
of the nal load (unloading to 60, 40, 20, and
10%
with a change in direction of either 0, 20, or 30

and to 10 and 0% with no change in the direction of the

load), for a total of 22 conditions. Because the number
of trials was nearly doubled (132 trials for each initial
load), the experiment for these two subjects was performed in two separate sessions, one for the 0 load and
one for the 165 load.
Displacements provoked by sudden unloading are
usually not corrected if the perturbation does not aect
postural stability, even if no specic instructions are
given to the subject. The unloading reex occurs
naturally in na ve individuals and can be observed on
the rst trial without any instructions (Crago et al.
1976). It is on subsequent trials that they may attempt to
intervene. To reinforce the natural behavior in repeated
trials, subjects were requested not to intervene or not

Fig. 2 Experimental procedures. In (A), the subject is maintaining

the initial load at the initial position, by producing a force (F), in
one of ve initial directions (0165). After unloading, the subjects
arm moves to a new position (panel B displays an example for the
0 load direction). In panel B, the convention used for measurement of shoulder and elbow exion angle is shown (arrows). In
panel C, a trial in which the subject voluntarily intervened is readily
identied (thick line) by departure of the hand positionvelocity
prole from a template (thin line; shaded area represents the
standard deviation) obtained from the average trajectory and
velocity from ve other trials in the same experimental condition.
The movements represent unloading to 20% of the initial load, in
the 165 direction

229

to correct the eects of unloading. This meant letting

the arm reach a nal stable position and balance the new
load without having to think about it. At rst, the tendency to voluntarily react to unloading was generally
strong, and subjects typically needed 612 practice trials
to adapt to the task. Practice ended when subjects reliably produced movements containing a single peak in
the hand velocity prole for at least three consecutive
trials. Subjects practiced only a small subset of the
unloading conditions. No training was necessary when
switching the initial load direction.
Data recording
Kinematic data were sampled at 100 Hz using an Optotrak system (model 3010, Northern Digital, Canada),
with markers placed on the handle of the manipulandum
and on bony landmarks of the right wrist (radial styloid), right elbow (lateral epicondyle of the humerus),
and both shoulders (acromion) processes. Elbow exion
angle was calculated using the arccosine of the normalized dot product of the vectors formed by the wrist and
elbow markers, and the right shoulder and elbow
markers, respectively. Shoulder horizontal exion angle
was obtained likewise, using the horizontal components
of the two vectors composed of the right shoulder and
elbow markers, and by the left and right shoulder
markers, respectively. For the elbow, 0 corresponded to
complete extension with values increasing with exion.
For the shoulder, 0 was dened as having the upper
arm parallel with the vector formed by the two shoulder
markers, with positive values for rotations in the forward direction (Fig. 2B).
Torque applied to each of the manipulandums axes
was recorded with axial strain gauges. Using basic
geometry of the armmanipulandum system, kinematic
and kinetic data were used to calculate the force applied
at the level of the handle, and elbow and shoulder torques. Because the joint torques were derived from the
strain-gauge data on the manipulandums axis, they are
valid in the static case only, i.e. before and after movement. Accurate estimation of joint torques during
movement would have required taking into account the
dynamics of the armmanipulandum system (inertia,
elasticity, viscosity), which was unnecessary, because we
were mostly interested in steady states of the arm before
and after unloading.
Finally, we measured EMG activity using silver-plated bipolar surface electrodes and Grass ampliers for
the following muscles on the right side of the body:
brachioradialis and anconeus (BR and AN, elbow exor
and extensor), pectoralis major and posterior deltoid
(PM and DP, shoulder horizontal exion and extension), biceps and triceps brachii (BB and TB, doublejoint exor and extensor, respectively). The signals were
ltered at 5500 Hz and sampled at 1,500 Hz. They were
then ltered oine using a 55500 Hz third-order Butterworth lter to remove motion artifacts.

During oine analysis, trials in which the subjects

introduced a voluntary correction were identied visually from the presence of multiple peaks in the hand
phase diagram (position vs velocity plot) and were excluded from further analysis (Fig. 2C). On average,
115 of 144 trials (the number after is standard
deviation, SD) were rejected for each subject (range: 3
21 trials). There were no statistical dierences between
the number of rejected trials in the ve initial load
conditions.

Data analysis
Final endpoint positions obtained in the various
unloading conditions were compared using a modied
KolmogorovSmirnov test. This non-parametric procedure compares arbitrary two-dimensional distributions
by dividing the data into quadrants, then comparing the
proportion of each distribution falling within each
quadrant (Peacock 1983; Fasano and Franceschini
1987).
The relationship between joint torques and joint angles obtained during unloading from the same initial
conditions was estimated using a planar t:
  
    
Te
Aee Aes
Qe
Ce




1
Ts
Ase Ass
Qs
Cs
where Te and Ts represent elbow and shoulder torque,
Qe and Qs are elbow and shoulder angles, respectively,
and Aij and Ci are coecients. Data points were obtained by averaging the nal joint torques and angles for
all trials in each of the 12 unloading conditions. An
additional point was obtained by averaging the initial
values of joint torques and angles for all 72 trials. Thus,
13 points where available for each t, except for the two
subjects who worked under additional unloading conditions, where the data were tted using 23 experimental
points. It should be noted from Eq. 1 that two planes
were tted, one for the elbow and one for the shoulder.
Thus, each regression plane had three parameters and
therefore eight degrees of freedom (n
3
1), or 18 degrees of freedom for the subjects who performed additional unloading conditions. To assess the quality of the
regressions, 95% condence intervals were calculated
for the tted planes.
Initial and nal tonic EMG values (before and after
removal of the load) were assessed by computing the
root-mean-square average for two 100-ms windows
centered at 0.25 s before and 2 s after unloading. To
verify that voluntary corrections produced no systematic
eect in the remaining trials, an analysis was performed
based on the inter-trial variability of the tonic EMG
data. We assumed that, if subjects did not intervene, the
changes in tonic EMG activity would result from reex
reactions to unloading and, as a consequence, the intertrial SD of the tonic EMG obtained after a particular
unloading condition should be comparable with the

230

inter-trial SD before the change in load. However, as for

many biological signals, the SD of EMG data is not
constant but tends to vary linearly with magnitude.
Thus, we opted to compare the coecient of variability
(CV; SD divided by the mean value) of the tonic EMG
values.

Results
Hand kinematics
Sudden removal of the load induced a smooth transition
to a new hand position and conguration during a time
that was typically less than 1 s (Fig. 3). The hand moved
in a direction opposite to that of the load (maximum
peak velocity of approx. 0.5 m s
1 for unloading to

10% of the initial load; Table 1). The horizontal displacement and peak velocity of the hand, and the total
movement time, increased with the amount of unloading
for each of the three directions of the nal load (Figs. 3AD). This was the case for all subjects and for all
ve directions of the initial load.
Joint angles and torques were likewise graded with
the amount of unloading for each of the ve directions
of the initial load (Figs. 3GL). The only exception from
this rule was for the elbow angle and torque when the
165 load was used with no change in the direction of
residual loads. In these cases the amplitude of elbow
movements was small (subject meanSD: 89), which
can be explained by the low initial elbow torque (subject
meanSD:
0.31.5 N m). However, when the direction of the nal load was changed by20, substantial
load-dependent changes in elbow angle and torque were
observed (Figs. 3I, K and Table 1). The range of elbow
and shoulder motion was of the order of 1020,
depending on the direction of the initial load. The
direction of changes in the joint angles varied with the
direction of the initial load (Table 1). For the 165 load
direction elbow extension was observed in eight subjects
and exion in three. Overall, the variety of both the
initial and nal load conditions induced a broad range
of changes in joint angles and torques.
Each transition to the nal hand position was produced by a single main movement, as can be seen by the
presence of a single large peak in the velocity proles
and of a single large loop in the phase (velocity vs position) diagrams (Fig. 3CF). The transition was characterized by a bell-shaped velocity prole and was
usually followed by damped oscillations of the hand
around the nal position.
Although the unloading conditions were randomly
presented, hand trajectories were qualitatively similar
for the same change in load (Fig. 4A). The dierent
movement data (movement time, peak velocity, distance
traveled, joint angles and joint torques) and EMG
activity were likewise qualitatively reproducible for the
same subject and unloading condition (see also the error
bars in Figs. 3, 6, 9 and 10). For all subjects the mean

inter-trial variability ranged from 0.9 cm in the 60%

unloading condition to 2.6 cm in the
10% unloading
condition for the x dimension (0). For the y dimension,
the variability ranged from 0.6 to 1.2 cm (60 to

10% unloading condition, respectively). These values
were the same for all directions of the initial load.
Dierent levels of unloading without any change in
load direction brought the hand to nal points located
on the same curve at distances gradually increasing with
the amount of unloading (circles in Fig. 4B). When the
direction of the residual load changed by 20, the
hand trajectory deviated from that obtained without a
change in load direction. This eect was especially evident for the 165 condition (Fig. 4B, left panel).
The distributions of nal endpoint locations were
compared using the modied KolmogorovSmirnov test
for binary distributions (see Methods section). To
account for dierences in the level of the initial load
between subjects, the position data were normalized to
the maximum excursion recorded for each subject. We
compared the distributions of endpoint positions for
adjacent levels of unloading for conditions in which all
subjects participated: separate tests were made for the
initial 0 and the 165 loads and for the three directions
of the nal load. We then compared the distributions in
nal hand position between the 60 and 40% unloading
conditions, the 40 and 20% conditions, etc. All comparisons were signicant at P<0.01 for the 165 initial
load. For the 0 initial condition, endpoint distributions
were signicantly dierent except between the 10 and
0% nal load conditions (P<0.2 in that case).
Invariant characteristics
To verify our main hypothesis that each joint torque is a
function of both joint angles, we used a planar t for the
elbow and shoulder torque data (Eq. 1). Examples of the
planar ts obtained for the elbow and shoulder torques
with the 0 and 165 loads are shown in Fig. 5, for a
subject with 22 unloading conditions. For all subjects
and initial directions of the load, the elbow and shoulder
planar ts had high R2 values (Table 2). The regressions
were signicant in all but one case (<2% of all cases).
Moreover, the coecients of t obtained for each subject for the various directions of the initial load were
always dierent, both for the elbow and the shoulder.
This conrmed our second hypothesis that ICs are
condition-dependent.
To understand how the shoulder and elbow ICs are
combined to provide the appropriate force at the level of
the hand, we considered the intersections of the two
surfaces in Figs. 5A and B (shoulder and elbow ICs)
with the plane of zero torque. These intersections are
shown by the two lines in elbowshoulder co-ordinates
in Fig. 6A, (thick lines). These lines represent the combinations of joint angles where torque at the elbow
(thick solid line) or shoulder (thick dashed line) is zero.
The two lines separate the angular space into four areas

231

where shoulder and elbow torques are either positive or

negative. The long arrow indicates the direction of positive shoulder and elbow torques. For example, at any
conguration of the arm represented by a point within
the quadrant indicated by the arrow, the net joint torque
at the shoulder and elbow is positive and increases with
the distance between that point and the respective zerotorque line. The initial elbow angle for this subject is
very close to, and the initial shoulder angle is far from,

Fig. 3 Unloading produced a

smooth transition of the arm
from the initial position to a
nal position. Curves represent
the mean of all six trials in each
experimental condition for one
subject (thick curve is for the
trials in which the load was
completely removed). Graphs in
the left column are unloading
responses for the 165 initial
load condition when the
direction of the nal load
changed by +20 with respect
to that of the initial load
(unloading to 40, 20, 0 and

10% of the initial load).
Graphs on the right are
responses for the 0 initial load
condition. No change in the
direction of the nal load was
made for any of unloading steps
(unloading to 60, 40, 20, 10, 0
and
10%). Error bars indicate
the inter-trial standard
deviation, for the condition in
which it was the largest. Arrows
on the right side of each graph
indicate increasing amounts of
unloading. Bottom panels (K,
L) show mean static joint
torques obtained before
movement onset (I) and after
the transition of the arm to the
nal position for each amount
of unloading (numbers from 60
to
10, in %)

the zero torque elbow and shoulder lines (lled square in

Fig. 6A). This is consistent with the observation that, at
the initial arm conguration for this subject, near zero
elbow torque was combined with substantial positive
shoulder torque (Fig. 6A). For the 0 load direction, the
initial conguration was characterized by negative torque at the shoulder and elbow (Fig. 6D).
The intersection between the zero-torque lines (open
circles in Fig. 6) is of special interest. By denition, this

232
Table 1 Group means for arm-movement variables after unloading
Direction

Initial load (N)

Movement duration (s)
Peak velocity (m s
1)
Displacement (m)
Elbow movement
Shoulder movement
D Elbow angle ()
D Shoulder angle ()
D Elbow torque (N m)
D Shoulder torque (N m)

Pull (0)

41

82.5

124

Push (165)

21.9 (7.9)
1.05 (0.16)
0.49 (0.14)
0.27 (0.12)
Ext.
Abd.
19.6 (15.0)
17.7 (7.6)
3.8 (1.3)
5.1(1.6)

24.3 (5.9)
0.99 (0.13)
0.69 (0.12)
0.24 (0.06)
Ext.
Abd.
21.4 (6.9)
8.8 (2.5)
8.0 (2.1)
3.9(1.2)

25.5 (5.7)
0.81 (0.03)
0.78 (0.13)
0.18 (0.05)
Ext.
Add.
24.0 (7.5)
7.5 (2.2)
9.5 (2.3)
3.6(1.1)

26.8 (5.5)
0.86 (0.03)
0.57 (0.05)
0.15 (0.04)
Ext.
Add.
20.4 (7.2)
10.5 (3.6)
7.0 (1.5)
7.4(1.8)

26.5 (9.5)
0.92 (0.16)
0.50 (0.16)
0.19 (0.06)
Ext./ex.
Add.
17.1 (12.8)
20.1 (7.6)
4.6 (3.4)
8.4 (3.6)

Numbers indicate inter-subject means (standard deviation). For

movement duration, peak velocity, and displacement, the maximum values within all unloading conditions are reported. D:

maximum amplitude of change in joint torque or angle within all

the unloading conditions (maximum
minimum). For 165 and 0,
n=11 subjects; for the other directions n=3


 
 
 

is the point in angular space where both elbow and
Te
Aee Aes
Qe
Re




3
shoulder torques are null. It is also the conguration
Ts
Ase Ass
Qs
Rs
that the arm reaches when the initial load is completely
removed (see Figs. 6b, d for the arm conguration in with
 

Cartesian space). In terms of the EP hypothesis, this is 
Ass Ce
Aes Cs
Re
the point that describes the referent conguration of the

 Ase Aes
Aee Ass
1 4

Rs
Aee Cs
Ase Ce
arm (see Introduction section). The existence of
unambiguous surfaces describing the relationships beThe mean regression coecients for all subjects are
tween joint torques and joint angles (Fig. 5) shows that
shown
in Table 3, as expressed in the form of Eq. 3. The
the net muscle torques can be expressed as a function of
errors
in Re and Rs were calculated using the 95%
the dierence between the referent conguration (R) and
condence
intervals of the regression planes (Fig. 6a)
the actual conguration of the shoulderelbow system
and
are
reported
in Table 3 (Erre, Errs). The regression
(Q):
coecients were analyzed statistically between subjects,
but only for the 0 and 165 conditions where the
T f Q
R
number of subjects was suciently high. The referent
where
congurations (Re, Rs) constitute two-dimensional dis

tributions that were signicantly dierent from each
Te
T
2 other according to the initial load condition (modied
Ts
KolmogorovSmirnov test; P<0.001). The comparison
Specically, for the linear approximation described of the slope coecients yielded a signicant dierence
for Aee and Ase (paired t-tests; P<0.05). Thus depending
by Eq. 1 for muscle torques,
on the direction of the initial load, not only the referent
conguration was modied but also the slope of the
shoulder and elbow ICs. The R congurations of all
subjects for these two initial load conditions are also
illustrated in Fig. 7.
To analyze the resultant force at the level of the hand
due to the interaction of the elbow and shoulder ICs, we
computed the forces at each point in space in a
25 cm30 cm grid using a simple planar two-joint model
of the arm (Figs. 6C, F). We rst calculated the elbow
and shoulder angles required to position the hand at
each point within the grid. From these angles, we obtained the joint torques from the ICs using Eqs. 3 and 4.
Fig. 4 Hand trajectories for dierent unloading conditions. A The magnitude and direction of the force at the level of
Individual traces for one subject (0 load condition) demonstrate the hand were then computed from the joint torques and
that the hand followed a similar path when unloading was made angles. In Cartesian space, the planar ICs are equivalent
without any change in the direction of the nal load. B When
to a force eld that directs the hand towards the referent
unloading involved not only a change in the amount of the load but
also in the direction of its action, dierent hand paths and nal point, i.e., the arm to its referent conguration. The
combination of dierent joint ICs for the 0 and 165
positions (averaged) were observed

233
Fig. 5 Torque-angle surfaces
(ICs) identied in unloading
experiments. The mean initial
and nal shoulder torques were
t to a plane, in torque
shoulderelbow angle space, for
a subject who performed the
task in 22 unloading conditions.
The tted plane is a measured
IC for the shoulder joint. The
thick line represents the 0torque line, or the intersection
between the regression plane
and the zero torque plane.
Panels A, B are for the 165
load and C, D for the 0 load.
Diamonds indicate the initial
condition (torque and joint
angles)

load led to the formation of hand force elds with different orientations and referent points (Figs. 6C, F).
Hand force elds and the referent congurations in
joint space are also shown for one of the three subjects
who performed unloading from ve dierent orientations of the initial load (Fig. 8). Results for the other
two subjects were similar. Qualitatively for the subject in
Fig. 8, both the orientation of the ICs (the direction of a
normal vector to the plane) and their intersection with
the zero-torque plane (the referent arm conguration),
and the shape of their associated hand force elds,
varied according to the initial direction of the load.
EMG activity
Activity of arm muscles was recorded in all subjects for
the 0 and 165 load directions. EMG activity of all

muscles was modied in response to unloading (Fig. 9).

For the shoulder, some muscles could be readily classied as agonists or antagonists according to the criterion
that they produce torques in the same direction (agonists), or in the opposite direction (antagonists) to that of
the recorded joint torque. In the pectoralis major
(shoulder agonist in the 165 load condition), unloading
caused a sudden decrease in activity, with sometimes a
subsequent short duration burst (Fig. 9A). At the end of
movement, the tonic activity was decreased compared
with its initial value. In the posterior deltoid (antagonist
at the shoulder joint to the 165 load), rapid unloading
elicited a short term burst of activity. An increase in the
nal tonic activity was observed for the larger changes in
load. These results were reversed for the 0 condition,
where posterior deltoid acted as agonist and pectoralis
major as antagonist (Fig. 9B). For the other elbow and
shoulder muscles, a general classication into agonists

Table 2 Results of planar ts (mean R2 values) for elbow and shoulder torques as a function of joint angles

Elbow
Shoulder

Pull
(0)

41

82.5

124

Push
(165)

0.89 (0.11)
0.78 (0.11)

0.89 (0.06)
0.78 (0.14)

0.84 (0.04)
0.84 (0.10)

0.85 (0.04)
0.84 (0.11)

0.87 (0.13)
0.84 (0.14)

Numbers indicate inter-subject means (standard deviation). For 165 and 0, n=11 subjects; for the other directions, n=3

234

Fig. 6 Referent congurations of the arm for unloading in the 165

and 0 load conditions. On the left, zero-torque lines are shown for
the elbow (solid) and shoulder joints (dashed) obtained from the
torque planar regressions (Fig. 5) for one subject, in the 165 (A)
and 0 (D) load conditions. Dashed lines represent the 95%
condence intervals of the torque regression, projected on the zerotorque plane. Long arrows show the direction of increasing torque.
The empty circles represent the referent conguration, or the
combination of joint angles where both elbow and shoulder joint
torques are null. The lled squares show the initial arm congu-

ration, before unloading. The referent congurations of the arm (B,

E; solid lines) where dierent for the 165 and 0 conditions, for a
similar initial conguration (dashed lines). The hand force elds (C,
F), computed based on the joint torque ICs (see Results section)
were also dierent for the two directions of the initial load. Error
bars represent, for the initial position, one standard deviation of the
initial joint conguration or hand position. For the referent
conguration, the error bars in B and C are a transposition in
Cartesian space of the condence intervals shown in A. When not
shown, the error bars were smaller than the symbols

or antagonists could not be made: although muscles of

individual subjects behaved in a consistent manner,
there were dierences across subjects in individual motor
patterns. This probably resulted from muscle redundancy or biomechanical variations.
To verify that the tonic activity of muscles was
changed due to the unloading movement, we compared
across subjects the level of EMG before and after the
complete unloading condition (unloading to 0%), using
paired t-tests. For the initial 0 load, there was a signicant change in tonic EMG in the BR and in all three
extensors (AN, TB, and DB). For the initial 165 load,
BP, PM, and DP displayed signicant changes in tonic
EMG.
Inter-trial variability of tonic EMG
Trials with an obvious sign of voluntary corrections (the
presence of multiple velocity peaks in the hand movement) were rejected (see Methods section). To further
verify that voluntary corrections produced no systematic
eect in the remaining trials, an analysis was performed
based on the inter-trial variability of the tonic EMG
data. Because the timing and the extent of the perturbation was unpredictable, an increase of the variability
would point toward a voluntary correction. Tonic EMG
values and inter-trial variability of a representative

Fig. 7 Referent congurations in all subjects for the 165 (lled

squares) and 0 load conditions (empty circles). Shown are referent
values of joint angles relative to the initial joint angles (0, 0) and the
95% condence ellipses of the distribution. For each data point,
the respective zero-torque lines are shown for the elbow (thick) and
for the shoulder (dotted) joints; arrows show the direction of
positive torque

235
Table 3 Group means for stiness-dimensional coecients, referent joint angles and error on referent angles

Aee
Aes
Ase
Ass
Re
Rs
Ee
Es

Pull (0)

41

82.5

124

Push (165)

6.9 (5.4)

6.3 (2.7)
9.7 (10.8)

16.5 (10.7)
86.1 (11.8)
40.4 (12.0)
3.8 (3.3)
6.1 (5.8)

13.1 (1.5)

14.0 (3.2)

3.8 (2.0)

25.3 (3.0)
92.8 (4.6)
52.6 (4.0)
1.1 (0.3)
6.1 (2.4)

22.6 (5.1)

13.0 (8.8)

3.2 (1.6)

20.3 (5.4)
94.3 (5.0)
62.6 (9.0)
2.6 (2.3)
6.2 (0.8)

17.6 (6.7)

1.5 (6.0)

5.6 (2.5)

24.4 (4.0)
98.3 (4.8)
77.2 (8.8)
2.1 (1.4)
2.8 (2.5)

16.6 (6.0)*

3.8 (8.7)

2.8 (7.3)*

19.7 (7.1)
87.9 (9.3)
79.1 (13.2)
2.8 (1.3)
1.5 (1.1)

Numbers indicate mean (standard deviation). Values are in N m rad
1 for Aii and in degrees () for Ri and Ei. * Signicant dierence
between the 0 and 165 directions (paired t-test, P<0.05). For 165 and 0, n=11 subjects; for the other directions, n=3.

subject are shown in Figs. 10A, B. We rst veried that

the inter-trial coecient of variability (CV) of the tonic
EMG obtained after the 12 dierent changes in load
were normally distributed using the Lilliefors test. This
analysis was performed for each subject, muscle, and
initial load direction and revealed that the nal CVs
were normally distributed for 124 out of 132 cases
(94%). For the nal CVs with a normal distribution, we
then checked that the initial inter-trial CV was within the
95% condence interval (Figs. 10C, D). This was true
for 120 out of 124 cases (97%). It can thus be said that
the inter-trial CV of the tonic EMG remained constant
before and after unloading. We therefore felt condent
that subjects complied with the instruction to not
intervene voluntarily following the change in load.
Threshold mechanisms of muscle activation and control
It has been suggested that a threshold mechanism of
activation/deactivation of muscles is an essential deterFig. 8 Hand force elds and
referent arm congurations for
ve directions of the initial
load, for one subject. The initial
and the referent arm
congurations and respective
hand positions are shown,
respectively, by squares and
circles in the hand (AE) and
joint (angular) workspaces (F).
In (F), numbers indicate the
direction of the initial load; the
respective zero-torque lines are
shown for the elbow (thick) and
for the shoulder (dotted) joints;
arrows show the direction of
positive torque. One can see
that the points representing the
referent congurations are
located dierently from the
point (square) representing the
initial conguration of the arm

minant of motor behavior and that central resetting of

the arm position at which the muscle activation thresholds are reached underlies the changes in the referent
conguration and voluntary motor actions (Feldman
and Levin 1995). That the threshold mechanism was
functional in the present experiments could be demonstrated in two ways. First, the EMG patterns observed
in the present study suggest that the adjustment of the
motor performance to the new initial condition was
associated with a change in the muscle activation
thresholds. This follows from the nding that some
muscles become active while others became silent when
the direction of the initial load changed (Figs. 9 and 10).
In particular, between subjects, there was a signicant
change in the initial tonic activity levels of all six recorded muscles, when compared for the 0 and the 165
load directions (paired t-tests, P<0.05). Because the
muscle lengths were approximately the same in the two
conditions, the transition of the respective muscles to the
supra- threshold or sub-threshold state could be
achieved by appropriate changes in the threshold muscle

236
Fig. 9 EMG activity of all
muscles for one subject (A for
the 165 and B for the 0
condition). The EMG signals
were ltered using RMS
averaging, then averaged over
multiple trials. Only three
unloading conditions are
displayed for each muscle:
unloading to 60, 20 and 0% (top
to bottom). The time of
unloading is indicated by the
vertical dashed lines at 0.5 s.
The error bars indicate the
standard deviation (inter-trial)
during the tonic phase before
and after unloading. The same
scaling was used for the 165
and 0 load conditions. For
abbreviations see Methods
section

lengths. This shows that subjects did produce a taskdependent adjustment of muscle activation thresholds.
Second, after complete unloading the arm reached a
referent conguration when muscles generated net zero
torques. These congurations were dierent depending
on the initial conditions (Fig. 8). The presence of coactivation of muscles might cover-up a dierence in
muscle activation thresholds at these congurations. In
this situation, the dierence in thresholds could be
manifested by shifts in the arm position at which a
minimum in the EMG activity of each arm muscle is
reached. Such shifts were regularly observed in the
present study. It can be seen (Fig. 11) that the arm
congurations at which minimum EMG activity was
observed for the two initial load directions (0 and 165)
were clearly dierent for each of the six arm muscles.
This further suggests that the activation thresholds for
the six muscles were related to the direction of the initial
load (see Discussion section).

initial position. For each of the ve initial load directions the net joint torque (T) was a function of the difference between the actual (Q) and the referent
conguration of the arm (R), the conguration at which
muscles generate zero net torques. The R was constant
for the whole set of responses to unloading for the same
initial condition but dierent for dierent initial conditions.
By changing the initial load direction before
unloading, we implicitly forced subjects to intentionally
modify their control variables to accommodate these
changes. Our results showed that these actions were
associated with a resetting of the muscle-activation
thresholds, a change in the referent conguration of the
arm, and, as a consequence, a repositioning of the elbow
and shoulder ICs in joint space, usually accompanied by
a change in the slopes of the surfaces representing the
ICs. These intentional actions were also associated with
shifts in the arm positions at which minimum EMG
activity of muscles occurred.

Discussion
Do not intervene paradigm
Basic ndings
When subjects were instructed not to intervene, sudden
unloading of the shoulderelbow system provoked an
arm movement to a new steady state conguration. The
nal conguration of the arm depended on the amount
of unloading and on the direction of the load at the

In this study, subjects were instructed to not intervene

voluntarily in response to rapid removal of the load. In
other words, they were asked to preserve the behavior
(changes in the arm position) that occurs naturally,
without specic instructions, when the arm is subjected
to unloading for the rst time. It is usually believed that

237

Fig. 10 Tonic EMG values and inter-trial variability of a single

subject for the 165 (A, C) and for the 0 initial load (B, D). Panels
A and B illustrate the initial tonic EMG values (init) and the nal
values for two muscles in each unloading condition. Numbers on
the x-axis indicate the percentage of the nal load, and bars are
grouped according to each possible direction of the nal load (0,
+20 and
20, relative to the direction of the initial load). Error
bars indicate the inter-trial variability. The tonic EMG values were
normalized to the maximum observed value (initial or nal). In C

and D, the distributions of the coecients of variability (CV) in

tonic EMG are displayed for all muscles of the same subject shown
above. Each data point () indicates the inter-trial variability in
tonic EMG after one unloading condition. The mean of the nal
CVs and the initial CV are also displayed. Error bars indicate the
95% condence interval of the mean nal CV. An asterisk (*) after
the muscle labels indicates a normal distribution of the nal COVs
(Lilliefors; P<0.05). For muscle abbreviations, see Methods
section

with the instruction do not intervene, subjects issue no

changes in their control variables (Cesari et al. 2001;
Feldman 1966; Feldman and Levin 1995; Latash 1994;
Mah 2001). Unlike EMG signals (usually called motor
commands), control variables symbolize the inuence
of neural descending systems on specic parameters such
as the thresholds and gains of proprioceptive reexes.
Thereby, even when central commands are constant,
EMG signals could vary because of reex inuences.
Therefore, the EMG signals and movements evoked by
unloading are not considered to be caused by local
spinal reexes in the absence of central descending
inuences. Rather, they result from an integrative action
of constant descending commands and proprioceptive,
reex reactions involving spinal and possibly supraspinal (e.g., trans-cortical) pathways.
In theory, subjects had ample time to change their
control variables during the task. Intentional changes in
movement can be detected 250300 ms after the onset of
load perturbations in the hand kinematics (Adamovich
et al. 2001; Popescu and Rymer 2000) and after 100
150 ms in the EMG signals (Crago et al. 1976). When
the subject knows the direction of the perturbation in
advance, EMG changes occur even earlier (70 ms;

triggered reactions, Crago et al. 1976). It has been

shown that triggered reactions regularly occur in response to sudden loading of active muscles (Feldman
1979). One possible cause of such reactions would be to
prevent damage of sarcomeres following an abrupt
stretch of active muscles elicited by loading. Indeed,
muscle injury and soreness occur after repeated eccentric
contraction (Lieber and Friden 1999).
To minimize the occurrence of triggered changes in
the control variables, loading was not used in the present
experiments and, in addition, randomized trials were
used to discourage subjects from predicting the amount
and timing of unloading. A small number of trials in
which subjects corrected responses to unloading was
identied and excluded from the analysis.
An additional test that subjects did not produce
voluntary or involuntary (triggered) corrections of responses to unloading in the present study was based on
the known observation that such corrections cause a
large variability in the nal position especially when the
perturbation is unpredictable (Crago et al. 1976; Latash
1994). Instead, for each unloading condition, we
observed consistent nal hand positions, and joint torques and EMG activity. In addition, an expected result

238
Fig. 11 Joint congurations of
all subjects where the minimum
tonic EMG was observed for
the 165 (lled squares) and 0
load conditions (empty circles).
Values are relative to the initial
joint conguration (0, 0). The
95% condence ellipses of the
distribution are also shown and
indicate that the joint
congurations at which
minimum tonic EMG occurred
changed with dierent initial
load conditions

of voluntary and involuntary (triggered) corrections

would have been the observation of substantial variability in the EMG responses to changes in the load. In
contrast, we found that the coecient of variation in the
tonic EMG signals remained invariant regardless of the
amount of unloading, for all muscles, and was indistinguishable from that of EMG signals before unloading. This result implies that, if present, corrections of
responses were minor, and thus insignicantly inuenced
our results and conclusions. Thus several ndings in the
present study support the assumption that the subjects
followed the instruction to not intervene voluntarily in
response to unloading. Finally, subjects only needed a
few practice trials to reliably accomplish the task
according to the instructions, also implying that little
learning was involved and that voluntary corrections
were absent.
Role of muscle elasticity, proprioceptive reexes,
and descending control signals
Passive muscle forces produced in the absence of activation could play an, albeit minor, role in our observed
responses to unloading. Passive elbow muscles produce
torques that change approximately linearly in the range
between 20 and 130 of exion, with zero net torques
occurring in the middle of the whole biomechanical
range of the elbow (Feldman 1979). The elasticity constant of passive elbow muscles is about 2.0 N m rad
1,
which is much less than that observed in our study. The
values characterizing passive resistance of shoulder
muscles are not known, but one can expect they are of
the same order of magnitude as for the elbow muscles.
Thus, changes in active, rather than passive, joint torques played a mayor role in the responses of the arm to
unloading. This is corroborated by the observation that

unloading resulted in signicant changes in the tonic

EMG activity of most of the muscles studied. This
observation also rules out the possibility that the nervous system simply specied a constant level of muscle
activation and thus relied solely on the elasticity of active muscles in responses to changes in the load.
In general physiological terms, our basic results can
be explained in the following way. According to current
views, proprioceptive reexes are not xed entities
characterized by unambiguous stimulusresponse relationships. Rather, they are comparatively complex
structures, the parameters of which are tuned by the
central nervous system in a task-specic way (e.g., Houk
1976). All kinematic and EMG responses to unloading
from the same initial position and load direction probably resulted from proprioceptive or, more generally,
somato-sensory reexes while their parameters specied
by descending systems were kept constant (as implied by
the instruction to not intervene). To compensate for a
new initial load acting in a dierent direction (e.g., 165)
the threshold lengths at which muscle activation begins
were increased for those muscles that counteracted the
previous load. The actual lengths of these muscles now
appeared to be below thresholds and muscles became
silent (e.g., posterior deltoid in Fig. 9). At the same time,
the threshold lengths were decreased for muscles counteracting the new load. The actual length of these muscles now appeared to be above thresholds and the muscle
became active (e.g., PM in Fig. 9).
We can assume that the nervous system, by specifying
appropriate muscle thresholds, selected a set of coordinated proprioceptive reexes in order to oppose the
initial load and achieve the responses observed in this
study. However, because of the redundant number of
muscles, the nervous system could have selected many
dierent combinations of threshold lengths to produce
the same initial force and oppose the initial load. Only a

239

subset of those combinations leads to a stable solution,

exemplied by the converging force elds in Figs. 6 and
8. Producing single, smooth movements after load perturbations may be desirable, for example, by allowing
one to quickly recover. The idea that the nervous system
makes uses of redundancy to select specic coordination
patterns is also present in the complex manifold
hypothesis (Scholz and Schoner 1999; Scholz et al.
2000).
Explanations in terms of the k model
In this study, we measured static angles and torques at
the level of the elbow and shoulder, both before and
after rapid removal of the load from an initial stable arm
posture. Our results are consistent with the concept of
the referent arm conguration, associated with the notion that a deviation from the referent conguration
evokes non-zero net torques increasing as a function of
the dierence between the actual and the referent congurations (Feldman and Levin 1995). For each initial
condition, this function describes transitions between
dierent steady states resulting from unloading while the
referent conguration remains unchanged. In the k
model, the referent conguration is a major control
variable underlying intentional movements. The invariance of this control variable for each of the torqueangle
functions obtained by unloading justies our reference
to them as to ICs.
Our main hypothesis that intentional actions are
associated with resetting the referent arm conguration
was also conrmed in the present study. This conclusion
follows from the nding that the torqueangle surfaces
or ICs describing responses to unloading were shifted in
spatial coordinates when the direction of the initial load
was modied, suggesting that to accommodate these
changes in the motor task, control levels reset the referent arm conguration. Likewise, the orientation of the
hand force elds computed from the joint ICs diered,
depending on the direction of the initial load. Similar
force elds were reported from the measurement of the
restoring force after small passive displacements of the
stable arm in the horizontal plane (Shadmehr et al.
1993). These force elds were not the same for dierent
initial arm positions, which implies, as have previous
studies of single-joint tasks (Asatryan and Feldman
1965; Levin and Dimov 1997; Ostry et al. 1997), that
moving from one posture to another requires a spatial
shift of the joint ICs. These results, together with the
present data, imply that resetting of the referent arm
conguration is not only necessary to preserve the same
hand position when the load direction changes but also
to move the hand position to a new position. In other
words, the present analysis addresses not only the
question of which parameters remain invariant in response to unloading but also the question of which
parameters are controlled by the nervous system to
produce intentional movements or isometric torques.

The reason a linear t was used to compute the joint

ICs is that a plane is the simplest three-dimensional
surface, allowing for a small number of parameters.
However, we do not mean to imply that ICs are generally linear. Indeed, both active and passive muscle
characteristics are non-linear, so it is expected that ICs
should include non-linear terms also. For single joint
movements of the elbow and jaw, non-linear ICs have
been reported (Asatryan and Feldman 1965; Ostry et al.
1997).
Linear stiness values, as measured by the t coecients of the ICs, were of the same order as has been
previously reported when measuring the restoring forces
after a small displacement of the static two-joint arm
(Flash and Mussa-Ivaldi 1990; Gomi and Kawato 1997;
Mussa-Ivaldi et al. 1985; Tsuji et al. 1995). However in
those studies, the cross terms Ase and Aes (the relationship between rotation at one joint with torque at the
other joint) were found to be small when compared to
the symmetric terms Ass and Aee. This was conrmed in
this experiment for the 165 and the 124 conditions, but
not for the other three directions of the initial load,
where Aee, Ase and Aes had similar magnitude (Table 3).
It may be indicative of greater involvement of doublejoint muscles in movements generally directed towards
0, compared with 165 or for the maintenance of a
static posture in the absence of an external force. Indeed,
TB (a double-joint extensor) is at an advantage against
the 0 load, because in this condition subjects generally
produced extension torque at the shoulder and elbow. In
the other conditions, subjects generally produced torques of opposite directions at the elbow and shoulder, so
that neither the BB nor the TB could be at an advantage.
Taken together, our results are consistent with the
following explanations. To move the arm to the initial
position while balancing the initial load, the nervous
system shifted muscle activation thresholds to their
values determined previously during the short-term
practice session of reaching the target in the presence of
the same load. This control process set a referent arm
conguration, R, at which the system could generate
zero joint torques. Because of the dierence between the
actual and the referent congurations, muscle activation
and torques emerged tending to change the actual conguration, Q, in the direction minimizing the dierence.
The process was accomplished when the dierence, Q

R, was reduced to a value that was just sucient to
provide muscle forces required to balance the initial load
force when the hand reached the initial target. In response to unloading, the system maintained the same R
conguration thus relying on the ability of muscles
autogenic and heterogenic proprioceptive reexes to
bring the arm to an equilibrium position depending on
the residual load. To accommodate a change in the
initial load condition, the system specied a dierent R
conguration. This process could be combined with a
change in the degree of co-activation of opposing muscle
groups determined by the dierences between their
activation thresholds (k1 and k2 in Fig. 1a), which is

240

consistent with the observation that the slopes of ICs

were usually dierent for dierent initial conditions.
Alternative explanations
Experiments on adaptation to variable force elds have
led to the idea that the nervous system makes use of
inverse dynamics models to explicitly calculate the joint
torques needed to produce movements along a desired
trajectory while compensating for external forces (Bhushan and Shadmehr 1999; Kawato 1999; Wolpert et al.
1998). It is also assumed that reex and sensory subsystems stabilize the on-going movement by providing
feedback with respect to the desired trajectory (Shadmehr and Mussa-Ivaldi 1994; Wolpert et al. 1998). These
models have primarily been designed to provide a desired trajectory for pointing, but not to specically explain the responses in a postural task, such as unloading
with the instruction do not intervene. Many authors
indeed consider that posture and movement, although
linked, are controlled separately by the nervous system
(e.g., Massion 1992). An alternative opinion is that
posture and movement would stem from the same neural
processes (Feldman and Levin 1995; Von Holst 1950).
In the context of our results, it is important to know
whether or not the explanations of pointing movements
in the framework of internal models and inverse
dynamics force computations can be extended to include
unloading responses. In this framework, one can assume
that control levels rst compute and then specify a
constant level of muscle activation and thus rely on the
elasticity of active muscles to respond to changes in the
load. This assumption conicts with the observation that
the EMG activity was load- and position-dependent in
the present experiments.
Alternatively, one could accept the idea that posture
and movement are controlled separately. Thus, once the
position before unloading has been reached, the movement controller could abandon its inverse and forward
computations of muscle activation and torques and
hand over control to the postural system. Thus, control
levels would let the muscle-reex system manifest its
natural, direct dynamical properties to provide the systematic EMG, force and kinematic responses to
unloading. This mixed strategy has recently been proposed to explain the decrease in muscle co-contraction
following learning of a novel motor task (Osu et al.
2002). A potential problem with this explanation is that
in our experiments, the nal EP for reaching movement
to match the initial load was at the same time a departure point for unloading and thus belonged to the set of
points comprising the joint ICs. Therefore, the tonic
EMG level at the departure point of unloading had the
same dynamical, non-computational nature as at any
other point of the IC.
We would like to emphasize that we are not questioning the ability of the neuromuscular system to deal
with external loads and adapt to new conditions based

on some predictive mechanisms or expected events in the

environment. What is doubtful in the light of the present
results and those from other studies based on unloading
experiments (Asatryan and Feldman 1965; Biryukova
et al. 1999; Levin and Dimov 1997; Ostry et al. 1997) is
that the central nervous system uses internal models
principally based on inverse dynamics computations, for
the control of both posture and movement. In contrast,
the k model is able to explain unloading movements and
also applies to voluntary movement (see Introduction
section). A successful two degrees of freedom model of
the arm was developed using the k model that correctly
describes the kinematics and dynamics of point-to-point
movement (Flanagan et al. 1993). Recently, this model
was used to show how the nervous system could adapt to
velocity-dependent force-elds without needing to
explicitly compute the forces acting on the hand (Gribble and Ostry 2000). EP theory was also successfully
applied to the study of multi-joint arm movement (Cesari et al. 2001; Latash et al. 1999), and whole-body
movements (Domen et al. 1999; Feldman et al. 1998;
Gunther and Ruder 2003; Lestienne et al. 2000).
Acknowledgements This work was supported by FRSQ (Fonds de
Recherche en Sante du Quebec, Canada), CIHR (Canadian Institutes of Health Research, Canada) and NSERC (Natural Science
and Engineering Council, Canada). We would like to thank Dr
David Ostry for his helpful comments on the paper.

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