Exp Brain Res (2002) 142:112

DOI 10.1007/s00221-001-0904-9

R E S E A R C H A RT I C L E

Daniel M. Corcos Hai-Ying Jiang Janey Wilding

Gerald L. Gottlieb

Fatigue induced changes in phasic muscle activation patterns

for fast elbow flexion movements
Received: 3 January 2001 / Accepted: 7 September 2001 / Published online: 20 November 2001
Springer-Verlag 2001

Abstract The present study investigated how muscle fatigue influences single degree-of-freedom elbow flexion
movements and their associated patterns of phasic muscle activation. Maximal unfatigued voluntary isometric
elbow flexor and extensor joint torque was measured at
the beginning of the experiment. Subjects then performed elbow flexion movements over two distances as
fast as possible, and movements over the longer distance
at an intentionally slower speed. The slower speed was
close to what would become the maximal speed in the
fatigued state. Subjects then performed a fatiguing protocol of 20 sustained isometric flexion contractions of 25 s
duration with 5 s rest at 50% maximal unfatigued voluntary force. After a recovery period they repeated the
movements. The fatigue protocol was successful in inducing muscle fatigue, the evidence being decreased isometric maximal joint torque of over 20%. Fatigued
movements had lower peak muscle torque and speed.
Our principal finding was of changes in the timing of the
D.M. Corcos () J. Wilding
School of Kinesiology (M/C 194),
University of Illinois at Chicago, 901 West Roosevelt Road,
Chicago, IL 60680, USA
e-mail: dcorcos@uic.edu
Tel.: +1-312-3551708, Fax: +1-312-3552305
D.M. Corcos
Department of Psychology, University of Illinois at Chicago,
Chicago, IL 60680, USA
D.M. Corcos
Department of Neurological Sciences, Rush Medical College,
Chicago, IL 60612, USA
H.-Y. Jiang
Department of Speech-Language Pathology,
University of Toronto, 6 Queen's Park Crescent West, Toronto,
Ontario M5S 3H2, USA
J. Wilding
Department of Physical Therapy and Human Movement Sciences,
Northwestern University Medical School, Chicago, IL 60611,
USA
G.L. Gottlieb
NeuroMuscular Research Center, Boston University,
19 Deerfield Street, Boston, MA 02215, USA

phasic patterns of fatigued muscle activation. There was

an increase in the duration of the agonist burst and a delay in the timing of the antagonist muscle as measured
by the centroid of the EMG signals. We conclude that
these changes serve as partial but incomplete, centrally
driven compensation for fatigue induced changes in
muscle function. An additional, unexpected finding was
how small an effect fatigue had on movement performance when using a recovery time of 10 min that is long
enough to allow muscle membrane conduction velocity
to return to normal. This raises questions concerning the
behavioral significance of classical laboratory studies of
human fatigue mechanisms.
Keywords Motor control Fatigue Electromyography
Movement Neural control

Introduction
Motor control models help us relate changes in movement task to predictable changes in EMG pattern. For
example, movements of longer distances or with heavier
loads are associated with longer and larger agonist EMG
bursts and delayed antagonist muscle activation (Berardelli
et al. 1984; Gottlieb et al. 1989; Pfann et al. 1998).
Movements performed over the same distance that are
made more quickly are associated with larger, more
steeply rising EMG bursts and earlier antagonist activation (Mustard and Lee 1987; Corcos et al. 1989). These
studies changed movement by instruction or external
conditions such as load, target position or target size.
Movement also changes when muscles fatigue, a condition deliberately avoided in the studies cited above. Here
we raise the question of whether, to reduce the kinematic
consequences of muscle fatigue, there are compensatory
neural adaptations that modify muscle activation patterns. If so, are those changes predictable from studies of
unfatigued movement?
There is much research on the neural mechanisms that
underlie muscle fatigue (Gandevia et al. 1995b). Most

studies examine changes in the electromyogram during

steady state isometric contractions (Bigland-Ritchie et al.
1983b; Marsden et al. 1983; Garland et al. 1994; cf.
Enoka and Stuart 1992), whereas relatively few studies
have addressed changes that occur during movement.
Berardelli and colleagues (1984), and Tschoepe et al.
(1994) found fatigue induced slowing and increased the
duration of the first agonist EMG burst. They suggested
that the increase in the duration of the first agonist burst
partially compensates for the decrease in maximal motoneuron firing frequency that had been observed in isometric contractions (Bigland-Ritchie et al. 1983a). Some
recent studies, however, suggest that motor unit firing
rates can increase during fatigue (Miller et al. 1996), and
fire at very short interspike intervals (Griffin et al. 1998).
Lucidi and Lehman (1992) found that although the kinematics of the movement after an hour of recovery were
not distinguishable from those made before the fatiguing
task, there remained an increase in the width of the first
agonist burst. All three studies that investigated the time
course of the agonist EMG suggest that fatigue causes
changes in the temporal profile of the agonist electromyogram and, if the fatigue is great enough and the recovery interval is not too long, a slowing of the movements.
The present study was intended to test three hypotheses related to the effects of muscle fatigue on patterns of
muscle activation and movement performance. The first
is that the way the CNS compensates for fatigue-induced
muscle weakness is similar to its compensation for a
heavier load. In both cases, we postulate that there are
similar changes in the patterns of muscle activation to increase or maintain force output. These changes are prolongation of agonist activation, delay of antagonist activation and an increase in the peak amplitude of the agonist EMG with no change in the rate of rise of agonist
muscle activation. This strategy, which we have termed a
speed insensitive strategy (Gottlieb et al. 1989) for controlling movement distance as well as controlling load
changes in unfatigued muscle, does not preserve movement time and therefore is an incomplete compensation
for changing task conditions. The rationale for this hypothesis is based in part on previous studies showing fatigue induced temporal changes in agonist and antagonist
EMG waveforms. We tested a second hypothesis that the
EMG compensation under fatigued conditions would be
greater for short movements than for long movements
but that the reduction in peak velocity would be greater
for long movements than for short ones. The rationale is
that because short movements need lower forces and use
less muscle activation, additional motor units might be
available for compensatory recruitment. This is based on
previous studies that have shown EMG increases for
submaximal isometric contractions (Kirsch and Rymer
1987), and additional motor units being recruited in submaximal isotonic tasks (Miller et al. 1996). We tested a
third hypothesis that the increase in agonist duration observed during fatigue would not be observed for unfatigued movements that were intentionally slowed to a fatigued speed. The rationale for this hypothesis is that the

neural control signals associated with weakness induced

by neuromuscular fatigue are different from those associated with intentional reductions in movement speed.

Materials and methods

Subjects
Eight male subjects were used in this study. Males were selected
because in laboratory protocols, they fatigue more rapidly than females (Scalzitti 1994). Our subjects were between the ages of 21
and 33 years, in good health, and without any history of joint or
neuromuscular disease. They performed elbow flexion isometric
and isotonic contractions and elbow extension isometric contractions with their right arms in the horizontal plane. All subjects
gave informed consent according to University IRB protocols before participation in the experiment.
Equipment
A manipulandum was used to support the subject's forearm and restrict movement to one degree of freedom. A capacitative transducer
on the axis of rotation of the manipulandum measured angular displacement. Joint acceleration was measured by a piezoresistive accelerometer mounted 47.6 cm from the center of rotation. A torque
transducer was attached to the manipulandum. A torque motor was
used to move the manipulandum so that the moment of inertia of
each subject's forearm could be measured. Joint velocity was computed from the measured angle. Pairs of pediatric EKG electrodes
were placed 2 cm apart over the bellies of the biceps brachii, and the
lateral and long heads of triceps to measure the EMG signals that
were amplified (1600) and band pass filtered (60300 Hz). Joint
angle, acceleration and the EMG signals were digitized with 12-bit
resolution by a data acquisition computer at a rate of 1000/s.
Procedure
The subject sat in a chair with his right arm abducted 90 away
from his body on the manipulandum on which he grasped a vertical handle. The elbow joint was aligned with the rotational axis of
the manipulandum. The manipulandum was locked in place for
isometric contractions and rotated freely when movements were
performed. A weight of 20 lb was added to the end of the manipulandum to increase the moment of inertia of the manipulandum to
2.28 kg.m2 in order to increase the force requirements during the
movement and thus accentuate the effects of neuromuscular fatigue. Pilot experiments had shown that if the force requirements
of the task are low, fatigue had little effect on either mechanical or
EMG parameters. In addition, our previous work has shown that
the EMG patterns of movements performed against both small and
large inertias are qualitatively the same. The quantitative difference is that the EMG bursts are longer and larger for larger inertias, and the antagonist is delayed (Gottlieb et al. 1989).
A computer monitor was located in front of the subject. There
was a cursor on the monitor to display the angular position of the
manipulandum and give the subject feedback about the movement.
A narrow green marker on the screen represented the starting position. A broad red marker was located as a target at the desired angular distance. The width of the broad marker corresponded to 9
of angular elbow rotation in all the experiments reported here.
Subjects were instructed that when a computer-generated tone
sounded, they should accurately move to the target zone as quickly as possible. They were asked to perform the following tasks.
Maximal and 50% of maximal isometric contractions
The manipulandum was locked in place at 90. The subject performed four isometric flexions and four isometric extensions at

3
100% of his maximal voluntary contraction (MVC), and then four
isometric flexions and four isometric extensions at 50% of the just
measured maximal torque. The purpose of measuring 100% MVC
torque was to determine the extent to which fatigue reduces maximal voluntary torque. The purpose of measuring 50% MVC was
to be able to determine whether contractile fatigue has occurred.
Contractile fatigue would result in an increase in EMG at a given
level of torque (Kirsch and Rymer 1987).

Isometric fatigue protocol repetition 2

The subject repeated the fatigue protocol but did only 11 repetitions since the protocol was quite painful. These 11 repetitions
were intended to restore the muscle's fatigued state.
Rest period 2
The subject rested for the same interval as in Rest period 1 above.

Fast unfatigued flexion

The subject performed 11 voluntary elbow flexions over 20
(5575, 0 being full elbow extension) and over 60 (55115) as
fast as possible. The purpose of this was to determine the unfatigued mechanical and EMG parameters of fast voluntary movements over two fixed distances.

Fast fatigued flexions at distance 2

Intentionally slowed unfatigued flexion

Fatigued maximal isometric and 50% isometric

The subject performed 20 flexions of 60 at a speed that was 10%

less than the unfatigued maximum velocity for the 60 distance.
The purpose of this was to collect data in which speed was intentionally reduced in order to compare these data with movements in
which speed was reduced by fatigue. Pilot studies had shown that
our fatigue protocol for the longer movement distance reduced
peak movement velocity by approximately 10%. The effect of fatigue on peak velocity was less than 10% for the shorter movements, and so we chose not to conduct this experiment at the
shorter distances. To assist the subject, we monitored peak velocity and reported its value to the subject after each movement, along
with encouragement, if necessary, to move faster or slower.

The subject again performed four isometric flexions and four isometric extensions at 100% of his maximal voluntary contraction
(MVC), and then at 50% of his unfatigued MVC.
The protocol developed by Kirsch and Rymer (1987) produces
significant muscle fatigue. Fatigue causes a fall in the mean frequency of the EMG spectrum as a consequence of changes in conduction velocity in the muscle fibers. However, Kirsch and Rymer
(1987) showed that 10 min of rest following the fatigue protocol
returns the mean power frequency of the EMG signal to the prefatigue levels in both the biceps and the brachialis muscles. Thus,
after 10 min, any changes in the electromyogram induced by fatigue can be attributed to factors other than changes in conduction
velocity.
Subjects practiced the whole experimental protocol once before they took part in the experiment. The time interval between
practice and experiment was at least 48 h. Subjects did not do any
intensive exercise before they participated in the experiment.

Isometric fatigue protocol repetition 1

The fatigue protocol consisted of 20 repetitions of a 50% MVC
isometric flexion at the elbow joint for 25 s, followed by 5 s of
rest between the repetitions.

The subject performed 11 voluntary elbow flexion movements as

fast as possible over either 20 or 60, whichever distance was not
performed under Fast fatigue flexions above.

Data analysis
Rest period 1
After the fatigue protocol, the subject rested for ten minutes to allow muscle membrane conduction velocity to return to normal
values (Kirsch and Rymer 1987). In another group of four subjects, we used only a 2-min recovery period. We used two recovery time periods so that we could both minimize the effects of recovery time on motor performance (2-min recovery protocol), and
collect data in which the EMG signal is not affected by changes in
conduction velocity (10-min recovery protocol). Since the shorter
recovery period causes ambiguities in interpreting EMG changes,
the EMG signal is not analyzed for this recovery time period.
However, the magnitude of the kinematic changes was larger for
the shorter recovery interval and allows us to demonstrate the effectiveness of this fatigue protocol.
Fast fatigued flexions at distance 1
The subject performed 11 voluntary elbow flexion movements as
fast as possible either over 20 or over 60. The order in which the
distances were performed was counterbalanced such that half of
the subjects performed the 20 movement before the 60 movement. These movements were analyzed to determine the mechanical and EMG parameters of fatigued muscle when completing voluntary movements.

The digitized EMG signals were full wave rectified and filtered
with a 10-ms moving average window for plotting the EMG time
series data (Fig. 1, Fig. 2, Fig. 5). The data in these figures were
all aligned with respect to the onset of the agonist EMG. The following parameters were calculated.
Isometric parameters
1. Maximal elbow torque (Nm): the maximal elbow torque in the
isometric contraction.
2. Integrated EMG (arbitrary unit): the EMG was integrated over
200 ms centered about the time of peak isometric elbow
torque. We chose this time interval since it was the longest
time interval that all subjects maintained a steady-state maximum contraction in the fatigued condition.
3. Torque/EMG ratio: the peak of the torque in the 50% isometric
condition divided by the EMG integrated over 200 ms centered
about the time of peak isometric elbow torque. One data set
was lost to equipment malfunction, and so these data were only
collected on seven subjects.
Movement parameters
1. Movement time (ms): the time interval from 1% of peak acceleration to the time when the velocity falls to 5% of peak velocity.
2. Peak velocity (Vmaxdeg/s): The largest value of movement velocity.

4
3. Peak elbow torque (Nm): for voluntary movement, elbow
torque was the maximum muscle torque during the acceleration phase of the movement. Elbow torque was calculated by
multiplying acceleration by the effective moment of inertia
(forearm plus manipulandum).
4. Q30 (arbitrary unit): the integral of the agonist EMG signal
from the visually marked onset to 30 ms thereafter. This parameter is used to characterize the initial slope of the agonist
EMG burst.
5. Qag (arbitrary unit): the integral of the agonist EMG from the
marked onset to the time of peak velocity. This parameter is
used to characterize the area of the first agonist EMG burst
which is responsible for the limb accelerating towards the target.
6. Qant (arbitrary unit): the integral of the antagonist EMG from
the marked onset of the agonist burst to the end of the movement (the distance at which velocity drops below 5% of Vmax).
This parameter is used to characterize the area of the antagonist burst.
7. Agonist EMG peak amplitude (arbitrary unit): the EMG peak
amplitude was measured as the maximal value in the filtered
and averaged agonist burst.
8. Cant ms: the centroid of the antagonist burst. This value is calculated by the following equation:
(1)
u (t)=1 if emg(t)K emgmax
u (t)=0 if emg(t)<K emgmax
MT is movement time, t0 is the time of start of acceleration,
emg(t) is the EMG signal in the lateral head of triceps, K is
0.75, emgmax is the peak EMG of the lateral head of triceps.
This equation resolves the location of the burst and ignores
low level activity (less than Kemgmax ). The algorithm is similar to locating the peak of the EMG burst but is less sensitive
to the details of the EMG waveform.
9. Cag ms: the centroid of the agonist burst. It is computed by
equation 1 with the integration interval bounded by the time of
peak velocity, and K is the same value as used for computing
Cant (0.75). The centroid of the agonist burst is a measure of
the duration of the biceps EMG burst.
Statistical analysis
For the maximal voluntary contractions, a paired t-test was performed to examine the effects of fatigue on the maximal elbow
torque and the EMG integral for both flexion and extension contractions. A paired t-test was also used to compare the
torque/EMG ratio in the non-fatigued condition and the fatigued
condition. For the isotonic movements, a two-way repeated-measures ANOVA was used to examine the effects of fatigue and
movement distance. A paired t-test was performed to compare the
intentionally slowed unfatigued movements with the fatigued
movements.

Results
The results are divided into four parts. Part 1 describes
the effects of fatigue on isometric muscle torque and
EMG. Part 2 describes the effects of fatigue on movement kinematics and EMG patterns. Part 3 compares the
EMG patterns of intentionally slowed unfatigued movements with those of fatigue-slowed movements. Part 4
compares the kinematic effects of a 2-min recovery interval with that of a 10-min recovery interval.

Changes in muscle torque and EMG in maximal

voluntary contractions
On average there was a statistically significant decline of
21.2% in flexion torque [meanSE pre-fatigue=
69.14.2 Nm, fatigued=54.54.3 Nm, t(7)=5.98,
P=0.001]. From this fact we conclude that the protocol
developed by Kirsch and Rymer (1987) was effective in
producing fatigue in the agonist biceps muscle. This reduction in maximum flexion torque is shown for a representative subject in Fig. 1A. Even though the fatigue
protocol did not call for strong contraction of the extensor muscles, maximum extension torque was reduced
4.1% following the fatigue protocol as shown in Fig. 1B,
but the decline was not statistically significant [mean
SE pre-fatigue=432.66 Nm, fatigued=41.23 Nm,
t(7)=1.18, P=0.278]. The integrated EMG during MVC
activity was not statistically significantly different between the fatigued and unfatigued conditions for either
the biceps muscle in flexion [t(7)=1.99, P=0.087] or the
triceps muscle in extension [t(7)=1.82, P=0.111]. In the
agonist muscle, the ratio of torque to EMG, the measure
usually considered the defining characteristic of physiological fatigue, was significantly smaller in the fatigued
than the unfatigued state in the 50% MVC condition
[mean ratioSE pre-fatigue=85.9613.32; mean ratio fatigued=55.1210.3, t(6)=2.73, P=0.03].
Comparison between fatigued movements
and unfatigued movements
Fatigue decreased movement velocity and increased
movement time. The data from one representative subject are shown in Fig. 2. The peak elbow torque in the
acceleration phase of the movement decreased. The initial rising phase of the EMG (Q30) in the agonist is similar. However, the rate of rise was not sustained with fatigue and, as a consequence, the EMG peak amplitude of
the biceps muscle decreased. These observations apply
to both 20 and 60 movements. The late component of
the antagonist burst (beginning approximately 160 ms
after the agonist onset) is delayed in both the lateral head
of triceps and the long head of triceps as a consequence
of fatigue.
These findings are summarized in Fig. 3 and Fig. 4
and in Table 1 for all eight subjects. There was no
change in movement amplitude with respect to fatigue or
distance. Movement time significantly increased by
7.38% (averaged over 20 and 60), and was longer for
longer movements. Movement time can be partitioned
into both acceleration time and deceleration time. Acceleration time increased significantly while deceleration
time was unchanged. There was a statistically significant
interaction between fatigue and distance for peak movement velocity. As such, paired t-tests were performed on
both the 20 movements and the 60 movements. This
analysis showed that fatigue significantly decreased peak
velocity in the 60 movements by 7.2% [t(7)=4.33,

5
Fig. 1 Averaged maximum
voluntary isometric contractions in flexion (A) and extension (B) for a representative
subject. The data depict elbow
torque, biceps EMG, and lateral head of triceps EMG. The
data are from subject 7

P=0.003] while the decrease in peak velocity in the 20

movements (4.89%) did not quite reach statistical significance [t(7)=2.16, P=0.067]. Peak elbow torque
dropped significantly (by 15.22% averaged over 20 and
60). Q30 dropped by 24.95% (averaged over 20 and
60) as a result of fatigue but this result was not statistically significant. Inspection of the data of individual subjects showed that Q30 dropped by as much as 50% in one
subject, and not at all in other subjects. The agonist peak
amplitude dropped significantly (by 30.53% averaged
over 20 and 60). The integrals of the agonist burst
(6.83% decrease) and antagonist EMG burst (2.06% decrease), averaged over 20 and 60, did not change significantly. However, the timing of the centroid of the agonist burst (14% change) and the antagonist burst (12%
change), averaged over 20 and 60, occurred significantly later in the fatigued condition.

Comparison between the intentionally slowed unfatigued

movements and fatigued movements
Before performing the fatigue protocol, subjects performed 20 movements over 60 at a peak velocity that
was 10% less than their unfatigued maximal speed. From
this set of 20 movements, we later selected those that
were closest to the maximal speed of the fatigued movements. The average number of trials that were selected as
the intentionally slowed pre-fatigued movements was
10 (range 617).
Intentionally slowed pre-fatigued movements were kinematically indistinguishable from fatigued movements
but the patterns of muscle activation differed as shown in
the time series plot for one subject in Fig. 5.
A paired t-test was used to determine if there were
significant differences in selected movement and EMG
parameters between fatigued and intentionally slowed
pre-fatigued movements. There were no significant differences in movement amplitude, movement time, peak
velocity, Q30, the peak of the agonist burst or the integral

6
Fig. 2 Averaged position, velocity, elbow torque, biceps
(agonist) EMG, lateral head of
triceps (antagonist), and long
head of triceps EMG for movements over 20 (A) and 60
(B). The data are averaged over
11 trials. Movements were performed prior to the fatiguing
protocol (pre-fatigue) and following the fatigue protocol (fatigued). The data are from subject 4

of the antagonist burst as shown in Table 2. However,

the integral of the agonist burst was significantly larger
in the fatigued movements. The centroid of the fatigued
agonist burst (Cag) was significantly later which indicates an increase in EMG burst duration, and is consistent with the fact that burst area increased although burst
peak amplitude did not. The centroid of the antagonist
burst (Cant) was significantly later in the fatigued movements than the intentionally slowed pre-fatigued movements. This is consistent with the fact that it was an increase in acceleration time that produced an increase in
movement time in the fatigued movements. The data in
Fig. 6 depict Cag (part A) and Cant (part B) in the prefatigue condition, the fatigued condition and in the intentionally slowed pre-fatigued condition.
Effect of fatigue recovery interval
All the fatigue measures above were made after the subjects had a 10 minute recovery period so that muscle
conduction velocities would return to normal (Kirsch
and Rymer 1987). To confirm the return of membrane
conduction velocity to pre-fatigue levels, a power spectrum analysis was performed on agonist EMG data from
the isotonic movements. There is a methodological issue
in performing a power spectrum analysis on EMG data
from isotonic movements. Normally, median frequency
is calculated on steady state data (e.g. Kirsch and Rymer
1987). The EMG bursts of isotonic movements are not
stationary and rarely exceed 300 ms in duration. We calculated median frequency using 300 ms of data starting
from the marked agonist onset and padded with 700 ms
of zeros. This method examines frequency changes in
the agonist burst with a resolution of 1 Hz (DeLuca
1985). Consistent with the findings of Kirsch and Rymer
(1987), with 10 min of recovery, we found no statistical
difference in median frequency when comparing pre-fatigued to fatigued movements [mean 20: pre=72.4 and
post=73.1; mean 60: pre=71.0 and post=73.1; F(1,7)=
0.22, P=0.65].
We also performed a study on four subjects with only
two minutes of recovery (Jiang 1996). All of the kinematic effects described above were larger in this group of
four subjects. Peak velocity of 60 movements dropped
by 25% after 2 min of recovery but only by 7.2% after
10 min as shown in Fig. 3D. For 20 movements, the
drop was 11.9% after 2 min of recovery and 4.89% after
10 min. These results show that 10 min of recovery allows not only recovery in muscle fiber conduction velocity but also substantial recovery in kinematic performance.
Reduction of muscle fiber conduction velocity increases the magnitude of the recorded EMG waveform.
Fig. 3 Movement time (A), acceleration time (B), deceleration
time (C), peak movement velocity (D) and peak elbow torque (E)
for 20 (dashed line) and 60 (solid line) movements are shown in
pre-fatigue and fatigued states. The data are averaged over eight
subjects. The data are meanSE

8
Fig 4 The integral of the first
30 ms of the agonist EMG (A),
the agonist peak amplitude (B),
the integral of the agonist burst
(C), the integral of the antagonist burst (D), the centroid of
the agonist (E), and the antagonist (F) for 20 (dashed line)
and 60 (solid line) movements
pre-fatigue and fatigued. The
data are averaged over eight
subjects. The data are
meanSE

Table 1 Effects of fatigue and distance. The results of two-way

factorial repeated measures ANOVA on eight subjects comparing
pre-fatigue movements and fatigued movements and movements
Fatigue
Pre vs Post

Movement amplitude
Movement time
Peak velocity
Acceleration time
Deceleration time
Peak elbow torque
Q30
Agonist peak
Qag
Qant
Centroid agonist
Centroid antagonist

over two different distances. All degrees of freedom for the statistical analysis are 1, 7
Distance
20 vs 60

Interaction
Fatigue by Distance

0.38
35.14
12.79
11.85
0.02
74.63
3.33
13.66
1.30
0.32
14.94
46.84

0.555
0.001
0.009
0.011
0.882
0.000
0.111
0.008
0.291
0.591
0.006
0.000

7942
187.1
2002
81.81
90.99
14.55
0.46
8.22
39.35
10.61
111.9
183.1

0.000
0.000
0.000
0.000
0.000
0.007
0.519
0.024
0.000
0.014
0.000
0.000

0.029
0.46
26.68
0.46
0.26
0.91
2.95
0.01
0.28
0.26
0.05
0.35

0.869
0.520
0.001
0.52
0.63
0.371
0.130
0.925
0.614
0.624
0.833
0.572

Fig. 6 The centroid of the agonist (A) and the centroid of the antagonist (B) in the pre-fatigue condition, the fatigued condition
and in the intentionally slowed pre-fatigue movement condition.
The data are meanSE

This increase could be confused with an increase in recruitment or firing frequency. Therefore, even though the
changes in EMG reported after 10 min of recovery were
also seen after 2 min, we have not presented those results, since their interpretation is open to question.

Discussion

Fig. 5 Averaged position, velocity, elbow torque, biceps EMG

(agonist) and lateral head of triceps EMG (antagonist) for intentionally slowed pre-fatigue movements and fatigued movements.
The data are from the same subject as in Fig. 2

Our first hypothesis was that the rules that the CNS uses
for compensating for a fatigue-weakened muscle are the
same as those for compensating for a larger inertial load.
Our reasoning is that it is the change in the ratio of required to available force that drives the compensatory
strategy. This implies that it does not matter whether the
ratio changes because the muscle gets weaker or the load
gets heavier. This strategy has three principal rules: prolonged agonist activation, delayed activation of the late
component of the antagonist burst, and no change in the
rate at which the agonist EMG burst rises. This hypothesis was confirmed by the data. One additional finding is
that the peak agonist EMG is reduced which was not predicted. This change would tend to reduce muscle force
and therefore speed, which would be kinematically noncompensatory. On the other hand, by reducing muscle
activation, this would tend to slow the progression of fatigue, an effect that might be desirable but is incompatible with kinematic compensation.
Our second hypothesis was that the EMG changes
would be greater for short movements than for long
movements but that the kinematic effects of fatigue
would be greater for long movements than for short
ones. We found that the degree of slowing was indeed

10
Table 2 A comparison of fatigued movements and intentionally slowed pre-fatigue
movements. The results of
paired sample t-tests on the data of eight subjects when comparing the intentionally slowed
pre-fatigue movements with the
fatigued movements. The data
are averaged over eight subjects (meanSE)

Movement amplitude
Movement time
Peak velocity
Q30
Peak of agonist burst
Integral of agonist burst
Integral of antagonist burst
Centroid of agonist burst
Centroid of antagonist burst

greater for longer distance movements than for shorter

distance movements. However, the EMG did not show
greater changes for shorter movements than for longer
movements, which is in contrast to the findings of
Berardelli and colleagues (1984). This hypothesis, therefore, was not confirmed by the data.
We tested a third hypothesis that the EMG patterns
associated with fatigue-induced slowing would differ
from those of intentional slowing. This hypothesis was
confirmed by the data.
These findings question whether the reduction in
torque during movement is exclusively a consequence of
peripheral, contractile fatigue, i.e. a decrease in the capacity of the biceps to generate force. It might also represent a change in the way the CNS activates the muscle that would serve to slow the progression of fatigue.
An additional interesting finding is the fact that
movement velocity was reduced by less than 10% after
ten minutes of recovery. This finding is consistent with
that of Raastad and Halln (2000), who showed a
1214% reduction in isokinetic performance following a
high-intensity exercise protocol, and a 67% reduction
after a moderate intensity protocol with a recovery time
of 520 min. The finding is also supported by the work
of Miller et al. (1987), who showed that a 4-min fatiguing protocol can reduce MVC to less than 10% but that it
returns to almost 90% after 10 min of recovery. We also
used a large load to increase the effects of fatigue as
much as possible during the movement. Thus we believe
that we achieved a level of fatigue that was typical of
what has been done by many others. These results all
demonstrate that despite the fact we know how to fatigue
a muscle in order to produce an arbitrary decrement in
isometric force, it is exceedingly difficult to produce
substantial decrements in movement speed, while also
allowing sufficient time for conduction velocity to return
to normal.
Peripheral fatigue
We can draw conclusions similar to those of Kirsch and
Rymer (1987), and Griffin et al. (1998) about decreases
in dynamic torque/EMG ratios from our isometric and
movement data. When fatigued, our subjects showed an

Intentionally slowed

Fatigued

Significance

MeanSE

MeanSE

62.180.41
71115
1834
4.000.623
0.9990.198
156.122.8
245.139.3
1638
43610

62.80.61
72519
1854
4.720.934
0.9950.171
190.127.9
253.633.8
1789
46110

1.15
1.68
0.93
1.41
0.04
2.44
0.71
3.56
2.78

0.287
0.137
0.386
0.201
0.968
0.045
0.499
0.009
0.027

increase in EMG during a 50% MVC isometric contraction. Fatigue also produced a decrease in peak elbow
torque during isotonic movements without a significant
change in the area of the agonist burst. Both findings reveal a decrease in the torque/EMG relationship. Such observations are also consistent with a number of other
studies (Edwards and Lippold 1956; Hagberg 1981;
Maton and Gamet 1989; Garland et al. 1994; Miller et al.
1996; Potvin 1997). These findings define the presence
of a peripheral fatigue component, a diminished ability
of muscle to produce force.
Central fatigue and rules for muscle activation
The presence of peripheral fatigue does not rule out central fatigue as an additional factor. Central fatigue during
exercise has been defined by Gandevia et al. (1995a) as:
The decrease in muscle force attributable to a decline in
motoneuronal output (p. 281). Three of our measures of
the strength of activation, Q30, Qag and Qant were slightly
reduced by fatigue, but none of the changes reached statistical significance. The largest and most variable reduction was in Q30, which suggests that some subjects reduce the initial excitation of the muscle when fatigued
but others do not. The peak of the agonist burst was significantly reduced by fatigue and this could have reduced
peak muscle force. Hence, using Gandevia's definition,
there is evidence for central fatigue in only one of our
four measures of motoneuronal output.
However, the timing of the EMG bursts in both agonist and antagonist muscles was changed by fatigue to a
degree that could not be predicted by the way subjects
intentionally slow their movements. Fatigue prolonged
the agonist burst. If the level of muscle activation is unchanged, this increases the force output of the muscle.
Were the CNS not to do this, the movement would be
even slower. Hence, this prolongation is compensatory
for the effects of peripheral fatigue and is consistent with
the changes seen when moving a heavier inertial load in
the unfatigued state. However, the compensation is not
complete and the fatigued movement is, never the less,
slower than the unfatigued movement.
Since the fatigued movement time is greater than that
of an unfatigued movement, delay of the antagonist is

11

biomechanically appropriate. However, fatigue delayed

the antagonist burst to a degree that exceeded the amount
we would expect from the antagonist timing of unfatigued movements of a similar speed. Furthermore, since
the fatigued movement's prolongation is due almost entirely to prolongation of the acceleration time, and this is
not true of unfatigued movements with equal movement
times, it is also appropriate that the antagonist burst that
leads to decelerating torque be slightly more delayed.
This additional delay of the antagonist burst, like the
prolongation of the agonist burst, tends to increase
movement speed and may prevent stopping the movement too soon. The limb's final resting position depends
on coactivation of the flexor and extensor muscles to
create a position of equilibrium. To perform an accurate
movement, the point at which movement speed reaches
zero during the deceleration phase should coincide with
this equilibrium position. This requires a delay in braking and hence a delay in antagonist onset.
How should we describe these changes? They do not
fit Gandevia's definition of central fatigue since there is
no overall decline in motoneuronal output. In fact, they
do not represent central fatigue if by that term, we wish
to imply something that diminishes motor performance.
We suggest that these changes represent a central fatigue strategy. By this we mean that the CNS changes
the patterns of muscle excitation in order to reduce the
effects of peripheral fatigue (as in agonist prolongation)
and prevent moving incorrect distances due to peripheral
fatigue (as in antagonist delay). The reduction seen in
peak agonist EMG might also be considered part of a
central fatigue strategy. This reduction in peak agonist
EMG could be attributable to lower motoneuron firing
rates, so-called muscle wisdom (Marsden et al. 1983),
that are sufficient to fully activate a muscle in the fatigued state secondary to the concurrent reduction seen
in muscle fiber relaxation rate when fatigued. This might
serve to prevent neuromuscular transmission failure.
It is also worth noting something that we did not find
to be part of a central fatigue strategy. We know that submaximal isometric torque can be preserved in a fatigued
muscle by stronger activation of the muscle. Our second
hypothesis raises the question of whether subjects have a
reserve of performance that they can use, despite instructions to move as fast as possible. This reserve of performance can usually be exploited only by extensive practice (Corcos et al. 1993). If true, then in the presence of
peripheral fatigue, subjects could, in theory, compensate
more fully by harnessing that reserve. To do this they
would increase the initial firing rates and number of recruited motor units and this would be observed as an increase in Q30. We had predicted that if this were the case,
compensation would be greater for shorter movements
than longer ones. This was based on the rationale that
shorter movements require lower forces and therefore
less muscle activation, leaving a reserve of motor units
that could be recruited. We did not find this. Hence, either our subjects had a reserve that they were not sufficiently motivated to use, or contrary to our supposition,

the reserve does not exist. These experiments do not allow us to decide this issue. That the reserve does not exist is supported by the fact that Q30 was the same for
both short and long movements in the unfatigued state.
Additionally, it has been shown that subjects can produce maximum or near maximum voluntary activation of
their muscles under laboratory conditions (see Gandevia
et al. 1998), thus suggesting that under these conditions,
a reserve does not exist.
Finally, what is the relationship between the fatigue
we have studied and the fatigue that is experienced as
the consequence of sustained hard work or exercise? One
possibility is that exercise fatigue (as we might call it) is
simply greater and less well compensated. If so, were we
to repeat our fatigue protocol enough times, we would
get larger and more significant effects. The protocol we
used was difficult and unpleasant so such an experiment
would not be easy to perform. Another possibility is that
using a less intense and noxious protocol over a longer
period of time would produce more profound and less
compensated fatigue. This should be explored. A third
possibility is that the behavioral consequences of exercise fatigue are different from the slowing of elbow flexions that we are measuring here. This would suggest that
exercise fatigue is not simply a loss of muscle strength
due to muscular and neural factors, but a loss of coordination among muscles, a very different effect, and one
that is not expressed by the study of single-joint movement. This too should be explored.
Acknowledgements This study was supported in part by the National Institute of Arthritis and Musculoskeletal and Skin Diseases
Grant R01-AR 33189 and by the National Institute of Neurological and Communicative Disorders and Stroke Grants K04-NS
01508, R01-NS 28127 and RO1-NS40902. We would also like to
acknowledge the valuable comments of Dr. Ziaul Hasan, and the
advice of Dr. Paolo Bonato and Dr. David Vaillancourt.

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