Exp Brain Res (2002) 142:1 12
DOI 10.1007/s00221-001-0904-9
RESEARCH ARTI CLE
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 fa- phasic patterns of fatigued muscle activation. There was
tigue influences single degree-of-freedom elbow flexion an increase in the duration of the agonist burst and a de-
movements and their associated patterns of phasic mus- lay in the timing of the antagonist muscle as measured
cle activation. Maximal unfatigued voluntary isometric by the centroid of the EMG signals. We conclude that
elbow flexor and extensor joint torque was measured at these changes serve as partial but incomplete, centrally
the beginning of the experiment. Subjects then per- driven compensation for fatigue induced changes in
formed elbow flexion movements over two distances as muscle function. An additional, unexpected finding was
fast as possible, and movements over the longer distance how small an effect fatigue had on movement perfor-
at an intentionally slower speed. The slower speed was mance when using a recovery time of 10 min that is long
close to what would become the maximal speed in the enough to allow muscle membrane conduction velocity
fatigued state. Subjects then performed a fatiguing proto- to return to normal. This raises questions concerning the
col of 20 sustained isometric flexion contractions of 25 s behavioral significance of classical laboratory studies of
duration with 5 s rest at 50% maximal unfatigued volun- human fatigue mechanisms.
tary force. After a recovery period they repeated the
movements. The fatigue protocol was successful in in- Keywords Motor control · Fatigue · Electromyography ·
ducing muscle fatigue, the evidence being decreased iso- Movement · Neural control
metric 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
Introduction
D.M. Corcos (
') · J. Wilding
Motor control models help us relate changes in move-
School of Kinesiology (M/C 194),
ment task to predictable changes in EMG pattern. For
University of Illinois at Chicago, 901 West Roosevelt Road,
example, movements of longer distances or with heavier
Chicago, IL 60680, USA
e-mail: [e-mail]
loads are associated with longer and larger agonist EMG
Tel.: [phone], Fax: [phone]
bursts and delayed antagonist muscle activation (Berardelli
D.M. Corcos et al. 1984; Gottlieb et al. 1989; Pfann et al. 1998).
Department of Psychology, University of Illinois at Chicago,
Movements performed over the same distance that are
Chicago, IL 60680, USA
made more quickly are associated with larger, more
D.M. Corcos steeply rising EMG bursts and earlier antagonist activa-
Department of Neurological Sciences, Rush Medical College,
tion (Mustard and Lee 1987; Corcos et al. 1989). These
Chicago, IL 60612, USA
studies changed movement by instruction or external
H.-Y. Jiang
conditions such as load, target position or target size.
Department of Speech-Language Pathology,
Movement also changes when muscles fatigue, a condi-
University of Toronto, 6 Queen's Park Crescent West, Toronto,
tion deliberately avoided in the studies cited above. Here
Ontario M5S 3H2, USA
we raise the question of whether, to reduce the kinematic
J. Wilding
consequences of muscle fatigue, there are compensatory
Department of Physical Therapy and Human Movement Sciences,
neural adaptations that modify muscle activation pat-
Northwestern University Medical School, Chicago, IL 60611,
terns. If so, are those changes predictable from studies of
USA
unfatigued movement?
G.L. Gottlieb
There is much research on the neural mechanisms that
NeuroMuscular Research Center, Boston University,
19 Deerfield Street, Boston, MA 02215, USA underlie muscle fatigue (Gandevia et al. 1995b). Most
2
studies examine changes in the electromyogram during neural control signals associated with weakness induced
steady state isometric contractions (Bigland-Ritchie et al. by neuromuscular fatigue are different from those asso-
1983b; Marsden et al. 1983; Garland et al. 1994; cf. ciated with intentional reductions in movement speed.
Enoka and Stuart 1992), whereas relatively few studies
have addressed changes that occur during movement.
Berardelli and colleagues (1984), and Tschoepe et al. Materials and methods
(1994) found fatigue induced slowing and increased the
Subjects
duration of the first agonist EMG burst. They suggested
that the increase in the duration of the first agonist burst
Eight male subjects were used in this study. Males were selected
partially compensates for the decrease in maximal moto-
because in laboratory protocols, they fatigue more rapidly than fe-
neuron firing frequency that had been observed in iso- males (Scalzitti 1994). Our subjects were between the ages of 21
and 33 years, in good health, and without any history of joint or
metric contractions (Bigland-Ritchie et al. 1983a). Some
neuromuscular disease. They performed elbow flexion isometric
recent studies, however, suggest that motor unit firing
and isotonic contractions and elbow extension isometric contrac-
rates can increase during fatigue (Miller et al. 1996), and
tions with their right arms in the horizontal plane. All subjects
fire at very short interspike intervals (Griffin et al. 1998). gave informed consent according to University IRB protocols be-
fore participation in the experiment.
Lucidi and Lehman (1992) found that although the kine-
matics of the movement after an hour of recovery were
not distinguishable from those made before the fatiguing
Equipment
task, there remained an increase in the width of the first
A manipulandum was used to support the subject's forearm and re-
agonist burst. All three studies that investigated the time
strict movement to one degree of freedom. A capacitative transducer
course of the agonist EMG suggest that fatigue causes
on the axis of rotation of the manipulandum measured angular dis-
changes in the temporal profile of the agonist electromy- placement. Joint acceleration was measured by a piezoresistive ac-
ogram and, if the fatigue is great enough and the recov- celerometer mounted 47.6 cm from the center of rotation. A torque
transducer was attached to the manipulandum. A torque motor was
ery interval is not too long, a slowing of the movements.
used to move the manipulandum so that the moment of inertia of
The present study was intended to test three hypothe-
each subject's forearm could be measured. Joint velocity was com-
ses related to the effects of muscle fatigue on patterns of
puted from the measured angle. Pairs of pediatric EKG electrodes
muscle activation and movement performance. The first 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
is that the way the CNS compensates for fatigue-induced
were amplified (×1600) and band pass filtered (60 300 Hz). Joint
muscle weakness is similar to its compensation for a
angle, acceleration and the EMG signals were digitized with 12-bit
heavier load. In both cases, we postulate that there are
resolution by a data acquisition computer at a rate of 1000/s.
similar changes in the patterns of muscle activation to in-
crease or maintain force output. These changes are pro-
Procedure
longation of agonist activation, delay of antagonist acti-
vation and an increase in the peak amplitude of the ago- The subject sat in a chair with his right arm abducted 90° away
from his body on the manipulandum on which he grasped a verti-
nist EMG with no change in the rate of rise of agonist
cal handle. The elbow joint was aligned with the rotational axis of
muscle activation. This strategy, which we have termed a
the manipulandum. The manipulandum was locked in place for
speed insensitive strategy (Gottlieb et al. 1989) for con-
isometric contractions and rotated freely when movements were
trolling movement distance as well as controlling load
performed. A weight of 20 lb was added to the end of the manip-
changes in unfatigued muscle, does not preserve move- ulandum to increase the moment of inertia of the manipulandum to
2.28 kg.m2 in order to increase the force requirements during the
ment time and therefore is an incomplete compensation
movement and thus accentuate the effects of neuromuscular fa-
for changing task conditions. The rationale for this hy-
tigue. Pilot experiments had shown that if the force requirements
pothesis is based in part on previous studies showing fa-
of the task are low, fatigue had little effect on either mechanical or
tigue induced temporal changes in agonist and antagonist EMG parameters. In addition, our previous work has shown that
the EMG patterns of movements performed against both small and
EMG waveforms. We tested a second hypothesis that the
large inertias are qualitatively the same. The quantitative differ-
EMG compensation under fatigued conditions would be
ence is that the EMG bursts are longer and larger for larger iner-
greater for short movements than for long movements
tias, and the antagonist is delayed (Gottlieb et al. 1989).
but that the reduction in peak velocity would be greater A computer monitor was located in front of the subject. There
was a cursor on the monitor to display the angular position of the
for long movements than for short ones. The rationale is
manipulandum and give the subject feedback about the movement.
that because short movements need lower forces and use
A narrow green marker on the screen represented the starting posi-
less muscle activation, additional motor units might be
tion. A broad red marker was located as a target at the desired an-
available for compensatory recruitment. This is based on
gular distance. The width of the broad marker corresponded to 9°
of angular elbow rotation in all the experiments reported here.
previous studies that have shown EMG increases for
Subjects were instructed that when a computer-generated tone
submaximal isometric contractions (Kirsch and Rymer
sounded, they should accurately move to the target zone as quick-
1987), and additional motor units being recruited in sub-
ly as possible. They were asked to perform the following tasks.
maximal isotonic tasks (Miller et al. 1996). We tested a
third hypothesis that the increase in agonist duration ob-
Maximal and 50% of maximal isometric contractions
served during fatigue would not be observed for unfa-
tigued movements that were intentionally slowed to a fa-
The manipulandum was locked in place at 90°. The subject per-
tigued speed. The rationale for this hypothesis is that the formed four isometric flexions and four isometric extensions at
3
100% of his maximal voluntary contraction (MVC), and then four Isometric fatigue protocol repetition 2
isometric flexions and four isometric extensions at 50% of the just
measured maximal torque. The purpose of measuring 100% MVC The subject repeated the fatigue protocol but did only 11 repeti-
torque was to determine the extent to which fatigue reduces maxi- tions since the protocol was quite painful. These 11 repetitions
mal voluntary torque. The purpose of measuring 50% MVC was were intended to restore the muscle's fatigued state.
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).
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°
Fast fatigued flexions at distance 2
(55 75°, 0° being full elbow extension) and over 60° (55 115°) as
fast as possible. The purpose of this was to determine the unfa- The subject performed 11 voluntary elbow flexion movements as
tigued mechanical and EMG parameters of fast voluntary move- fast as possible over either 20° or 60°, whichever distance was not
ments over two fixed distances.
performed under Fast fatigue flexions above.
Intentionally slowed unfatigued flexion
Fatigued maximal isometric and 50% isometric
The subject performed 20 flexions of 60° at a speed that was 10%
The subject again performed four isometric flexions and four iso-
less than the unfatigued maximum velocity for the 60° distance.
metric extensions at 100% of his maximal voluntary contraction
The purpose of this was to collect data in which speed was inten-
(MVC), and then at 50% of his unfatigued MVC.
tionally reduced in order to compare these data with movements in
The protocol developed by Kirsch and Rymer (1987) produces
which speed was reduced by fatigue. Pilot studies had shown that
significant muscle fatigue. Fatigue causes a fall in the mean fre-
our fatigue protocol for the longer movement distance reduced
quency of the EMG spectrum as a consequence of changes in con-
peak movement velocity by approximately 10%. The effect of fa-
duction velocity in the muscle fibers. However, Kirsch and Rymer
tigue on peak velocity was less than 10% for the shorter move-
(1987) showed that 10 min of rest following the fatigue protocol
ments, and so we chose not to conduct this experiment at the
returns the mean power frequency of the EMG signal to the pre-
shorter distances. To assist the subject, we monitored peak veloci-
fatigue levels in both the biceps and the brachialis muscles. Thus,
ty and reported its value to the subject after each movement, along
after 10 min, any changes in the electromyogram induced by fa-
with encouragement, if necessary, to move faster or slower.
tigue can be attributed to factors other than changes in conduction
velocity.
Subjects practiced the whole experimental protocol once be-
Isometric fatigue protocol repetition 1
fore they took part in the experiment. The time interval between
practice and experiment was at least 48 h. Subjects did not do any
The fatigue protocol consisted of 20 repetitions of a 50% MVC
intensive exercise before they participated in the experiment.
isometric flexion at the elbow joint for 25 s, followed by 5 s of
rest between the repetitions.
Data analysis
Rest period 1
The digitized EMG signals were full wave rectified and filtered
with a 10-ms moving average window for plotting the EMG time
After the fatigue protocol, the subject rested for ten minutes to al-
series data (Fig. 1, Fig. 2, Fig. 5). The data in these figures were
low muscle membrane conduction velocity to return to normal
all aligned with respect to the onset of the agonist EMG. The fol-
values (Kirsch and Rymer 1987). In another group of four sub-
lowing parameters were calculated.
jects, we used only a 2-min recovery period. We used two recov-
ery time periods so that we could both minimize the effects of re-
covery time on motor performance (2-min recovery protocol), and
Isometric parameters
collect data in which the EMG signal is not affected by changes in
conduction velocity (10-min recovery protocol). Since the shorter
1. Maximal elbow torque (Nm): the maximal elbow torque in the
recovery period causes ambiguities in interpreting EMG changes,
isometric contraction.
the EMG signal is not analyzed for this recovery time period.
2. Integrated EMG (arbitrary unit): the EMG was integrated over
However, the magnitude of the kinematic changes was larger for
200 ms centered about the time of peak isometric elbow
the shorter recovery interval and allows us to demonstrate the ef-
torque. We chose this time interval since it was the longest
fectiveness of this fatigue protocol.
time interval that all subjects maintained a steady-state maxi-
mum contraction in the fatigued condition.
3. Torque/EMG ratio: the peak of the torque in the 50% isometric
Fast fatigued flexions at distance 1
condition divided by the EMG integrated over 200 ms centered
about the time of peak isometric elbow torque. One data set
The subject performed 11 voluntary elbow flexion movements as
was lost to equipment malfunction, and so these data were only
fast as possible either over 20° or over 60°. The order in which the
collected on seven subjects.
distances were performed was counterbalanced such that half of
the subjects performed the 20° movement before the 60° move-
ment. These movements were analyzed to determine the mechani-
Movement parameters
cal and EMG parameters of fatigued muscle when completing vol-
untary movements.
1. Movement time (ms): the time interval from 1% of peak accel-
eration to the time when the velocity falls to 5% of peak veloc-
ity.
2. Peak velocity (Vmax deg/s): The largest value of movement ve-
locity.
4
3. Peak elbow torque (Nm): for voluntary movement, elbow
Changes in muscle torque and EMG in maximal
torque was the maximum muscle torque during the accelera-
voluntary contractions
tion phase of the movement. Elbow torque was calculated by
multiplying acceleration by the effective moment of inertia
On average there was a statistically significant decline of
(forearm plus manipulandum).
4. Q30 (arbitrary unit): the integral of the agonist EMG signal 21.2% in flexion torque [meanÄ…SE pre-fatigue=
from the visually marked onset to 30 ms thereafter. This pa-
69.1Ä…4.2 Nm, fatigued=54.5Ä…4.3 Nm, t(7)=5.98,
rameter is used to characterize the initial slope of the agonist
P=0.001]. From this fact we conclude that the protocol
EMG burst.
developed by Kirsch and Rymer (1987) was effective in
5. Qag (arbitrary unit): the integral of the agonist EMG from the
marked onset to the time of peak velocity. This parameter is producing fatigue in the agonist biceps muscle. This re-
used to characterize the area of the first agonist EMG burst
duction in maximum flexion torque is shown for a repre-
which is responsible for the limb accelerating towards the tar-
sentative subject in Fig. 1A. Even though the fatigue
get.
protocol did not call for strong contraction of the exten-
6. Qant (arbitrary unit): the integral of the antagonist EMG from
the marked onset of the agonist burst to the end of the move- sor muscles, maximum extension torque was reduced
ment (the distance at which velocity drops below 5% of Vmax).
4.1% following the fatigue protocol as shown in Fig. 1B,
This parameter is used to characterize the area of the antago-
but the decline was not statistically significant [meanÄ…
nist burst.
SE pre-fatigue=43Ä…2.66 Nm, fatigued=41.2Ä…3 Nm,
7. Agonist EMG peak amplitude (arbitrary unit): the EMG peak
t(7)=1.18, P=0.278]. The integrated EMG during MVC
amplitude was measured as the maximal value in the filtered
and averaged agonist burst. activity was not statistically significantly different be-
8. Cant ms: the centroid of the antagonist burst. This value is cal-
tween the fatigued and unfatigued conditions for either
culated by the following equation:
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
(1)
agonist muscle, the ratio of torque to EMG, the measure
usually considered the defining characteristic of physio-
u (t)=1 if emg(t)e"K emgmax
u (t)=0 if emg(t)than the unfatigued state in the 50% MVC condition
MT is movement time, t0 is the time of start of acceleration,
[mean ratioÄ…SE pre-fatigue=85.96Ä…13.32; mean ratio fa-
emg(t) is the EMG signal in the lateral head of triceps, K is
tigued=55.12Ä…10.3, t(6)=2.73, P=0.03].
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 simi-
lar to locating the peak of the EMG burst but is less sensitive
Comparison between fatigued movements
to the details of the EMG waveform.
and unfatigued movements
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
Fatigue decreased movement velocity and increased
Cant (0.75). The centroid of the agonist burst is a measure of
movement time. The data from one representative sub-
the duration of the biceps EMG burst.
ject are shown in Fig. 2. The peak elbow torque in the
acceleration phase of the movement decreased. The ini-
Statistical analysis
tial rising phase of the EMG (Q30) in the agonist is simi-
For the maximal voluntary contractions, a paired t-test was per- lar. However, the rate of rise was not sustained with fa-
formed to examine the effects of fatigue on the maximal elbow
tigue and, as a consequence, the EMG peak amplitude of
torque and the EMG integral for both flexion and extension con-
the biceps muscle decreased. These observations apply
tractions. A paired t-test was also used to compare the
to both 20° and 60° movements. The late component of
torque/EMG ratio in the non-fatigued condition and the fatigued
condition. For the isotonic movements, a two-way repeated-mea- the antagonist burst (beginning approximately 160 ms
sures ANOVA was used to examine the effects of fatigue and
after the agonist onset) is delayed in both the lateral head
movement distance. A paired t-test was performed to compare the
of triceps and the long head of triceps as a consequence
intentionally slowed unfatigued movements with the fatigued
of fatigue.
movements.
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
Results
distance. Movement time significantly increased by
7.38% (averaged over 20° and 60°), and was longer for
The results are divided into four parts. Part 1 describes
longer movements. Movement time can be partitioned
the effects of fatigue on isometric muscle torque and
into both acceleration time and deceleration time. Accel-
EMG. Part 2 describes the effects of fatigue on move-
eration time increased significantly while deceleration
ment kinematics and EMG patterns. Part 3 compares the
time was unchanged. There was a statistically significant
EMG patterns of intentionally slowed unfatigued move-
interaction between fatigue and distance for peak move-
ments with those of fatigue-slowed movements. Part 4
ment velocity. As such, paired t-tests were performed on
compares the kinematic effects of a 2-min recovery in-
both the 20° movements and the 60° movements. This
terval with that of a 10-min recovery interval.
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 contrac-
tions in flexion (A) and exten-
sion (B) for a representative
subject. The data depict elbow
torque, biceps EMG, and later-
al head of triceps EMG. The
data are from subject 7
P=0.003] while the decrease in peak velocity in the 20° Comparison between the intentionally slowed unfatigued
movements (4.89%) did not quite reach statistical signif- movements and fatigued movements
icance [t(7)= 2.16, P=0.067]. Peak elbow torque
dropped significantly (by 15.22% averaged over 20° and Before performing the fatigue protocol, subjects per-
60°). Q30 dropped by 24.95% (averaged over 20° and formed 20 movements over 60° at a peak velocity that
60°) as a result of fatigue but this result was not statisti- was 10% less than their unfatigued maximal speed. From
cally significant. Inspection of the data of individual sub- this set of 20 movements, we later selected those that
jects showed that Q30 dropped by as much as 50% in one were closest to the maximal speed of the fatigued move-
subject, and not at all in other subjects. The agonist peak ments. The average number of trials that were selected as
amplitude dropped significantly (by 30.53% averaged the  intentionally slowed pre-fatigued movements was
over 20° and 60°). The integrals of the agonist burst 10 (range 6 17).
(6.83% decrease) and antagonist EMG burst (2.06% de- Intentionally slowed pre-fatigued movements were ki-
crease), averaged over 20° and 60°, did not change sig- nematically indistinguishable from fatigued movements
nificantly. However, the timing of the centroid of the ag- but the patterns of muscle activation differed as shown in
onist burst (14% change) and the antagonist burst (12% the time series plot for one subject in Fig. 5.
change), averaged over 20° and 60°, occurred signifi- A paired t-test was used to determine if there were
cantly later in the fatigued condition. significant differences in selected movement and EMG
parameters between fatigued and intentionally slowed
pre-fatigued movements. There were no significant dif-
ferences in movement amplitude, movement time, peak
velocity, Q30, the peak of the agonist burst or the integral
6
Fig. 2 Averaged position, ve-
locity, elbow torque, biceps
(agonist) EMG, lateral head of
triceps (antagonist), and long
head of triceps EMG for move-
ments over 20° (A) and 60°
(B). The data are averaged over
11 trials. Movements were per-
formed prior to the fatiguing
protocol (pre-fatigue) and fol-
lowing the fatigue protocol (fa-
tigued). The data are from sub-
ject 4
7
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 indi-
cates an increase in EMG burst duration, and is consis-
tent 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 move-
ments than the intentionally slowed pre-fatigued move-
ments. This is consistent with the fact that it was an in-
crease 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 pre-
fatigue condition, the fatigued condition and in the inten-
tionally slowed pre-fatigued condition.
Effect of fatigue recovery interval
All the fatigue measures above were made after the sub-
jects 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 spec-
trum 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 cal-
culated 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-fa-
tigued 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 kinemat-
ic 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 al-
lows not only recovery in muscle fiber conduction veloci-
ty but also substantial recovery in kinematic performance.
Reduction of muscle fiber conduction velocity in-
creases 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 meanÄ…SE
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 antago-
nist burst (D), the centroid of
the agonist (E), and the antago-
nist (F) for 20° (dashed line)
and 60° (solid line) movements
pre-fatigue and fatigued. The
data are averaged over eight
subjects. The data are
meanÄ…SE
Table 1 Effects of fatigue and distance. The results of two-way over two different distances. All degrees of freedom for the statis-
factorial repeated measures ANOVA on eight subjects comparing tical analysis are 1, 7
pre-fatigue movements and fatigued movements and movements
Fatigue Distance Interaction
Pre vs Post 20° vs 60° Fatigue by Distance
FP FP FP
Movement amplitude 0.38 0.555 7942 0.000 0.029 0.869
Movement time 35.14 0.001 187.1 0.000 0.46 0.520
Peak velocity 12.79 0.009 2002 0.000 26.68 0.001
Acceleration time 11.85 0.011 81.81 0.000 0.46 0.52
Deceleration time 0.02 0.882 90.99 0.000 0.26 0.63
Peak elbow torque 74.63 0.000 14.55 0.007 0.91 0.371
Q30 3.33 0.111 0.46 0.519 2.95 0.130
Agonist peak 13.66 0.008 8.22 0.024 0.01 0.925
Qag 1.30 0.291 39.35 0.000 0.28 0.614
Qant 0.32 0.591 10.61 0.014 0.26 0.624
Centroid agonist 14.94 0.006 111.9 0.000 0.05 0.833
Centroid antagonist 46.84 0.000 183.1 0.000 0.35 0.572
9
Fig. 6 The centroid of the agonist (A) and the centroid of the an-
tagonist (B) in the pre-fatigue condition, the fatigued condition
and in the intentionally slowed pre-fatigue movement condition.
The data are meanÄ…SE
This increase could be confused with an increase in re-
cruitment 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 re-
sults, since their interpretation is open to question.
Discussion
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 re-
quired 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: pro-
longed 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 hypothe-
sis was confirmed by the data. One additional finding is
that the peak agonist EMG is reduced which was not pre-
dicted. This change would tend to reduce muscle force
and therefore speed, which would be kinematically non-
compensatory. On the other hand, by reducing muscle
activation, this would tend to slow the progression of fa-
Fig. 5 Averaged position, velocity, elbow torque, biceps EMG tigue, an effect that might be desirable but is incompati-
(agonist) and lateral head of triceps EMG (antagonist) for inten-
ble with kinematic compensation.
tionally slowed pre-fatigue movements and fatigued movements.
Our second hypothesis was that the EMG changes
The data are from the same subject as in Fig. 2
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 fa-
Intentionally slowed Fatigued Significance
tigued movements and inten-
tionally slowed pre-fatigue
MeanÄ…SE MeanÄ…SE tP
movements. The results of
paired sample t-tests on the da-
Movement amplitude 62.18Ä…0.41 62.8Ä…0.61  1.15 0.287
ta of eight subjects when com-
Movement time 711Ä…15 725Ä…19 1.68 0.137
paring the intentionally slowed
Peak velocity 183Ä…4 185Ä…4 0.93 0.386
pre-fatigue movements with the
Q30 4.00Ä…0.623 4.72Ä…0.934 1.41 0.201
fatigued movements. The data
Peak of agonist burst 0.999Ä…0.198 0.995Ä…0.171 0.04 0.968
are averaged over eight sub-
Integral of agonist burst 156.1Ä…22.8 190.1Ä…27.9 2.44 0.045
jects (meanÄ…SE)
Integral of antagonist burst 245.1Ä…39.3 253.6Ä…33.8 0.71 0.499
Centroid of agonist burst 163Ä…8 178Ä…9 3.56 0.009
Centroid of antagonist burst 436Ä…10 461Ä…10 2.78 0.027
greater for longer distance movements than for shorter increase in EMG during a 50% MVC isometric contrac-
distance movements. However, the EMG did not show tion. Fatigue also produced a decrease in peak elbow
greater changes for shorter movements than for longer torque during isotonic movements without a significant
movements, which is in contrast to the findings of change in the area of the agonist burst. Both findings re-
Berardelli and colleagues (1984). This hypothesis, there- veal a decrease in the torque/EMG relationship. Such ob-
fore, was not confirmed by the data. servations are also consistent with a number of other
We tested a third hypothesis that the EMG patterns studies (Edwards and Lippold 1956; Hagberg 1981;
associated with fatigue-induced slowing would differ Maton and Gamet 1989; Garland et al. 1994; Miller et al.
from those of intentional slowing. This hypothesis was 1996; Potvin 1997). These findings define the presence
confirmed by the data. of a peripheral fatigue component, a diminished ability
These findings question whether the reduction in of muscle to produce force.
torque during movement is exclusively a consequence of
 peripheral, contractile fatigue , i.e. a decrease in the ca-
pacity of the biceps to generate force. It might also re- Central fatigue and rules for muscle activation
present a change in the way the CNS activates the mus-
cle that would serve to slow the progression of fatigue. The presence of peripheral fatigue does not rule out cen-
An additional interesting finding is the fact that tral fatigue as an additional factor. Central fatigue during
movement velocity was reduced by less than 10% after exercise has been defined by Gandevia et al. (1995a) as:
ten minutes of recovery. This finding is consistent with  The decrease in muscle force attributable to a decline in
that of Raastad and Hallén (2000), who showed a motoneuronal output (p. 281). Three of our measures of
12 14% reduction in isokinetic performance following a the strength of activation, Q30, Qag and Qant were slightly
high-intensity exercise protocol, and a 6 7% reduction reduced by fatigue, but none of the changes reached sta-
after a moderate intensity protocol with a recovery time tistical significance. The largest and most variable reduc-
of 5 20 min. The finding is also supported by the work tion was in Q30, which suggests that some subjects re-
of Miller et al. (1987), who showed that a 4-min fatigu- duce the initial excitation of the muscle when fatigued
ing protocol can reduce MVC to less than 10% but that it but others do not. The peak of the agonist burst was sig-
returns to almost 90% after 10 min of recovery. We also nificantly reduced by fatigue and this could have reduced
used a large load to increase the effects of fatigue as peak muscle force. Hence, using Gandevia's definition,
much as possible during the movement. Thus we believe there is evidence for central fatigue in only one of our
that we achieved a level of fatigue that was typical of four measures of motoneuronal output.
what has been done by many others. These results all However, the timing of the EMG bursts in both ago-
demonstrate that despite the fact we know how to fatigue nist and antagonist muscles was changed by fatigue to a
a muscle in order to produce an arbitrary decrement in degree that could not be predicted by the way subjects
isometric force, it is exceedingly difficult to produce intentionally slow their movements. Fatigue prolonged
substantial decrements in movement speed, while also the agonist burst. If the level of muscle activation is un-
allowing sufficient time for conduction velocity to return changed, this increases the force output of the muscle.
to normal. 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
Peripheral fatigue the changes seen when moving a heavier inertial load in
the unfatigued state. However, the compensation is not
We can draw conclusions similar to those of Kirsch and complete and the fatigued movement is, never the less,
Rymer (1987), and Griffin et al. (1998) about decreases slower than the unfatigued movement.
in dynamic torque/EMG ratios from our isometric and Since the fatigued movement time is greater than that
movement data. When fatigued, our subjects showed an of an unfatigued movement, delay of the antagonist is
11
biomechanically appropriate. However, fatigue delayed the reserve does not exist. These experiments do not al-
the antagonist burst to a degree that exceeded the amount low us to decide this issue. That the reserve does not ex-
we would expect from the antagonist timing of unfa- ist is supported by the fact that Q30 was the same for
tigued movements of a similar speed. Furthermore, since both short and long movements in the unfatigued state.
the fatigued movement's prolongation is due almost en- Additionally, it has been shown that subjects can pro-
tirely to prolongation of the acceleration time, and this is duce maximum or near maximum voluntary activation of
not true of unfatigued movements with equal movement their muscles under laboratory conditions (see Gandevia
times, it is also appropriate that the antagonist burst that et al. 1998), thus suggesting that under these conditions,
leads to decelerating torque be slightly more delayed. a reserve does not exist.
This additional delay of the antagonist burst, like the Finally, what is the relationship between the fatigue
prolongation of the agonist burst, tends to increase we have studied and the fatigue that is experienced as
movement speed and may prevent stopping the move- the consequence of sustained hard work or exercise? One
ment too soon. The limb's final resting position depends possibility is that exercise fatigue (as we might call it) is
on coactivation of the flexor and extensor muscles to simply greater and less well compensated. If so, were we
create a position of equilibrium. To perform an accurate to repeat our fatigue protocol enough times, we would
movement, the point at which movement speed reaches get larger and more significant effects. The protocol we
zero during the deceleration phase should coincide with used was difficult and unpleasant so such an experiment
this equilibrium position. This requires a delay in brak- would not be easy to perform. Another possibility is that
ing and hence a delay in antagonist onset. using a less intense and noxious protocol over a longer
How should we describe these changes? They do not period of time would produce more profound and less
fit Gandevia's definition of central fatigue since there is compensated fatigue. This should be explored. A third
no overall decline in motoneuronal output. In fact, they possibility is that the behavioral consequences of exer-
do not represent central fatigue if by that term, we wish cise fatigue are different from the slowing of elbow flex-
to imply something that diminishes motor performance. ions that we are measuring here. This would suggest that
We suggest that these changes represent a  central fa- exercise fatigue is not simply a loss of muscle strength
tigue strategy. By this we mean that the CNS changes due to muscular and neural factors, but a loss of coordi-
the patterns of muscle excitation in order to reduce the nation among muscles, a very different effect, and one
effects of peripheral fatigue (as in agonist prolongation) that is not expressed by the study of single-joint move-
and prevent moving incorrect distances due to peripheral ment. This too should be explored.
fatigue (as in antagonist delay). The reduction seen in
Acknowledgements This study was supported in part by the Na-
peak agonist EMG might also be considered part of a
tional Institute of Arthritis and Musculoskeletal and Skin Diseases
central fatigue strategy. This reduction in peak agonist
Grant R01-AR 33189 and by the National Institute of Neurologi-
EMG could be attributable to lower motoneuron firing
cal and Communicative Disorders and Stroke Grants K04-NS
rates, so-called muscle wisdom (Marsden et al. 1983),
01508, R01-NS 28127 and RO1-NS40902. We would also like to
acknowledge the valuable comments of Dr. Ziaul Hasan, and the
that are sufficient to fully activate a muscle in the fa-
advice of Dr. Paolo Bonato and Dr. David Vaillancourt.
tigued state secondary to the concurrent reduction seen
in muscle fiber relaxation rate when fatigued. This might
serve to prevent neuromuscular transmission failure.
References
It is also worth noting something that we did not find
to be part of a central fatigue strategy. We know that sub-
Berardelli A, Rothwell JC, Day BL, Kachi T, Marsden CD (1984)
maximal isometric torque can be preserved in a fatigued
Duration of the first agonist EMG burst in ballistic arm move-
ments. Brain Res 304:183 187
muscle by stronger activation of the muscle. Our second
Bigland-Ritchie B, Johansson R, Lippold OCJ, Smith S, Woods JJ
hypothesis raises the question of whether subjects have a
(1983a) Changes in motoneurone firing rates during sustained
reserve of performance that they can use, despite instruc-
maximal voluntary contractions. J Physiol (Lond) 340:335 346
tions to move as fast as possible. This reserve of perfor-
Bigland-Ritchie B, Johansson R, Lippold OCJ, Woods JJ (1983b)
mance can usually be exploited only by extensive prac- Contractile speed and EMG changes during fatigue of sus-
tained maximal voluntary contractions. J Neurophysiol
tice (Corcos et al. 1993). If true, then in the presence of
50:313 324
peripheral fatigue, subjects could, in theory, compensate
Corcos DM, Gottlieb GL, Agarwal GC (1989) Organizing princi-
more fully by harnessing that reserve. To do this they
ples for single-joint movements: II. A speed-sensitive strategy.
would increase the initial firing rates and number of re- J Neurophysiol 62:358 368
Corcos DM, Jaric S, Agarwal, GC, Gottlieb GL (1993) Principles
cruited motor units and this would be observed as an in-
for learning single-joint movements I. Enhanced performance
crease in Q30. We had predicted that if this were the case,
by practice. Exp Brain Res 94:499 513
compensation would be greater for shorter movements
De Luca CJ (1985) Myoelectric manifestations of localized mus-
than longer ones. This was based on the rationale that
cular fatigue in humans. CRC Crit Rev Biomed Eng 11:251
279
shorter movements require lower forces and therefore
Edwards RG, Lippold OC (1956) The relation between force and
less muscle activation, leaving a reserve of motor units
integrated electrical activity in fatigued muscle. J Physiol
that could be recruited. We did not find this. Hence, ei-
132:677 681
ther our subjects had a reserve that they were not suffi-
Enoka RM, Stuart DG (1992) Neurobiology of muscle fatigue. J
ciently motivated to use, or contrary to our supposition, Appl Physiol 72:1631 1648
12
Gandevia SC, Allen GM, McKenzie DK (1995a) Central fatigue: peak rates of motoneuron discharge and slowing of discharge
critical issues, quantification and practical implications. In: during fatigue. In: Desmedt JE (ed) Motor control mechanisms
Gandevia SC, Enoka RM, McComas AJ, Stuart DG, Thomas in health and disease. Raven Press, New York, pp 169 211
CK (eds) Fatigue: neural and muscular mechanisms. Plenum Maton B, Gamet D (1989) The fatigability of two agonistic mus-
Press, New York, pp 281 294 cles in human isometric voluntary submaximal contraction: an
Gandevia SC, Enoka RM, McComas AJ, Stuart DG, Thomas CK EMG study. II. Motor unit firing and recruitment. Eur J App
(eds) (1995b) Fatigue: neural and muscular mechanisms. Ple- Physiol 58:369 374
num Press, New York Miller KJ, Garland SJ, Ivanova T, Ohtsuki T (1996) Motor-unit
Gandevia SC, Herbert RD, Leeper JB (1998) Voluntary activation behavior in humans during fatiguing arm movements. J Neu-
of human elbow flexor muscles during maximal concentric rophysiol 75:1629 1636
contractions. J Physiol: 512.2:595 602 Miller RG, Giannini D, Milner-Brown HS, Layzer RB, Koretzky
Garland SJ, Enoka RM, Serrano LP, Robinson GA (1994) Behav- AP, Hooper D, Weiner, MW (1987) Effects of fatiguing exer-
ior of motor units in human biceps brachii during a submaxi- cise on high-energy phosphates, force and EMG: evidence for
mal fatiguing contraction. J App Physiol 76:2411 2419 three phases of recovery. Muscle Nerve 10:810 821
Gottlieb GL, Corcos DM, Agarwal GC (1989) Organizing princi- Mustard BE, Lee RG (1987) Relationship between EMG patterns
ples for single-joint movements: I. A speed-insensitive strate- and kinematic properties for flexion movements at the human
gy. J Neurophysiol 62:342 357 wrist. Exp Brain Res 66:247 256
Griffin L, Garland SJ, Ivanova T (1998) Discharge patterns in hu- Pfann KD, Hoffman DS, Gottlieb GL, Strick PL, Corcos DM
man motor units during fatiguing arm movements. J App (1998) Common principles underlying the control of rapid,
Physiol 85:1684 92 single degree-of-freedom movements at different joints. Exp
Hagberg, M. (1981) Muscular endurance and surface electromyo- Brain Res 118:35 51
gram in isometric and dynamic exercise. J App Physiol: Resp Potvin JR (1997) Effects of muscle kinematics on surface EMG
Env Exer Physiol 51:1 7 amplitude and frequency during fatiguing dynamic contrac-
Jiang, H. Gottlieb, GL, Corcos, DM (1996) Effects of fatigue on tions. J App Physiol 82:144 151
voluntary elbow flexion movements. Soc Neurosci Abstr Raastad T, Hallén J (2000) Recovery of skeletal muscle contractil-
22:129 ity after high- and moderate-intensity strength exercise. Eur J
Kirsch RF, Rymer WZ (1987) Neural compensation for muscular Appl Physiol 82:206 214
fatigue: evidence for significant force regulation in man. J Scalzitti DA (1994) Effects of age and gender on quadriceps fem-
Neurophysiol 57:1893 1910 oris muscle force production and anaerobic metabolism. Mas-
Lucidi CA, Lehman SL (1992) Adaptation to fatigue of long dura- ter thesis, University of Illinois at Chicago
tion in human wrist movements. J App Physiol 73:2596 2603 Tschoepe BA, Sherwood DE, Wallace SA (1994) Localized mus-
Marsden CD, Meadows JC, Merton PA (1983)  Muscular wis- cular fatigue duration, EMG parameters and accuracy of rapid
dom that minimizes fatigue during prolonged effort in man: limb movements. J Electromyogr Kinesiol 4:218 229