Strategies for delaying
muscle failure during
repetitive dynamic
performance of human skeletal muscle.
M. B. Kebaetse1 S. A. Binder-Macleod2
1 Interdisciplinary Programs in Biomechanics and Movement Science, McKinly Laboratory, University of Delaware, Newark, Delaware, USA., 41429@udel.edu
2 Department of Physical Therapy, University of Delaware, Newark, Delaware, USA., sbinder@udel.edu
The purpose of this study was to identify
the best stimulation strategy for delaying muscle fatigue and maximizing
dynamic muscle performance from the human quadriceps femoris muscle. Data were collected from 18 healthy subjects
(12 females), ages 21-35 years. The quadriceps muscle was stimulated using
20-Hz constant-frequency trains (CFT20), CFT40, or 36-Hz novel stimulation
trains consisting of pairs of closely spaced pulses called doublets
(doublet-frequency trains (DFT36)). In
addition, two patterns using combinations of trains were tested. The combinations were: 15 CFT20s followed by
DFT36s (CFT20-DFT36), and 15 DFT36s followed by CFT20s (DFT36-CFT20). Each
pattern was tested on a separate day. Stimulation began with the knee in 90º of
flexion and the train was automatically cut off when the knee reached a target
angle of 40º. Testing was stopped when
the subject failed to reach the target three consecutive times. Targets were
reached (mean±SD) 35.7±12.7, 43.8±19.7, 45.1±17.5, 56.3±33.1, and 26.8±6.1
times for the CFT20, CFT40, DFT36, CFT20-DFT36, and DFT36-CFT20, respectively.
The strategy using the DFT36 followed by the CFT20 produced significantly more
successful contractions than any of the other stimulation patterns. These results showed that the use of
lower-frequency CFTs followed by higher-frequency stimulation trains delayed
muscle failure during repetitive, non-isometric contractions.
FES typically
activates muscles with equally spaced pulses arranged in stimulation patterns
called constant frequency trains (CFTs). Recently, train patterns that vary the
frequency within the stimulation train have been shown to produce greater
forces from skeletal muscles during isometric contractions [1,2,4,11] and
produce greater peak power and excursions during non-isometric contractions
[5,8,10] than CFTs, particularly when the muscle is fatigued. The most commonly
studied variable-frequency trains (VFTs) have used a high-frequency burst at
the beginning of the train, followed by a low-frequency portion of equally
spaced pulses [4,9,12]. Interestingly,
our laboratory has recently identified a slightly different pattern of pulses
that appears capable of producing greater force augmentation than the commonly
tested VFTs [6,7]. These trains use
closely spaced (~5 ms) pairs of pulses (doublets) separated by longer intervals
(inter-doublet intervals) and we have termed these trains doublet-frequency
trains (DFTs) [6,7].
Although varying
the frequency within the train may allow skeletal muscles to produce greater
performance than using CFTs, this augmented performance does not occur without
some cost. Specifically, repetitive isometric activation with VFTs or DFTs has
been shown to be more fatiguing than repetitive activation with CFTs
[3,4,6]. However, recent evidence
suggests that repetitive non-isometric activation of muscles with CFTs followed
by DFTs may produce better performance than activation with CFTs alone or DFTs
alone [7]. The purpose of this study
was, therefore, to investigate the effect of combining different train patterns
on repetitive dynamic quadriceps muscles contraction to determine the
stimulation pattern that maximizes the muscle’s performance.
Data were
collected from eighteen healthy subjects (12 females) ranging in age from 21 to
35 years. Subjects were seated on a
computer-controlled dynamometer (KinCom III 500-11, Chattecx, Chatanooga, TN)
with their hips flexed to ~85°. Self-adhesive stimulating electrodes were
placed over the rectus femoris and vastus medialis motor points. A Grass S8800 stimulator with a SIU8T
stimulus isolation unit was used for stimulation.
Stimulation
train patterns: Five different stimulation train
patterns were tested using 3 basic trains
(Figure 1). Each train was ≤1200 ms in duration. Each pattern was tested on a separate
day. Sessions were at least 48 hours
apart. Each train was identified by the pattern (CFT or DFT) followed by the
train’s mean frequency in Hz (total number of pulses in a 1-s period). The
train patterns were a CFT20, a CFT40, a DFT36 (consisted of a 5-ms doublet
interpulse interval and a 50-ms interdoublet interval), a CFT20-DFT36
combination pattern (15 CFT20s followed by DFT36s), and a DFT36-CFT20
combination pattern (15 DFT36s followed by CFT20s).

Figure 1. The three basic trains used to make the five
stimulation patterns. Each vertical line represents a 600 µs pulse. Trains
could continue for up to 1200 ms.
Experimental
Testing: Testing
first involved measuring the subject’s maximum voluntary isometric contraction
(MVIC) force for the quadriceps muscle with the knee at 90° of flexion. The
stimulation intensity was then set while the knee was held at 90° of flexion so
that a 1000-ms CFT20 produced 20% of the subject’s MVIC force. The intensity
was not changed for the remainder of the test. The dynamometer was then
switched to the isotonic mode, which was set to provide a load equal to 50% of
the subject’s electrically elicited force produced by the 1000-ms CFT (i.e.,
10% of the subject’s MVIC force). A predetermined train pattern was delivered
to the muscle. Stimulation was interrupted when the knee reached the
40°-flexion target angle (i.e., a 50° range of motion). Stimulation was repeated every 2000 ms. Testing was terminated when the leg failed
to reach the target 3 consecutive times.
A One-way
repeated measure analysis of variance (ANOVA) was used to determine the effect
of stimulation train pattern (CFT40, CFT20, DFT36, CFT20-DFT36, or DFT36-CFT20)
on the number of times the target was reached. Post-hoc paired testing compared
the CFT20-DFT36 train combination to each of the other patterns.

Figure 2. Number of times
(means and S.E.) the target was reached with each stimulation pattern.
Significance is shown for the CFT20-DFT36 vs. the CFT20, DFT36, CFT40, and
DFT36-CFT20 . *p≤0.05; **p≤0.01.
The ANOVA showed
significant differences in the number of times each pattern produced the
targeted excursion (p≤0.001; F=8.012). The CFT20-DFT36 train combination
produced a significantly greater number of contractions than all other train
patterns (see Figure 2).
In the present
study, we investigated the effect of using individual or combined train
patterns on repetitive dynamic contractions during knee extension. Consistent
with our hypothesis, repetitively activating the quadriceps femoris muscles
with the CFT20 immediately followed by the DFT36 resulted in the leg completing
the targeted excursion the most times.
Future studies should evaluate the effectiveness of additional train
combinations and frequencies. In
addition, the effects of more sophisticated switching strategies from one train
to the next and the effects of such patterns when testing paralyzed human
skeletal muscles need to be explored.
This work was supported by NIH Grant HD-41254 to Dr. Binder-Macleod.
[1] L. Bevan., Y. Laouris., M. Reinking, and
D.G. Stuart, “The Effect of the Stimulation
Pattern on the Fatigue of Single Motor Units in Cats,” J. Physiol.
(Lond), Vol. 449, pp. 85-108, 1992.
[2] S.A. Binder-Macleod, and C.B. Barker III,
“Use of Catchlike Property of Human Skeletal Muscle Fatigue,” Muscle Nerve,
Vol. 14, pp. 850-857, 1991.
[3] S.A. Binder-Macleod, and D.W. Russ,
“Effects of Activation Frequency and Force on Low-frequency Fatigue in Human
Skeletal Muscle,” J. Appl. Physiol.,
Vol. 86, pp. 1337-1346, 1999.
[4] S.A. Binder-Macleod, S.C.K. Lee, D.W. Russ, and L.J. Kucharski,
“Effects of Activation Pattern on Human Skeletal Muscle Fatigue,” Muscle Nerve,
Vol. 21, pp. 1145-1152, 1998.
[5] S.A. Binder-Mcleod, and S.C.K. Lee,
“Catchlike Property of Human Skeletal Muscle During Isovelocity Movements,” J.
Appl Physiol., Vol. 80, pp. 2051-2059, 1996.
[6] S.A. Binder-Macleod, and W.B. Scott,
“Comparison of fatigue produced by various electrical stimulation trains,” Acta Physiol. Scand., Vol. 172, pp. 195-203,
2001.
[7] M.B. Kebaetse, S.C.K. Lee, and S.A.
Binder-Macleod, “A novel stimulation pattern improves performance during
repetitive dynamic contractions,” Muscle Nerve, Vol. 24, pp. 744-752, 2001.
[8] S.C.K. Lee, C.N. Becker, and S.A. Binder-Macleod,
“Catchlike-Inducing Train Activation of Human Muscle During Isotonic
Contractions: Burst Modulation,” J. Appl. Physiol., Vol. 87, pp. 1758-1767,
1999.
[9] G.H. Otazu, R. Futami, and N.A.
Hoshimiya, “A muscle activation model of variable stimulation frequency
response and stimulation history, based on positive feedback in calcium
dynamics,” Biol Cybern., Vol. 84, pp.193-206, 2001.
[10]T.G.
Sandercock, and C.J. Heckman, “Doublet Potentiation During Eccentric and
Concentric Contractions of Cat Soleus Muscle,” J. Appl. Physiol., Vol. 82, pp.
1219-1228, 1997.
[11] R.B. Stein, and F. Parmiggiani, “Optimal
Motor Patterns for Activating Mammalian Muscle,” Brain Res., Vol. 175, pp.
372-376, 1979.
[12]
E. Van
Lunteren, and C.B. Sankey, “Catchlike property of rat diaphragm: subsequent
train frequency effects in variable-train stimulation,” J. Appl. Physiol., Vol. 88, pp. 586-598, 2000.