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Department of Physiology, Northwestern University Medical School, Chicago, Illinois 60611
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Sandercock, Thomas G., and C. J. Heckman. Doublet
potentiation during eccentric and concentric contractions of cat soleus
muscle. J. Appl. Physiol. 82(4):
1219-1228, 1997.
The addition of an extra stimulus pulse, or
doublet, at the beginning of a low-frequency train has been shown to
substantially increase isometric force. This study examined the effects
of muscle movement on this doublet potentiation. The soleus muscles of
anesthetized cats were stimulated at 10 Hz for 1 s, with and without an
added doublet (0.01-s interval). Isovelocity releases reduced but did
not eliminate peak and early doublet potentiation (average 0.0-0.5
s after the doublet). Large releases, >0.4 s after the doublet,
completely abolished sustained doublet potentiation (average
0.5-1.0 s after the doublet). In contrast, early isovelocity
stretches boosted peak doublet potentiation. Yet, large stretches later
in the stimulus almost completely eliminated sustained doublet
potentiation. This suggests that a different mechanism is responsible
for early and sustained doublet potentiations. Because peak and average
initial doublet potentiation were not strongly affected by movement,
doublets still offer a viable control strategy to increase force during movement while minimizing the number of stimulus pulses.
catch; motor control; fatigue
INTRODUCTION WHEN A WHOLE MUSCLE, or a motor unit, is stimulated
with a low-frequency train, the addition of a single extra pulse, or
doublet, ~0.01 s after the first pulse of the train can dramatically
increase isometric tension (7). Under optimal conditions,
the additional tension from a doublet lasts for several seconds and
greatly exceeds the tension produced by a single twitch.
The terminology used to describe doublets has varied. Burke et al. (7)
referred to the phenomenon as "catchlike" to distinguish it from
the catch property seen in invertebrate muscles. The
catchlike property appears to be an extreme example of the nonlinear
summation of force from single stimulus pulses that was first reported
by Cooper and Eccles (10) and then was studied more systematically by
other investigators (8, 11, 17, 24). Investigators recording from
spontaneously firing motor units have noticed that a train will
sometimes begin with two or more closely spaced impulses, followed by
pulses with longer interimpulses (2, 11, 25). Such a train is capable
of producing the catchlike property described by Burke et al. (7). They
have referred to the pulses with short interpulse intervals as
doublets. Because the terminology "nonlinear summation of force"
and catchlike are rather awkward, the same phenomena will be referred
to here as "doublet potentiation."
Conceivably, the extra force provided by doublets can provide an
enhancement in force that could maximize force output per stimulus
(24). Recently Binder-Macleod and Barker (3) demonstrated that during
fatigue the effectiveness of doublets was further enhanced. They
suggested it may be an effective stimulus strategy to prevent fatigue
during functional electrical stimulation (FES) of paralyzed muscle in
humans. However, as yet most studies of the mechanical effects of
doublet potentiation have been in isometric conditions. The exceptions
are a preliminary study by Callister et al. (9) in turtles and a recent
study by Binder-Macleod and Lee (5) in humans. They examined shortening
and lengthening contractions and showed that doublets produce
additional force, although the augmentation is somewhat diminished
compared with isometric contractions. Because most voluntary movements
involve nonisometric contractions, it is important to further
understand when doublets are beneficial during dynamic conditions.
Movement may also shed light on the mechanism of doublet potentiation,
which is as yet unclear. The initial potentiation is probably due to
increased release of calcium (12). However, because calcium events are
generally rapid (23), it is possible that the sustained component of
doublet potentiation may reflect a different mechanism, such as the
persistence of attached cross bridges. Changing muscle length would be
likely to break attached cross bridges yet may have no effect on
calcium release. This suggests the hypothesis that the initial increase
in force from a doublet remains large during eccentric or concentric
contractions but that the sustained increase in force is greatly
reduced. The purpose of this study was to investigate the effects of
muscle movement on doublet potentiation by using isovelocity stretches and releases of the cat soleus muscle.
METHODS The data presented in this paper were obtained from eight cats (male
and female). All surgical procedures conformed with the policy
statement outlining the care and use of animals published by the
American Physiological Society. The cats were anesthetized with
isoflurane in a 3:1 mixture of O2
and N2O during the surgical procedures and later switched to intravenous pentobarbital sodium (initial dose 30 mg/kg) for data collection. Blood pressure was monitored throughout both surgery and data collection. At the end of
the experiments the animals were killed without regaining consciousness
with an overdose of pentobarbital sodium (100 mg/kg).
Force was recorded from the soleus muscle while length was controlled
by a servomechanism and the muscle stimulated via the ventral roots.
The muscles in the left hindlimb were denervated except for the soleus
muscle. The soleus was exposed and freed from adjacent tissue, with
care taken to preserve the blood supply. The cat was mounted in a rigid
frame with the leg secured at the hips, knee, and ankle. The calcaneus
was cut so a chip of bone remained on the tendon, allowing a secure
connection to a force transducer. The force transducer was connected in
series with a length transducer and servomechanism (custom-built device
with a compliance of 0.01 mm/N), allowing the soleus to be moved under computer control while muscle force from the same end of the muscle was
simultaneously measured. Skin flaps were pulled up, and the soleus was
immersed in mineral oil maintained at 35°C. A laminectomy exposed
the L7 and
S1 ventral roots, which were cut
and bathed in mineral oil. The soleus was activated by supramaximal
stimulation of the L7 and
S1 ventral roots by using separate
hook electrodes.
The experiments were fully controlled by computer (Macintosh Quadra 950 with National Instruments I/O boards), allowing precise timing of the
stimulus trains and muscle movements. The muscle force and length
signals were sampled at 1 kHz. Before the tendon was freed, the foot
was manually dorsiflexed, and a thread was tied to the tendons of the
soleus and medial gastrocnemius. After the soleus was attached to the
puller, alignment of the two threads was defined as maximum
physiological length (0 mm). Passive tension was always measured and
subtracted from active tension. Because most of the measurements were
made between Doublet potentiation was quantified by digitally subtracting the
waveform produced by a constant-frequency-stimulus train from the
waveform produced when a doublet was added to the constant-stimulus train. Constant-frequency trains of 6-14 Hz were tested in each muscle. Because 10 Hz seemed to produce close to maximal doublet potentiation, to minimize the number of trials and simplify data analysis, only the 10-Hz data are reported in this paper. For each
movement under study, the muscle was stimulated four different times by
using 1) a constant 10-Hz train,
2) a constant train with an added
doublet, 3) a repeat of the
constant-frequency train, and 4) a
single pulse. The timing and movement history between each trial were
reproduced exactly by a computer program. A 30-s rest was used between
trials, and the muscle was always passively moved to a rest length of
Three phases of doublet potentiation were quantified. Peak potentiation
was measured at the maximum of the doublet potentiation waveform, which
usually occurred within 0.1 s of the doublet. Initial potentiation was
measured from the average level for the first 0.5 s of the 1.0 s train.
Sustained potentiation was measured from the average level in the last
0.5 s of the 1.0-s train.
Within each experiment the effect of velocity and muscle length on
doublet potentiation was quite consistent. However, the overall level
of potentiation varied from animal to animal, and this masked the
effect of velocity. To minimize this variability, all data, used in
either statistical tests or in plots depicting the average response,
were normalized by the average doublet potentiation, measured in the
same animal during isometric contractions across all lengths. A
single-factor one-way analysis of variance (ANOVA) was used to test for
influence of length on peak, initial, or sustained doublet
potentiation. t-Tests (2 sample groups
with variance assumed unequal) were used to test for the significance of velocity, step size, and timing on doublet potentiation. Doublet potentiation (peak, initial, or sustained) after a step was compared with a group comprising doublet potentiation (peak, initial, or sustained) at the shortest and longest isometric length. The Bonferroni correction for multiple comparisons was used.
RESULTS
Table 1.
Statistics on isometric doublet potentiation at
6 and 16 mm, passive tension was <0.2 N in
contrast to active tension of 5-10 N. During a slow walk the
excursion of the soleus is 0 to 16 mm (13).
16 mm and then returned to the desired start length exactly 1 s
before the next stimulus began. The additional pulse (doublet) was
added 10 ms after the first pulse in the constant-frequency train.
During the initial studies the timing of the doublet was varied, but,
as in agreement with other investigators, 10 ms was found to produce
optimal results, and this interval was used for the remainder of the
experiments (4, 7, 24). The constant-frequency stimulus was repeated
because the force from the first train in the sequence was sometimes
slightly different from the force from subsequent trials. The
difference occurred when the trial began at a short muscle length and
the previous active contraction had ended at a long muscle length. It
appears to be related to time needed for the muscle to take up the
slack produced by passive shortening. (See Fig. 1 in Ref. 18.)
Otherwise, trials 1 and
3 (both constant-frequency simulii)
produced the same tension due to the fatigue resistance of the soleus.
Because the problem occurred with the first trial, doublet potentiation
was always determined from trains 2 and 3 specified above. In one
experiment the order of the doublet and constant trains was reversed,
and no ordering effect was observed.
16 mm substantially less
force was produced by the constant-frequency train compared with 0 mm.
This resulted from the steepness of the length-tension curve at low
stimulation frequencies (19). This effect was also reflected in the
small twitch seen at 16 compared with 0 mm.
Fig. 1.
Typical example of whole muscle force resulting from twitch, constant
10-Hz train, and 10-Hz train plus doublet during isometric, ramp
shortening, and ramp lengthening movements.
Left: force from isometric
contractions at 0 mm (A), 6
mm (B), and 16 mm
(C); D: muscle lengths corresponding to
waveforms in A-C.
Middle: force resulting from
isovelocity ramps coincident with start of stimulation: 20 mm/s
for 0.5 s (E) 10 mm/s for 0.5 s (F), and 5 mm/s for 0.5 s
(G);
H: isovelocity ramps corresponding to
waveforms in E-G.
Right is similar to
middle except it presents results of isovelocity stretches: 20 mm/s for 0.5 s
(I), 10 mm/s for 0.5 s
(J), and 5 mm/s for 0.5 s
(K);
L: isovelocity ramps corresponding to
waveforms in I-K. Thick solid
lines, force from constant-frequency stimulus; thin solid lines, force
from doublet stimuli; dotted lines, force from single pulse stimuli.
See text for details.
[View Larger Version of this Image (31K GIF file)]
Fig. 2.
Doublet potentiation during isometric, ramp shortening, and ramp
lengthening movements. Shown is digital subtraction of data presented
in Fig. 1. B,
D, and
F: muscle length waveforms
corresponding to force plot immediately above.
A: doublet potentiation during isometric contractions at 6 and 16 mm.
C: doublet potentiation from
shortening isovelocity ramps lasting 0.5 s at 20, 10, and 5 mm/s. E: doublet potentiation
from lengthening isovelocity ramps lasting 0.5 s at 20, 10, and 5 mm/s.
[View Larger Version of this Image (18K GIF file)]
10 mm. To minimize this
variability, as mentioned in METHODS,
the data from each cat were normalized by the average doublet
potentiation measured during isometric contractions across all lengths.
10 mm
Mean
SD
Minimum
Maximum
Whole muscle
Po, N
21.7
3.9
14.5
25.0
Peak doublet
potentiation (normalized by Po)
0.275
0.023
0.240
0.301
Average early (0- to 0.05-s) doublet
potentiation (normalized by Po)
0.123
0.040
0.086
0.181
Average sustained (0.5- to 1.0-s) doublet
potentiation (normalized by Po)
0.054
0.031
0.032
0.075
n = 6 Muscles. Po, maximal tetanic force.
Effect of movement. The strong effect of length on doublet potentiation complicated measurement of the influence of movement on doublet potentiation. It was difficult to determine whether the effect of movement was due to the velocity of the movement or simply to the effects of length. Because of this problem, the isometric data at the start and end lengths of the ramps are always presented along with the isovelocity data. To accentuate doublet potentiation, the general operating range for isovelocity data reported in this paper was between
6 and
16 mm.
Typical examples of the effect of negative (shortening) isovelocity
ramps are shown in Fig. 1, E-H.
All waveforms in Figs. 1 and 2 were taken from the same muscle, so the
ramp results can be directly compared with the isometric trials in Fig.
1, A-D. The
isovelocity ramps began at the same time as the first pulse in the
stimulus train. First, consider results from the ramp with a velocity
of 20 mm/s and lasting for 0.5 s (Fig.
1E). During the ramp, the forces
from both the constant-frequency-stimulus train and the train with
added doublet were reduced. This resulted from the force-velocity
properties of the muscle. Note that peak and initial doublet
potentiation still existed but were reduced compared with the isometric
trials (Fig. 1, B and
C). After the completion of the
ramp, sustained doublet potentiation was abolished. Note that in the
isometric trials, doublet potentiation lasted over the full 1-s
stimulus. Slower ramps, 10 mm/s for 0.5 s (Fig. 1F) and 5 mm/s for 0.5 s (Fig.
1G), had a lesser, but still
noticeable, effect on doublet potentiation. During the isovelocity
shortening, doublet potentiation was diminished compared with the
isometric start or finish length. They also reduced, but did not fully
eliminate, sustained doublet potentiation after ramp completion. In
summary, negative isovelocity ramps decreased doublet potentiation both during and after completion of the ramp.
Figure 2C shows that after the fastest
ramp (20 mm/s for 0.5 s) doublet potentiation was slightly
negative. This was observed in most animals after large ramps or steps
(also see Figs. 3 and 6). This was not an ordering effect because the
same results were obtained regardless of whether the constant-impulse
train was measured before or after the train with the doublet.
Typical examples showing the effect of positive (lengthening) isovelocity ramps are presented in Fig. 1, I-L. The ramp at 20 mm/s for 0.5 s (Fig. 1I) shows doublet potentiation was large during the ramp but was almost completely abolished after the ramp was complete. This pattern was repeated for ramps that were both slower and shorter. Positive (lengthening) isovelocity ramps increased doublet potentiation during the ramp, but after the ramp, doublet potentiation was diminished compared with the isometric trials. Figure 3 shows the average of six muscles subjected to the same isovelocity ramps depicted in Fig. 1. Figure 3, middle shows the effects of shortening while Fig. 3, right shows the effects of lengthening. The effect of movement on the normalized peak doublet potentiation (top) probably resulted from the force-velocity relationship: shortening decreased potentiation while lengthening increased it (both results are statistically significant; P < 0.05 in all cases). At the other extreme (bottom), the normalized sustained doublet potentiation, which occurred entirely after movement has ceased (see Fig. 1, H and L), was sharply reduced by both lengthening and shortening movements. Statistical analyses of sustained potentiation during movement showed that movement significantly reduced sustained potentiation in all cases except for the slowest lengthening (5 mm/s; P < 0.02 in all cases). In fact, application of a doublet for the fastest velocities of shortening actually resulted in slightly less force than did the constant-rate train. The normalized initial potentiation during the first 0.5 s is affected in an intermediate manner: shortening significantly reduced the potentiation (P < 0.05 in all cases), whereas lengthening had no significant effect (P > 0.05 in all cases). These data support the hypothesis that the initial increase in force from a doublet remains large during eccentric or concentric contractions, but the sustained increase in force is greatly reduced (see DISCUSSION). Timing and amplitude of movement. The results so far have considered ramps beginning at the same time as the stimulus train. The next set of experiments examined how the timing and magnitude of a ramp or step affected sustained doublet potentiation. The timing of a ramp critically effected the long-term force enhancement from a doublet. During an isometric contraction, doublet potentiation remained for the full 1.0-s stimulus period. Figure 4 shows the results of moving a muscle at 100 mm/s, over a distance of 10 mm, at various times. Large positive or negative stretches delivered 0.4 s or more after the doublet almost completely eliminated sustained doublet potentiation after the ramp. Large positive or negative ramps occurring early in the stimulus train did not eliminate sustained doublet potentiation. Note that in Fig. 4D, the ramp began at the same time as did the doublet and almost completely eliminated tension during the ramp. However after the ramp, tension redeveloped and the doublet enhancement lasted for a full second. A single twitch subjected to the same ramp did not redevelop tension.
The total distance moved by a ramp is another critical variable in the elimination of long-term force enhancement. Figure 5 shows step movements of varying amplitudes starting at the same time (0.4 s after the doublet). It is clear that either shortening or lengthening steps larger than ~6 mm greatly reduced or eliminated sustained doublet potentiation.
2, 6, and 10 mm in amplitude.
Right: corresponding stretch
data.
These two variables, time of onset and amplitude, were systematically studied in four muscles. Step amplitudes of
2, 6, 10, 2, 6, and 10 mm were each applied at times of 0.0, 0.2, and 0.4 s after the start of the stimulus train, giving a total of 18 conditions. Figure 6 summarizes the results
for normalized, sustained doublet potentiation across the four
experiments. Large steps coincident with the start of the stimulus had
only a small effect on sustained doublet potentiation, which was not
statistically significant across the four experiments
(P > 0.05, t-test). Large shortening steps
(6 or 10 mm) applied at 0.2 or 0.4 s reduced or
eliminated sustained doublet potentiation
(P <0.05,
t-test). A smaller but still
significant effect was found for lengthening steps of 10 mm at 0.2 s
and 6 and 10 mm at 0.4 s (P < 0.05, t-test).
DISCUSSION
The effect of isovelocity ramps on doublet potentiation was studied in whole cat soleus muscle. A basic stimulation protocol was used, consisting of a constant-frequency-stimulus train of 10 Hz with and without a doublet added 10 ms after the first pulse. In general, a ramp decrease in muscle length decreased the force produced by a doublet. A ramp increase in muscle length increased the force from a doublet early in the ramp, but it later decreased doublet potentiation. During isometric contractions doublet potentiation in the soleus can last for >1 s. This sustained potentiation was almost abolished by either large increases or decreases in muscle length, provided they occurred >0.4 s after the doublet.
Comparison to other studies measuring doublet potentiation. Burke et al. (7) reported the catchlike property of motor units in cat soleus and gastrocnemius muscles. They added a pulse to constant-frequency-stimulus train and showed the additional tension was much greater than expected for a single twitch. The stimulation protocol used in this study is quite similar to that used by Burke et al., so, as expected, during isometric conditions the results are qualitatively similar. In this study a different method was used to quantify doublet potentiation, so an exact comparison is not possible. Other investigators have used more elaborate protocols whereby a pair of pulses or a full train is constructed pulse by pulse to determine the force contributed by each pulse (8, 11, 17, 22, 24). These studies were all performed under isometric conditions. This technique enables one to test to what degree the total force output from a train can be considered the linear summation of the individual pulses. All reports have demonstrated that the system transforming action potentials to muscle force is highly nonlinear. While doublet potentiation during isometric contraction has received considerable attention, fewer studies have examined its effectiveness during movement. Binder-Macleod and Lee (5) studied doublets in human quadriceps femoris muscles during eccentric and concentric contractions, when the muscle was fresh and fatigued. Although their method of quantifying doublet potentiation is slightly different, based on their figures showing the raw data, their results are quite similar to this study. They found the rate of rise of force was enhanced by doublets for both eccentric and concentric contractions. Doublets were less effective in increasing average force during movement, particularly for eccentric contractions. They found the effectiveness of doublets increased during fatigue. Mechanisms underlying doublet potentiation. The mechanism behind doublet potentiation remains unclear. This is in part because the mechanisms behind excitation-contraction coupling and cross-bridge dynamics are themselves not fully understood. The potential causes of doublet potentiation can be roughly classified as 1) changes in muscle-tendon stiffness, 2) effects on excitation-contraction coupling, and 3) cross-bridge dynamics. Parmiggiani and Stein (17) suggested that changes in muscle stiffness may contribute to doublet potentiation. They measured the stiffness in cat soleus muscle, showing stiffness roughly increased with force but reached a peak after the peak in force. They suggested that the first stimulus may produce changes in the series stiffness (possibly stretch of nonlinear elastic elements such as tendon) that facilitate the transmission of force produced internally by subsequent stimuli. They did not attempt to apportion the observed changes in stiffness to the cross bridges or the tendon. Their hypothesis that tendon stiffness contributes to initial doublet potentiation may be partially correct, but tendon stiffness alone cannot explain sustained doublet potentiation. Changes in excitation or excitation-contraction coupling account for at least part of doublet potentiation. Doublet potentiation is most pronounced under conditions where excitation-contraction coupling is compromised, suggesting a "saturation process" is involved (12). The data from this study show doublet potentiation is greatest at short muscle lengths where cross-bridge sensitivity to calcium is reduced (1). Rack and Westbury (19) showed that the length tension curve in cat soleus fell more rapidly at short muscle lengths during low- compared with high-frequency stimulation, indicating excitation-contraction coupling is reduced at short muscle lengths. Burke et al. (8) and Duchateau and Hainaut (11) showed that when a muscle was fully potentiated, doublet potentiation was reduced. Duchateau and Hainaut also showed training influenced doublet potentiation proportionally to changes in the twitch-to-tetanus ratio. Finally, during low-frequency fatigue, which is characterized by excitation-contraction coupling deficits, doublet potentiation is enhanced (3). Duchateau and Hainaut (12) used the photoprotein aequorin to measure calcium transients in barnacle muscle fibers during stimulation with doublets. They found an increase in the cytosolic calcium concentration with the second pulse. This was due to intensified calcium release rather than prolonged release or slowed reuptake. It is difficult to study the effects of velocity on doublet potentiation independently from the effects of length. It is well known that sarcomere length affects the force-frequency properties of muscle (19). Calcium release in frog fibers was reported to be dependent on sarcomere length (6). Balnave and Allen (1) recently demonstrated that in mammalian fibers calcium concentration in the myoplasm was not length dependent. They attributed the effect of length to changing calcium sensitivity. The exact mechanism was uncertain but may be dependent on factors such as cross-bridge attachment and developed force. In this study an attempt was made to mitigate the effects of length by recording doublet potentiation during isometric contraction at the starting and ending length of the ramps. Muscle movement is likely to affect doublet potentiation by altering cross-bridge dynamics. Huxley (16) developed a cross-bridge model capable of explaining the force-velocity characteristics of muscle. The same model can be used to explain the increase in doublet potentiation during lengthening and decrease during shortening. A doublet probably increases the release of calcium, which, provided no part of the excitation-contraction coupling chain is saturated, will increase the rate of cross-bridge formation. Muscle movement will alter the length of the attached cross bridges and, in turn, modify the force from the muscle and the rate at which the cross-bridges break. Thus shortening ramps will shorten the bond length of attached cross bridges, which will decrease the force and will increase the detachment rate. Lengthening ramps will increase the bond length of attached cross bridges, which will increase force and may increase the detachment rate (20). One of the more interesting features of the data from this study is that 0.4 s after the doublet, large movements abolish most of the sustained doublet potentiation. Without movement, doublet potentiation can remain for over 1.0 s, much longer than the tension from a single twitch. A possible hypothesis is that the doublet initially causes a release of Ca2+, but within 0.4 s most of this extra Ca2+ may be sequestered in the sarcoplasmic reticulum. The long-term doublet potentiation may be due to a slow rate of detachment cross bridges formed with the initial extra calcium. The dissociation rate of Ca2+ from troponin is slower when the cross bridges are attached (23). If existing bridges are forcibly broken by movement, new cross-bridge formation, and therefore force, will depend solely on the existing calcium concentration. A release of 4-6 mm is a large enough step to unload the series elasticity in soleus and allow tension to fall to zero. It is possible all existing cross bridges are broken at this point (20). The effect of stretch on the state of the attached cross bridges is less clear. Failure to completely eliminate sustained potentiation during stretches may be related to the fact that force never falls to zero and so all cross bridges are never broken simultaneously. The large step may, however, stretch the cross bridges to a length where the rate of detachment is so high that cross bridges activated by the earlier doublet are quickly broken. Figure 2C shows that after a large ramp, doublet potentiation is negative. This observation is consistent with the hypothesis that sustained cross bridges may explain persistent doublet potentiation. The production of a large force initially may put some processes in a state such that when movement breaks the cross bridges, the muscle is less able to regenerate force. For example, if a doublet causes more calcium to be released initially, this extra calcium may have been resequestered or bound to intracellular buffers such that it is not available for rerelease later in the train. Thus a doublet may cause slightly less intracellular calcium later in the train. Without movement, the established cross bridges can still provide more force. With movement, less calcium is available to form new cross bridges. Significance of doublets for motor control. Binder-Macleod (3) has recently demonstrated that doublets can reduce muscle fatigue. A doublet at the beginning of a train allows a target force to be reached with fewer total stimulus pulses in the train compared with constant-frequency stimulation. When a muscle is artificially stimulated muscle action potentials may fail to propagate along the muscle fibers or down the t tubules (high-frequency fatigue). This type of fatigue is likely to occur during FES of paralyzed muscle (21). Muscle fatigue is a problem with FES. High-frequency fatigue might be prevented by using trains containing doublets because the average stimulation frequency can be reduced if the train begins with a high-frequency burst. Under different activation conditions, muscle fatigue may be caused primarily by a failure in excitation coupling. It is not clear whether this type of fatigue may be reduced by decreasing the number of action potentials used to stimulate a muscle. Uncertainty remains as to whether doublets are used in normal movements. Action potential trains with short interspike intervals for the first one or two pulses have been recorded during stepping movements in decerebrate cats (25) but are infrequent in locomotion in the unanesthetized freely moving cat (15). Doublets have also been recorded in human flexor carpi radialis muscle during isometric contractions (2) and in rat soleus and gastrocnemius muscles in freely moving adult rats (14). Although this study provides no data on normal firing rates, it does show that the initial component of doublet potentiation is still effective during movement. Summary. The purpose of this study was to test the effects of movement on doublet potentiation, specifically to test the hypothesis that the initial increase in force from a doublet remains large during eccentric or concentric contractions but that the sustained increase in force is greatly reduced. The data are consistent with this hypothesis. A doublet effectively increases the initial force during positive or negative changes in muscle length. However, >0.4 s after the doublet, movement reduces doublet potentiation. Further experiments are needed in isolated fibers to understand the mechanism. In addition, further work is needed to understand the role doublets play in volitional movements.ACKNOWLEDGEMENTS
The authors acknowledge Kathy Paul for the development of the data-collection software, initial surgical preparation, and proofreading the manuscript.
FOOTNOTES
Address for reprint requests: T. G. Sandercock, Dept. of Physiology, M211, Ward 5-295, Northwestern Univ. School of Medicine, 303 E. Chicago Ave., Chicago, IL 60611 (E-mail: sanderco{at}merle.acns.nwu.edu).
Received 14 March 1996; accepted in final form 13 December 1996.
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