JOURNAL OF PHYSIOLOGY AND PHARMACOLOGY 2004, 55, 2, 291–303
www.jpp.krakow.pl
J. CELICHOWSKI, P. KRUTKI, D. £OCHYÑSKI, K. GROTTEL, W. MRÓWCZYÑSKI
TETANIC DEPRESSION IN FAST MOTOR UNITS
OF THE CAT GASTROCNEMIUS MUSCLE
Department of Neurobiology, University School of Physical Education, Poznañ, Poland
Ability of muscle fibers to generate force is decreased when higher frequency of
stimulation of motor units immediately follows lower frequency. This phenomenon
called tetanic depression was found in rat medial gastrocnemius. However, it was not
clear whether tetanic depression occurred only in rat muscle or it concerns all
mammals. This study was conducted on motor units of cat medial gastrocnemius.
Analyses were made at three successive trains of stimulation: 30 Hz, 20 and 30 Hz
and again 30 Hz (the first pattern) or 40 Hz, 25 and 40 Hz and 40 Hz (the second
pattern). In all fast units force generated within the middle tetanus was lower than
force generated at the same, but constant frequency of stimulation applied earlier or
later. The mean tetanic depression in 30 Hz tetani amounted to 10.9% for fast
fatigable (FF) and 15.9% for fast resistant (FR) motor units, whereas in 40 Hz tetani
mean values were 5.6% and 7.3% for FF and FR motor units, respectively. In slow
motor units tetanic depression was not observed. These results proved the existence
of tetanic depression in the feline muscle and indicated that its intensity depends on
the fusion of tetanus. It has been concluded, that the tetanic depression is a general
property of fast motor units in mammals.
Key
w o r d s : contractile force; skeletal muscle; stimulation frequency; fusion index; cat.
INTRODUCTION
Fast motor units are very sensitive to even very small changes in the pattern
of interpulse intervals of a motoneuronal firing (1-3) and therefore, force of
unfused tetani of fast motor units is highly susceptible to modifications during
their activity.
The motor unit force may be influenced by several phenomena:
potentation of the unfused tetanus (4, 5), the presence of
well as
"sag" profile (6, 7), as
"catch effect" (1). Tetanic depression is the next factor modifying force
292
of unfused tetani in fast motor units. Its appearance clearly shows significance of
changes
in
motoneuronal
firing
rate
and
the
activation
history
for
the
development of force generated by fast motor units. It has been observed in rat
that forces of tetani evoked at two frequencies, lower followed immediately by
higher one, are decreased in comparison to forces of the control tetani evoked at
the same higher stimulation frequency, either before or after each dual-frequency
tetanus. This phenomenon, named tetanic depression, has been described in the
previous paper (8). The mean force decrease measured in depressed tetani of FF
and FR units amounted to 9% and 5%, respectively, while the maximum observed
decrease was 27.5%. Therefore, tetanic depression seems to be the important
factor
reducing
force
generated
at
progressively
increasing
frequency
of
the
motoneuronal firing rate.
The
observation
of
tetanic
depression
has
led
to
the
important
question,
whether it is the specific property of fast muscle fibers in the rat or the common
property that can be observed in other mammals, including humans. In the present
paper we will demonstrate that this phenomenon is also present in cat muscles
and, using the medial gastrocnemius as a model muscle, we will analyze the
extent of tetanic depression in fast fatigable and fast resistant to fatigue motor
units. Possible mechanisms of its appearance and contribution to the control of a
motor unit tension will be discussed.
MATERIAL AND METHODS
Experiments were performed on six adult female cats of a weight 3.0-3.15 kg. For the initial
surgery they were anesthetized by ketamine hydrochloride, 30-40 mg/kg, i.m. Throughout the rest
of each experiment anesthesia was maintained by
α-chloralose
(5-7 mg/kg, i.v., supplemented as
required, up to a total dose 50-60 mg/kg). The withdrawal reflexes, diameter of pupils and the heart
rate were continuously monitored during the whole experiment, and blood pressure was measured
and kept between 90 and 130 mmHg. The animal's core temperature was monitored and maintained
by automatic heating system at 37±1°C. At the end of experiments animals were killed by an
overdose of pentobarbital sodium (Vetbutal), in the lethal dose of 100 mg/kg, i.v. All procedures
followed the European Union guidelines of animal care as well as principles of the Polish Law on
The Protection of Animals.
The skin of the hind limb (back part of the tibia) was cut to expose the medial head of the
gastrocnemius
muscle.
The
medial
gastrocnemius
was
carefully
isolated
from
other
tissues,
dissected from the lateral head of the muscle, whereas blood vessels to this muscle were left intact.
All
branches
of
the
sciatic
nerve
were
cut,
except
the
one
to
medial
gastrocnemius.
The
laminectomy was made over the lumbar and sacral spinal cord and right dorsal and ventral roots
were cut as proximally to the spinal cord as possible. The animals were immobilized with steel
clamps on the upper thoracic and lumbar vertebrae, the hip and the tibia of the right hindlimb, while
the cat's foot was attached to the steel rod.
The studied muscle, and the isolated spinal cord and
spinal roots were covered with warm paraffin oil. Its temperature was kept at a constant level of
37±1°C by radiant heat.
The Achilles tendon was cut close to its attachment to the calcaneum and connected to the force
transducer. The muscle was stretched up to a passive tension of 400 mN what made possible
293
recording the highest contractile force for majority of individual motor units. As thin as possible
filaments
of
ventral
roots
were
carefully
isolated
by
microdissection.
They
were
electrically
stimulated by a bipolar silver electrode, with electrical pulses produced by the dual channel square
pulse stimulator (Grass Instrument Company, model S88). Rectangular pulses of 0.1 ms duration
and variable amplitudes (up to 0,5 V) were organized in trains of various frequencies in the range
of 1-150 Hz.
Action potentials from the studied muscle were recorded with a silver bipolar electrode inserted
into the medial gastrocnemius and amplified using the low-noise multi-channel preamplifier (WPI,
model ISO-DAM8-A, with a high-pass filter at 0.1 Hz and a low-pass filter at 10 kHz). Force was
measured under isometric conditions by the force transducer (model FT-510, force sensitivity of
100 µm per 100 mN). Force and electromyogram were monitored and displayed on an oscilloscope
screen, and stored on a computer disc using the analogue-to-digital 12-bit converter (RTI-800
Utilities) with the sampling frequency 1 kHz for force records and 10 kHz for action potentials. "All
or none" twitch contractions and muscle action potentials were used as the criteria confirming the
isolation of a single motor unit (7, 9).
A computer program creating various patterns of pulses was used for stimulation of each
isolated motor unit. The following stimulating protocol was applied: 1) five single pulses at 1 Hz
(twitch forces and action potentials were averaged); 2) three trains of pulses at 15, 20, 25 Hz
stimulation frequency, during 500 ms (unfused tetani were evoked); 3) one train of pulses at 100 Hz
during 300 ms of stimulation (a fused tetanus was evoked). The stimulations were separated one
from another by 10-seconds intervals. Then, the presence of tetanic depression was tested in the
following pattern of stimulations: 600 ms train of impulses at 30 Hz; 1200 ms train of impulses at
two frequencies (600 ms at 20 Hz and 600 ms at 30 Hz) (20-30 Hz stimulation); and 600 ms train
of impulses at 30 Hz once again. All these stimulations were also separated by 10 s intervals. Forces
of both trains of stimuli at 30 Hz (the first and the last) were averaged and compared to the force of
the dual-frequency tetanus (30 Hz preceded by 20 Hz). Additionally, for several motor units (18
recordings) a pattern of stimulation with the same time duration of 1200 ms for all three successive
tetani (30 Hz, 20-30 Hz, 30 Hz) was applied. In all trials, these force measurements were made for
the last components of single and dual-frequency tetani, to ascertain that differences in force output
were compared at the same point during the time course of each tetanus. The decline of force in
dual-frequency tetani in comparison to the constant-rate tetani was analyzed. In addition, in 40 out
of 71 fast motor units, the tetanic depression was tested at higher frequencies of stimulation at the
same procedure arranged into trains of 40, 25-40 and 40 Hz frequencies.
Finally, the resistance to fatigue was tested in all studied units with the classical fatigue test (14
impulses at 40 Hz repeated every second within 3 min) (6). Fatigue index was measured as a ratio
of
the
contractile
force
generated
two
minutes
after
the
most
potentiated
contraction
at
the
beginning of the fatigue test to the highest initial force.
Division of motor units was based on appearance of a sag effect (visible in unfused tetani of fast
motor units at 15, 20 or 25 Hz stimulation) or its lack (slow motor units) and the values of the
fatigue index (6). They were divided into following categories: fast fatigable (FF) motor units with
the fatigue index under 0.5; fast resistant (FR) units with the fatigue index above 0.5 and slow (S)
units which had the fatigue index close to 1.0. In this paper, 12 S, 15 FR and 56 FF type motor units
were studied.
For each averaged twitch record, the force, the contraction time and the half-relaxation time
were measured. The contraction time was calculated as period of time from the beginning of
mechanical activity to the peak twitch force, and the half-relaxation time was calculated as the time
between the peak twitch force and its decrease to the half of the peak value. For each fused tetanus
record, the maximum tetanic force was measured.
294
Extent of the fusion of each tetanus was measured as the "fusion index" (10, 11). This expresses
the
ratio
of
the
amplitude
measured
from
the
baseline
to
the
maximal
relaxation
before
the
successive contraction within tetanus, to the amplitude of this contraction. The fusion index was
calculated for the last contraction within each part of tetanus evoked at constant frequency. The
index can vary from 0.0 for sub-fused twitches throughout higher values for unfused tetani up to 1.0
for the fused tetanus.
Student's t-test was used for statistical evaluation of obtained results.
RESULTS
Mean values and standard deviations of the main contractile properties of all
motor units studied are given in Table 1. 12 units with long twitch contraction
times (> 44 ms) and small variability with respect to twitch force and fatigability
were classified as slow whereas 71 units with the contraction time
≤44
ms and
great variability of fatigue resistance were classified as fast ones. This division
was fully equivalent with the observation of a sag effect. The majority of fast
units (n=56) appeared to be fast fatigable. Our results are similar to those obtained
in previous papers of other authors (6, 12).
Tetanic depression was visible in all motor units classified as fast (n = 71, Fig.
1A, B) but was not present in slow motor units (Fig. 1C). Tetanic forces generated
by the applied patterns of stimulations were considerably decreased in dualfrequency tetani in comparison to constant-rate tetani. Tetanic depression in a part
of
the
tetanus
evoked
at
30
Hz
stimulation
frequency
directly
following
stimulation at 20 Hz frequency was observed in unfused tetani of all fast motor
units. However, its degree varied between individual units in a very wide range.
The comparison of absolute values of tetanic depression was difficult due to large
differences in maximal tetanic forces between particular fast motor units (force
range 140-1974 mN, see Table 1). Therefore relative values in percents of the
force decrease were calculated for each motor unit. The depression was barely
Table 1. Contractile properties of the three different types of motor units studied.
Motor unit
type
FF
n = 56
FR
CT
(ms)
25.9 ± 5.2
19.0 - 41.0
32.5 ± 6.5
n = 15
24.0 - 44.0
S
58.4 ± 11.0
n = 12
45.0 - 79.0
HRT
TwF
TetF
FI
832.8 ± 392.4
0.15 ± 0.14
516.4 ± 404.4
0.83 ± 0.10
171.8 ± 126.1
0.88 ± 0.09
(ms)
(mN)
24.7 ± 9.7
227.0 ± 135.2
33.9 ± 9.2
83.8 ± 114.4
6.4 - 360.2
140.0 - 1320.0
69.8 ± 23.3
12.1 ± 13.7
13.0 - 58.0
22.0 - 60.0
42.0 - 116.0
10.3 - 530.8
2.4 - 48.4
(mN)
251.0 - 1974.0
48.0 - 380.0
0.01- 0.49
0.56 - 1.0
0.70 - 1.0
For each type of motor units: upper line - mean values ± standard deviations, lower line - variability
range. CT, contraction time; HRT, half-relaxation time; TwF, twitch force; TetF, maximum tetanus
force; FI, fatigue index.
295
Fig. 1. Records of tetanic forces (lower traces in A-C) and muscle fiber action potentials (upper
traces in A-C) of FF, FR and S motor units, respectively. For the three units, the left and right tetani
were evoked at 30 Hz of stimulation, while the middle recording was at 20-30 Hz of stimulation.
Dashed horizontal lines denote the mean values of forces of the last components of 30 Hz tetani to
make apparent the depression of 20-30 Hz tetanic contractions. The arrows manifest the force
decrease expressed in percents.
visible in few FR and FF motor units (in 15 was less than 5%, and in 19 was
comprised in the range of 5-10%), while in most cases (n=37) its degree exceeded
10%, in some being higher than 30% (n=4). The mean values and ranges of the
tetanic depression for FF and FR units are presented in Table 2. Differences
296
Table
2.
The
mean
values
and
range
of
variability
of
tetanic
depression
for
two
patterns
of
stimulations.
Pattern
20-30 Hz
(n = 56)
mean ± S.D.
25-40 Hz
(n = 31)
1.6 - 42.5 %
mean ± S.D.
8.6 - 608.0 mN
(n = 15)
15.9 ± 13.4%
P < 0.05
25.4 ± 29.9 mN
*
P< 0.05
*
P < 0.05
0.0 - 109.4 mN
mean ± S.D.
64.6 ± 55.4 mN
(n = 9)
7.3 ± 5.9%
0.7 - 50.7 %
range
*
FR motor units
mean ± S.D.
range
5.6 ± 4.5 %
0.1 - 15.5 %
65.7 ± 86.0 mN
range
of differences
FF motor units
10.9 ± 7.8%
range
The significance
0.6 - 17.1 %
41.1 ± 41.4 mN
1.0 - 163.2 mN
1.3 - 126.8 mN
n.s.
P > 0.05
Relative (%) and absolute (mN) values of the force depression compared for the two applied
patterns of stimulation, for FF and FR motor units, respectively. *, difference significant (P<0.05);
n.s., difference non-significant (P>0.05) (Student's t-test). Note that mean relative values of force
decrease are higher for FR motor units during both analyzed patterns of stimulations.
between the two types of fast units with respect to absolute and relative values of
tetanic depressions were not statistically significant (P>0.05, Student's t-test).
Similar results were obtained when frequencies 40 Hz, 25-40 Hz and 40 Hz
were applied to 40 fast motor units (Fig. 2). Tetanic depression measured in the
units tested with these patterns of stimulations was comprised in the range of 0.118.5%, being higher than 5% in 17 cases. The detailed data for all tested motor
units are given in Table 2.
In order to verify the influence of duration of stimulation on the amplitude of
tetanic depression, the tetani of the same length were studied. The additional
protocol comprised 1200 ms long trains of stimulations for both single- (30 Hz)
and dual-frequency (20-30 Hz) tetani and was tested in 18 cases. As expressed in
Fig. 3, results obtained during such pattern of excitation were fully comparable to
those
measured
for
600
ms
trains
and
considerable
tetanic
depression
was
observed in these cases as well.
Comparison of two patterns of stimulation: 30 Hz, 20-30 Hz, 30 Hz and 40 Hz,
25-40 Hz, 40 Hz, revealed that lower frequencies were more potent in evoking
tetanic depression, with statistically significant differences (Table 2). Thus, the
amplitude of tetanic depression appeared to depend on the degree of fusion of an
unfused tetanus. For each motor unit studied, tetanic depression was higher in less
fused tetani (20-30 Hz). Fig. 4 presents tetanic depression measured for all units
as a function of fusion index of the first (20 Hz - Fig. 4A) and the second (30 Hz
- Fig. 4B) part of each dual-frequency tetanic contraction. The lowest depression
of the force was observed in tetani fused almost maximally (the fusion index
297
Fig. 2. Tetanic depression for FF motor unit tetani evoked at two different patterns of stimulations.
Upper traces in each panel are muscle fiber action potentials; lower traces are force records evoked
by applied trains of stimuli at given frequencies. In upper panel, the left and right tetani were
recorded at 30 Hz stimulation and the middle recording was at 20-30 Hz stimulation. In lower panel,
the left and right tetani were recorded at 40 Hz stimulation and the middle recording was at 25-40
Hz stimulation. Dashed horizontal lines in both panels denote forces of the last components of each
single-frequency tetanus at 30 Hz or 40 Hz, respectively, to make apparent the depression in the
dual-frequency tetanic contractions at 20-30 Hz or 25-40 Hz, respectively. The arrows manifest the
force decrease expressed in percents.
close to 1.0). This observation concerned both parts of the 20-30 Hz tetanus.
However, the highest values of the force depression (> 30%) were found when the
fusion index of the 20 Hz part of tetanus was between 0.4 and 0.8.
Finally, it must be noted that motor unit action potentials were also analyzed
in our study. When potentials recorded during dual-frequency contractions were
compared to those accompanying single-frequency contractions, no differences
were observed between their amplitudes and time course in all fast motor units
(Figs. 1 and 2).
DISCUSSION
The results from the cat medial gastrocnemius muscle have proved that the
tetanic depression effect exists in fast motor units of this species, likewise in the
298
Fig. 3.
Tetanic depression observed in the FF motor unit when the same 1200 ms time course of
single and dual-frequency tetani was tested. Upper traces - muscle fiber action potentials, lower
traces - records of tetanic forces. Dashed horizontal line denotes forces of the last components of
30 Hz tetani to make apparent the depression of the 20-30 Hz tetanic contraction. The arrow
manifests the force decrease expressed in percents.
Fig. 4. The amplitude of tetanic depression as a function of the fusion index, calculated for the first
(20 Hz, A) and the second (30 Hz, B) parts of dual-frequency tetani for all motor units studied.
FF - fast fatigable, FR - fast resistant motor units.
299
rat, what has been first described in the previous report from our laboratory (8).
This discovery suggests that tetanic depression may be a general phenomenon
occurring among all mammals, including humans.
The motor unit force can be regulated by the rate of motoneuronal firing (13,
14, 15, 16, 17). The tetanic depression takes part in regulating the force during
unfused tetani of fast motor units. This limits the development of force when fast
muscle
fibres
expected
that
are
excited
during
with
impulses
voluntary
of
activity,
increasing
when
the
frequency.
It
motoneuronal
can
firing
be
rate
increases (similarly as observed in the described experiments with the increasing
stimulation frequency), the force of the second part of the contraction at higher
firing rate is limited. Moreover, we have found that the amplitude of tetanic
depression depends on the fusion degree of each contraction. In our experiments
the
effect
was
better
visible
in
less
fused
tetani,
at
lower
frequencies
of
stimulation (i.e., 20-30 Hz) than in more fused tetani (at 25-40 Hz stimulation). It
is likely that the fusion of both, the first and the second part of the tetanus
influences the amplitude of the force depression. However, this question remains
to be evaluated in a next series of experiments. We expect that this phenomenon
more
significantly
influences
the
force
development
at
the
beginning
of
a
contraction, probably just after the motor unit is recruited, when the contraction
is
weak
and
fairly
fused,
with
force
progressively
rising
in
parallel
with
increasing firing rate of a motoneuron (18).
Even temporary changes in the pattern of impulses generated by motoneurons
can
significantly
modify
the
force
generated
by
muscle
fibers
(1,
3).
Some
phenomena, the "catch effect" (1, 2), post-tetanic potentation (19, 20), or fatigue
(6,
21,
22)
are
factors
responsible
for
variability
of
forces
of
motor
unit
contractions. Moreover, motoneurons modify the development of force by two
firings in a short interval (doublet) at the beginning of their activity or during a
train of pulses in slightly fused tetani. This leads to immediate and considerable
increase of the generated force (1, 2, 23, 24) as well as increase of the force-time
area per pulse, reflecting the effectiveness of the muscle activity (25). Significant
differences between tetanic forces of motor units have also been observed when
comparing effects of stimulation at increasing or decreasing frequency. It has
been revealed that the contractile force of motor units measured at the same
instantaneous
frequency
can
be
kept
at
a
higher
level
when
stimulated
at
decreasing than at increasing frequency (26). This observation may be partly
explained
by
the
tetanic
depression
effect,
which
can
prevent
the
force
development during increasing frequency of stimulation. On the other hand, the
"catch effect" augmenting the force at decreasing frequency may be responsible
in this case as well (1, 27). In summary, generation of force of motor units is the
pattern sensitive process. Both phenomena, i.e., tetanic depression and the "catch
effect" influence effectiveness of the motoneuronal firing rate and explain why
higher force can be generated during a decreasing rather than increasing firing
300
rate.
We
may
expect,
that
the
tetanic
depression
is
one
of
the
mechanisms
influencing the force generated by active motor units during voluntary activity.
Tansey and Botterman (28) have studied the force of isolated motor units
evoked
by
mesencephalic
stimulation.
They
have
reported
that
motor
units
activated during smooth graded whole muscle contractions increase their firing
rates over a limited range of increasing muscle force, and inversely, when the
muscle force decreases, motor unit firing rates also decrease before units are
decruited.
The
significant
modulation
of
motor
unit
firing
rate
have
been
observed in numerous electromyographic human studies performed at variable
conditions during voluntary activity (29, 30, 31-33).
Mechanisms causing the tetanic depression have not been revealed so far. On
one hand, reasons for the "sag" behavior can be partly taken into account (Figs.
1B, 2, 3). On the other hand, the remaining example in which no sag has been
observed in force record (Fig. 1A) clearly shows that additional mechanisms must
be considered. In this study no reduction in amplitude of motor unit action
potentials
during
tetanic
force
depression
has
been
established.
This
result
suggests that the phenomenon is not due to weakness of propagation of action
potentials in the motor axon or at the neuromuscular junction (21, 22). Therefore,
some
intracellular
processes
are
probably
responsible
for
this
effect.
These
putative reasons include a diminution of depolarization-induced calcium release
mechanism (34, 35). Moreover, raised concentration of free magnesium (Mg
) in
2+
the cytoplasm during muscle fiber activity competes with Ca
2+
at the high affinity
site on the ryanodine receptor (RyR1 type 1) (36, 37). It is likely, that such
changes in the cytoplasm may occur during the initial (lower frequency) part of
tetanus. These intracellular mechanisms have been considered as a reason of 1015% attenuation of the force-generating ability of the muscle after repetitive
activation with variable frequency trains versus comparable constant-frequency
trains of stimulation (38).
In this point of view, lack of tetanic depression in slow motor units contrary to
its
presence
in
fast
motor
concentrations of Ca
2+
greater
maximal
units
may
be
explained
by
different
endogenous
in the sarcoplasmic reticulum in vivo due to 3 to 4 times
sarcoplasmic
reticulum
capacity
in
the
fast-twitch
fibers
comparing to the slow-twitch fibers (39). Interestingly, the cited experiments
have
indicated
the
same
amount
of
endogenous
Ca
in
2+
the
sarcoplasmic
reticulum, for both slow and fast muscle fibers at rest. The relatively depleted
status of the sarcoplasmic reticulum in fast-twitch muscle fibers may be important
factor enabling rapid Ca
2+
uptake by the sarcoplasmic reticulum. The difference
between relative sarcoplasmic loading and sensitivity to Ca
2+
-induced Ca
2+
release
(both parameters higher in slow-twitch fibers) between the fiber types could
explain, to some extent, why slow-twitch fibers have higher ability to keep the
force on a stable level during unfused tetanic contraction, in comparison to fasttwitch
fibers
(40).
It
should
be
stressed,
that
irrespective
of
what
is
the
301
mechanism of described phenomenon, it is present in fast muscle fibers in both
studied species of mammals, rats and cats.
In conclusion, it has been pointed out that tetanic depression occurs in fast
motor units in several species of mammals, likely including humans. This effect
is responsible for reducing the development of force during tetani evoked at the
increasing frequency of impulses. However, the question whether motoneurons
use effects of tetanic depression to regulate the muscle contractile force during
voluntary activity remains open.
Acknowledgement: The study was supported by the State Committee for Scientific Research
grant.
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R e c e i v e d : January 29, 2004
A c c e p t e d : May 7, 2004
Author's
Physical
address:
Education,
Jan
ul.
Celichowski,
Grunwaldzka
Department
55,
60-352
of
Neurobiology,
Poznañ,
fax: (+48 61) 835 54 44. E-mail: [email protected]
Poland.
Tel.
University
(+48
61)
School
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