BRIEF RESEARCH REPORT

published: 28 February 2020

doi: 10.3389/fphys.2020.00150

Frequency-Dependent Reaction of
the Triceps Surae Muscle of the
Mouse During Electromyostimulation
Sebastian Zart* , Joshua Berger, Oliver Ludwig, Janosch Knauth and Michael Fröhlich
Department of Sport Science, Technische Universität Kaiserslautern, Kaiserslautern, Germany

The difference in the efficacy of altered stimulation parameters in whole-body-

electromyostimulation training (WB-EMS) has hardly been examined. Higher impulse
frequencies (>50 Hz) might be most adequate for strength gains because of the force
frequency relationship (FFR), which describes a greater force production by increasing
the applied frequency. Frequencies below this value, however, also seem to have
positive influences on muscle strength increases. Therefore, the aim of this study was
to analyze possible muscle length changes to different stimulation frequencies of the
dissected mouse triceps surae muscle. A bending rod transducer was used to measure
Edited by: and compare changes in muscle lengths at different frequencies in relation to the initial
Jae-Young Lim,
length in the prepared muscle. We found significant differences between the muscle
Seoul National University Bundang
Hospital, South Korea shortening at different frequencies (p < 0.001). At 20 Hz the largest muscle shortening
Reviewed by: was observed (20 Hz = 3.32 ± 2.06, 60 Hz = 0.77 ± 0.58, 85 Hz = 0.32 ± 0.29,
Seung-Lyul Oh, 100 Hz = 0.31 ± 0.29). From a frequency of 60 Hz, the muscle shortening decreased
Seoul National University Bundang
Hospital, South Korea
progressively, at stimulation frequencies above 60 Hz the lowest shortenings were
Sang Yoon Lee, recorded. The results demonstrate a different behavior of the isolated triceps surae
Seoul National University Hospital
muscle of the mouse in an ex vivo environment. Even if there is no FFR in this
Seoul Boramae Hospital, South Korea
investigation, the results indicate a higher metabolic demand using higher frequencies in
*Correspondence:
Sebastian Zart electromyostimulation, despite the experimental execution in ex vivo design. Therefore,
zart@sowi.uni-kl.de future studies should take this faster fatigue into account when drawing up training
protocols in order to counteract possible frequency modulations.
Specialty section:
This article was submitted to Keywords: electrostimulation, mice, muscle activation, whole-body EMS, frequency
Exercise Physiology,
a section of the journal
Frontiers in Physiology
INTRODUCTION
Received: 12 February 2019
Accepted: 11 February 2020 Electromyostimulation (EMS) training has been an effective form of strength training for many
Published: 28 February 2020
years now, both in rehabilitation and in competitive and popular sports. However, there has been
Citation: no clear consensus on the selection of stimulation parameters in training planning and execution
Zart S, Berger J, Ludwig O, over the last decades. A stimulation parameter whose influence on the effectiveness of EMS training
Knauth J and Fröhlich M (2020)
has not yet been sufficiently clarified is the stimulation frequency. In conventional EMS training,
Frequency-Dependent Reaction
of the Triceps Surae Muscle of the
a frequency in the range around 85 Hz is usually used, but there is no evidence for this. Various
Mouse During Electromyostimulation. studies differentiate the frequency range used according to age or state of fatigue. Optimal force
Front. Physiol. 11:150. increases seem to take place at a frequency in the range of 76.4 ± 20.9 Hz (Filipovic et al., 2011).
doi: 10.3389/fphys.2020.00150 In general, more than 50 Hz seem to be necessary to generate optimal force increases, since at

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Zart et al. Frequency-Dependent Mouse Muscle Stimulation

a frequency below 50 Hz mainly slower Type I fibers and from TABLE 1 | Percentage of muscle fiber types in the soleus and gastrocnemius
muscle, modified according to Augusto et al. (2004).
50-120 Hz mainly faster Type II fibers are supposed to be
stimulated (Frenkel et al., 2004). According to Kramme (2007), Muscle fiber type m. soleus [%] m. gastrocnemius [%]
optimal faradic stimulation of the striated musculature occurs
from 50 Hz, while Moreno-Aranda and Seireg (1981) were able Type I 37.42 5.74
to generate maximum electrical muscle activity at a frequency in Type IIA 38.62 5.73

the range between 50 and 110 Hz. However, frequency ranges Type IID 5.69 2.26

below 50 Hz are also considered to have a positive influence on Other type II (AD, DB and B) 18.74 86.19

force increases. Dreibati et al. (2010) recommend a stimulation

frequency below 60 Hz in order to prevent a loss of strength
during training. TABLE 2 | Myosin isoform percentages (MHC) in the soleus and gastrocnemius
In animal experiments the muscle behavior was also muscle, modified according to Augusto et al. (2004).
investigated with different frequencies. 20 Hz seem to have MHC m. soleus [%] m. gastrocnemius [%]
a positive influence on strength increases in the m. soleus
of the mouse during a 14-day stimulation period (two times I 41.5 0.81
daily per 3 h of stimulation), furthermore positive influences IIa 57.56 17.01
on the development of the satellite cells can be determined IId 0.15 0.00
(Guo et al., 2012). Exemplary studies showed an increased force IIb 0.00 84.50
production and tension with increasing frequency (Guo et al.,
2012; Hering et al., 2016). However, an increased frequency
cannot be maintained indefinitely. A constant stimulation with After the preparation of the muscle, it was immediately
a higher frequency (e.g. 80 Hz or 100 Hz) results in a drop in clamped into the apparatus to avoid a long period of
force, which can be reduced by adjusting the frequency to 20 Hz time between preparation and analysis. At the lower end a
for example. This fatigue during high frequency stimulation may bending rod transducer with amplifier was fixed, the signal
be due to the failure of electrical propagation at the muscle fiber was amplified tenfold. The amplified signal was output and
membrane, a reduction in the activity of the motor unit activity stored optically and digitally via an oscilloscope (Tektronix
seems to minimize fatigue. A constant stimulation of 20 Hz TDS1001B, Tektronix, Schwalbach am Taunus, Germany) at
generates a constant force diagram with a force increase after 250 Hz. For the stimulation a clamp electrode was fixed to the
continuous stimulation. In comparison, in voluntary contraction paw and a needle electrode was inserted through the muscle
the force generation is optimized by a reduction in motor neuron belly of the muscle. The sequence of the selected frequencies
firing frequency to avoid this type of fatigue (Bigland-Ritchie was randomized from muscle to muscle so each frequency
et al., 1979; Jones et al., 1979). was used at each measurement time point. The monopolar
On this basis, the aim of the present study was to observe stimulation of the triceps surae muscle was performed by a
the frequency-dependent response behavior of the triceps surae self-developed stimulation generator which modulated the pulse
muscle of the mouse in EMS. duration (4 s), frequency (20, 60, 85, 100 Hz) and width
(350 µs) for a rectangular signal. The resulting stimulation
scheme largely corresponded to the electrical stimulation used
METHODS in a whole-body-EMS (WB-EMS) application. In order to realize
a stimulation at a desired current strength of 30 mA, a voltage
The experiments were performed on triceps surae muscle (m. of 8.7 V with a resistance of 270 Ohm was determined on
soleus and m. gastrocnemius) of 19 wild type laboratory mice the oscilloscope.
(C57BL/6N; age: 34.7 ± 2.2 days; weight: 17.2 ± 1.7 g). During the stimulations, the shortening of the triceps surae
Animals were raised in the animal facilities of the University muscle was measured via the bending rod transducer as
of Kaiserslautern under normal nutritional conditions. Lights relative units (here designated by a.u. = arbitrary units). The
were set to a 12 h day-12 h night cycle. Animal breeding and present equilibrium length of the muscles before stimulation
experiments were approved by the regional council according corresponded to the initial value of zero. Positive values during
to the German animal protection act (TSchG §4, Absatz 3) stimulation showed muscle shortening. Thus, a comparison
and in accordance with EU Directive 2010/63/EU. To carry between the frequencies was performed on the basis of the relative
out the experiment, the neck of 19 mice was broken with the unit. We determined maximum and mean shortening and the
preparation scissors and then the head was severed. The lower integral over the time-length diagram in relation to frequency.
leg was separated from the thigh 5 mm above the knee joint and The results are expressed as mean values and standard deviations.
the coat, skin and connective tissue were removed. The exact We included only measurements of 15 mice or mouse muscles
muscle fiber composition of the examined musculature is shown in the analysis because measurement errors occurred in four
in Table 1, the myosin isoform percentage (MHC) in Table 2. The cases. The statistical analysis was performed with IBM SPSS (SPSS
preparation was clamped vertically in the area of the tarsus as well Version 25.0, Chicago, IL, United States). Because of missing
as below the knee joint by two threads with the same pre-tension normal distributions Kruskal-Wallis-Tests were performed to
in a tripod apparatus (Figure 1). evaluate differences of mean value changes in relative muscle

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Zart et al. Frequency-Dependent Mouse Muscle Stimulation

DISCUSSION
In this study, the dissected triceps surae muscle of the mouse
was subjected to muscle stimulation corresponding to WB-
EMS training. Four frequencies were randomly applied and the
respective stimulus response was determined by means of relative
muscle length changes. On basis of this experimental setup with
the same external weight load and pre-tension of the triceps surae
muscle we found different muscle activation levels.
At 20 Hz, the largest change in muscle length was induced
approximately over the full stimulation time. Only for this
frequency a permanent and constant muscle shortening had
occurred and thus a tetanic contraction could be assumed. The
time-length-diagrams for the frequencies of 60, 85, and 100 Hz,
on the other hand, showed less muscle shortening. The question
now arises why we could not find an increased shortening at
higher frequencies, what the force frequency relationship (FFR)
suggests. Studies found an increase in muscle tension (Guo et al.,
2012) or strength production (Hering et al., 2016) due to an
increase in the frequency in animal experiments. First of all, it
has to be taken into account that our experiments are carried
out ex vivo, using a needle electrode, which complicates the
comparability to in vivo or in vitro studies.
According to Augusto et al. (2004), 2–3 months old mice have
a fiber composition with over 80% type II fibers in triceps surae
muscle. Due to the young age of the mice used, the differentiation
of the muscle fiber types are not complete, which could result
in an insufficient number of motor units responding to high
FIGURE 1 | Fixed mouse muscle with needle and clamp electrode. frequencies. It is known that muscle activity induced by EMS
causes altered recruitment behavior in muscle fibers compared
to voluntary contractions. Contrary to the activation sequence
of Henneman’s size principle, studies with EMS show either
lengths between the frequencies. Follow up Mann-Whitney-U-
a selective activation of fast motor units (Cabric et al., 1988;
tests were conducted to evaluate pairwise differences, controlling
Trimble and Enoka, 1991) or a non-selective, spatially fixed and
for Type I error across tests by using Bonferroni approach.
temporally synchronous recruitment pattern of muscle fibers
(Bickel et al., 2011). In the first case, there might be no increase
in muscle activity, since the muscle fibers of the growing mouse
RESULTS are not yet sufficiently differentiated and thus less fast-twitching
fibers can be activated. In addition, one could assume that most
With regard to the frequency-dependent, averaged integrals, no muscle fibers had already reached their stimulation threshold
significant differences in triceps surae muscle shortening could at low frequencies and therefore no increase in muscle activity
be observed depending on the selected frequency sequence. and further shortening of muscle length could be achieved at
Therefore, we could exclude a sequence-related fatigue effect. In higher frequencies. In the second case, slow and fast muscle fibers
spite of different preloads due to randomized stimulation, we are activated at both low and high strength levels (Gregory and
found the largest muscle shortenings at 20 Hz (Table 3). Bickel, 2005). Thus, according to Bickel et al. (2011), stimulation
In addition, we found continuous muscle shortening (tetanus) with low (20 Hz) and high frequency (>50 Hz) should have
during stimulation at 20 Hz. For frequencies above 50 Hz there activated all types of muscle fibers.
was no permanent and constant muscle shortening, the muscle However, it is assumed that higher frequencies may lead to
length increased again in the course of the stimulation. At 85 faster muscle fatigue, as during EMS it is not possible to reduce
and 100 Hz this course was even more obvious in the graph the innervation frequency or modulate the recruitment pattern
(Figure 2). Already after 0.5 s, the muscle almost regained its through physiological control processes (Gregory and Bickel,
equilibrium length. 2005; Dreibati et al., 2010). Experimental investigations on the
The Kruskal-Wallis-Test revealed significant differences soleus muscle of the mouse show exactly this behavior by means
between the frequencies used (p < 0.050). The results of of the force progression. At 100 Hz stimulation frequency, the
the Mann-Whitney-U-tests indicated a significant difference force drops to 10% of the initial value after 40 s. In contrast,
between 20 Hz and all other frequencies (all p < 0.050), but none force remains at the same level for at least 60 s when stimulated
in any other pairwise comparison. at 20 Hz (Jones et al., 1979). Compared to the results presented

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Zart et al. Frequency-Dependent Mouse Muscle Stimulation

TABLE 3 | Averaged results across all mice for the frequencies 20, 60, 85, and reduction of the membrane excitability and thus to a lower power
100 Hz.
development (Bigland-Ritchie et al., 1979). Binder-Macleod and
Stimulation Frequency (Hz) Integral (a.u.) Mean (a.u.) Maximum (a.u.) McDermond (1992) show that the contraction rate of skeletal
muscles slows down when tired muscles are excited voluntarily
20 13.27 ± 8.25 3.32 ± 2.06 3.71 ± 2.27
or by EMS. This means that although muscle twitching is
60 3.09 ± 2.32 0.77 ± 0.58 2.49 ± 1.64
faster when stimulated electrically, the half relaxation time is
85 1.27 ± 1.03 0.32 ± 0.29 1.68 ± 0.85
significantly longer. Thus, at high frequency, a new electrical
100 1.24 ± 1.14 0.31 ± 0.29 1.36 ± 1.00
stimulus occurs during the repolarization phase and therefore
Values are reported as means ± standard deviations. a.u. = arbitrary unit. remains ineffective. This could signify for WB-EMS that lower
frequencies guarantee an adequate repolarization time of the
muscle fiber membrane especially in a fatigued state, which could
in this study, only the time of fatigue differs significantly. The be important for the periodization of the WB-EMS training in
much earlier decrease in muscle activity could be explained by competitive sports. At a higher frequency, an increased metabolic
the experimental setup. In the study by Jones et al. (1979), the demand leads to a faster fatigue of the muscles. However, in WB-
mouse muscle is placed in a sodium solution so that an ion EMS this could be an important factor for modulating the applied
exchange between muscle tissue and fluid is possible. In the frequency during the training from a higher to a lower frequency
present study, the muscle was isolated and separated from any (Dreibati et al., 2010).
circulation, which would allow the fatigue processes to progress The study carried out here showed the highest force
more rapidly. Nevertheless, the graphs of force development at development at a frequency of 20 Hz. This could be a further
different frequencies from Bigland-Ritchie et al. (1979) show indication of an increased metabolic need of the muscle at higher
very strong similarities to the ex vivo results presented here. frequencies, since the musculature could only cause a continuous
A continuous force development at 20 Hz can be seen, whereas contraction at 20 Hz. Only at higher frequencies a lower force
higher frequencies (50 Hz and 80 Hz) already after a short impulse could be generated. A decisive factor here, however,
stimulation time of about 5 s lead to a continuous decrease is the conduct of the study in an ex vivo experimental design.
in force production, which remains constant until the end Nevertheless, other authors such as Glaviano and Saliba (2016) or
of the stimulation (Bigland-Ritchie et al., 1979). Furthermore, Dreibati et al. (2010) also describe an improved force production
frequency modulation from 100 Hz to 20 Hz after continuous at lower frequencies and stated an increased metabolic demand
stimulation can in turn bring about a clear increase in force in higher frequencies (ph level, inorganic phosphocreatine values,
(Jones et al., 1979). energy costs), which would confirm our results due to the lack of
With regard to the behavior of human muscles in comparison new energy production in the ex vivo muscle. A further reason
to mouse muscles during EMS, studies show the same fatigue for the strength loss with increased frequencies could be the
behavior (Jones et al., 1979; Moritani et al., 1985). As a reason for reduction in the extracellular Na+ due to the shorter action time
the decrease in strength during stimulation with high frequencies, for the sodium-potassium pump. The depletion of the Na+ (or
it is assumed that the transmission of the action potentials via the accumulation of K+ ) could reduce the muscle membrane
the T-tubules is no longer possible and therefore the strength excitability sufficiently to explain the force loss during a higher
production collapse. A changed ion concentration leads to a frequency (Moritani et al., 1985).

FIGURE 2 | Mean values of all frequencies.

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Zart et al. Frequency-Dependent Mouse Muscle Stimulation

Due to different stimulation protocols and other muscle strength compared to passive WB-EMS, the frequency
environmental conditions, the comparison of the results should be chosen accordingly in order to be able to perform
presented here to other animal studies remains complicated the movements in a controlled manner throughout the training
(Guo et al., 2012; Kobayashi et al., 2012; Tsutaki et al., 2013; (Kemmler et al., 2018).
Hering et al., 2016; Li et al., 2016; Valenzuela et al., 2017).
Nevertheless, similar results could be observed in the behavior
of the muscle during stimulation with different frequencies, DATA AVAILABILITY STATEMENT
even if the environmental influences and the way of stimulation
of the muscle (ex vivo, needle electrode) were different. In The raw data supporting the conclusions of this article will be
future experiments, the influence of surface electrodes and made available by the authors, without undue reservation, to any
needle electrodes on stimulation behavior of the muscle should qualified researcher.
be investigated. Since comparative studies in animals use
surface electrodes in the experiments, this could be a source of
interference in the experimental setup. It should also be examined ETHICS STATEMENT
to what extent an examination with intact blood circulation
would generate similar muscle behavior. In addition, the This study was carried out in accordance with the
relationship between stimulation frequency and intensity should recommendations of the regional council according to the
be further examined in a combined study protocol. Nevertheless, German animal protection act (TSchG §4, Absatz 3) and in
the available results provide an insight into the behavior of the accordance with EU Directive 2010/63/EU. The protocol was
ex vivo mice muscles at different applied frequencies. approved by the regional council.
In addition to the limitations described such as the use
of a needle electrode instead of surface electrodes and the
ex vivo implementation of the study without nutrient supply AUTHOR CONTRIBUTIONS
for the muscle, the lack of knowledge about the MHC
isoform of the muscles used is a further limitation. Although SZ, JB, JK, and MF conceived and designed the experiments. JK
comparisons can be made with the studies carried out by performed the experiments. JK, SZ, and JB analyzed the data. SZ
Augusto et al. (2004), future studies should carry out a and MF contributed materials and analysis tools. SZ, JB, and OL
detailed MHC isoform analysis of the examined muscles in wrote the manuscript.
each case in order to be able to interpret possible fluctuations
of the muscle fiber composition (Zhang et al., 2010) and
corresponding divergent reactions to an electrical stimulus ACKNOWLEDGMENTS
more accurately.
The frequency used seems to have a significant influence Many thanks to Prof. Eckhard Friauf (Department of
on fatigue, which must also be considered in the context of Animal Physiology, Technische Universität Kaiserslautern)
training planning for WB-EMS. Since active movements of without his help the implementation of this study would not
the athlete (e.g. light strengthening exercises) lead to greater have been possible.

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