Activation of human plantar flexor muscles increases

after electromyostimulation training

Nicola A. Maffiuletti, Manuela Pensini and Alain Martin
Journal of Applied Physiology 92:1383-1392, 2002. First published Nov 9, 2001;
doi:10.1152/japplphysiol.00884.2001

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Activation of human plantar flexor muscles increases
after electromyostimulation training
NICOLA A. MAFFIULETTI, MANUELA PENSINI, AND ALAIN MARTIN
Groupe Analyse du Mouvement, Unité de Formation et de Recherche Sciences et Techniques des
Activités Physiques et Sportives, Faculté des Sciences du Sport, Université de Bourgogne,
BP 27877-21078 Dijon Cedex, France
Received 27 August 2001; accepted in final form 5 November 2001
Maffiuletti, Nicola A., Manuela Pensini, and Alain
Martin. Activation of human plantar flexor muscles in-
creases after electromyostimulation training. J Appl Physiol
92: 1383–1392, 2002. First published November 9, 2001;
10.1152/japplphysiol.00884.2001.—Neuromuscular adapta-
tions of the plantar flexor muscles were assessed before and
subsequent to short-term electromyostimulation (EMS)
training. Eight subjects underwent 16 sessions of isometric
EMS training over 4 wk. Surface electromyographic (EMG)
activity and torque obtained under maximal voluntary and
electrically evoked contractions were analyzed to distinguish
neural adaptations from contractile changes. After training,
plantar flexor voluntary torque significantly increased under
isometric conditions at the training angle (⫹8.1%, P ⬍ 0.05)
and at the two eccentric velocities considered (⫹10.8 and
⫹13.1%, P ⬍ 0.05). Torque gains were accompanied by higher
normalized soleus EMG activity and, in the case of eccentric
contractions, also by higher gastrocnemii EMG (P ⬍ 0.05).
There was an 11.9% significant increase in both plantar
flexor maximal voluntary activation (P ⬍ 0.01) and postacti-
vation potentiation (P ⬍ 0.05), whereas contractile properties
did not change after training. In the absence of a change in
the control group, it was concluded that an increase in neural
activation likely mediates the voluntary torque gains ob-
served after short-term EMS training.
electromyogram; maximal voluntary activation; twitch con-
tractile properties; tetanus; M wave
THE USE OF HIGH-FREQUENCY electromyostimulation (EMS)
has previously been employed as a means to strengthen
healthy human skeletal muscle (8, 10, 12, 26, 27, 34).
Nevertheless, the physiological adaptations (muscular or
neural) induced by this form of involuntary training and
responsible for the increases in strength remain equivo-
cal. The assessment of muscular adaptations to EMS has
primarily been by direct observation in human (8) or rat
muscles (18), whereas the neural adaptations have been
inferred. Although very few studies have directly exam-
ined neural activity subsequent to EMS training, many
studies on healthy human muscles have proposed that
neural adaptations are largely responsible for the
strength gains observed (10, 26, 27). This conclusion is
based on the use of training periods that are too brief to
Address for reprint requests and other correspondence: N. A.
Maffiuletti, Groupe Analyse du Mouvement, UFR STAPS, Faculté
des Sciences du Sport, Université de Bourgogne, BP 27877-21078
Dijon Cedex, France (E-mail: Nicola.Maffiuletti@u-bourgogne.fr).
http://www.jap.org 8750-7587/02 $5.00 Copyright © 2002 the American Physiological Society
J Appl Physiol 92: 1383–1392, 2002.
First published November 9, 2001; 10.1152/japplphysiol.00884.2001.
induce muscular adaptations (see Refs. 31, 36). However,
neural adaptations are possible because EMS results in
excitation of intramuscular branches of the nerve and not
the muscle fibers directly (23), which likely induces anti-
dromic activation of the motoneurons. It could, therefore,
be hypothesized that the strength gains observed subse-
Downloaded from jap.physiology.org on October 28, 2005
quent to short-term EMS training are likely mediated by
enhanced neural activation, rather than muscle activa-
tion.
To our knowledge, only one investigation has focused
on the effects of EMS training on the surface electromyo-
graphic (EMG) activity of the agonist (i.e., stimulated)
muscle in humans (10). Although the EMG activity of the
biceps brachii significantly increased after 7 wk of elbow
flexor EMS training (10), EMG values were not normal-
ized to the compound action potential (M wave), and
maximal voluntary activation was not assessed. None-
theless, Colson et al. (10) observed changes in M-wave
characteristics with a concomitant increase in the twitch
time course, whereas Duchateau and Hainaut (12) re-
ported no changes in single-twitch contractile properties
but greater amplitude of the 100-Hz tetanus after 6 wk of
adductor pollicis EMS training. These disparate findings
may be due to the effect of EMS resistance training on the
muscular contractile properties assessed with single and
multiple stimuli, which has not been examined system-
atically.
The aim of the present investigation was to assess
the effects of 4 wk of EMS training on neuromuscular
properties of the plantar flexor (PF) muscles, with
special emphasis on changes in neural activation. The
EMG and mechanical responses obtained under maxi-
mal voluntary (isometric, concentric, and eccentric)
and electrically evoked (single, paired, or tetanic stim-
uli) conditions were assessed to distinguish neural
adaptations from contractile changes.
METHODS
Subjects
Eight healthy male individuals took part in this investiga-
tion and were tested before and after 4 wk of EMS training
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solely to indicate this fact.
1383
1384 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS
(EMS group, age 20.4 ⫾ 2.1 yr; height 186.4 ⫾ 8.0 cm; weight
83.5 ⫾ 9.6 kg, means ⫾ SD). A control group of six subjects
did not train and were tested before and after a 4-wk period
to assess the reliability of the observations (C group, age
26.0 ⫾ 5.1 yr; height 176.7 ⫾ 4.8 cm; weight 69.5 ⫾ 4.6 kg).
For all of the subjects, the PF and dorsiflexor (DF) muscles of
the right leg were tested. The subjects, all free from previous
ankle injury, agreed to participate in the study on a volun-
tary basis and signed an informed consent before involve-
ment in the investigation. Approval for the project was ob-
tained from the University of Burgundy Committee on
Human Research.
EMS Training Procedures
One week before the beginning of the stimulation period,
the EMS group participated in one practice session to ac-
quaint themselves with stimulation parameters. None of
these subjects had previously engaged in systematic strength
training or had experienced EMS. They completed sixteen
18-min sessions of isometric bilateral EMS over a 4-wk pe-
riod, with four sessions per week. Forty-five isometric con-
tractions were carried out during each training session. Dur-
ing the stimulation, subjects were seated on a calf machine
(Multi-Form, La Roque D’Anthéron, France) with the ankle,
knee, and hip joints flexed to ⬃90°. A portable battery-
powered stimulator (Compex Sport, Medicompex, Ecublens,
Switzerland) discharged rectangular-wave pulsed currents
(75 Hz) lasting 400 ␮s. Three 2-mm-thick, self-adhesive elec-
trodes were placed over each leg. The two positive electrodes,
each measuring 25 cm2 (5 ⫻ 5 cm), which had membrane
depolarizing properties, were placed over the superficial as-
pect of the soleus muscle, ⬃5 cm distal from where the two
heads of the gastrocnemius join the Achilles tendon. The
negative electrode, measuring 50 cm2 (10 ⫻ 5 cm), was placed
along the middorsal line of the leg, over both medial (MG)
and lateral gastrocnemius (LG). Each 4-s contraction was
followed by a pause lasting 20 s. Intensity (range 0–100 mA)
was monitored on-line and was gradually increased to a level
of maximally tolerated intensity, which varied between 30
and 90 mA, depending on differences among subjects in pain
threshold. No subject reported serious discomfort. The indi-
vidual level of isometric force developed during EMS was
measured once a week with a myostatic-type dynamometer
(Allegro, Sallanches, France), and this latter varied between
50 and 70% of the pretraining maximal voluntary contraction
(MVC). Each session was preceded by a standardized warm-
up, consisting of 5 min of submaximal EMS (5 Hz; pulses
lasting 200 ␮s).
Testing Sessions
PF and DF maximal voluntary torque. Before and after the
4-wk intervention period, two testing sessions were orga-
nized to assess voluntary and evoked PF and DF neuromus-
cular properties in both the EMS and C groups. In the first
testing session, maximal voluntary torque and the associated
EMG activity were measured for isometric, concentric, and
eccentric PF and DF contractions to determine the respective
torque- and EMG-angle and torque- and EMG-angular veloc-
ity relations (see also EMG activity). All of these contractions
were carried out by using a Biodex-type isokinetic ergometer
(Biodex, Shirley, NY), previously validated by Taylor et al.
(38). Subjects were seated on the dynamometer chair, and
their right knee joint was fixed at ⬃90° of flexion. To mini-
mize hip and thigh motion during the contractions and,
therefore, to avoid the contribution of muscles other than the
PF (e.g., knee extensors, hip extensors), straps were applied
J Appl Physiol • VOL
across the chest, pelvis, midthigh, and lower leg. The arms
were positioned across the chest, with each hand clasping the
opposite shoulder. A strap also secured the foot to the Biodex
footplate, and the alignment between the center of rotation of
the dynamometer shaft and the axis of the ankle joint was
checked at the beginning of each trial. In accordance with
Taylor et al. (38), all torques were gravity corrected by using
Biodex software after calibration to determine the maximal
effect of gravity on static torque.
Subjects warmed up by performing five submaximal con-
centric PF and DF contractions at the three experimental
angular velocities (i.e., 60, 120, and 240°/s), and three sub-
maximal isometric contractions were also performed for both
muscle groups at 0° (i.e., 90° ankle flexion). Maximal isomet-
ric measurements were then performed at three different
ankle angles: ⫺20° (dorsiflexed position), 0° (neutral posi-
tion), and ⫹30° (plantar flexed position), for both PF and DF
muscles. Subjects were instructed to produce their maximal
force (“hard”) without any concern for the rate of force devel-
opment. The total duration of these efforts was ⬃5 s. Isoki-
netic measurements involved three maximum concentric and
eccentric PF and DF contractions (range of motion: 50°),
Downloaded from jap.physiology.org on October 28, 2005
which were performed at five preset constant angular veloc-
ities (⫺120 and ⫺60°/s under eccentric conditions and 60,
120, and 240°/s under concentric conditions). In each case,
constant angular torque was measured at 0° and subse-
quently included in the PF and DF torque-angle and torque-
angular velocity relations. The velocity throughout each rep-
etition was analyzed, and it was also verified that, at the
higher angular velocity (i.e., 240°/s), constant angular torque
was developed during the constant velocity period. Isometric
and isokinetic PF and DF contractions were randomly pre-
sented with a 2-min rest between successive repetitions to
eliminate the effects of fatigue. In each case, only the best
performance was included in the analysis.
PF electrical stimulation. At least 48 h after the first
testing session, subjects reported to the laboratory for percu-
taneous stimulation of the tibial nerve. Single and paired
(doublet) stimuli and tetani were evoked at rest to investi-
gate PF contractile properties and the associated compound
action potentials (M waves, see EMG activity). Also, single
stimuli were delivered before, during, and immediately after
MVC to estimate maximal voluntary activation (i.e., twitch
interpolation technique) and to quantify postactivation po-
tentiation (PAP). During this session, subjects were exam-
ined under sitting conditions with the right knee and ankle
flexed to ⬃90° of flexion. The foot was secured to a pedal
equipped with strain gauges, which was developed by the
local engineering school, to record the PF mechanical re-
sponse. The posterior tibial nerve was stimulated by using a
cathode ball electrode (0.5-cm diameter) pressed in the pop-
litea fossa. The anode was a large electrode (10 ⫻ 5 cm),
placed on the anterior surface of the knee. The percutaneous
electrical stimulus was a rectangular pulse (1-ms duration)
delivered by a Digitimer stimulator (DS7, Herthfordshire,
UK). Each subject was initially familiarized with several
submaximal (range: 1–20 mA) electrical stimuli over a period
of 10–15 min. The current was then progressively increased
until maximal PF twitch torque and maximal soleus M-wave
amplitude were achieved. This intensity was further in-
creased by 10% (i.e., supramaximal) and then maintained for
1) four single twitches, each separated by 3 s, 2) four doublets
(10-ms interval) separated by 5 s, and 3) two tetani (100 Hz;
250 ms). Two-minute rest periods were allowed between
different stimuli and between tetani. Whatever the type of
stimuli, mechanical traces were digitized on-line (sampling
frequency: 2 kHz), averaged, and stored for analysis with
92 • APRIL 2002 • www.jap.org
 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS
commercially available software (Tida, Heka Elektronik,
Lambrecht/Pfalz, Germany). The following variables were
measured from the twitch traces associated with single and
paired stimuli: peak torque (Pt), contraction time, half relax-
ation time, and maximum rate of tension development (RD)
and relaxation (RR). Pt, RD, and RR were measured from the
tetanic stimulation and were named P0, RD0, and RR0, re-
spectively.
Subsequently, two maximal voluntary PF contractions
were held for 3–4 s in the same isometric position, each
separated by 5 min. Single stimuli were delivered 2 s before
the MVC (control twitch), over the isometric plateau (super-
imposed twitch), and 5 s after the contraction (potentiated
twitch) to assess the level of voluntary activation and the
PAP. PF maximal voluntary activation was thus estimated
according to the following formula (twitch interpolation tech-
nique) (2), i.e., %activation ⫽ (1 ⫺ superimposed twitch
amplitude ⫻ potentiated twitch amplitude⫺1) ⫻ 100 (%). PF
PAP was determined by computing the ratio between the
amplitude of the potentiated twitch and the control twitch.
EMG Activity
Silver chloride surface electrodes of 10-mm diameter, with
an interelectrode (center-to-center) distance of 2 cm, were
used to record the EMG activity of three PF muscles (soleus,
MG, and LG) and one DF muscle [tibialis anterior (TA)]
during voluntary torque assessment and the stimulation
test. For the soleus, recording electrodes were placed along
the middorsal line of the leg, ⬃5 cm distal from where the two
heads of the gastrocnemius join the Achilles tendon. MG, LG,
and TA EMG electrodes were fixed lengthwise over the mid-
dle of the muscle belly with the reference electrode placed on
the opposite wrist. Low impedance (⬍2 k⍀) at the skin-
electrode interface was obtained by abrading the skin with
emery paper and cleaning with alcohol. EMG signals were
amplified with a bandwidth frequency ranging from 1.5 Hz to
2 kHz (common mode rejection ratio ⫽ 90 dB; Z input ⫽ 100
M⍀; gain ⫽ 1,000) and subsequently stored for off-line anal-
ysis. For voluntary torque testing, the root mean square
(RMS) myoelectric activity of soleus, MG, LG, and TA was
calculated every 0.02 s over the period of interest. During
isometric actions, the RMS EMG was measured over a 1-s
period after the torque had reached a plateau, whereas,
during isokinetic actions, signals were analyzed between
⫺10 and ⫹10° of the complete movement (i.e., ⫾10° around
the constant angular torque). This interval was selected
because RMS values for the three PF muscles were then
normalized to the amplitude (peak to peak) of the respective
M wave of the session (measured at 0°), to avoid any system-
J Appl Physiol • VOL
1385
atic influence of muscle length on EMG amplitude and to
reduce the variability across sessions. For the TA, the level of
coactivation was determined by normalizing the RMS values
with respect to the TA RMS recorded at baseline during
maximal DF at 0°. The normalized RMS-angle and RMS-
angular velocity relations for soleus, MG, LG, and TA mus-
cles were thus determined before and after the 4-wk period.
Statistical Analyses
Ordinary statistical methods including means and their
SDs or SEs were calculated for each parameter. A repeated-
measures ANOVA was used to assess the effect of EMS
training (EMS group) and the reliability of the measures (C
group) on dependent variables. Independent two-tailed t-
tests were used to analyze differences between means of
variables for the EMS and C groups. In each case, the level of
significance was established at P ⱕ 0.05.
RESULTS
Maximal Voluntary Torque and Associated
EMG Activity
Downloaded from jap.physiology.org on October 28, 2005
The isometric PF torque significantly increased after
EMS training exclusively at the training position (Fig.
1A; P ⬍ 0.05), i.e., 0°, and, because of the great vari-
ability, the increase failed to reach a significant level at
⫺20° (P ⫽ 0.1). Under isokinetic conditions (Fig. 1B),
the eccentric PF torque significantly increased at the
two angular velocities considered (P ⬍ 0.01 for ⫺120°/s
and P ⬍ 0.05 for ⫺60°/s), whereas concentric torque
values were not significantly different after training.
When the DF torque is considered, the only significant
change observed after the present training protocol
was an increase at the isometric training angle (Table
1; P ⬍ 0.05).
During PF, the RMS-angle relation shifted upward
after EMS training for the three agonist muscles (so-
leus, MG, and LG) but the RMS values significantly
increased exclusively for the soleus at 0 and ⫺20° (Fig.
2A; P ⬍ 0.05). During isokinetic PF, posttraining RMS
EMG values were significantly higher for the soleus at
the two eccentric velocities (Fig. 3A; P ⬍ 0.05), for the
MG at ⫺60°/s (Fig. 3B; P ⬍ 0.05), and for the LG at
⫺120°/s (Fig. 3C; P 0.05). No significant changes were
observed under concentric conditions. The present
EMS training did not modify the level of coactivation of
Fig. 1. Torque-angle (A) and torque-
angular velocity (B) relations obtained
during maximal voluntary plantar
flexion, before (Pre) and after (Post) 4
wk of electromyostimulation training
of the plantar flexor muscles. All val-
ues are means ⫾ SE from 8 experimen-
tal subjects. Posttraining torque val-
ues were significantly higher than
pretraining values (ANOVA repeated
measures) at * P ⬍ 0.05 and ** P ⬍
0.01.
92 • APRIL 2002 • www.jap.org
1386 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS

Table 1. Torque-angle and torque-angular velocity over, no significant difference was observed at baseline
relations obtained during maximal voluntary between EMS and C groups for these variables.
dorsiflexion, before and after the 4-wk intervention
period, for EMS and C groups Electrical Stimulation Results
EMS C At baseline, independent two-tailed t-test showed no
Before After Before After significant difference between the two experimental
groups in M-wave amplitude and PF contractile prop-
Ankle angle, °
⫺20 19.3 ⫾ 3.9 19.5 ⫾ 4.0 21.2 ⫾ 6.9 18.4 ⫾ 5.9 erties, and EMS training did not modify any of these
0 41.6 ⫾ 7.1 44.5 ⫾ 7.1* 42.1 ⫾ 6.6 39.8 ⫾ 9.3 parameters (Table 3).
⫹30 47.4 ⫾ 6.3 48.9 ⫾ 5.6 37.9 ⫾ 9.8 38.8 ⫾ 12.9 Finally, the present training protocol resulted in a
Angular velocity, significant increase in PF activation level (Fig. 7A; P ⬍
°/s
⫺120 44.2 ⫾ 8.8 45.4 ⫾ 12.4 40.0 ⫾ 8.8 41.5 ⫾ 13.2 0.01) and in PAP (Fig. 7B; P ⬍ 0.05), both by 11.9%,
⫺60 41.6 ⫾ 9.1 43.8 ⫾ 11.9 39.1 ⫾ 9.6 38.8 ⫾ 10.8 whereas no significant changes were observed for the C
60 22.0 ⫾ 2.8 22.4 ⫾ 3.7 23.5 ⫾ 5.6 22.8 ⫾ 7.3 group.
120 13.9 ⫾ 2.2 16.5 ⫾ 3.5 15.6 ⫾ 3.3 16.5 ⫾ 4.3
240 5.3 ⫾ 3.5 5.9 ⫾ 4.0 7.9 ⫾ 3.7 6.8 ⫾ 4.1
DISCUSSION
Values are means ⫾ SD. EMS, electromyostimulation group
(n ⫽ 8); C, control group (n ⫽ 6). * Posttraining torque values were The major findings of this study were that, after 4 wk
significantly higher than pretraining values at P ⬍ 0.05. of EMS training, PF contractile properties did not

Downloaded from jap.physiology.org on October 28, 2005

the TA during isometric (Fig. 2D) and isokinetic PF
(Fig. 3D). Also, the RMS values when this muscle acted
as an agonist (i.e., during DF) and the concomitant
level of coactivation of the three PFs were unchanged
after training (Table 2).
In the C group, isometric (Fig. 4A) and isokinetic
(Fig. 4B) torque values during PF and DF (Table 1) and
the associated RMS EMG (Figs. 5 and 6, Table 2)
values were unchanged after the 4-wk period. More-
change, whereas isometric and eccentric voluntary
torque increased. The increase in strength was accom-
panied by 1) significantly higher EMG activity of the
agonist (i.e., stimulated) muscles and no changes in
antagonist coactivation, 2) enhanced maximal volun-
tary activation, and 3) augmented PAP. In the absence
of a change in the C group, these results suggest that
increases in neural activation are likely to mediate the
voluntary torque gains observed after 4 wk of EMS
training.

Fig. 2. Normalized root mean square

(RMS) electromyographic (EMG)-angle
relations for respective muscles ob-
tained during maximal voluntary plan-
tar flexion, before and after 4 wk of
electromyostimulation training of the
plantar flexor muscles. A: soleus; B:
medial gastrocnemius (MG); C: lateral
gastrocnemius (LG); D: tibialis ante-
rior (TA). RMS EMG values for soleus,
MG, and LG were normalized to the
respective M-wave amplitude of the
session. TA RMS values were normal-
ized with respect to the RMS value
obtained during maximal voluntary
dorsiflexion (DF) at 0° before the 4-wk
period. All values are means ⫾ SE
from 8 experimental subjects. * Post-
training RMS values were significantly
higher than pretraining values (ANOVA
repeated measures) at P ⬍ 0.05.

J Appl Physiol • VOL 92 • APRIL 2002 • www.jap.org

 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS
Changes in activation were studied with two differ-
ent techniques in the present investigation. The RMS
EMG values obtained during voluntary contractions
were normalized to the respective M wave, and maxi-
mal voluntary activation was assessed with the twitch
interpolation technique. To our knowledge, these
methods have not been utilized in previous EMS stud-
ies. However, one prior study recorded the surface
EMG activity of muscles that had been submitted to
EMS training (10), and, after 7 wk of stimulation to
agonist biceps brachii, EMG increased for isometric
and eccentric conditions, but no significant change in
the antagonist triceps brachii activity was observed.
Although EMG activity was not normalized to the M
wave in this previous study, EMG results from the
present study, which were normalized to the M wave,
demonstrated a similar increase. In addition to agonist
EMG activity, the level of voluntary activation and the
response of three PF muscles and one DF muscle were
assessed in the present experiment. Indeed, muscles
other than the one directly stimulated might be af-
fected by EMS training because of current diffusion. In
line with Colson et al. (10), the EMG activity from the
antagonist TA (i.e., the level of coactivation) was not
affected by the present isometric EMS training. How-
ever, voluntary isometric training has been reported to
involve a reduction in the coactivation level (9). This
result enabled us to exclude one potential site of adap-
tation in the central nervous system, i.e., a reduced
J Appl Physiol • VOL
1387
Fig. 3. Normalized RMS EMG-angular
velocity relations for respective mus-
cles obtained during maximal volun-
tary plantar flexion, before and after 4
wk of electromyostimulation training
of the plantar flexor muscles. A: soleus;
B: MG; C: LG; D: TA. All values are
means ⫾ SE from 8 experimental sub-
jects. * Posttraining RMS values were
significantly higher than pretraining
values (ANOVA repeated measures) at
P ⬍ 0.05.
Downloaded from jap.physiology.org on October 28, 2005
neural drive to the antagonist muscle, accounting for
the greater torque observed after EMS training. In-
deed, the net torque around a joint will increase be-
cause of removal of the negative torque contributed by
the antagonist muscle, but this was not the case with
this particular EMS protocol.
The normalized RMS EMG values enabled assess-
ment of each individual muscle composing the triceps
surae (the main PF) to be assessed in response to
training, whereas the twitch interpolation technique
provided an estimation of the compound level of volun-
tary activation of the muscles innervated by the tibial
nerve. In the present experiment, EMS training re-
sulted in a significant increase in the normalized EMG
activity during isometric and eccentric actions and not
during concentric contractions, particularly for the so-
leus muscle, which, in turn, indicates a “specific” in-
crease of the neural drive (1, 21, 22; see also herein).
Maximal voluntary activation significantly increased
by 11.9% after training, thus revealing that EMS train-
ing increased the overall activity of the agonist mus-
cles. This enhanced voluntary activity could be ac-
counted for by an increase in motor unit recruitment or
discharge rate (30), both mediated by changes in de-
scending cortical outflow. Although the present meth-
odology does not permit determination of the relative
contribution of motor unit recruitment vs. discharge
rate to activation increases and to the enhanced
strength, there are at least three lines of evidence that
92 • APRIL 2002 • www.jap.org
1388 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS

Table 2. Normalized RMS EMG-angle and RMS EMG-angular velocity relations for respective muscles obtained
during maximal voluntary dorsiflexion, before and after the 4-wk intervention period, for EMS and C groups
EMS C

Before After Before After

Tibialis anterior
⫺20° 0.937 ⫾ 0.105 0.986 ⫾ 0.205 0.989 ⫾ 0.087 0.919 ⫾ 0.191
0° 1.000 ⫾ 0.000 1.084 ⫾ 0.170 1.000 ⫾ 0.000 0.967 ⫾ 0.169
⫹30° 0.821 ⫾ 0.090 0.888 ⫾ 0.121 0.851 ⫾ 0.077 0.775 ⫾ 0.228
⫺120°/s 1.018 ⫾ 0.129 1.050 ⫾ 0.119 1.110 ⫾ 0.149 1.238 ⫾ 0.229
⫺60°/s 1.024 ⫾ 0.093 1.059 ⫾ 0.063 0.991 ⫾ 0.147 1.057 ⫾ 0.093
60°/s 0.943 ⫾ 0.093 0.959 ⫾ 0.079 0.974 ⫾ 0.108 1.108 ⫾ 0.221
120°/s 0.950 ⫾ 0.053 1.044 ⫾ 0.138 1.018 ⫾ 0.077 1.128 ⫾ 0.194
240°/s 1.030 ⫾ 0.157 0.997 ⫾ 0.127 1.070 ⫾ 0.164 1.073 ⫾ 0.300
Soleus
⫺20° 0.005 ⫾ 0.002 0.005 ⫾ 0.002 0.004 ⫾ 0.001 0.004 ⫾ 0.001
0° 0.005 ⫾ 0.002 0.006 ⫾ 0.002 0.005 ⫾ 0.002 0.005 ⫾ 0.002
⫹30° 0.006 ⫾ 0.001 0.006 ⫾ 0.001 0.006 ⫾ 0.001 0.007 ⫾ 0.003
⫺120°/s 0.005 ⫾ 0.002 0.005 ⫾ 0.002 0.006 ⫾ 0.002 0.006 ⫾ 0.003
⫺60°/s 0.005 ⫾ 0.002 0.006 ⫾ 0.002 0.005 ⫾ 0.001 0.006 ⫾ 0.002
60°/s 0.006 ⫾ 0.001 0.005 ⫾ 0.002 0.005 ⫾ 0.002 0.006 ⫾ 0.002
120°/s 0.005 ⫾ 0.001 0.006 ⫾ 0.002 0.006 ⫾ 0.002 0.006 ⫾ 0.002
240°/s 0.006 ⫾ 0.002 0.006 ⫾ 0.002 0.007 ⫾ 0.002 0.006 ⫾ 0.001

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Medial gastrocnemius
⫺20° 0.006 ⫾ 0.002 0.007 ⫾ 0.002 0.006 ⫾ 0.003 0.005 ⫾ 0.002
0° 0.006 ⫾ 0.002 0.007 ⫾ 0.002 0.006 ⫾ 0.003 0.006 ⫾ 0.002
⫹30° 0.007 ⫾ 0.002 0.008 ⫾ 0.002 0.009 ⫾ 0.004 0.007 ⫾ 0.003
⫺120°/s 0.008 ⫾ 0.004 0.007 ⫾ 0.003 0.007 ⫾ 0.003 0.007 ⫾ 0.004
⫺60°/s 0.007 ⫾ 0.003 0.007 ⫾ 0.003 0.007 ⫾ 0.003 0.007 ⫾ 0.003
60°/s 0.007 ⫾ 0.003 0.008 ⫾ 0.003 0.007 ⫾ 0.003 0.007 ⫾ 0.003
120°/s 0.007 ⫾ 0.003 0.008 ⫾ 0.003 0.008 ⫾ 0.004 0.007 ⫾ 0.003
240°/s 0.008 ⫾ 0.003 0.008 ⫾ 0.003 0.009 ⫾ 0.003 0.009 ⫾ 0.006
Lateral gastrocnemius
⫺20° 0.008 ⫾ 0.003 0.008 ⫾ 0.003 0.007 ⫾ 0.002 0.006 ⫾ 0.002
0° 0.009 ⫾ 0.003 0.009 ⫾ 0.004 0.008 ⫾ 0.003 0.010 ⫾ 0.007
⫹30° 0.009 ⫾ 0.003 0.010 ⫾ 0.004 0.010 ⫾ 0.003 0.009 ⫾ 0.002
⫺120°/s 0.008 ⫾ 0.002 0.009 ⫾ 0.004 0.009 ⫾ 0.003 0.007 ⫾ 0.002
⫺60°/s 0.009 ⫾ 0.003 0.009 ⫾ 0.004 0.008 ⫾ 0.004 0.007 ⫾ 0.002
60°/s 0.009 ⫾ 0.003 0.009 ⫾ 0.003 0.009 ⫾ 0.004 0.008 ⫾ 0.002
120°/s 0.009 ⫾ 0.003 0.010 ⫾ 0.003 0.010 ⫾ 0.005 0.008 ⫾ 0.003
240°/s 0.010 ⫾ 0.003 0.011 ⫾ 0.004 0.011 ⫾ 0.004 0.010 ⫾ 0.005
Values are means ⫾ SD. EMS group, n ⫽ 8; C group, n ⫽ 6. Tibialis anterior root mean square (RMS) values were normalized with
respect to the RMS value obtained during maximal voluntary dorsiflexion at 0° before the 4-wk period. RMS electromyographic (EMG) values
for soleus, medial gastrocnemius and lateral gastrocnemius were normalized to the respective M-wave amplitude of the session.

substantiate a significant role for altered recruitment
rather than discharge rate. First, Miller et al. (28) have
recently claimed that single electrical impulses deliv-
ered during MVC detect an inability to recruit motor
units, whereas pulse train stimulation is required to
detect suboptimal synchronization and frequency mod-
ulation of already recruited motor units. The first
method was adopted in the present study; thus our
results can be interpreted as an increased recruitment
of motor units. Second, although Van Cutsem et al. (39)

Fig. 4. Torque-angle (A) and torque-

angular velocity (B) relations obtained
during maximal voluntary plantar
flexion, before and after the 4-wk pe-
riod for the control group. All values
are means ⫾ SE from 6 subjects.

J Appl Physiol • VOL 92 • APRIL 2002 • www.jap.org

 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS
have reported an increase in discharge rate of the TA
motor units after 12 wk of voluntary ballistic training,
it is still not clear if this mechanism contributes di-
rectly to increased force production (35). Indeed,
greater MVC force can be produced without the need to
drive motor units at excessively high discharge rates
(33). Third, improved motor unit recruitment can be
considered as an early response to resistance training,
explaining rapid increases in voluntary force produc-
tion (33), such as those observed in the present study.
Future investigations of EMS training will need to
determine the relative contribution of motor unit re-
cruitment and discharge rate to voluntary torque
gains, but also other motor unit properties (e.g., syn-
chronization), to better comprehend the neural adap-
tations associated with this form of training.
Although the neural mechanism, which is altered
subsequent to EMS training, cannot be directly eluci-
dated from this experiment, supraspinal centers, inter-
neurons that project to the motoneurons innervating
the triceps surae muscles, and, as previously dis-
cussed, ␣-motoneurons could be proposed as the site of
adaptation, accounting for the increased descending
outflow. Although EMS likely induces antidromic acti-
vation of the motoneurons, adaptations at the spinal
cord level are unlikely, because we observed no signif-
icant changes for the soleus reflex response evoked at
rest (H reflex) after the present EMS training (unpub-
lished observations). These observations suggest that
adaptation in motoneuron excitability and in afferent
J Appl Physiol • VOL
1389
Fig. 5. Normalized RMS EMG-angle
relations for respective muscles ob-
tained during maximal voluntary plan-
tar flexion, before and after the 4-wk
period for the control group. A: soleus;
B: MG; C: LG; D: TA. All values are
means ⫾ SE from 6 subjects.
Downloaded from jap.physiology.org on October 28, 2005
neurons or interneurons did not play a major role in
the increased activation that we found after training.
Consequently, the mechanism most likely accounting
for our results could be an increased volitional drive
from the supraspinal centers that causes greater acti-
vation of the muscles that assist the prime movers.
Although incomplete activation of the PF muscles
has previously been reported (6, 17, 24), the maximal
voluntary activation values estimated here might ap-
pear low (EMS group ⬃82%, C group ⬃80%). However,
similar values have been reported in many recent in-
vestigations that have focused on the knee extensor
muscles (3, 7, 19). Furthermore, the precision of the
twitch interpolation technique has been questioned (5),
and the actual position of the research community is
still equivocal (see Ref. 4). As a consequence, the
present activation level results cannot be interpreted
alone but in conjunction with the normalized EMG
activity recorded during voluntary contractions. As a
matter of fact, the results obtained in the C group
before and after the 4-wk period clearly confirm the
reliability of the present twitch interpolation data.
Because it is likely that EMS results in a reversal of
the recruitment order of motor units, and it may even
preferentially activate the largest motor units first (13,
16, 20), another intriguing observation of this type of
training is the possible preferential adaptation of the
type II motor units (10, 12, 26). This assumption is
supported by the increase in voluntary eccentric torque
that has been observed after EMS training (10, 26, 34)
92 • APRIL 2002 • www.jap.org
1390 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS
Fig. 6. Normalized RMS EMG-angular
velocity relations for respective mus-
cles obtained during maximal volun-
tary plantar flexion, before and after
the 4-wk period for the control group.
A: soleus; B: MG; C: LG; D: TA. All
values are means ⫾ SE from 6 sub-
jects.
and by a concomitant increase of the agonist EMG
activity (10). Results from the present study extend
these findings and confirm that neural activity, which
increases after EMS training, could be ascribed to
adaptations in the largest motor units. This assump-
tion is further supported by the significant EMG in-
crease that was observed for the two gastrocnemii
during eccentric PF and not during isometric and con-
centric contractions (Figs. 2 and 3) after EMS training.
Indeed, it has been reported that high-threshold motor
units of the LG (and probably of the MG) are selectively
activated during eccentric contractions (32), although
this is not a general finding (see Ref. 14). This is,
therefore, not surprising to observe significant torque
increases under isometric and eccentric conditions
without concomitant concentric torque increases.
It has recently been shown that a correlation exists
between postactivation twitch potentiation (i.e., the
increased force of a twitch after a MVC) and muscle
fiber type (19), with type II fibers conferring greater
potentiation (29). Although the exact peripheral mech-
anism by which training increases PAP is not fully
understood (19), phosphorylation of myosin light
chains during the MVC, which renders actin-myosin
more sensitive to Ca2⫹ in a subsequent twitch (37), has
been suggested as a possible mechanism. Furthermore,
the observation of greater PAP in type II fibers is likely
related to a greater capacity of the myosin light chains
J Appl Physiol • VOL
Downloaded from jap.physiology.org on October 28, 2005
to be phosphorylated in these fibers in response to
high-frequency activation. Only a few longitudinal
strength-training studies have tested for changes in
PAP, and to date there has been no attempt to inves-
tigate the effects of EMS training on PAP. If EMS
preferentially activates the largest motor units, one
could expect PAP increases after EMS training. Inter-
estingly, in the present investigation, PAP signifi-
cantly increased by 11.9% after training, whereas no
changes were observed in the C group.
In the present training protocol, PF twitch and dou-
blet and tetanus contractile properties evoked at rest
(i.e., not potentiated) were not modified. These evoked
contractions provide an indication of changes in muscle
properties and enable psychological factors and alter-
ations in the central recruitment pattern to be ex-
cluded. In this study, both electrical (M-wave) and
mechanical (contractile) properties were not affected
by training, and thus one can argue that 4 wk of EMS
have no significant effect on peripheral components of
the triceps surae neuromuscular system. In addition,
an increase in surface EMG activity in the absence of
M-wave modification supports results from prior stud-
ies (39) that neural adaptations mediate the increase
in voluntary torque subsequent to EMS training. Our
results for twitch contractile properties and the related
surface action potentials from the PF muscles are sim-
ilar to prior reports for the adductor pollicis (12). How-
92 • APRIL 2002 • www.jap.org
 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS 1391

Table 3. M-wave amplitude and plantar flexor contractile properties associated with single-twitch, paired
(doublet), and tetanic stimulation, before and after the 4-wk intervention period, for EMS and C groups
EMS C

Before After Before After

M-wave amplitude, mV
Soleus 9.46 ⫾ 2.77 8.99 ⫾ 1.93 10.93 ⫾ 2.76 10.34 ⫾ 2.99
MG 6.60 ⫾ 2.56 5.86 ⫾ 2.39 7.80 ⫾ 3.92 7.42 ⫾ 4.04
LG 5.51 ⫾ 3.42 5.06 ⫾ 2.84 4.72 ⫾ 1.31 6.47 ⫾ 2.61
Twitch properties
Pt, N 䡠 m 20.99 ⫾ 4.29 19.89 ⫾ 4.19 17.48 ⫾ 3.63 16.28 ⫾ 5.51
CT, ms 128.38 ⫾ 11.96 128.53 ⫾ 7.88 136.02 ⫾ 9.22 135.11 ⫾ 9.59
HRT, ms 90.28 ⫾ 16.68 93.81 ⫾ 17.34 94.43 ⫾ 10.85 98.64 ⫾ 8.39
RD, N 䡠 m 䡠 ms⫺1 0.300 ⫾ 0.053 0.285 ⫾ .065 0.244 ⫾ 0.060 0.242 ⫾ 0.086
RR, N 䡠 m 䡠 ms⫺1 0.185 ⫾ 0.038 0.167 ⫾ 0.042 0.141 ⫾ 0.042 0.134 ⫾ 0.052
Doublet properties
Pt, N 䡠 m 41.20 ⫾ 7.76 38.93 ⫾ 9.04 35.72 ⫾ 8.30 33.43 ⫾ 10.49
CT, ms 145.93 ⫾ 11.88 144.94 ⫾ 11.58 150.38 ⫾ 9.27 150.39 ⫾ 9.91
HRT, ms 108.21 ⫾ 17.39 109.88 ⫾ 11.18 104.34 ⫾ 5.43 106.56 ⫾ 10.98
RD, N 䡠 m 䡠 ms⫺1 0.540 ⫾ 0.092 0.510 ⫾ 0.123 0.460 ⫾ 0.122 0.446 ⫾ 0.148
RR, N 䡠 m 䡠 ms⫺1 0.339 ⫾ 0.055 0.296 ⫾ 0.068 0.286 ⫾ 0.077 0.253 ⫾ 0.083
Tetanus properties
Pt0, N 䡠 m 94.70 ⫾ 31.83 102.59 ⫾ 25.52 96.54 ⫾ 21.71 92.36 ⫾ 31.93

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RD0, N 䡠 m 䡠 ms⫺1 0.714 ⫾ 0.242 0.814 ⫾ 0.282 0.794 ⫾ 0.188 0.877 ⫾ 0.220
RR0, N 䡠 m 䡠 ms⫺1 0.718 ⫾ 0.220 0.849 ⫾ 0.126 0.703 ⫾ 0.213 0.614 ⫾ 0.297
Values are means ⫾ SD; EMS group, n ⫽ 8; C group, n ⫽ 6. MG, medial gastrocnemius; LG, lateral gastrocnemius; Pt, peak torque; CT,
contraction time; HRT, half relaxation time; RD, maximum rate of tension development; RR, maximum rate of tension relaxation; Pt0, RD0,
and RR0: Pt, RD, and RR measured from the tetanic stimulation, respectively. The interspike interval for paired stimulation was 10 ms, and
the duration of the 100-Hz tetanus was 250 ms.

ever, Duchateau and Hainaut (12) observed an in-
crease in maximal tetanic (100 Hz) tension after
training, which allowed these authors to conclude that
intracellular processes were altered subsequent to
EMS training and that muscle contractile kinetics
were not altered.
In the present experiment, a slight increase in teta-
nus contractile properties was observed, and perhaps
these changes did not achieve significance because the
duration of EMS training in the present study was only
Fig. 7. Plantar flexor maximal voluntary activation (A) and postac-
tivation potentiation (B) for EMS and control (C) group, before and
after the 4-wk period. All values are means ⫾ SE from 8 subjects
(EMS group) and 6 subjects (C group). Posttraining values were
significantly higher than pretraining values (ANOVA repeated mea-
sures) at * P ⬍ 0.05 and ** P ⬍ 0.01.
J Appl Physiol • VOL 92 • APRIL 2002 •
4 wk, whereas Duchateau and Hainaut (12) stimulated
for 6 wk. It is well known that several weeks of training
are necessary to observe changes at the muscle level
(e.g., hypertrophy), whereas neural adaptations likely
account for torque gains that occur after the first few
weeks of strength training (13, 36). In support of this
assumption, Eriksson et al. (15) showed that, in the
quadriceps femoris, muscle enzyme activities and fiber
size of mitochondrial properties did not change after 15
EMS training sessions spread over 4–5 wk. Finally, in
our experimental conditions, the observation that, af-
ter training, PF MVC significantly increased whereas
electrically evoked contractions did not change sup-
ports the viewpoint that adaptations at the muscle
level after 4 wk of EMS are unlikely.
In accordance with Behm et al. (5), it is not surpris-
ing to observe a great disparity between the PF MVC
and the maximal tetanic tension. It must, therefore, be
considered that, when voluntary vs. evoked PF con-
tractions are compared, muscles other than the soleus
and gastrocnemii (e.g., peroneus longus and brevis)
likely contribute to voluntary ankle joint torque but
not to the evoked torque (6). Moreover, the contribution
from the gastrocnemii to the voluntary ankle torque
measured with the knee flexed at 90° was reduced
because of shortened muscle length (11), consequently
resulting in a recruitment alteration (25).
We conclude that the increases in voluntary torque
after 4 wk of EMS training were largely due to an
increase in activation of the agonist (i.e., stimulated)
muscles. The most obvious change in the function of
the nervous system is an increase in the quantity of the
neural drive to muscle from the supraspinal centers.
www.jap.org
1392 ELECTROSTIMULATION TRAINING-INDUCED ADAPTATIONS
Also, preferential adaptation of the type II motor units
could be conjectured to explain the increases in PAP
and in gastrocnemii EMG observed after short-term
EMS training.
The authors are especially indebted to Drs. Roger M. Enoka and
Jennifer M. Jakobi from the Neural Control of Movement Laboratory
(Department of Kinesiology and Applied Physiology, University of
Colorado at Boulder) for critical reading of the paper, and to all of the
members of the laboratory for friendly support during data analysis
and redaction. We gratefully acknowledge the cooperation of all of
our subjects and the excellent technical assistance of Yves Ballay.
We also thank Gilles Cometti for providing the Compex stimulators.
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