gobbo2011

Eur J Appl Physiol (2011) 111:2451–2459
DOI 10.1007/s00421-011-2047-4
O R I G I N A L A R T I CL E
Transcutaneous neuromuscular electrical stimulation:
inXuence of electrode positioning and stimulus amplitude
settings on muscle response
M. Gobbo · P. GaVurini · L. Bissolotti ·
F. Esposito · C. Orizio
Received: 15 February 2011 / Accepted: 8 June 2011 / Published online: 30 June 2011
© Springer-Verlag 2011
Abstract The aim of the study was to investigate the
inXuence of two diVerent transcutaneous neuromuscular
electrical stimulation procedures on evoked muscle torque
and local tissue oxygenation. In the Wrst one (MP mode),
the cathode was facing the muscle main motor point and
stimulus amplitude was set to the level eliciting the maximal myoelectrical activation according to the amplitude of
the evoked electromyogram (EMG); in the second one (RC
mode), the electrodes were positioned following common
reference charts for electrode placement while stimulus
amplitude was set according to subject tolerance. Tibialis
Anterior (TA) and Vastus Lateralis (VL) muscles of 10
subjects (28.4 § 8.2 years) were tested in speciWc dynamometers to measure the evoked isometric torque. The
EMG and near-infrared spectroscopy probes were placed
on muscle belly to detect the electrical activity and local
metabolic modiWcations of the stimulated muscle, respectively. The stimulation protocol consisted of a gradually
increasing frequency ramp from 2 to 50 Hz in 7.5 s. Compared to RC mode, in MP mode the contractile parameters
(peak twitch, tetanic torque, area under the torque build-up)
and the metabolic solicitation (oxygen consumption and
hyperemia due to metabolites accumulation) resulted signiWcantly higher for both TA and VL muscles. MP mode
resulted also to be more comfortable for the subjects. Based
on the assumption that proper mechanical and metabolic
stimuli are necessary to induce muscle strengthening, our
results witness the importance of an optimized, i.e., comfortable and eVective, stimulation to promote the aforementioned muscle adaptive modiWcations.
Communicated by R. Bottinelli.
Keywords Neuromuscular electrical stimulation · Motor
point · Near-infrared spectroscopy · Muscle strengthening
This article is published as part of the Special Issue Cluster on the
XVIII Congress of the International Society of Electrophysiology and
Kinesiology (ISEK 2010) that took place in Aalborg, Denmark on
16–19 June 2010.
M. Gobbo (&) · C. Orizio
Department of Biomedical Sciences and Biotechnologies,
University of Brescia, Brescia, Italy
e-mail: [email protected]
M. Gobbo · P. GaVurini · L. Bissolotti · C. Orizio
Laboratory of Neuromuscular Rehabilitation (LaRiN),
Domus Salutis, Brescia, Italy
P. GaVurini
Faculty of Motor Sciences, University of Verona, Verona, Italy
F. Esposito
Department of Sport, Nutrition and Health Sciences,
University of Milan, Milan, Italy
Introduction
Skeletal muscles develop tension to accomplish diVerent
functions: besides being motor system actuators, they are
responsible for posture maintenance and they contribute as
active factors to joint functional stability.
Electrical stimulation, by exploiting the adaptive potential of skeletal muscles to increased loads, is widely applied
to maintain, improve or restore muscle trophism, and therefore function, in sports practice and rehabilitation settings
(Hainaut and Duchateau 1992; Lake 1992; Fluck and Hoppeler 2003; MaYuletti 2006). For the aforementioned purposes, stimulation of impaired or unimpaired muscles
predominantly adopts skin-adhesive pad electrodes placed
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over the target muscles to provide a transcutaneous neuromuscular electrical stimulation (TNMES).
TNMES generates an electric Weld between the two surface electrodes and creates a current Xow from anode to
cathode into the tissue: for innervated muscles, the current
evokes nervous action potentials from the intramuscular
unmyelinated motor axon terminal branches and hence elicits muscle Wber contraction (Salmons 1994; Farina et al.
2004); concomitantly, current stimulates sensory nervous
structures leading TNMES to be generally coupled to the
sensation of discomfort or pain (Reilly 1992) and to be plausibly ill tolerated by subjects. The occurrence of discomfort
or pain represents a major limiting factor for the strength
development with TNMES (Selkowitz 1985) as the operator/user is forced to lower the stimulus amplitude which
determines the amount of simultaneously active MUs and
therefore the entity of the evoked tension (Davies et al.
1985). As a consequence, the bearable low stimulation
intensities may be insuYcient to induce muscle adaptive
responses since, by analogy with voluntary exercise (Salmons 1994), the beneWcial eVects of TNMES are obtained by
an adequate intensity of contraction able to provide a proper
workload (mechanical stress) and an increased local oxygen
consumption (metabolic stress) (Hainaut and Duchateau
1992; Fluck and Hoppeler 2003). Indeed, in their review
Fluck and Hoppeler (2003) described the role of the
mechanical factor, i.e., the degree of tension, in activating
the multiple pathways that inXuence gene expression linked
to muscle hypertrophy, as well as the role of several metabolic perturbations occurring in severely exercised skeletal
muscle that serve as control in transcriptional induction.
Among metabolic stimuli, local tissue hypoxia has been
assumed to be an important sensing mechanism that links
muscle metabolic perturbations to plastic remodeling of the
muscle. For this, both mechanical output and indexes of
metabolic stress should be evaluated when assessing the
eVectiveness of a particular strengthening modality.
Although TNMES has gained a well established role as
main tool or in adjunction to other training or therapeutic
regimes within rehabilitation and sports practice (Hainaut
and Duchateau 1992; Snyder-Mackler et al. 1994; Stevens
et al. 2004; Callaghan and Oldham 2004; Talbot et al. 2003;
MaYuletti 2006), the procedures adopted by diVerent operators vary considerably incurring the risk of disparate and
inconsistent outcomes. As a matter of fact, out of some basic
studies on neuromuscular electromechanical features (e.g.,
KnaXitz et al. 1990; Merletti et al. 1990, Farina et al. 2004,
Gobbo et al. 2006, Minetto et al. 2008) in which the electrical stimulation is delivered via the main motor point (MP),
TNMES is commonly applied by referring to charts for surface electrode placement or atlases illustrating motor point
standard locations which quite markedly diVer one from
each other (Botter et al. 2011). Moreover, it is widespread to
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Eur J Appl Physiol (2011) 111:2451–2459
set the amplitude of stimulation according to subject tolerance, which might be substantially conditioned by several
factors: anatomical (inter-individual variability in the spatial
distribution of sensory and motor Wbers), physiological
(individual level of tolerance to electrical stimuli and adaptation over time) and psychological. In other words, at present,
a standard procedure for electrode positioning and amplitude
settings is lacking. As a consequence, systematic comparisons between diVerent procedures are essential to identify
the most eVective TNMES setting up.
Based on the hypothesis (Watson 2000) that the methodological procedures aVect the physical eVects of TNMES
(i.e., the distribution of the electric Weld and its relative
density through muscle tissue and on motor-sensory nerve
structures) which, in turn, inXuence the physiological
response, aim of the study was to compare two diVerent
procedures: in the Wrst one, the cathode was facing the muscle main motor point and stimulus amplitude was set to the
level eliciting the maximal myoelectrical activation according to the entity of the evoked electromyogram (EMG); in
the second one, electrodes were positioned following common legally marketed reference charts for electrode placement while stimulus amplitude was set according to subject
tolerance. With reference to the previously cited principle
stating that mechanical and metabolic stress represent the
stimuli needed for strengthening adaptation to occur, the
study focuses on acute eVects of the two above-mentioned
TNMES procedures, applied on diVerent human leg muscles, in terms of the entity of the evoked muscle mechanical
response and the related local oxygen expenditure and
regional blood supply.
Methods
Subjects
Ten subjects (six males, four females; age 28.4 § 8.2 years),
without neurological or orthopedical diseases, gave their
informed consent to participate to the study after being
given a full explanation of the experimental procedure
according to the Declaration of Helsinki (1964). The subjects had no previous experience with similar experiments
and underwent the two designed trials of stimulation (see
later for details) 1 week before the actual experimental session in order to be accustomed to the sensation of TNMES.
The local Ethical Research Committee approved the
proposed experimental design.
Measurements
For each subject, the dominant Tibialis Anterior (TA) and
Vastus Lateralis (VL) were investigated. The leg was Wxed
Eur J Appl Physiol (2011) 111:2451–2459
2453
Fig. 1 Experimental setup for
TA (left panels) and VL (right
panels) muscles. MP mode (top
panels) and RC mode (bottom
panels) stimulation setups are
presented. Black circles indicate
cathodes while gray circles indicate anode electrodes. The NIRS
probe is marked with N; the
EMG probe is marked with E
in a speciWcally designed dynamometer equipped with a
load–cell (Interface, model SM-500 N, linear response
between 0 and 500 N). Load–cell signal was sampled at
1,024 Hz and the isometric torque exerted by the muscle
was oZine calculated. To evaluate the electrical activity of
the stimulated muscle (M-wave) the electromyogram
(EMG) was detected by a probe, placed on the muscle
belly, with a linear array of four silver bars electrodes
0.5 cm spaced. The single diVerential EMG from the two
middle bars was ampliWed, Wltered (bandpass: 10–512 Hz)
and recorded at 1,024 samples/s. A near-infrared spectroscopy (NIRS) system (NIRO-200, Hamamatsu Photonics
K.K, Japan) was employed to study local muscle oxygenation and perfusion dynamics: the optode assembly was
secured to the skin surface close to the EMG probe and
covered with an optically dense sheet to minimize intrusion
of ambient light. NIRS measures relative changes in the
oxygenation status of hemoglobin (the concomitant minor
myoglobin changes can be neglected) and in the total
hemoglobin amount that is related to regional blood Xow
(Cettolo et al. 2007). The NIRO-200 device refreshed the
analog output signal with a 6 Hz frequency. The four NIRS
signals were sampled by the same analog-to-digital converter used for torque and EMG signals.
Experimental procedures
Subjects underwent two experimental sessions, one for TA
and one for VL. In each experimental session, bipolar stimulation was administered to the investigated muscle follow-
ing two diVerent procedures. In the Wrst one (MP mode),
the cathode electrode (5 £ 5 cm) was placed on the main
motor point (see Fig. 1, top panels). The motor points
(MPs) have been deWned as the superWcial points of stimulation with the lowest motor threshold, i.e., the points on
the skin over the muscle belly at which the smallest amount
of current is required to produce muscle contraction
(Delitto and Robinson 1989; KnaXitz et al. 1990; Lions
et al. 2004). Accordingly, the main MP was identiWed,
while stimulating at 2 Hz and gradually increasing the stimulation intensity, by moving a pen electrode (area = 1 cm2)
on the skin overlying the target muscle until a location providing a minimal detectable mechanical response was
found. Subsequently, the amplitude of the stimulus was set
to the one providing the maximal M-wave response, i.e.,
the compound muscle action potential for that MP, and
was termed AMPmax. The overall procedure took nearly
2–4 min for each subject. The anode electrode (5 £ 5 cm
for TA; 10 £ 5 for VL) was positioned distally over the
muscle–tendon junction for TA stimulation and on the
proximal fourth of the thigh for VL stimulation (see Fig. 1).
In the second procedure (RC mode), a physical therapist
was asked to place the cathode electrode (see Fig. 1, bottom
panels) according to the most common electrode positioning reference charts available on the market, while stimulation amplitude was set to the maximum level tolerated by
the subject. The mentioned most common electrode position areas for TA and VL are shown in Fig. 2 and were
inferred from a collection of 12 legally marketed charts
(Acuneeds, Australia; Anne Hartley Agency, USA; Beauty
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Eur J Appl Physiol (2011) 111:2451–2459
that has been used in a previous paper by Orizio et al.
(2004) to investigate the mechanical behavior of human
TA muscle, allows to study the muscle response from low
to more eYcient high stimulation rates thus mimicking the
natural increase in the Wring rate of the recruited MUs.
This pattern represents a well-tolerated tool to assess the
various muscle responses and has also been preferred to
the much more common constant frequency tetanic stimulation in light of the possibility to reach high mechanical
and metabolic responses in a few seconds, avoiding the
rapid onset of fatigue induced by sustained tetanic stimulation rates.
After administration of the frequency ramp, a 3 min
recovery period was allowed in each trial.
Comfort evaluation
At the end of each stimulation, subject perception of discomfort was quantiWed by a numeric rating scale (NRS):
the subjects were asked to indicate the level of discomfort
on a scale ranging from no pain (score = 0) to worst possible pain (score = 10).
Fig. 2 Most common cathode locations for TNMES of TA and VL
muscles inferred from a collection of 12 legally marketed charts.
Circle size is proportional to the number of charts indicating the same
location for cathode placement
Center Biosan, Biosan World Corporation S.r.l., Italy;
Compex®, Compex Medical SA, Switzerland; Cosmogamma®, Cosmogamma S.r.l., Italy; Globus, Globus Italia
S.r.l., Italy; IntelliSTIM®, Beac Biomedical, Italy; Neurotrac™, Verity Medical Ltd, UK; CefarCompex®, Djo LLC,
USA; Samms®, Italy; Tesmed®, Tesmed, Italy; WinForm®,
WinForm S.r.l., Italy) by digitally overlapping the scans
from the diVerent sources and matching the anatomical reference points (software for graphical editing: Adobe®
Photoshop®, Adobe Systems Incorporated, CA, USA). As
suggested by the selected manufacturer’s instructions, the
anode electrode (5 £ 5 cm) was placed proximally and
close to the cathode for TA while, for VL, the anode
(10 £ 5 cm) was kept on the proximal fourth of the thigh
(see Fig. 1).
Signal analysis
From the torque traces recorded during the frequency ramp
administration in MP mode and RC mode, the following
contractile parameters were investigated: the peak twitch
(pT) at 2 Hz, the tetanic tension at 50 Hz (T50), and the tension–time area (TT area) calculated as the area between
baseline and the tension signal.
To study the metabolic perturbations induced by the contractions elicited with the two stimulation modalities, the
proWles of the NIRS parameters, i.e., the oxy-hemoglobin
(O2Hb) and deoxy-hemoglobin (HHb) changes, the tissue
oxygenation index (TOI), and the normalized total hemoglobin index (THI), were considered. With reference to
baseline (average value during a 30 s rest just before stimulation) the values corresponding to the largest negative variation of O2Hb, TOI and THI (THImin) dynamics during
contraction and the values corresponding to the largest positive variation of HHb and THI (THImax) during recovery
were calculated.
Statistics
Stimulation protocols
The stimulation pattern consisted of a frequency ramp
with stimulation rate linearly increasing from 2 to 50 Hz in
7.5 s in order to retrieve information from both single
twitch and tetanic torque levels. Stimulus characteristics
were: biphasic square wave; 100 s duration. The pattern,
123
Data are reported as mean § standard deviations (SD)
for each trial. Paired t test was performed (SigmaPlot,
Systat Software Inc.) to identify, for each muscle, signiWcant diVerences in the analyzed parameters between the
two investigated trials. SigniWcance level was set to
p < 0.05.
Eur J Appl Physiol (2011) 111:2451–2459
Torque (N·m)
MP mode
RC mode
6
4
2
0
O2Hb (µmol/L) - HHb (µmol/L)
Fig. 3 Torque traces and related
NIRS proWles, from a representative subject, recorded during
the frequency ramp contraction
and during the recovery phase.
The signals refer to TA stimulation in MP mode (left panels)
and RC mode (right panels).
Dashed lines indicate baselines
used as reference for parameter
changes quantiWcation
2455
10
5
0
-5
-10
TOI (%)
70
60
50
THI (relative value)
40
1.2
1.1
1.0
0.9
0.8
0
5
10
15
20
0
Time (s)
Results
10
15
20
Time (s)
Table 1 Mechanical parameters from MP mode and RC mode stimulations of TA and VL muscles
Mechanical parameters
Typical isometric torque traces obtained from TA during
the frequency increasing ramp are reported in Fig. 3. The
entity of the mechanical signals resulted lower in RC mode
with respect to MP mode. In Table 1, for each muscle, the
mean (§SD) pT, T50 and TT area values obtained in MP
mode and RC mode trials are reported. All the parameters
showed signiWcant diVerence (p < 0.05) between the two
stimulation modalities.
5
pT (Nm)*
T50 (Nm)*
TT area (Nm s)*
TA
MP
0.68 § 0.43
4.78 § 3.44
59.6 § 42.3
RC
0.48 § 0.28
3.23 § 2.22
38.6 § 25.2
MP
1.68 § 0.87
11.3 § 5.65
131.1 § 72.6
RC
1.15 § 0.89
7.6 § 5.45
72.2 § 54.4
VL
Mean (N = 10) and SD values are reported
* SigniWcant diVerence (p < 0.05) between modalities
NIRS parameters
Figure 3 shows typical changes in NIRS parameters during
contraction and recovery phase. In Table 2, the averaged
(§SD) minimum values for O2Hb, TOI and THI (THImin)
and the averaged (§SD) maximum values for HHb and
THI (THImax) in response to TA and VL stimulation are
presented. All the investigated parameters were signiWcantly diVerent (p < 0.05) in the two applied stimulation
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Eur J Appl Physiol (2011) 111:2451–2459
Table 2 NIRS parameters changes in MP mode and RC mode stimulations of TA and VL muscles
O2Hb (mol/l)*
HHb (mol/l)*
TOI (%)*
THImin (r.v.)*
THImax (r.v.)*
MP
¡13.9 § 7.6
7.4 § 4.8
¡11.1 § 6.6
¡0.19 § 0.12
0.09 § 0.05
RC
¡10.1 § 7.5
4.1 § 3.4
¡8.5 § 6.7
¡0.15 § 0.11
0.05 § 0.03
MP
¡10.5 § 4.1
5.9 § 1.8
¡13.5 § 3.4
¡0.14 § 0.06
0.04 § 0.03
RC
¡5.8 § 3.3
1.8 § 0.9
¡5.9 § 2.9
¡0.07 § 0.02
0.03 § 0.02
TA
VL
Mean (N = 10) and SD values are reported. THImin (largest negative variation from baseline during contraction) and THImax (largest positive
variation from baseline during recovery) are reported in relative values (r.v.) with respect to 1
For each parameter there was a signiWcantly (*p < 0.05) lesser variation from baseline in RC mode with respect to MP mode
Table 3 NRS scores for pain evaluation collected after each trial
Subjects
Tibialis Anterior
Vastus Lateralis
MP mode
RC mode
MP mode
RC mode
1
0
3
0
1
2
0
2
0
3
3
0
0
0
0
4
0
3
0
3
5
0
6
0
0
6
1
8
0
4
7
0
0
0
6
8
0
2
0
0
9
1
3
1
3
10
0
5
0
2
Mean § SD
0.2 § 0.42
3.3 § 2.54
0.1 § 0.31
2.2 § 1.98
Score 0, no discomfort or pain; score 10, the worst possible pain
SigniWcant diVerence (p < 0.05) was present between MP mode and
RC mode for both the investigated muscles
modalities, indicating lower deviations from baseline in RC
mode with respect to MP mode.
Discomfort/pain perception
NRS scores for comfort level evaluation are presented in
Table 3. During MP mode trials, eight subjects indicated no
change in their comfort level, whereas two subjects for TA
and one subject for VL reported mild discomfort. During
RC trial most of the subjects complained of discomfort or
frank pain. NRS scores resulted signiWcantly higher
(p < 0.05) in RC mode than in MP mode for both the investigated muscles.
Discussion
In this work, the inXuence of two diVerent muscle transcutaneous electrical stimulation procedures on the evoked
123
muscular activity was studied. The work focused on the
analysis of torque and NIRS signals and demonstrated that
MP mode evoked larger mechanical and metabolic stress in
the muscle. As a consequence, based on Fluck and Hoppeler (2003) review, which described the role of mechanical factors and metabolic perturbations in conditioning
skeletal muscle tissue, our results indicate that the stimulation procedure might be a key factor in determining muscle
functional improvements induced by TNMES.
Unlike RC modality, which is adopted by most professionals and non-professional users, MP mode elicited signiWcantly greater mechanical responses evaluated by the
peak tension during single twitches, the maximum tetanic
tension and the area under the torque build-up during the
frequency ramp. In particular, according to Celichowski
et al. (1998) the tension–time area has been proven to be a
proper parameter for the estimation of the actual work performed by the contracting motor units and therefore for predicting the eVectiveness of muscle contraction. Evidence
exists that this area is proportional to the energy utilized by
the contracting skeletal muscle Wbers during brief periods
of isometric activity (De Haan et al. 1986; Jobsis and
DuYeld 1967; Lochynski et al. 2007). On this basis, an
optimal stimulation is obtained when the maximal area during contraction is reached: this was the case of MP modality, indicating a signiWcantly greater workload achieved by
the muscle when stimulated on the main MP at AMPmax.
Given the analogy of muscle adaptive responses to
increased tendon load by either volitional or stimulated
muscle actions (Salmons 1994), it is safe to consider that
the amount of the evoked muscle contractile work is crucial
to determine a proper conditioning eVect for TNMES as
well. In fact, Atha (1981) concluded that “muscles
strengthen in response to an appropriate stress”, Lai et al.
(1988) demonstrated that high training intensities (50% of
the maximal voluntary contraction) produced greater
strength gains than low training intensities (25% of the
maximal voluntary contraction) and MacDougall (1992)
stated more speciWcally that muscle mass increases after
Eur J Appl Physiol (2011) 111:2451–2459
working at intensities exceeding 60–70% of their forcegenerating capacity. To sum up, the higher the contractile
activity, i.e., the mechanical stress, achieved during the
stimulation regime, the greater the chance to exceed the
threshold levels of activity required to induce muscle
strengthening adaptation. The improved mechanical outcomes attained in MP mode trials are explainable by the
nearly total absence of discomfort or pain during the stimulation (see later) which is known (Selkowitz 1985) to represent a major limiting factor for TNMES eVectiveness. Poor
unpleasant sensory manifestations allow the technique to
deliver high current doses which, from the existing linear
relationship between stimulus amplitude and tension output
(Davies et al. 1985; MaYuletti 2010), suit a maximized
activation of the stimulated muscle portion.
MP mode resulted also in signiWcantly greater changes
in the investigated NIRS parameters with respect to RC
mode. From a metabolic standpoint, the energy required to
maintain the ATP turnover during muscle contraction is
initially derived from immediate intramuscular phosphocreatine stores, which are subsequently restored in the
recovery phase by oxidative metabolism (Hamaoka et al.
2007). The higher the oxygen consumption after contraction, the greater the energy expenditure during the previous contractile activity. HHb dynamics studied with NIRS
is well accepted to describe local muscle oxygen consumption (Chiappa et al. 2008): in MP mode, the more pronounced HHb increase during recovery suggests a greater
metabolic solicitation. Furthermore, considering that the
regulation of muscle perfusion depends on an auto-adaptation phenomenon proportional to the local release of
metabolites (Dyke et al. 1995), the hyperemic response
observed in the recovery phase by studying the THI proWles (Cettolo et al. 2007) indicates a stronger metabolic
stress induced by MP mode stimulation. The decrease in
TOI (tissue oxygen saturation) during contraction has been
attributed to the enhanced cellular oxygen uptake by mitochondria as a consequence of the increased metabolism of
the active motor units and to the increased intramuscular
pressure that reduces muscle blood supply and oxygen
delivery to muscle Wbers (Cettolo et al. 2007; Jensen et al.
1999). In the current study, the signiWcantly larger
decrease in TOI coupled with the pronounced decrease in
THI obtained in MP mode indicated that the contraction
was associated with a prominent drop in muscle O2 tension
probably due to either a greater local oxygen consumption
and a reduced oxygen supply caused by the increased
intramuscular pressure. Since local tissue hypoxia represents an important stimulus for muscle tissue adaptation, a
stimulation modality able to induce a more evident hypoxic state in the muscle, like MP mode, should be preferred in the light of the purposes of TNMES to improve
muscle trophism and function.
2457
Finally, in parallel with the sought mechanical and metabolic stress increases, the resulting NRS scores indicated a
much lower discomfort/pain perception during stimulation
in MP mode, thus assuring the maximum level of comfort
for the subject. The issue of discomfort/pain due to surface
electrical stimulation becomes particularly considerable
when sustained electrically evoked contractions need to be
induced, typically for rehabilitation purposes, leading some
subjects to totally reject TNMES as a treatment option and
others not to tolerate the optimal or necessary stimulus
amplitude and treatment duration. Selkowitz (1985) advocates that in order to strengthen skeletal muscle using ES
the relative increase in strength “may be determined by the
ability of the subject to tolerate longer and more forceful
contractions”. According to Table 3, most of the subjects
referred no discomfort during the MP mode stimulation
while the presence of a little discomfort or even frank pain
was constant in RC mode. This remarkable diVerence likely
relates to the peripheral nerve sensory/motor-speciWc subdivision pattern: the distinct path of the motor nerve
branches would then underlie the possibility of current
injection via MP (without exceeding AMPmax) to induce a
strong selective excitation of the axonal terminations
belonging to the motor trunk branched out from the mixed
spinal nerve, with a poor or absent concurrent depolarization of somatosensitive nerve Wbers. In favor of this explanation are some recent and preliminary data from our group
that resulted from experiments aimed at clarifying which
nervous structures are exactly excited during TNMES with
diVerent modalities, indicating that AMPmax current injection through areas adjacent to MP constantly involved the
simultaneous direct excitation of aVerent somatosensory
nerve fascicles, as attested by the peculiar quality of the
perceived pain, namely radiating, electric and tingling. It is
known that many individuals can develop tolerance to highamplitude painful TNMES after several days of familiarization (Stevenson and Dudley 2001), but it is reasonable to
expect that, using an optimized (comfortable and eVective)
TNMES procedure as MP mode, subjects might exploit
muscle adaptive responses from the early beginning of the
treatment program with no need for an initial period of
familiarization. In this line, the time required (2–4 min or
even less in subsequent sessions) to locate the main MP and
to search for AMPmax before the administration of the stimulation would likely result in the enhancement of the outcomes of TNMES. To note that, a proper stimulus
amplitude setting, in order to maximally recruit the MUs of
the stimulated MP without exceeding AMPmax, represents a
keypoint when selective stimulation of a speciWc muscle or
muscle group is needed. Indeed, this issue becomes crucial
when TNMES is applied to recover the balance between
agonist and antagonist muscle functions, a particular condition in which the possible activation and strengthening of
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the antagonists, resulting from excessively spreading current, should be prevented to avoid counterproductive
eVects.
Last consideration pertains to the activation of central
nervous structures during peripheral TNMES: an increased
and dose-dependent activity of speciWc neural areas
involved in motor control and somatosensory perception
such as primary sensorimotor cortex, cerebellum and cingulate gyrus (Smith et al. 2003) has been recently demonstrated. As reviewed by MaYuletti (2010), this feature
might have a relevant role in enhancing restoration or
improvement of neuromuscular eYciency and, in line with
the current intensity dependence of the mentioned central
contributions, MP mode should again be expected to maximize speciWc, in particular cerebellar and motor cortical,
supraspinal eVects of TNMES.
Conclusions
The results from this study conWrm the inXuence of electrode positioning on discomfort/pain perception during
TNMES (Lions et al. 2004) and deepen the relation
between stimulation sites and the entity of the evoked
mechanical and metabolic muscle responses. In particular,
stimulation in the more advanced MP mode was found to
be considerably more bearable, torque-producing and
energy-demanding, leading to greater mechanical and metabolic stress that represent the basic factors for muscle
strengthening adaptation. These are relevant Wndings since
TNMES of leg muscles has widespread application in
research and clinical settings: the evidences from this study
might be taken into account to promote the methodological
improvements and standardization of the technique allowing subjects to fully tolerate and beneWt from TNMES treatments and leading professionals to attain more consistent
and comparable outcomes between trials.
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