Atlas of the muscle motor points for the lower limb: implications for ...
Atlas of the muscle motor points for the lower limb: implications for ...
Atlas of the muscle motor points for the lower limb: implications for ...
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Eur J Appl Physiol (2011) 111:2461–2471<br />
DOI 10.1007/s00421-011-2093-y<br />
ORIGINAL ARTICLE<br />
<strong>Atlas</strong> <strong>of</strong> <strong>the</strong> <strong>muscle</strong> <strong>motor</strong> <strong>points</strong> <strong>for</strong> <strong>the</strong> <strong>lower</strong> <strong>limb</strong>: <strong>implications</strong><br />
<strong>for</strong> electrical stimulation procedures and electrode positioning<br />
Alberto Botter • Gianmosè Oprandi •<br />
Fabio Lanfranco • Stefano Allasia •<br />
Nicola A. Maffiuletti • Marco Alessandro Minetto<br />
Received: 23 February 2011 / Accepted: 4 July 2011 / Published online: 28 July 2011<br />
Ó Springer-Verlag 2011<br />
Abstract The aim <strong>of</strong> <strong>the</strong> study was to investigate <strong>the</strong><br />
uni<strong>for</strong>mity <strong>of</strong> <strong>the</strong> <strong>muscle</strong> <strong>motor</strong> point location <strong>for</strong> <strong>lower</strong><br />
<strong>limb</strong> <strong>muscle</strong>s in healthy subjects. Fifty-three subjects <strong>of</strong><br />
both genders (age range: 18–50 years) were recruited. The<br />
<strong>muscle</strong> <strong>motor</strong> <strong>points</strong> were identified <strong>for</strong> <strong>the</strong> following ten<br />
<strong>muscle</strong>s <strong>of</strong> <strong>the</strong> <strong>lower</strong> <strong>limb</strong> (dominant side): vastus medialis,<br />
rectus femoris, and vastus lateralis <strong>of</strong> <strong>the</strong> quadriceps<br />
femoris, biceps femoris, semitendinosus, and semimembranosus<br />
<strong>of</strong> <strong>the</strong> hamstring <strong>muscle</strong>s, tibialis anterior, peroneus<br />
longus, lateral and medial gastrocnemius. The <strong>muscle</strong><br />
<strong>motor</strong> point was identified by scanning <strong>the</strong> skin surface<br />
with a stimulation pen electrode and corresponded to <strong>the</strong><br />
location <strong>of</strong> <strong>the</strong> skin area above <strong>the</strong> <strong>muscle</strong> in which an<br />
electrical pulse evoked a <strong>muscle</strong> twitch with <strong>the</strong> least<br />
injected current. For each investigated <strong>muscle</strong>, 0.15 ms<br />
square pulses were delivered through <strong>the</strong> pen electrode at<br />
low current amplitude (\10 mA) and frequency (2 Hz). 16<br />
<strong>motor</strong> <strong>points</strong> were identified in <strong>the</strong> 10 investigated <strong>muscle</strong>s<br />
<strong>of</strong> almost all subjects: 3 <strong>motor</strong> <strong>points</strong> <strong>for</strong> <strong>the</strong> vastus lateralis,<br />
2 <strong>motor</strong> <strong>points</strong> <strong>for</strong> rectus femoris, vastus medialis,<br />
biceps femoris, and tibialis anterior, 1 <strong>motor</strong> point <strong>for</strong> <strong>the</strong><br />
remaining <strong>muscle</strong>s. An important inter-individual variability<br />
was observed <strong>for</strong> <strong>the</strong> position <strong>of</strong> <strong>the</strong> following 4 out<br />
<strong>of</strong> 16 <strong>motor</strong> <strong>points</strong>: vastus lateralis (proximal), biceps<br />
femoris (short head), semimembranosus, and medial gastrocnemius.<br />
Possible <strong>implications</strong> <strong>for</strong> electrical stimulation<br />
procedures and electrode positioning different from those<br />
commonly applied <strong>for</strong> thigh and leg <strong>muscle</strong>s are discussed.<br />
Keywords Neuromuscular electrical stimulation <br />
Motor entry point Motor branch Lower <strong>limb</strong><br />
Communicated by Roberto Bottinelli.<br />
This article is published as part <strong>of</strong> <strong>the</strong> Special Issue Cluster on <strong>the</strong><br />
XVIII Congress <strong>of</strong> <strong>the</strong> International Society <strong>of</strong> Electrophysiology and<br />
Kinesiology (ISEK 2010) that took place in Aalborg, Denmark on<br />
16–19 June 2010.<br />
A. Botter G. Oprandi M. A. Minetto<br />
Laboratory <strong>for</strong> Engineering <strong>of</strong> <strong>the</strong> Neuromuscular System<br />
(LISiN), Department <strong>of</strong> Electronics, Politecnico di Torino,<br />
Turin, Italy<br />
F. Lanfranco S. Allasia M. A. Minetto (&)<br />
Division <strong>of</strong> Endocrinology, Diabetology and Metabolism,<br />
Department <strong>of</strong> Internal Medicine, Molinette Hospital,<br />
University <strong>of</strong> Turin, C.so Dogliotti 14, 10126 Turin, Italy<br />
e-mail: marcominetto@libero.it<br />
N. A. Maffiuletti<br />
Neuromuscular Research Laboratory, Schul<strong>the</strong>ss Clinic, Zurich,<br />
Switzerland<br />
Introduction<br />
Neuromuscular electrical stimulation (NMES) involves <strong>the</strong><br />
transcutaneous application <strong>of</strong> electrical stimuli to superficial<br />
skeletal <strong>muscle</strong>s, with <strong>the</strong> main objective to trigger<br />
visible <strong>muscle</strong> contractions due to <strong>the</strong> activation <strong>of</strong> <strong>motor</strong><br />
neuron axons or intramuscular axonal branches (Hultman<br />
et al. 1983).<br />
Two stimulation techniques are commonly used <strong>for</strong><br />
NMES-based testing and training <strong>of</strong> <strong>the</strong> neuromuscular<br />
function: <strong>the</strong>y are referred to as monopolar and bipolar<br />
stimulation. The differences between <strong>the</strong>se two techniques<br />
are mainly related to <strong>the</strong> geometry and relative position <strong>of</strong><br />
<strong>the</strong> stimulation electrodes over <strong>the</strong> skin area. In <strong>the</strong><br />
monopolar configuration, two electrodes <strong>of</strong> different<br />
dimensions are used and <strong>the</strong> stimulation takes place in <strong>the</strong><br />
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proximity <strong>of</strong> only one <strong>of</strong> <strong>the</strong> two electrodes and not at <strong>the</strong><br />
o<strong>the</strong>r (Merletti et al. 1992). The active stimulation electrode<br />
(usually called ‘‘negative’’ electrode) has small<br />
dimensions (usually a few square centimeters) and is<br />
located ei<strong>the</strong>r near a nerve (nerve stimulation) or above a<br />
<strong>muscle</strong> <strong>motor</strong> point (<strong>muscle</strong> stimulation). The second<br />
electrode (usually called ‘‘reference’’ or ‘‘dispersive’’ or<br />
‘‘positive’’ or ‘‘return’’ electrode) is larger than <strong>the</strong> active<br />
electrode (around tens <strong>of</strong> square centimeters) and is generally<br />
placed over <strong>the</strong> antagonist <strong>muscle</strong> or opposite to <strong>the</strong><br />
active electrode. With this electrode configuration, <strong>for</strong> a<br />
certain current level, <strong>the</strong> current density in <strong>the</strong> proximity <strong>of</strong><br />
<strong>the</strong> active electrode may exceed <strong>the</strong> excitation level <strong>of</strong> <strong>the</strong><br />
axons/axonal branches, whereas <strong>the</strong> large dimensions <strong>of</strong><br />
<strong>the</strong> reference electrode assure that in its proximity <strong>the</strong><br />
current density remains below <strong>the</strong>ir excitation threshold.<br />
There<strong>for</strong>e, this technique allows <strong>the</strong> stimulation <strong>of</strong> localized<br />
populations <strong>of</strong> superficial <strong>motor</strong> units. In <strong>the</strong> bipolar<br />
arrangement, two electrodes <strong>of</strong> similar dimensions are<br />
applied over <strong>the</strong> <strong>muscle</strong>. With respect to <strong>the</strong> monopolar<br />
stimulation, current distribution is more confined in space<br />
and current density is more uni<strong>for</strong>m along <strong>the</strong> current path.<br />
Ano<strong>the</strong>r difference between <strong>the</strong> two configurations is <strong>the</strong><br />
number <strong>of</strong> electrodes needed <strong>for</strong> a multichannel stimulation:<br />
in <strong>the</strong> monopolar arrangement <strong>the</strong>re is only one reference<br />
electrode shared by all <strong>the</strong> active ones, while in <strong>the</strong><br />
bipolar case each active electrode has its own reference<br />
electrode. In both monopolar and bipolar <strong>muscle</strong> stimulation,<br />
<strong>the</strong> position <strong>of</strong> <strong>the</strong> stimulation electrodes is a critical<br />
issue: a proper electrode positioning over <strong>the</strong> main <strong>muscle</strong><br />
<strong>motor</strong> <strong>points</strong> is necessary to optimize <strong>the</strong> stimulation paradigm,<br />
that is, to maximize <strong>muscle</strong> tension and <strong>the</strong>re<strong>for</strong>e<br />
<strong>for</strong>ce output (Gobbo et al. 2011) and avoid/minimize<br />
discom<strong>for</strong>t.<br />
Muscle <strong>motor</strong> point, also known as <strong>motor</strong> entry point,<br />
represents <strong>the</strong> location where <strong>the</strong> <strong>motor</strong> branch <strong>of</strong> a nerve<br />
enters <strong>the</strong> <strong>muscle</strong> belly. It can be non-invasively identified<br />
by NMES as <strong>the</strong> skin area above <strong>the</strong> <strong>muscle</strong> in which an<br />
electrical pulse evokes a visible <strong>muscle</strong> twitch with <strong>the</strong><br />
least injected current. Its precise localization is paramount<br />
not only <strong>for</strong> proper positioning <strong>of</strong> <strong>the</strong> stimulation electrodes,<br />
but also <strong>for</strong> improving <strong>the</strong>rapeutic effectiveness and<br />
minimizing complications <strong>of</strong> anes<strong>the</strong>tic or neurolytic <strong>motor</strong><br />
nerve blocks (Karaca et al. 2000). Despite <strong>the</strong> pervasive<br />
diffusion <strong>of</strong> anatomic <strong>motor</strong> point charts (Prentice 2005;<br />
Reid 1920), that are <strong>of</strong>ten provided with <strong>the</strong> user manuals<br />
<strong>of</strong> commercially available stimulators, <strong>the</strong> uni<strong>for</strong>mity <strong>of</strong><br />
<strong>the</strong> <strong>motor</strong> point position <strong>for</strong> <strong>lower</strong> <strong>limb</strong> <strong>muscle</strong>s has never<br />
been investigated in a large group <strong>of</strong> healthy subjects.<br />
There<strong>for</strong>e, <strong>the</strong> aim <strong>of</strong> this study was to assess <strong>the</strong> interindividual<br />
variability <strong>of</strong> <strong>muscle</strong> <strong>motor</strong> point positions.<br />
Some <strong>of</strong> <strong>the</strong>se data have been presented in abstract <strong>for</strong>m<br />
(Oprandi et al. 2010).<br />
Materials and methods<br />
Subjects<br />
Fifty-three healthy subjects <strong>of</strong> both genders (28 males, 25<br />
females; age range: 18–50 years; body mass, mean ± SD:<br />
64.4 ± 11.4 kg; stature: 1.69 ± 0.08 m; body mass index:<br />
22.5 ± 3.5 kg/m 2 ) volunteered to participate in <strong>the</strong> study.<br />
They were free from neuromuscular or skeletal impairments.<br />
Health status was assessed by medical history,<br />
physical exam, blood count and chemistry, urinalysis, and<br />
electrocardiogram. The subjects received a detailed<br />
explanation <strong>of</strong> <strong>the</strong> procedures and gave written in<strong>for</strong>med<br />
consent prior to participation. The study con<strong>for</strong>med with<br />
<strong>the</strong> guidelines in <strong>the</strong> Declaration <strong>of</strong> Helsinki and was<br />
approved by <strong>the</strong> local ethics committee.<br />
Motor point identification, stimulation technique,<br />
and ultrasound examination<br />
The <strong>muscle</strong> <strong>motor</strong> <strong>points</strong> were identified <strong>for</strong> <strong>the</strong> dominant<br />
side <strong>of</strong> ten <strong>muscle</strong>s <strong>of</strong> <strong>the</strong> <strong>lower</strong> <strong>limb</strong> (see <strong>the</strong> list in<br />
Table 1). The <strong>motor</strong> <strong>points</strong> were identified while <strong>the</strong> subjects<br />
were positioned as follows: (a) seated, with <strong>the</strong> knee<br />
angle at 90°, <strong>for</strong> <strong>the</strong> investigation <strong>of</strong> <strong>the</strong> quadriceps <strong>muscle</strong>s;<br />
(b) prone, with <strong>the</strong> knee fully extended and <strong>the</strong> ankle<br />
at 150° (180° corresponded to full plantar flexion), <strong>for</strong> <strong>the</strong><br />
investigation <strong>of</strong> <strong>the</strong> hamstring <strong>muscle</strong>s and gastrocnemii;<br />
(c) supine, with <strong>the</strong> knee fully extended and <strong>the</strong> ankle at<br />
150° (180° corresponded to full plantar flexion), <strong>for</strong> <strong>the</strong><br />
investigation <strong>of</strong> <strong>the</strong> tibialis anterior and peroneus longus<br />
<strong>muscle</strong>s.<br />
For each <strong>muscle</strong>, <strong>the</strong> position <strong>of</strong> <strong>the</strong> identified <strong>motor</strong><br />
<strong>points</strong> was determined as absolute and relative distances<br />
along a reference line which was measured between a<br />
proximal and a distal anatomical landmark (see <strong>the</strong> list in<br />
Table 1).<br />
The <strong>muscle</strong> <strong>motor</strong> <strong>points</strong> corresponded to <strong>the</strong> locations<br />
<strong>of</strong> <strong>the</strong> skin area above <strong>the</strong> <strong>muscle</strong> in which an electrical<br />
pulse evoked a <strong>muscle</strong> twitch (as determined by visual<br />
inspection and manual palpation <strong>of</strong> <strong>the</strong> <strong>muscle</strong> and its<br />
proximal or distal tendon) with <strong>the</strong> least injected current.<br />
These locations were identified by scanning <strong>the</strong> skin surface<br />
with a stimulation pen electrode (small size cathode:<br />
1cm 2 surface; Globus Italia, Codognè, Italy) and with a<br />
large (50 9 80 mm) reference electrode placed over <strong>the</strong><br />
antagonist <strong>muscle</strong> to close <strong>the</strong> stimulation current loop<br />
(monopolar stimulation). The pen electrode was moved<br />
over <strong>the</strong> skin, while <strong>the</strong> stimulation current was slowly<br />
increased (starting from 1 to 2 mA) by <strong>the</strong> operator until a<br />
clear <strong>muscle</strong> twitch could be observed. Then, <strong>the</strong> stimulation<br />
current was decreased to a value that could still elicit a<br />
small mechanical response <strong>of</strong> <strong>the</strong> <strong>muscle</strong>. This <strong>motor</strong> point<br />
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Eur J Appl Physiol (2011) 111:2461–2471 2463<br />
Table 1 Muscles, anatomical landmarks, and thickness <strong>of</strong> <strong>the</strong> subcutaneous layer are reported<br />
Muscle Proximal–distal anatomical landmarks <strong>of</strong> <strong>the</strong> reference line Average (±SD)<br />
values <strong>of</strong><br />
subcutaneous layer<br />
thickness (mm)<br />
Vastus lateralis: proximal <strong>motor</strong><br />
point<br />
Vastus lateralis: central <strong>motor</strong><br />
point<br />
Vastus lateralis: distal <strong>motor</strong><br />
point<br />
Rectus femoris: proximal <strong>motor</strong><br />
point<br />
Rectus femoris: distal <strong>motor</strong><br />
point<br />
Vastus medialis: proximal<br />
<strong>motor</strong> point<br />
Vastus medialis: distal <strong>motor</strong><br />
point<br />
Anterior superior iliac spine–superolateral border <strong>of</strong> <strong>the</strong> patella 10 ± 5<br />
Apex <strong>of</strong> greater trochanter–superolateral border <strong>of</strong> <strong>the</strong> patella 7 ± 3<br />
Apex <strong>of</strong> greater trochanter–superolateral border <strong>of</strong> <strong>the</strong> patella 7 ± 3<br />
Anterior superior iliac spine–superior border <strong>of</strong> <strong>the</strong> patella 10 ± 5<br />
Anterior superior iliac spine–superior border <strong>of</strong> <strong>the</strong> patella 10 ± 4<br />
Anterior superior iliac spine–superomedial border <strong>of</strong> <strong>the</strong> patella 8 ± 3<br />
Anterior superior iliac spine–joint space in front <strong>of</strong> <strong>the</strong> anterior border <strong>of</strong> <strong>the</strong> medial<br />
collateral ligament<br />
Biceps femoris: long head Ischial tuberosity–apex <strong>of</strong> <strong>the</strong> fibular head 12 ± 4<br />
Biceps femoris: short head Ischial tuberosity–apex <strong>of</strong> <strong>the</strong> fibular head 9 ± 4<br />
Semitendinosus Ischial tuberosity–medial epicondyle <strong>of</strong> <strong>the</strong> tibia 10 ± 4<br />
Semimembranosus Ischial tuberosity–medial epicondyle <strong>of</strong> <strong>the</strong> tibia 7 ± 3<br />
Tibialis anterior: proximal Apex <strong>of</strong> <strong>the</strong> fibular head–apex <strong>of</strong> <strong>the</strong> medial malleolus 5 ± 2<br />
<strong>motor</strong> point<br />
Tibialis anterior: distal <strong>motor</strong> Apex <strong>of</strong> <strong>the</strong> fibular head–apex <strong>of</strong> <strong>the</strong> medial malleolus 4 ± 2<br />
point<br />
Peroneus longus Apex <strong>of</strong> <strong>the</strong> fibular head–apex <strong>of</strong> <strong>the</strong> lateral malleolus 5 ± 2<br />
Medial gastrocnemius Medial knee joint line–posterior superior portion <strong>of</strong> <strong>the</strong> calcaneal tuberosity 7 ± 2<br />
Lateral gastrocnemius Apex <strong>of</strong> <strong>the</strong> fibular head–posterior superior portion <strong>of</strong> <strong>the</strong> calcaneal tuberosity 6 ± 2<br />
6 ± 3<br />
position was temporarily marked with ink and subsequently<br />
measured with respect to <strong>the</strong> reference line. The position <strong>of</strong><br />
<strong>the</strong> reference electrode was <strong>the</strong> following: (a) just above<br />
<strong>the</strong> popliteal cavity/patella <strong>for</strong> <strong>the</strong> investigation <strong>of</strong> <strong>the</strong><br />
quadriceps/hamstring <strong>muscle</strong>s, respectively; (b) just below<br />
<strong>the</strong> tibial tuberosity/popliteal cavity <strong>for</strong> <strong>the</strong> investigation <strong>of</strong><br />
<strong>the</strong> gastrocnemii/tibialis anterior and peroneus longus<br />
<strong>muscle</strong>s, respectively. For all <strong>muscle</strong>s and subjects,<br />
0.15 ms square pulses were delivered through <strong>the</strong> pen<br />
electrode at a frequency <strong>of</strong> 2 Hz: <strong>the</strong> minimum current<br />
amplitude required to produce a visible contraction was<br />
\10 mA. Electrical stimulation was provided by a constant-current<br />
stimulator (DS7A, Digitimer Ltd, Welwyn<br />
Garden City, England).<br />
Since <strong>the</strong> thickness <strong>of</strong> <strong>the</strong> subcutaneous layer significantly<br />
affects <strong>the</strong> effectiveness <strong>of</strong> <strong>the</strong> stimulation (and<br />
<strong>the</strong>re<strong>for</strong>e <strong>the</strong> detectability <strong>of</strong> <strong>the</strong> <strong>muscle</strong> <strong>motor</strong> <strong>points</strong>), it<br />
was measured by ultrasonography (FFSonic UF-4000L,<br />
7.5 MHz linear array transducer, Fukuda Denshi, Tokyo,<br />
Japan), at <strong>the</strong> position <strong>of</strong> <strong>the</strong> identified <strong>motor</strong> <strong>points</strong>, as <strong>the</strong><br />
perpendicular distance between <strong>the</strong> bottom <strong>of</strong> <strong>the</strong> skin and<br />
<strong>the</strong> superior <strong>muscle</strong> fascial layers, thus <strong>the</strong> superficial<br />
aponeurosis was not included (Nordander et al. 2003). A<br />
water-soluble transmission gel was placed over <strong>the</strong> head <strong>of</strong><br />
<strong>the</strong> probe to increase acoustic coupling. Care was taken to<br />
exert minimal pressure to avoid compression <strong>of</strong> <strong>the</strong><br />
underlying tissues. For <strong>the</strong> different <strong>muscle</strong>s, <strong>the</strong> mean<br />
values <strong>of</strong> <strong>the</strong> subcutaneous layer thickness (Table 1) were<br />
comparable to previously reported data <strong>for</strong> normal weight<br />
subjects (Davies et al. 1986; Jones et al. 1986; Wallner<br />
et al. 2004).<br />
Statistical analysis<br />
Motor point positions along <strong>the</strong> reference lines are reported<br />
in both absolute (mean ± SD) and percentage values in<br />
relation to <strong>the</strong> total length <strong>of</strong> <strong>the</strong> reference line, starting<br />
from <strong>the</strong> proximal or distal anatomical landmark (that<br />
corresponded to a landmark <strong>of</strong> <strong>the</strong> knee joint <strong>for</strong> most <strong>of</strong><br />
<strong>the</strong> investigated <strong>muscle</strong>s).<br />
The uni<strong>for</strong>mity (across all subjects) <strong>of</strong> <strong>the</strong> <strong>motor</strong> point<br />
position along <strong>the</strong> reference line was estimated <strong>for</strong> each<br />
<strong>muscle</strong> on <strong>the</strong> basis <strong>of</strong> <strong>the</strong> spread (standard deviation, SD)<br />
<strong>of</strong> <strong>the</strong> normalized <strong>motor</strong> point position: normalization was<br />
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done with respect to <strong>the</strong> estimated length <strong>of</strong> <strong>the</strong> <strong>muscle</strong> (i.e.,<br />
average length <strong>of</strong> <strong>the</strong> reference line/2 <strong>for</strong> <strong>the</strong> short head <strong>of</strong><br />
<strong>the</strong> biceps femoris; average length <strong>of</strong> <strong>the</strong> reference line <strong>for</strong><br />
all <strong>the</strong> o<strong>the</strong>r <strong>muscle</strong>s). We arbitrarily defined ‘‘good’’ uni<strong>for</strong>mity<br />
<strong>for</strong> values\4%, ‘‘fair’’ uni<strong>for</strong>mity <strong>for</strong> values in <strong>the</strong><br />
range 4–6%, and ‘‘poor’’ uni<strong>for</strong>mity <strong>for</strong> values [6%. To<br />
verify <strong>the</strong> statistical significance <strong>of</strong> <strong>the</strong> differences among<br />
<strong>the</strong>se three uni<strong>for</strong>mities, we adopted <strong>the</strong> F test (MedCalc<br />
S<strong>of</strong>tware, Mariakerke, Belgium) <strong>for</strong> comparing <strong>the</strong> standard<br />
deviations (<strong>of</strong> <strong>the</strong> normalized <strong>motor</strong> point positions) <strong>of</strong><br />
different <strong>motor</strong> <strong>points</strong> identified in each <strong>muscle</strong>.<br />
Results<br />
Sixteen <strong>motor</strong> <strong>points</strong> were identified in <strong>the</strong> ten investigated<br />
<strong>muscle</strong>s <strong>of</strong> almost all subjects: <strong>the</strong> average positions <strong>of</strong><br />
<strong>the</strong>se <strong>motor</strong> <strong>points</strong> along <strong>the</strong> respective reference lines and<br />
<strong>the</strong>ir uni<strong>for</strong>mity are reported in Table 2.<br />
Three different <strong>motor</strong> <strong>points</strong> were identified <strong>for</strong> <strong>the</strong><br />
vastus lateralis <strong>muscle</strong>: a proximal <strong>motor</strong> point (blue<br />
circles in Fig. 1a) was identified in 51 out <strong>of</strong> 53 subjects, a<br />
central <strong>motor</strong> point (white circles in Fig. 1a) was identified<br />
in 42 out <strong>of</strong> 53 subjects, and a distal <strong>motor</strong> point (yellow<br />
circles in Fig. 1a) was identified in all subjects. Visual<br />
inspection and manual palpation <strong>of</strong> <strong>the</strong> <strong>muscle</strong> and its<br />
patellar tendon during stimulation allowed to distinguish<br />
among <strong>the</strong>se different <strong>motor</strong> <strong>points</strong> which activated different<br />
<strong>muscle</strong> portions (identified along <strong>the</strong> reference line<br />
from <strong>the</strong> proximal to distal aspect <strong>of</strong> <strong>the</strong> <strong>muscle</strong>): stimulation<br />
<strong>of</strong> <strong>the</strong> proximal <strong>motor</strong> point excited <strong>muscle</strong> fibers<br />
located proximally and medially, stimulation <strong>of</strong> <strong>the</strong> distal<br />
<strong>motor</strong> point excited fibers located distally and laterally, and<br />
stimulation <strong>of</strong> <strong>the</strong> central <strong>motor</strong> point excited fibers located<br />
in an intermediate position.<br />
Two different <strong>motor</strong> <strong>points</strong> were identified <strong>for</strong> <strong>the</strong> rectus<br />
femoris <strong>muscle</strong>: a proximal <strong>motor</strong> point (blue circles in<br />
Fig. 1b) was identified in all subjects and a distal <strong>motor</strong><br />
point (yellow circles in Fig. 1b) was identified in 52 out <strong>of</strong><br />
53 subjects. Proximal and distal stimulation excited fibers<br />
located laterally and medially to <strong>the</strong> reference line,<br />
respectively.<br />
Table 2 Muscles, number <strong>of</strong> cases, average positions <strong>of</strong> <strong>the</strong> <strong>motor</strong> <strong>points</strong> and <strong>the</strong>ir uni<strong>for</strong>mity are reported<br />
Muscle<br />
Number<br />
<strong>of</strong> cases<br />
Average (±SD)<br />
position <strong>of</strong> <strong>the</strong> <strong>motor</strong><br />
point along <strong>the</strong><br />
reference line (cm)<br />
Average (95% confidence<br />
limits) position <strong>of</strong> <strong>the</strong> <strong>motor</strong><br />
point along <strong>the</strong> reference line (%)<br />
Uni<strong>for</strong>mity<br />
<strong>of</strong> <strong>the</strong> <strong>motor</strong> point<br />
position (%)<br />
F statistics<br />
(significance<br />
level)<br />
Vastus lateralis: proximal<br />
<strong>motor</strong> point<br />
Vastus lateralis: central<br />
<strong>motor</strong> point<br />
Vastus lateralis: distal<br />
<strong>motor</strong> point<br />
Rectus femoris: proximal<br />
<strong>motor</strong> point<br />
Rectus femoris: distal<br />
<strong>motor</strong> point<br />
Vastus medialis: proximal<br />
<strong>motor</strong> point<br />
Vastus medialis: distal<br />
<strong>motor</strong> point<br />
51 22.5 (±4.1) a 50.3 (47.7–53.1) a 9.6 Poor F = 2.61<br />
(P = 0.002)<br />
42 15.0 (±3.2) b 34.3 (29.5–39.1) b 6.0 Fair F = 3.79<br />
53 9.5 (±1.6) b 20.6 (19.7–21.4) b 3.1 Good<br />
(P \ 0.001)<br />
53 24.8 (±2.8) b 53.2 (51.8–54.6) b 5.1 Fair F = 1.10<br />
(P = 0.73)<br />
52 16.0 (±2.4) b 35.8 (34.5–37.2) b 4.9 Fair<br />
53 10.3 (±1.6) b 22.7 (21.8–23.6) b 3.3 Good F = 1.53<br />
(P = 0.13)<br />
53 7.5 (±1.3) b 15.6 (14.9–16.4) b 2.7 Good<br />
Biceps femoris: long head 53 12.5 (±1.8) a 33.5 (32.3–34.8) a 4.5 Fair F = 10.22<br />
Biceps femoris: short head 53 13.2 (±2.6) b 39.3 (37.4–41.4) b 14.5 Poor<br />
(P \ 0.001)<br />
Semitendinosus 53 13.6 (±2.0) a 37.5 (36.1–39.0) a 5.3 Fair –<br />
Semimembranosus 53 15.5 (±2.5) b 42.6 (40.1–44.4) b 6.5 Poor –<br />
Tibialis anterior: proximal<br />
<strong>motor</strong> point<br />
52 10.5 (±1.6) a 27.5 (26.4–28.7) a 4.0 Fair F = 1.45<br />
(P = 0.18)<br />
Tibialis anterior: distal 52 16.5 (±1.9) a 43.1 (41.8–44.4) a 4.8 Fair<br />
<strong>motor</strong> point<br />
Peroneus longus 53 7.8 (±1.5) a 20.2 (19.1–21.3) a 3.9 Good –<br />
Medial gastrocnemius 53 10.1 (±2.6) a 26.0 (24.2–26.7) a 6.4 Poor –<br />
Lateral gastrocnemius 53 9.8 (±2.3) a 25.3 (23.8–26.8) a 5.5 Fair –<br />
Motor point position was measured starting from <strong>the</strong> a proximal or b distal anatomical landmark (landmarks are defined in Table 1)<br />
123
Eur J Appl Physiol (2011) 111:2461–2471 2465<br />
Fig. 1 Position <strong>of</strong> <strong>the</strong> <strong>motor</strong> <strong>points</strong> <strong>for</strong> <strong>the</strong> quadriceps <strong>muscle</strong>s in 53<br />
healthy subjects. The arrows indicate <strong>the</strong> average positions <strong>of</strong> <strong>the</strong><br />
<strong>motor</strong> <strong>points</strong> along <strong>the</strong> respective reference lines. a Motor <strong>points</strong><br />
identified in <strong>the</strong> vastus lateralis (blue circles, proximal <strong>motor</strong> point;<br />
white circles, central <strong>motor</strong> point; yellow circles, distal <strong>motor</strong> point).<br />
Continuous black line is <strong>the</strong> reference line <strong>for</strong> <strong>the</strong> proximal <strong>motor</strong><br />
point, while dashed black line is <strong>the</strong> reference line <strong>for</strong> <strong>the</strong> central and<br />
Two different <strong>motor</strong> <strong>points</strong> were identified in all subjects<br />
<strong>for</strong> <strong>the</strong> vastus medialis <strong>muscle</strong>: a proximal <strong>motor</strong><br />
point (blue circles in Fig. 1c) and a distal <strong>motor</strong> point<br />
(yellow circles in Fig. 1c). Proximal and distal stimulation<br />
excited fibers <strong>of</strong> <strong>the</strong> longus and obliquus portions <strong>of</strong> <strong>the</strong><br />
<strong>muscle</strong>, respectively.<br />
Two different <strong>motor</strong> <strong>points</strong> were identified in all subjects<br />
<strong>for</strong> <strong>the</strong> biceps femoris <strong>muscle</strong>: stimulation <strong>of</strong> <strong>the</strong><br />
proximal <strong>motor</strong> point excited fibers <strong>of</strong> <strong>the</strong> long head<br />
(Fig. 2a), whereas stimulation <strong>of</strong> <strong>the</strong> distal <strong>motor</strong> point<br />
excited fibers <strong>of</strong> <strong>the</strong> short head (Fig. 2b).<br />
Two different <strong>motor</strong> <strong>points</strong> were identified (by visual<br />
inspection and manual palpation <strong>of</strong> <strong>the</strong> <strong>muscle</strong> and its distal<br />
tendon during stimulation) in 52 out <strong>of</strong> 53 subjects <strong>for</strong> <strong>the</strong><br />
tibialis anterior <strong>muscle</strong>: stimulation <strong>of</strong> <strong>the</strong> proximal <strong>motor</strong><br />
point (blue circles in Fig. 3a) excited fibers located<br />
superficially and medially to <strong>the</strong> reference line, whereas<br />
stimulation <strong>of</strong> <strong>the</strong> distal <strong>motor</strong> point (yellow circles in<br />
Fig. 3a) excited fibers located deeply and laterally to <strong>the</strong><br />
reference line.<br />
One <strong>motor</strong> point was identified in all subjects <strong>for</strong> <strong>the</strong><br />
o<strong>the</strong>r <strong>muscle</strong>s investigated: semitendinosus (Fig. 2c),<br />
distal <strong>motor</strong> point. b Motor <strong>points</strong> identified in <strong>the</strong> rectus femoris<br />
(blue circles, proximal <strong>motor</strong> point; yellow circles, distal <strong>motor</strong><br />
point). c Motor <strong>points</strong> identified in <strong>the</strong> vastus medialis (blue circles,<br />
proximal <strong>motor</strong> point; yellow circles, distal <strong>motor</strong> point). Continuous<br />
black line is <strong>the</strong> reference line <strong>for</strong> <strong>the</strong> proximal <strong>motor</strong> point, while<br />
dashed black line is <strong>the</strong> reference line <strong>for</strong> <strong>the</strong> distal <strong>motor</strong> point<br />
semimembranosus (Fig. 2d), peroneus longus (Fig. 3b),<br />
medial (blue circles in Fig. 3c) and lateral gastrocnemius<br />
(yellow circles in Fig. 3c).<br />
An important inter-individual variability was observed<br />
<strong>for</strong> <strong>the</strong> position <strong>of</strong> <strong>the</strong> following 4 out <strong>of</strong> 16 <strong>motor</strong><br />
<strong>points</strong> (‘‘poor’’ uni<strong>for</strong>mity <strong>of</strong> <strong>the</strong> <strong>motor</strong> point position):<br />
vastus lateralis (proximal), biceps femoris (short head),<br />
semimembranosus, and medial gastrocnemius. On <strong>the</strong><br />
contrary, low variability was observed <strong>for</strong> <strong>the</strong> following<br />
4 out <strong>of</strong> 16 <strong>motor</strong> <strong>points</strong> (‘‘good’’ uni<strong>for</strong>mity <strong>of</strong> <strong>the</strong><br />
<strong>motor</strong> point position): vastus lateralis (distal), vastus<br />
medialis (proximal and distal), and peroneus longus<br />
(Table 2).<br />
Discussion<br />
Sixteen <strong>motor</strong> <strong>points</strong> were identified as maximum number<br />
in each subject and <strong>the</strong> uni<strong>for</strong>mity <strong>of</strong> <strong>the</strong>ir position along<br />
<strong>the</strong> respective reference lines was quantified <strong>for</strong> ten <strong>lower</strong><br />
<strong>limb</strong> <strong>muscle</strong>s. Quadriceps and tibialis anterior <strong>muscle</strong>s<br />
showed two or three <strong>motor</strong> <strong>points</strong> innervating different<br />
123
2466 Eur J Appl Physiol (2011) 111:2461–2471<br />
Fig. 2 Position <strong>of</strong> <strong>the</strong> <strong>motor</strong> <strong>points</strong> <strong>for</strong> <strong>the</strong> hamstring <strong>muscle</strong>s in 53<br />
healthy subjects, along <strong>the</strong> respective reference lines (continuous<br />
black lines): a long head <strong>of</strong> <strong>the</strong> biceps femoris; b short head <strong>of</strong> <strong>the</strong><br />
biceps femoris; c semitendinosus; d semimembranosus. The arrows<br />
indicate <strong>the</strong> average positions <strong>of</strong> <strong>the</strong> <strong>motor</strong> <strong>points</strong> along <strong>the</strong> respective<br />
reference lines<br />
<strong>muscle</strong> portions, whereas <strong>the</strong> o<strong>the</strong>r <strong>muscle</strong>s showed only<br />
one <strong>motor</strong> point.<br />
Motor point location and uni<strong>for</strong>mity<br />
The existence <strong>of</strong> three <strong>motor</strong> <strong>points</strong> <strong>for</strong> <strong>the</strong> vastus lateralis<br />
is in agreement with <strong>the</strong> anatomical dissection study by<br />
Sung et al. (2003) who found that <strong>the</strong> <strong>motor</strong> branch <strong>of</strong> <strong>the</strong><br />
vastus lateralis branches out from <strong>the</strong> femoral nerve trunk<br />
and divides into two primary sub-branches that penetrate<br />
<strong>the</strong> medial surface <strong>of</strong> <strong>the</strong> <strong>muscle</strong> at <strong>the</strong> proximal (superior<br />
sub-branch) and distal (inferior sub-branch) one-third <strong>of</strong><br />
<strong>the</strong> vastus lateralis, respectively (Fig. 4a). Moreover, in<br />
one case out <strong>of</strong> 22 cadaveric dissections (5%) <strong>the</strong>y found<br />
three sub-branches <strong>of</strong> <strong>the</strong> vastus lateralis <strong>motor</strong> branch. In a<br />
recent anatomical investigation, Becker et al. (2010)<br />
showed that on <strong>the</strong> basis <strong>of</strong> architecture and innervation,<br />
<strong>the</strong> vastus lateralis comprises four partitions which were<br />
named <strong>the</strong> superficial proximal, deep proximal, central, and<br />
deep distal partitions. Each <strong>of</strong> <strong>the</strong>se partitions was found to<br />
receive its unique nerve branch: two primary nerve<br />
branches (proximal and distal) which arise from <strong>the</strong> femoral<br />
nerve and subdivide in two secondary sub-branches<br />
(superficial proximal and deep proximal sub-branches from<br />
<strong>the</strong> proximal primary branch and mid-distal and distal subbranches<br />
from <strong>the</strong> distal primary branch) were found in<br />
most <strong>of</strong> <strong>the</strong> specimens (Fig. 4b). We observed in almost all<br />
subjects two <strong>motor</strong> <strong>points</strong> (proximal and distal) and in <strong>the</strong><br />
80% <strong>of</strong> <strong>the</strong> subjects, an additional (central) <strong>motor</strong> point<br />
innervating an intermediate portion <strong>of</strong> <strong>the</strong> <strong>muscle</strong>. It may<br />
be hypo<strong>the</strong>sized that <strong>the</strong> three <strong>motor</strong> <strong>points</strong> we identified in<br />
<strong>the</strong> vastus lateralis (by visual inspection and manual palpation<br />
<strong>of</strong> <strong>the</strong> <strong>muscle</strong> and its patellar tendon during stimulation)<br />
corresponded to <strong>the</strong> innervation pattern <strong>of</strong> <strong>the</strong><br />
superficial proximal, central, and deep distal partitions and<br />
that <strong>the</strong> <strong>motor</strong> point <strong>of</strong> <strong>the</strong> deep proximal partition was not<br />
identified due to <strong>the</strong> deep course <strong>of</strong> <strong>the</strong> deep proximal<br />
secondary sub-branch. Alternatively, it may be hypo<strong>the</strong>sized<br />
that <strong>the</strong> proximal <strong>motor</strong> point we identified corresponding<br />
to <strong>the</strong> entry point <strong>of</strong> <strong>the</strong> superficial proximal<br />
secondary sub-branch in some subjects and <strong>of</strong> <strong>the</strong> deep<br />
proximal secondary sub-branch in o<strong>the</strong>r subjects. This<br />
123
Eur J Appl Physiol (2011) 111:2461–2471 2467<br />
Fig. 3 Position <strong>of</strong> <strong>the</strong> <strong>motor</strong><br />
<strong>points</strong> <strong>for</strong> <strong>the</strong> leg <strong>muscle</strong>s in 53<br />
healthy subjects, along <strong>the</strong><br />
respective reference lines:<br />
a tibialis anterior (blue circles,<br />
proximal <strong>motor</strong> point; yellow<br />
circles, distal <strong>motor</strong> point);<br />
b peroneus longus; c medial<br />
(blue circles) and lateral (yellow<br />
circles) gastrocnemii. The<br />
arrows indicate <strong>the</strong> average<br />
positions <strong>of</strong> <strong>the</strong> <strong>motor</strong> <strong>points</strong><br />
along <strong>the</strong> respective reference<br />
lines<br />
could explain <strong>the</strong> poor uni<strong>for</strong>mity <strong>of</strong> <strong>the</strong> proximal <strong>motor</strong><br />
point position observed in this study.<br />
In <strong>the</strong> above-mentioned anatomical dissection study by<br />
Sung et al. (2003), it has also been shown that <strong>the</strong> <strong>motor</strong><br />
branch <strong>of</strong> <strong>the</strong> rectus femoris divides into two sub-branches:<br />
(a) <strong>the</strong> superior sub-branch, which runs laterally under <strong>the</strong><br />
posterior surface <strong>of</strong> <strong>the</strong> <strong>muscle</strong> and enters it on <strong>the</strong> posterior<br />
surface at a proximal one-third point <strong>of</strong> <strong>the</strong> rectus<br />
femoris; (b) <strong>the</strong> inferior sub-branch that pierces <strong>the</strong> <strong>muscle</strong><br />
fascia at <strong>the</strong> medial border <strong>of</strong> <strong>the</strong> <strong>muscle</strong> and runs downward<br />
along <strong>the</strong> medial margin <strong>of</strong> <strong>the</strong> <strong>muscle</strong>. This finding is<br />
in agreement with our observation <strong>of</strong> two <strong>motor</strong> <strong>points</strong> <strong>for</strong><br />
<strong>the</strong> rectus femoris whose stimulation activated different<br />
portions <strong>of</strong> <strong>the</strong> <strong>muscle</strong>.<br />
The observation <strong>of</strong> two <strong>motor</strong> <strong>points</strong> <strong>for</strong> <strong>the</strong> vastus<br />
medialis is also in agreement with two anatomical studies<br />
(Thiranagama 1990; Lefebvre et al. 2006) in which <strong>the</strong><br />
<strong>motor</strong> branch <strong>of</strong> <strong>the</strong> vastus medialis has been shown to<br />
divide into two sub-branches (Fig. 4c): (a) <strong>the</strong> short and<br />
lateral sub-branch supplying <strong>the</strong> proximal <strong>muscle</strong> fibers,<br />
that is <strong>the</strong> longus portion <strong>of</strong> <strong>the</strong> <strong>muscle</strong> (Lieb and Perry<br />
1968; Travnik et al. 1995), and (b) <strong>the</strong> long and medial subbranch<br />
supplying <strong>the</strong> distal fibers, that is <strong>the</strong> obliquus<br />
portion <strong>of</strong> <strong>the</strong> <strong>muscle</strong> (Lieb and Perry 1968; Travnik et al.<br />
1995).<br />
Only few anatomical studies investigated <strong>the</strong> <strong>motor</strong><br />
point location <strong>for</strong> <strong>the</strong> hamstring <strong>muscle</strong>s. Sunderland and<br />
Hughes (1946) and Seidel et al. (1996) studied <strong>the</strong> biceps<br />
femoris <strong>of</strong> adult cadaver <strong>limb</strong>s and found a dominant<br />
innervation pattern consisting <strong>of</strong> two primary <strong>motor</strong> branches<br />
issued from <strong>the</strong> sciatic nerve which supply <strong>the</strong> long<br />
head <strong>of</strong> <strong>the</strong> biceps femoris. Differently, An et al. (2010)<br />
showed in most <strong>of</strong> <strong>the</strong> examined <strong>muscle</strong>s (41 out <strong>of</strong> 50<br />
<strong>lower</strong> <strong>limb</strong>s from adult human cadavers) an innervation<br />
pattern consisting <strong>of</strong> one primary <strong>motor</strong> branch with <strong>the</strong><br />
<strong>motor</strong> entry point located at *40% <strong>of</strong> a reference line that<br />
connected <strong>the</strong> ischial tuberosity to <strong>the</strong> most proximal<br />
aspect <strong>of</strong> <strong>the</strong> medial femoral epicondyle. This result is in<br />
line with our observation <strong>of</strong> one <strong>motor</strong> point <strong>of</strong> <strong>the</strong> biceps<br />
femoris long head located at *33% <strong>of</strong> a reference line that<br />
connected <strong>the</strong> ischial tuberosity to <strong>the</strong> apex <strong>of</strong> <strong>the</strong> fibular<br />
head. Our observation <strong>of</strong> one <strong>motor</strong> point <strong>of</strong> <strong>the</strong> biceps<br />
femoris short head at *60% <strong>of</strong> <strong>the</strong> same reference line<br />
(starting from <strong>the</strong> proximal anatomical landmark) is also in<br />
agreement with <strong>the</strong> study <strong>of</strong> An et al. (2010) who observed<br />
one primary <strong>motor</strong> branch with <strong>the</strong> <strong>motor</strong> entry point<br />
located at *56% <strong>of</strong> <strong>the</strong> reference line between ischial<br />
tuberosity and medial femoral epicondyle. They also found<br />
one primary <strong>motor</strong> branch <strong>for</strong> <strong>the</strong> semimembranosus with<br />
<strong>the</strong> <strong>motor</strong> entry point located at *60% <strong>of</strong> <strong>the</strong> distance<br />
between ischial tuberosity and medial femoral epicondyle,<br />
in agreement with our observation <strong>of</strong> one <strong>motor</strong> point at<br />
*60% <strong>of</strong> <strong>the</strong> distance between ischial tuberosity and<br />
medial epicondyle <strong>of</strong> <strong>the</strong> tibia (starting from <strong>the</strong> proximal<br />
anatomical landmark). Differently from our observation <strong>of</strong><br />
one <strong>motor</strong> point <strong>for</strong> <strong>the</strong> semitendinosus <strong>muscle</strong>, An et al.<br />
123
2468 Eur J Appl Physiol (2011) 111:2461–2471<br />
A B C<br />
1<br />
2<br />
3<br />
4<br />
7<br />
8<br />
5<br />
6<br />
1<br />
2<br />
3<br />
4<br />
1<br />
2<br />
(2010) showed a dominant innervation pattern consisting <strong>of</strong><br />
two primary <strong>motor</strong> branches supplying <strong>the</strong> upper and <strong>lower</strong><br />
part <strong>of</strong> <strong>the</strong> <strong>muscle</strong>, with a proximal and a distal entry point<br />
located, respectively, at *20 and *60% <strong>of</strong> <strong>the</strong> distance<br />
between ischial tuberosity and medial femoral epicondyle.<br />
They also indicated that <strong>the</strong> <strong>motor</strong> entry point <strong>of</strong> <strong>the</strong> <strong>lower</strong><br />
part <strong>of</strong> <strong>the</strong> semitendinosus and that <strong>of</strong> <strong>the</strong> semimembranosus<br />
were closely located to each o<strong>the</strong>r. Since <strong>the</strong><br />
semimembranosus can be found at a deeper level than <strong>the</strong><br />
semitendinosus, it may be hypo<strong>the</strong>sized that <strong>the</strong> stimulation<br />
level we adopted to localize <strong>the</strong> <strong>motor</strong> point <strong>of</strong> <strong>the</strong> semimembranosus<br />
also activated <strong>the</strong> <strong>lower</strong> part <strong>of</strong> <strong>the</strong> more<br />
superficial semitendinosus. The inspection and palpation<br />
method we adopted has <strong>the</strong> advantages <strong>of</strong> simplicity and<br />
quickness. However, visual inspection <strong>of</strong> <strong>muscle</strong> contraction<br />
and surface palpation <strong>of</strong> semitendinosus and semimembranosus<br />
and <strong>the</strong>ir distal tendons could not aid in<br />
distinguishing between <strong>the</strong> two <strong>muscle</strong>s. Accordingly, a<br />
localization <strong>of</strong> <strong>the</strong> distal <strong>motor</strong> point <strong>of</strong> <strong>the</strong> semitendinosus<br />
more precise than that obtained by <strong>the</strong> inspection and<br />
palpation method we adopted may be required.<br />
The course <strong>of</strong> <strong>the</strong> tibial nerve has been widely studied.<br />
However, only a few authors investigated <strong>the</strong> course <strong>of</strong> its<br />
Fig. 4 Schematic view <strong>of</strong> <strong>the</strong> <strong>motor</strong> branches <strong>of</strong> <strong>the</strong> femoral nerve<br />
supplying <strong>the</strong> quadriceps <strong>muscle</strong>. a 1 Femoral nerve; 2 inguinal<br />
ligament; 3 <strong>motor</strong> branch <strong>of</strong> <strong>the</strong> rectus femoris; 4 <strong>motor</strong> branch <strong>of</strong> <strong>the</strong><br />
vastus lateralis with its superior (5) and inferior (6) sub-branches; 7<br />
<strong>motor</strong> branch <strong>of</strong> <strong>the</strong> vastus intermedius; 8 <strong>motor</strong> branch <strong>of</strong> <strong>the</strong> vastus<br />
medialis (adapted from Sung et al. 2003). Dotted lines indicate <strong>the</strong><br />
deep course <strong>of</strong> <strong>the</strong> <strong>motor</strong> branch <strong>of</strong> <strong>the</strong> vastus lateralis and its subbranches<br />
(which run under <strong>the</strong> vastus medialis and rectus femoris<br />
<strong>muscle</strong>s). b Superficial proximal (1) and deep proximal (2) subbranches<br />
<strong>of</strong> <strong>the</strong> proximal primary branch <strong>of</strong> <strong>the</strong> vastus lateralis; middistal<br />
(3) and distal (4) sub-branches <strong>of</strong> <strong>the</strong> distal primary branch <strong>of</strong><br />
<strong>the</strong> vastus lateralis (adapted from Becker et al. 2010). c Short and<br />
lateral (1) and long and medial (2) sub-branches <strong>of</strong> <strong>the</strong> <strong>motor</strong> branch<br />
<strong>of</strong> <strong>the</strong> vastus medialis (adapted from Thiranagama 1990)<br />
<strong>motor</strong> branches and <strong>the</strong> <strong>motor</strong> point distribution <strong>of</strong> <strong>the</strong><br />
gastrocnemius <strong>muscle</strong>s. Yoo et al. (2002) per<strong>for</strong>med <strong>the</strong><br />
anatomic dissection <strong>of</strong> 40 cadaver knees and localized <strong>the</strong><br />
<strong>motor</strong> <strong>points</strong> <strong>of</strong> <strong>the</strong> medial and lateral gastrocnemius<br />
<strong>muscle</strong>s at an absolute distance <strong>of</strong> *4.0 and *3.5 cm,<br />
respectively, from <strong>the</strong> medial and lateral epicondyle <strong>of</strong> <strong>the</strong><br />
femur. In ano<strong>the</strong>r dissection study, Sook Kim et al. (2002)<br />
showed a dominant innervation pattern consisting <strong>of</strong> one<br />
<strong>motor</strong> branch supplying <strong>the</strong> lateral gastrocnemius and one<br />
<strong>motor</strong> branch supplying <strong>the</strong> medial gastrocnemius, with <strong>the</strong><br />
respective <strong>motor</strong> entry <strong>points</strong> located at *10% <strong>of</strong> <strong>the</strong><br />
distance between <strong>the</strong> intercondylar and <strong>the</strong> intermalleolar<br />
line. The same authors also localized, in healthy subjects,<br />
<strong>the</strong> <strong>motor</strong> <strong>points</strong> <strong>of</strong> <strong>the</strong> medial and lateral gastrocnemius at<br />
*12 and *10% <strong>of</strong> <strong>the</strong> same distance, respectively (Lee<br />
et al. 2009). Fur<strong>the</strong>r, Kim et al. (2005) showed that <strong>the</strong><br />
<strong>motor</strong> <strong>points</strong> <strong>of</strong> <strong>the</strong> medial and lateral gastrocnemius were<br />
diffusely distributed along <strong>the</strong> longitudinal bulk <strong>of</strong> <strong>the</strong> two<br />
<strong>muscle</strong> heads: <strong>the</strong> range <strong>of</strong> <strong>motor</strong> point locations was from<br />
*10 to *37% <strong>of</strong> <strong>the</strong> distance between <strong>the</strong> intercondylar<br />
and <strong>the</strong> intermalleolar line <strong>for</strong> <strong>the</strong> medial gastrocnemius,<br />
and from *12 to *38% <strong>of</strong> <strong>the</strong> same distance <strong>for</strong> <strong>the</strong> lateral<br />
gastrocnemius. Consistently, we found an average<br />
123
Eur J Appl Physiol (2011) 111:2461–2471 2469<br />
position <strong>of</strong> <strong>the</strong> two gastrocnemius <strong>motor</strong> <strong>points</strong> at *25%<br />
<strong>of</strong> respective reference lines, with poor (<strong>for</strong> medial gastrocnemius)<br />
or fair (<strong>for</strong> lateral gastrocnemius) uni<strong>for</strong>mity<br />
across subjects.<br />
The innervation <strong>of</strong> <strong>the</strong> tibialis anterior and peroneus<br />
longus <strong>muscle</strong>s is provided by <strong>the</strong> common peroneal nerve<br />
which first originates from <strong>the</strong> sciatic nerve in <strong>the</strong> popliteal<br />
fossa region and travels across <strong>the</strong> lateral head <strong>of</strong> <strong>the</strong><br />
gastrocnemius toward <strong>the</strong> fibular head, and <strong>the</strong>n separates<br />
into <strong>the</strong> superficial and deep peroneal nerves. The superficial<br />
peroneal nerve innervates <strong>the</strong> peroneus longus and<br />
brevis <strong>muscle</strong>s, while <strong>the</strong> deep peroneal nerve innervates<br />
<strong>the</strong> anterior leg <strong>muscle</strong>s. In agreement with our findings,<br />
Lee et al. (2011) recently demonstrated that <strong>the</strong> <strong>motor</strong> entry<br />
<strong>points</strong> <strong>of</strong> <strong>the</strong> superficial peroneal nerve supplying <strong>the</strong> peroneus<br />
longus <strong>muscle</strong> were located from 10 to 60% <strong>of</strong> <strong>the</strong><br />
distance between <strong>the</strong> apex <strong>of</strong> <strong>the</strong> fibular head and <strong>the</strong> apex<br />
<strong>of</strong> <strong>the</strong> lateral malleolus. To our knowledge, no previous<br />
study attempted to localize <strong>the</strong> <strong>motor</strong> <strong>points</strong> <strong>of</strong> <strong>the</strong> deep<br />
peroneal nerve to <strong>the</strong> tibialis anterior <strong>muscle</strong>. However, it<br />
has been shown that <strong>the</strong> <strong>muscle</strong>s <strong>of</strong> <strong>the</strong> deep posterior<br />
compartment <strong>of</strong> <strong>the</strong> leg (popliteus, flexor hallucis longus,<br />
tibialis posterior, flexor digitorum longus) are innervated<br />
by one or two primary <strong>motor</strong> branches arising from <strong>the</strong><br />
tibial nerve (Apaydin et al. 2008). Similarly, it is not surprising<br />
that <strong>the</strong> tibialis anterior <strong>muscle</strong> had more than one<br />
<strong>motor</strong> point in our study, which could correspond to <strong>the</strong><br />
entry <strong>points</strong> <strong>of</strong> different nerve branches supplying different<br />
portions <strong>of</strong> <strong>the</strong> <strong>muscle</strong>. In fact, <strong>the</strong> bipennate <strong>muscle</strong><br />
architecture (Maganaris and Baltzopoulos 1999) could<br />
imply that <strong>the</strong> superficial and deep unipennate parts have a<br />
distinct pattern <strong>of</strong> innervation: this hypo<strong>the</strong>sis is in agreement<br />
with our observation <strong>of</strong> a differential activation <strong>of</strong><br />
<strong>the</strong> superficial and deep portion <strong>of</strong> <strong>the</strong> <strong>muscle</strong> following<br />
stimulation <strong>of</strong> <strong>the</strong> proximal and distal <strong>motor</strong> point,<br />
respectively.<br />
Implications <strong>for</strong> electrical stimulation procedures<br />
and electrode positioning<br />
The demonstration that different <strong>motor</strong> <strong>points</strong> can be<br />
identified in <strong>the</strong> three superficial <strong>muscle</strong>s <strong>of</strong> <strong>the</strong> quadriceps,<br />
<strong>the</strong> most <strong>of</strong>ten stimulated <strong>muscle</strong> <strong>for</strong> NMES rehabilitation,<br />
‘‘prehabilitation’’, and training purposes (Bax et al. 2005;<br />
Maffiuletti 2010), may have relevant <strong>implications</strong> <strong>for</strong> <strong>the</strong><br />
placement <strong>of</strong> stimulation electrodes. It is well-known that<br />
<strong>motor</strong> unit recruitment during NMES is spatially fixed<br />
(Bigland-Ritchie et al. 1979; Gregory and Bickel 2005),<br />
thus implying that <strong>the</strong> same <strong>muscle</strong> units are repeatedly<br />
activated by <strong>the</strong> same amount <strong>of</strong> electrical current, which,<br />
in turn, hastens <strong>the</strong> onset <strong>of</strong> <strong>muscle</strong> fatigue (Bigland-<br />
Ritchie et al. 1979; Binder-Macleod and Snyder-Mackler<br />
1993). Such early occurrence <strong>of</strong> fatigue represents a major<br />
limitation <strong>of</strong> NMES. In order to maximize <strong>the</strong> spatial<br />
recruitment during NMES, thus minimizing <strong>the</strong> extent <strong>of</strong><br />
<strong>muscle</strong> fatigue, it has been recommended to adopt different<br />
subterfuges during a treatment session such as <strong>the</strong> progressive<br />
increase in current intensity, alteration in <strong>muscle</strong><br />
length, and displacement <strong>of</strong> active electrodes (Maffiuletti<br />
2010). The existence <strong>of</strong> different <strong>motor</strong> <strong>points</strong> within each<br />
<strong>of</strong> <strong>the</strong> three superficial heads <strong>of</strong> <strong>the</strong> quadriceps suggests<br />
that a change in <strong>the</strong> population <strong>of</strong> activated fibers could<br />
also be obtained through a multichannel stimulation technique<br />
that involves a non-synchronous activation <strong>of</strong> different<br />
<strong>muscle</strong> volumes. Consistently, Malesević et al.<br />
(2010) recently showed in paraplegic patients that NMES<br />
delivered to one quadriceps via multi-pad electrodes (one<br />
anode positioned at <strong>the</strong> distal part <strong>of</strong> <strong>the</strong> quadriceps and<br />
four cathodes distributed over <strong>the</strong> quadriceps <strong>muscle</strong>s)<br />
delayed <strong>the</strong> occurrence <strong>of</strong> fatigue with respect to a conventional<br />
stimulation (one electrode positioned over <strong>the</strong> top<br />
<strong>of</strong> <strong>the</strong> quadriceps and <strong>the</strong> o<strong>the</strong>r over <strong>the</strong> distal part <strong>of</strong> <strong>the</strong><br />
<strong>muscle</strong>).<br />
Besides neuromuscular training, NMES finds application<br />
in <strong>the</strong> in vivo assessment <strong>of</strong> <strong>muscle</strong> contractile properties,<br />
fatigue pr<strong>of</strong>ile, and level <strong>of</strong> voluntary activation<br />
(Maffiuletti 2010). For example, supramaximal stimulation<br />
<strong>of</strong> <strong>the</strong> femoral nerve during a maximal voluntary contraction<br />
is an established technique <strong>for</strong> <strong>the</strong> assessment <strong>of</strong><br />
quadriceps activation (Gandevia 2001). Place et al. (2010)<br />
recently showed that quadriceps <strong>muscle</strong> belly stimulation<br />
can be used to assess <strong>the</strong> level <strong>of</strong> voluntary activation as a<br />
valid alternative to <strong>the</strong> femoral nerve stimulation that may<br />
be associated with discom<strong>for</strong>t and/or stimulation electrode<br />
displacement during <strong>the</strong> voluntary ef<strong>for</strong>t. It may be<br />
hypo<strong>the</strong>sized that a multichannel NMES technique per<strong>for</strong>med<br />
with several electrodes placed over <strong>the</strong> different<br />
<strong>motor</strong> <strong>points</strong> <strong>of</strong> <strong>the</strong> superficial heads <strong>of</strong> quadriceps can<br />
increase <strong>the</strong> validity <strong>of</strong> <strong>the</strong> neuromuscular testing and<br />
minimize subjective discom<strong>for</strong>t.<br />
Electrical stimulation <strong>of</strong> <strong>the</strong> gastrocnemii is usually<br />
per<strong>for</strong>med with two large rectangular electrodes placed<br />
below <strong>the</strong> popliteal cavity and over <strong>the</strong> distal portion <strong>of</strong> <strong>the</strong><br />
two <strong>muscle</strong> heads, with <strong>the</strong> major side <strong>of</strong> <strong>the</strong> electrodes<br />
perpendicular to <strong>the</strong> longitudinal axis <strong>of</strong> <strong>the</strong> triceps surae<br />
(Bergquist et al. 2011). On <strong>the</strong> basis <strong>of</strong> <strong>the</strong> <strong>motor</strong> point<br />
distribution we found in <strong>the</strong> gastrocnemii, it may be proposed<br />
that an alternative placement <strong>of</strong> <strong>the</strong> electrodes (one<br />
over <strong>the</strong> lateral head and <strong>the</strong> o<strong>the</strong>r over <strong>the</strong> medial head),<br />
with <strong>the</strong>ir major side parallel to <strong>the</strong> <strong>muscle</strong> longitudinal<br />
axis, can be used as a valid and more effective alternative<br />
to <strong>the</strong> usual electrode placement.<br />
Finally, <strong>the</strong> existence <strong>of</strong> two distinct <strong>motor</strong> <strong>points</strong> could<br />
imply that <strong>the</strong> tibialis anterior has to be stimulated with <strong>the</strong><br />
two electrodes located above both <strong>motor</strong> <strong>points</strong> in case <strong>of</strong><br />
bipolar arrangement, or with <strong>the</strong> active electrode properly<br />
123
2470 Eur J Appl Physiol (2011) 111:2461–2471<br />
positioned over <strong>the</strong> main <strong>motor</strong> point in case <strong>of</strong> monopolar<br />
stimulation.<br />
However, it is not possible to infer from <strong>the</strong> present data<br />
if <strong>the</strong>se electrode configurations or <strong>the</strong> above-mentioned<br />
multichannel stimulation can improve <strong>the</strong> effectiveness <strong>of</strong><br />
<strong>the</strong> electrical stimulation procedures. Fur<strong>the</strong>r studies<br />
comparing <strong>the</strong> electromechanical responses obtained by<br />
different stimulation sites and modalities are required to<br />
resolve elements <strong>of</strong> confusion and controversy and improve<br />
standardization <strong>of</strong> electrical stimulation procedures.<br />
In conclusion, this study demonstrates that <strong>muscle</strong> <strong>motor</strong><br />
<strong>points</strong> can be easily and quickly localized in <strong>the</strong> <strong>lower</strong> <strong>limb</strong><br />
through visual inspection and manual palpation <strong>of</strong> <strong>the</strong><br />
<strong>muscle</strong> during electrical stimulation and that an interindividual<br />
variability in <strong>the</strong> <strong>motor</strong> point position exists and<br />
may limit <strong>the</strong> usefulness <strong>of</strong> <strong>the</strong> anatomic <strong>motor</strong> point<br />
charts, especially <strong>for</strong> posterior thigh and leg <strong>muscle</strong>s.<br />
Acknowledgments Musculoskeletal Images are from <strong>the</strong> University<br />
<strong>of</strong> Washington ‘‘Musculoskeletal <strong>Atlas</strong>: A Musculoskeletal <strong>Atlas</strong> <strong>of</strong><br />
<strong>the</strong> Human Body’’ by Carol Teitz, M.D. and Dan Graney, Ph.D.<br />
Copyright 2003–2004 University <strong>of</strong> Washington. All rights reserved<br />
including all photographs and images. No re-use, re-distribution or<br />
commercial use without prior written permission <strong>of</strong> <strong>the</strong> authors and<br />
<strong>the</strong> University <strong>of</strong> Washington. The authors are grateful to Pr<strong>of</strong>.<br />
R. Merletti (LISiN, Politecnico di Torino, Italy) <strong>for</strong> his careful review<br />
<strong>of</strong> <strong>the</strong> final version <strong>of</strong> <strong>the</strong> manuscript and to Dr. D. Antista (School <strong>of</strong><br />
Motor Sciences, Turin, Italy) <strong>for</strong> his valuable assistance in subject<br />
recruitment and evaluation. This study was supported by Regional<br />
Health Administration Project ‘‘Ricerca Sanitaria Finalizzata 2009’’<br />
and by bank foundations ‘‘Compagnia di San Paolo’’ (Project<br />
‘‘Neuromuscular Investigation and Conditioning in Endocrine<br />
Myopathy’’), ‘‘Fondazione Cariplo’’ (Project ‘‘Steroid myopathy:<br />
Molecular, Histopathological, and Electrophysiological Characterization’’)<br />
and ‘‘Fondazione Cassa di Risparmio di Saluzzo’’.<br />
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