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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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2462 Eur J Appl Physiol (2011) 111:2461–2471<br />

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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2464 Eur J Appl Physiol (2011) 111:2461–2471<br />

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 />

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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 />

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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 />

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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 />

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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 />

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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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