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THE ANATOMICAL RECORD 249:276–284 (1997)

Human Facial Muscles: Dimensions, Motor Endplate Distribution,


and Presence of Muscle Fibers With Multiple Motor Endplates
WOLFGANG HAPPAK,1* JI LIU,2 GEORG BURGGASSER,3 AMANDA FLOWERS,4
HELMUT GRUBER,4 AND GERHARD FREILINGER5
1Division of Plastic and Reconstructive Surgery, Department of Surgery,

University of Vienna, Vienna, Austria


2Department of Orthopedic Surgery, National University of Singapore, Singapore
3Department A, Eye Clinic, University of Vienna, Vienna, Austria
4Third Department of Anatomy, University of Vienna, Vienna, Austria
5KH Goldenes Kreuz, Vienna, Austria

ABSTRACT Background: Extrafusal muscle fibers of human striated


skeletal muscles are known to have a uniform innervation pattern. Motor
endplates (MEP) of the ‘‘en plaque’’ type are located near the center of
muscle fibers and distributed within the muscles in a narrow band. The
aim of this study was to evaluate the innervation pattern of human facial
muscles and compare it with that of skeletal muscles.
Methods: Ten facial muscles from 11 human cadavers were dissected, the
nerve entrance points located, and the dimensions measured. All muscles
were stained in toto for MEPs using Acetylcholinesterase (AChE) and
examined under the microscope to determine their location. Single muscle
fibers were teased to evaluate the stained MEPs.
Results: The length of the different facial muscles varied from 29 to 65
mm, which correlated to the length of the corresponding muscle fibers.
MEP zones were found on the muscles in the immediate vicinity of the
nerves’ entrance points and located eccentrically. Numbers and locations
varied from muscle to muscle. Three MEP zone distribution patterns were
differentiated: numerous small MEP zones were evenly spread over the
muscle, a predominant MEP zone and two to three small zones were
spread at random, and two to four MEP zones of equal size were randomly
scattered.
One MEP of the ‘‘en plaque’’ type was found in 73.8% of the muscle fibers
and two to five MEPs were found in 26.2%. The distances between the
multiple MEPs on one muscle fiber varied from 10 to 500 µm.
Conclusions: This study suggests that facial muscles differ from skeletal
muscles regarding distribution and number of MEPs. The eccentric
location of MEP zones and multiple MEPs suggests there is an indepen-
dent mechanism of neural regulation in the facial muscle system. Anat.
Rec. 249:276–284, 1997. r 1997 Wiley-Liss, Inc.

Key words: human facial muscles; dimensions; innervation pattern; mo-


tor zone; extrafusal muscle fibers; motor endplate; multifocal
innervation; Acetylcholinesterase (AChE)

Mammalian skeletal muscles are known to consist of thought to be similar to the skeletal muscles of the
phasic extrafusal muscle fibers arranged in bundles of trunk and limbs. Varying studies on the facial nerve
various sizes. They are innervated by one motor axon (Fujita, 1934; Freilinger et al., 1987) and its branching
and bear one motor endplate (MEP) (Ogata, 1988; pattern (Davis et al., 1956; Bernstein and Nelson, 1984;
Vrbová et al., 1995). Human skeletal muscles consist of Katz and Catalano, 1987) as well as the number of
muscle fibers up to 18 cm in length, with a single MEP muscle fibers per motor unit (Feinstein et al., 1955),
in the middle of the fiber (Desmedt, 1958; Christensen,
1959; Schwarzacher, 1959; Aquilonius et al., 1984).
These MEPs are arranged in such a fashion that they
*Correspondence to: Dr. Wolfgang Happak, Division of Plastic and
form a narrow band stretching across the central zone Reconstructive Surgery, Department of Surgery, Währinger Gürtel
of the skeletal muscles, described as a motor band 18-20, A-1090 Vienna, Austria.
(Gray, 1989). Until recently, human facial muscles were Received 17 July 1995; Accepted 7 April 1997

r 1997 WILEY-LISS, INC.


MOTOR ENDPLATE DISTRIBUTION IN FACIAL MUSCLES 277
and histochemical and immunohistochemical character- slipped. Each specimen was examined under the micro-
istics of facial muscles (Happak et al., 1988; Freilinger scope. Those specimens were excluded from the final
et al., 1990; Stal, 1994), showed significant differences examination and measurements where clear identifica-
from the skeletal muscles of the trunk and limbs. The tion and differentiation of the MEPs was impossible.
aim of this study was to determine the innervation During teasing it is inevitable that some MEPs, as well
pattern of the facial muscle system, the location of the as muscle fibers, are destroyed and some MEPs are
motor bands in each different facial muscle, as well as hidden by artefacts or are projected over each other.
the position and number of MEPs on single muscle The MEPs of the remaining specimens were identi-
fibers. This knowledge may lead to a better understand- fied and photographed. Measurements were carried out
ing of the neural regulation and the emotional expres- on the photographs using measurement forceps accord-
sion of human facial muscles. ing to the calibration bar for each magnification. The
length of each MEP and the distances between the
MATERIALS AND METHODS MEPs were determined on each of the teased muscle
Eleven human cadavers (seven female and four male, fibers.
age 55–73, mean age 5 67) from body donors to
research and teaching (Department of Anatomy) were RESULTS
used in this study. The cause of death was either acute All facial muscles were flat in shape except the
cardiovascular or pulmonary disease. Dissection was orbicularis oris muscle. The zygomatic minor was the
carried out within 2 to 6 days postmortem. only rectangular and the depressor labii inferioris the
Ten facial muscles (zygomaticus major and minor, only quadrilateral-shaped muscle. All other facial
levator labii superioris, levator labii superioris alaeque muscles were of trapezoidal shape and converged from
nasi, levator anguli oris, depressor anguli oris, depres- a wider origin to a narrow insertion. In the zygomatic
sor labii inferioris, buccinator, orbicularis oculi, and major and levator labii superioris, the medial portions
orbicularis oris) and the corresponding innervating of the muscle fibers were shorter than those on the
branches of the facial nerve were dissected. The length lateral side. The cranial portions of muscle fibers in the
and width of each muscle, except the orbicularis oris buccinator muscle that were aligned horizontally were
muscle, was measured in situ using measurement shorter than its caudal portion. Table 1 shows the
forceps. The terminal facial nerve branches were lo- length and width of each muscle. Each muscle was
cated and the entrance points into the muscle deter- innervated by several branches of the facial nerve and
mined and documented on a schematic diagram. corresponding blood vessels were rarely seen. Each
After removal from the cadavers, the muscles were nerve branch divided into multiple smaller branches in
stretched to their original length and fastened on an the distal 5–10 mm before entering the muscle.
expanded polystyrene plate using pins. The muscles
were fixed for 1 hr with 10% formaldehyde and then
Gross Anatomy and Dimensions
kept in 0.1 M cacodylate-buffer. Remaining pieces of
connective tissue and fat were removed. The MEPs The zygomatic major and minor muscles originate
were stained for AChE by incubating the muscles for 6 from the zygomatic arch. In the zygomatic major, the
hrs in the medium described by Koelle and Friedenwald laterally located larger portion of muscle fibers insert at
(1949), followed by further incubation in 1% ammo- the modiolus at the angle of the mouth. Its smaller
nium sulfide and finally postfixed in 3.6% formalde- medial portion and the zygomatic minor insert into
hyde. A control was set up using in vivo dissected sheep the orbicularis oris at the upper lip. The mean length of
rectus femoris muscles, which were stained following the zygomatic major was 65.6 mm (6 3.8) and of the
the same procedure. Evaluation and further prepara- zygomatic minor was 51.8 mm (6 7.4) (Table 1). The
tion of all muscles was carried out under the OP- zygomatic branches innervated each muscle with two to
microscope (Zeiss Universal S3, Carl Zeiss, Oberko- four branches from its deep surface.
chen, Germany). The location of stained MEPs was The levator labii superioris muscle originates from
determined in each of the dissected muscles and docu- the lower margin of the orbita at the maxilla and
mented on a schematic diagram. inserts into the orbicularis oris at the upper lip. The
The schematic diagrams, depicting nerve entrance mean length was 47 mm (6 7.5). The levator labii
points and the position of MEP zones for each muscle, superioris alaeque nasi originates from the medial
were compared with each other. Finally, the positions of angle of the orbital rim and fuses with the levator labii
the MEP zones were determined in each of the ten superioris. The mean length was 61.6 mm (6 7.6). Both
dissected facial muscles by comparing the diagrams of muscles were innervated from their deep surface by two
the corresponding muscles. branches emerging from the peripheral anastomosis
Initially, each muscle was dissected into bundles between the zygomatic and buccal branches.
containing up to 100 muscle fibers. These were then The levator anguli oris muscle originates from the
further divided into smaller bundles, until it was canine fossa at the maxilla. It inserts into the orbicu-
possible to examine each muscle fiber from its origin to laris oris at the upper lip and the modiolus. The
its insertion and determine the location of the MEPs. depressor anguli oris originates from the lower margin
Only those parts of muscle fibers showing AChE- of the mandible. It inserts into the orbicularis oris at
stained MEPs and myotendinous junctions were teased the lower lip and the modiolus. The levator anguli oris
out of the small bundles. The remaining parts of the muscle had a mean length of 42 mm (6 2.5) and the
fibers where AChE activity was negative were removed depressor anguli oris muscle had a mean length of 48
if they had not already broken. The relevant parts of mm (6 5.1). Both muscles were innervated from their
the teased fibers were placed on slides and cover- lateral margin by two branches. The branches emerged
278 W. HAPPAK ET AL.

TABLE 1. Dimensions of facial muscles


Max. width Min. width at
Muscle Max. length Min. length at the origin the insertion
Zygomaticus major 65.6 6 3.81 59.8 6 2.92 8.4 6 1.7 5.4 6 1
Zygomaticus minor 51.8 6 7.4 3.8 6 0.8
Levator labii superioris 47 6 7.51 42 6 5.12 16.4 6 7 963
Lev. lab. sup. alaeque nasi 61.6 6 7.6 7.2 6 1.7 4.6 6 1
Levator anguli oris 42 6 2.5 14 6 5.8 7.8 6 2
Depressor anguli oris 48 6 5.1 35.4 6 8.2 8.8 6 0.8
Depressor labii inferioris 29 6 4.9 21.6 6 2
Buccinator 56 6 7.43 49.4 6 54 48.6 6 4.2 40.6 6 12.3
Orbicularis oculi 65 6 5.65 60 6 9.66
Measurements of ten facial muscles in millimeters. Mean 6 SD of the in situ measured muscles. Each side of the
trapezoid-shaped muscles was measured.
1Lateral edge.
2Medial edge.
3Caudal edge.
4Cranial edge.
5Horizontal diameter.
6Vertical diameter.

from the peripheral anastomosis between the zygo- like distribution of MEPs that varied in size (Fig. 1).
matic and buccal branches and between buccal and Only one cluster of MEPs was determined on each of
marginal mandibular branches, respectively. the separated muscle fiber bundles. Its position differed
The depressor labii inferioris muscle originates from from bundle to bundle. However, the cluster of MEPs
the anterior side of the mandible, adjacent to the was always located in an eccentric position and never in
mental foramen. The muscle inserts at the modiolus the middle of the fiber bundle.
and blends into the inferior part of the orbicularis oris Great variability in the location of the clusters of
and the skin of the lower lip. The muscle had a mean MEPs were observed when comparing the schematic
length of 29 mm (6 4.9). The muscle was innervated by drawings of each facial muscle with its corresponding
several branches of the marginalis mandibular branch, muscle in the 11 human cadavers. The locations varied
which accessed from the lateral side. from muscle to muscle between the origin and the
The buccinator originates from the maxilla, pterygo- insertion. Determining an exact location for the clus-
mandibular raphe, and mandible. The muscle fibers ters of MEPs with regard to the muscles’ dimensions
converge to a plate of insertion at the angle of the was impossible, due to the diversity of their locations.
mouth and the modiolus. The mean muscle length was The locations of the MEP clusters and the previously
56 mm (6 7.4). Numerous buccal branches innervated determined nerve entrance points were identical. On
the muscle from its superficial surface. each of the assessed muscles we determined several
The orbicularis oculi muscle originates from the round or oval-shaped MEP clusters which we therefore
medial palpebral ligament and has no direct attach- called ‘‘motor zones.’’ The number of motor zones de-
ment to the bone. The concentrically aligned bundles of pended on the number of terminal facial nerve branches
muscle fibers were embedded in the septal structure of entering the muscle.
the eyelid. The mean vertical diameter was 65 mm A predominant motor zone could not be found in
(6 5.6) and the mean horizontal diameter was 60 mm either the orbicularis oculi, orbicularis oris, or buccina-
(6 9.6). The muscle was innervated by four or five tor muscle. The MEPs were evenly spread over the
temporal branches and by two or three zygomatic muscles, either isolated or in a great number of small
branches from its deep surface. motor zones (Fig. 2a).
In contrast, the orbicularis oris muscle is the only The zygomatic major and minor muscles showed a
round-shaped muscle in the face. It has neither bony predominant motor zone located near the origin, in the
nor tendinous origin. It was held in position by all the proximal third of the muscles. Two to three additional
inserting muscles mentioned above. The fibers contin- small motor zones were found in an eccentric position,
ued within the orbicularis oris, becoming an integral in the proximal and distal third of the muscles (Fig. 2b).
part of the muscle. The muscle was innervated from its The levator labii superioris, levator labii superioris
lateral side by two branches emerging from peripheral alaeque nasi, levator anguli oris, depressor anguli oris,
anastomosis between the lower buccal and the mar- and depressor labii inferioris muscles showed two to
ginal mandibular branches. four large motor zones distributed over the muscle in
Motor Zone eccentric positions (Fig. 2c).
Only these three types of motor zone distributions
All in toto stained human facial muscles, as well as were distinguished in the ten evaluated facial muscles.
the control rectus femoris muscles from sheep, were
successfully stained for MEPs. Deeper portions of the
Muscle Fiber Length
muscles were not satisfactorily stained, due to the
technique applied (Koelle and Friedenwald, 1949). The evaluated facial muscles were composed of
Examination of each facial muscle in toto, as well as bundles, consisting of parallel muscle fibers. These
the separated muscle fiber bundles, showed a cluster- continued from origin to insertion without interruption.
MOTOR ENDPLATE DISTRIBUTION IN FACIAL MUSCLES 279

Fig. 1. Cluster-like arrangement of AChE-stained MEPs. A typical


motor zone on a muscle fiber bundle of the zygomatic major muscle.
350X.

None of the muscles inserting in the orbicularis oris


muscle showed a tendinous insertion. The length of the
bundles and therefore the length of the individual
muscle fibers correlated with the length of the in situ
measured facial muscle (Table 1).
Motor Endplate
Several hundred muscle fiber bundles were exam-
ined from the different facial muscles to determine the
locations of the motor zones. According to the position of
the motor zones, the MEPs were located in an eccentric
position on each muscle fiber. The MEPs of the muscle
fibers could be clearly identified during further division
of the bundles. All the examined MEPs were of the ‘‘en Fig. 2. Schematic drawing of facial muscles showing the motor zone
locations, indicated by circular and oval grids. (a) Left M. orbicularis
plaque’’ type (Figs. 3a,b, 4b,c). None of the examined oculi with MEPs evenly spread over the muscle. (b) Left M. zygomati-
MEPs were of the ‘‘en grappe’’ type. No differences in cus major with a main motor zone located near the origin and two to
the staining intensity were observed between the hu- three additional small motor zones near the insertion. (c) Left M.
man muscles dissected 2 to 6 days postmortem. The levator labii superioris with two to four large motor zones in eccentric
position.
staining intensity of the MEPs in the sheep muscles
was somewhat darker than that seen in the human
muscles. Examining the human muscle fibers in the
divided bundles, a great number of fibers were identi- ● Single muscle fibers focally innervated by one MEP
fied bearing more than one MEP. Fibers with more than (Fig. 4a).
one endplate were seen in each of the ten facial ● Single muscle fibers multifocally innervated by two
muscles. Many of these fibers were destroyed during adjacent MEPs (Fig. 4b).
teasing due to the poorer quality of the material. ● Single muscle fibers multifocally innervated by two
Finally, a total of 567 muscle fibers, with clearly visible MEPs located further apart (Figs. 3a,b).
MEPs, were examined from the ten facial muscles. ● Single muscle fibers multifocally innervated by more
In all, 418 fibers (73.8%) showed only one MEP, 121 than two MEPs (Figs. 4c,d).
fibers (21.3%) showed two MEPs, and 28 fibers (4.9%)
showed more than two MEPs. The focally innervated muscle fibers showed a MEP
The multiple MEPs, distributed on the fibers as length of 27.6 µm (6 6.3). Those muscle fibers multifo-
described above, were found within a distance of up to cally innervated by two MEPs showed a MEP length of
500 µm (Figs. 3a,b, 4b,c,d). These fibers were differenti- 28.0 µm (6 5.4). Muscle fibers multifocally innervated
ated into three groups according to the distances be- by three or more MEPs showed a MEP length of 25.2
tween the multiple MEPs: 45% of the muscle fibers µm (6 6.4).
showed MEPs within a distance of up to 50 µm (Fig. 4b);
48% showed MEPs within a distance of 50–200 µm Myotendinous and Myomyous Junctions
(Figs. 3a, 4c); and 7% of the muscle fibers showed MEPs All muscle fiber bundles and teased single muscle
within a distance of more than 200 µm (Fig. 3b). fibers were examined under the microscope for myoten-
Four different MEP distributions were found on the dinous and myomyous junctions. AChE-stained myoten-
teased muscle fibers, depending on the number and dinous junctions were found at the bony origin of the
location of the MEPs: muscle fibers but not at their insertion. However, in
280 W. HAPPAK ET AL.

Fig. 3. (a) Multifocally innervated muscle fiber of the M. levator labii superioris bearing two MEPs
within a distance of 200 µm. (b) Multifocally innervated muscle fiber of the M. zygomaticus major bearing
two MEPs within a distance of 500 µm. Magnification, see calibration bar.

spite of an intensive search for myomyous junctions no It has been described that 21 paired facial muscles
further AChE-stained junctions could be found on the are innervated by the facial nerve (Gray, 1989). The
muscle fibers. The single muscle fibers, therefore, con- current study deals only with the ten most important
tinued from origin to insertion without interruption or facial muscles, responsible for facial movements and
furcation. emotional expression. Our foremost interest was to
acquire more information on their innervation pattern,
DISCUSSION especially the clinical aspect of facial palsy and the
According to Austrian law, all corpses must be cleared dynamic reconstruction with skeletal muscles. Further-
by a pathologist before the body donors can be trans- more, the technique of teasing muscle fibers is ex-
ferred to the Department of Anatomy for research and tremely time-consuming, so that we concentrated on
teaching. This meant that the dissection of the body the most important muscles and excluded the remain-
donors used in this study could not be carried out until ing 11 from this study.
2 to 6 days postmortem. The first stage of this study was It is generally assumed that a great number of
to determine the efficiency of the staining method on human skeletal muscles, as well as extraocular muscles,
MEPs described by Koelle and Friedenwald (1949). have a well-defined neurovascular hillum. Long skel-
Human cadaver muscles, which had been kept in cold etal muscles (M. gracilis, M. sartorius), or flat skeletal
storage for several days postmortem, as well as fresh muscles (abdominal muscles) can be innervated by two
sheep muscles were used. All the muscles’ MEPs were or more motor nerves with well-defined nerve entrance
successfully stained for AChE. Most authors using the points. In most of the skeletal muscles, the MEPs are
AChE staining method (Koelle and Friedenwald, 1949) arranged as one or more (abdominal muscles) narrow
fix the muscles as described, immediately after removal bands, stretching midway across the muscle fiber
from the donor. Successful staining of MEPs up to 18 hr bundles as one or more so-called ‘‘motor bands’’ (Gray,
postmortem was described by Dietert (1965). We were 1989). The neurovascular hillum is always found lo-
able to successfully stain muscles up to 6 days postmor- cated in the muscle at a considerable distance from the
tem, provided the cadavers were refrigerated in the motor band.
morgue soon after death. It seems that AChE is more In contrast to the nerves innervating the skeletal
stable than generally assumed and can be applied, like muscles of the trunk and limbs, the facial nerve already
other histochemical techniques (Eriksson et al., 1980; divides in the parotid gland into multiple branches. It
Happak et al., 1988) up to 6 days postmortem. A control forms an elaborate network of anastomosis and inter-
was set up with sheep muscle to ensure the efficiency of laced branches before finally entering the facial muscles
the applied staining technique. The sheep muscles were (Fujita, 1934; Davis et al., 1956; Bernstein and Nelson,
stained simultaneously with the human specimens. 1984; May, 1986a; Katz and Catalano, 1987). Each
The consistency of the human muscle fibers was of facial muscle was, however, innervated by multiple
somewhat poorer quality, due to the onset of autolysis, terminal branches of the facial nerve without being
which made the teasing of whole fibers extremely accompanied by the corresponding blood vessels. The
difficult. Consequently, a different approach was taken plexus of the facial nerve, as well as the route of each
to determine the position of MEPs on the muscle fibers terminal nerve branch to the muscle, was described by
prior to teasing. The locations of the MEPs were Fujita (1934) and Freilinger et al. (1987). Our observa-
evaluated twice within the entire muscle, once in the tions were in accordance with these findings and in
endplate zones and once in the divided bundles. This addition we found that each motor zone was always
approach facilitated the teasing procedure considerably positioned in the immediate vicinity of the entrance
as it was then only necessary to tease and evaluate point of the small, terminal facial nerve branch. There-
small pieces of the fibers bearing MEPs. fore, no distance between the nerve entrances and the
MOTOR ENDPLATE DISTRIBUTION IN FACIAL MUSCLES 281

Fig. 4. Teased single muscle fibers of different facial muscles showing tor muscle with one nerve fiber and two MEPs. (c). Multifocally
the AChE-stained MEPs of the different innervation patterns. (a) innervated muscle fiber of the depressor angular oris muscle with
Focally innervated muscle fiber of the zygomatic major muscle show- three MEPs and (d) the complete teased muscle fiber. Magnification,
ing one MEP. (b) Multifocally innervated muscle fiber of the buccina- see calibration bar.

motor zones was observed as it is typically seen in the type of motor zone distribution not only applied to the
skeletal muscles of the trunk and limbs. orbicularis oculi muscle but also to the orbicularis oris
Furthermore, we found round or oval-shaped cluster- and buccinator muscles. These three muscles showed
like arrangements of MEPs on the facial muscles, similar distributions as described for the laryngeal
varying in size, which we named ‘‘motor zones.’’ None of muscles by Rossi and Cortesina (1965). For the remain-
the evaluated facial muscles displayed a motor band- ing facial muscles, two unknown types of motor zone
like MEP distribution. The orbicularis oculi muscle has distribution were determined, also according to the
a great number of small MEP clusters that are evenly number and size of the motor zones. Two muscles
spread over the muscle (Desmedt 1958). We found this showed a predominant motor zone with two to three
282 W. HAPPAK ET AL.

additional small motor zones and five muscles showed µm. In contrast, our study shows that 45% of the facial
two to four large motor zones. Except for the number muscle fibers exhibited multiple MEPs within a dis-
and size of motor zones in the facial muscles, no further tance of 50 µm. Approximately the same numbers of
similarities could be differentiated. This, therefore, facial muscle fibers (48%) were found with multiple
enabled only a descriptive classification into the three MEPs between 50 and 200 µm, and only a few muscle
groups mentioned above. fibers (7%) had multiple MEPs within a distance of up
When reviewing the facial nerve literature, espe- to 500 µm. It therefore appears that muscles stemming
cially the schematic drawings of Fujita (1934), it can be from the branchial arches, with multifocally innervated
considered that the great variability of the motor zone muscle fibers, show great variability in their innerva-
distribution corresponds to the great variability of the tion pattern.
facial nerve route. The location of the motor zones was Studies by Rossi and Cortesina (1965), Benediksen et
seen to vary as the branching of the facial nerve varied al. (1981), and Rossi (1990) revealed that a great
from specimen to specimen (Davis et al., 1956). There- number of laryngeal muscle fibers (70–80% vocalis,
fore, the diversity of motor zones on the entire muscle 50% cricothyroid and lat. cricoarytenoid, 5% posterior
was such that no general statement can be made cricoarytenoid) were multifocally innervated in the
concerning their exact positioning. current study 26% of the facial muscle fibers showed
Comparable characteristics have already been de- more than one MEP. It seems that there is great
scribed for the different laryngeal muscles (Rossi and variability in the number of MEPs per muscle fiber in
Cortesina, 1965), which is another muscle system stem- the muscles stemming from the third and fourth bran-
ming from the branchial arches (Gray, 1989). Here, chial arch (5–80%). Our method of preparation and
similar variability of eccentric motor zone distribution staining was chosen in order to evaluate the distribu-
was seen, such as a random distribution in the medial tion, location, and size of MEPs whereby only the
two-thirds of the muscles (Rosen et al., 1983; De Vito et superficial layers of the muscles were closely scruti-
al., 1985; Freije et al., 1986), a banded or Y-shaped nized. To establish the number of muscle fibers with one
motor zone distribution (Freije et al., 1986, 1987) and MEP and the number of those with two or more MEPs
an arc-like patterned distribution (Gambino et al., and give a precise ratio, it would be necessary to use a
1985). The facial muscles show a unique innervation different technique than the one applied here. Future
pattern unlike that seen in the skeletal muscles of the
studies may answer this question.
trunk and limbs (Desmedt, 1958; Christensen, 1959;
Former studies by other authors concerning the
Schwarzacher, 1959; Aquilonius et al., 1984). It appears
innervation of human skeletal muscles (Desmedt, 1958;
to be common among several muscles stemming from
the branchial arches. Christensen, 1959; Schwarzacher, 1959; Aquilonius et
Most of the authors who have examined human al., 1984; Carlson, 1986; Wokke et al., 1990; Hessel-
skeletal muscle fibers have described a single MEP, mans et al., 1993) have shown that focal innervation of
always positioned, with respect to the longitudinal axis, muscle fibers with one MEP is the predominant type.
in the middle of each muscle fiber (Desmedt, 1958; We conclude that multifocally innervated fibers would
Christensen, 1959; Schwarzacher, 1959; Aquilonius et have been found by these authors if present. Multifo-
al., 1984; Carlson, 1986; Vrbová et al., 1995). This, cally innervated fibers are present in the facial muscle
however, cannot be said for facial muscles, where one to as in the laryngeal muscles. Laryngeal muscles are
five MEPs were seen, always in an eccentric position on dependent on a specific neural regulation (Rossi, 1990).
a single muscle fiber. It is reasonable to assume that the same is true for the
Based on his electrophysiological results, Desmedt facial muscles, especially as both are capable of very
(1958) postulated that the muscle fibers of the orbicu- fine adjustments for speech, emotional expression, and
laris oculi muscle may have a ‘‘multiple innervation.’’ defence reflexes.
All facial muscles were also assumed to contain ‘‘multi- Studies on animal muscles (Barker and Ip, 1966;
ply innervated muscle fibers’’ (Coers, 1967). We were Wernig et al., 1984) determined that the presence of
able to find such muscle fibers in all ten human facial multiple MEPs may be due to MEP regeneration. This
muscles by using the AChE staining method for MEPs. was observed in 8.1% of the investigated fibers (Barker
Nowadays, such ‘‘multiply innervated muscle fibers’’ and Ip, 1966). In contrast, 26% of facial muscles fibers
with ‘‘en plaque’’ MEPs should be referred to as ‘‘multi- and up to 80% of laryngeal muscle fibers showed
focally innervated muscle fibers’’ (Zenker et al., 1990). multifocal innervation. Therefore, we would exclude
Namba et al. (1968) described that in human extraocu- that all these fibers have been subjected to continuous
lar muscles, besides slow multiply innervated fibers MEP regeneration. Furthermore, it seems to be rare in
with ‘‘en grappe’’ MEPs, focally and multifocally inner- humans (Wokke et al., 1990) and no author at present
vated twitch fibers with one or two ‘‘en plaque’’ MEPs has described regenerated or remodelled MEPs at a
were also present. distance up to 500 µm. In our opinion, the above-
Human laryngeal muscles mainly contain twitch mentioned specific neural regulation is responsible for
fibers with ‘‘en plaque’’ MEPs. Up to 80% of the fibers the multifocal innervation of muscle fibers and MEP
were multifocally innervated (Rossi and Cortesina, regeneration plays a minor role.
1965; Benediksen et al., 1981; De Vito et al., 1985; Few studies exist where the length of human ‘‘en
Rossi, 1990). Benediksen et al. (1981) showed that most plaque’’ MEPs have been evaluated. The measured data
of the multiple MEPs on the laryngeal muscle fibers of MEP lengths from 18–27 µm (Namba et al., 1968;
were positioned at distances between 100–200 µm. Wokke et al., 1990; Hesselmans et al., 1993) are in
Furthermore, they found a larger number of MEPs with accordance with the evaluated facial MEP lengths of
an even greater distance between the MEPs, up to 5000 25–27 µm.
MOTOR ENDPLATE DISTRIBUTION IN FACIAL MUSCLES 283
It is apparent that the innervation of human facial Even after reconstruction of facial palsy with a
muscle fibers is complex. It is not yet known if multiple cross-facial nerve graft and a free-muscle graft deficits
endplates on a single facial muscle fiber are innervated remain, which are especially seen when smiling. This
mono- or polyneuronally. The great number of anasto- may not only be due to the decreased number of
mosing nerve branches in the lateral face and the regenerating motor units in the facial muscles (Ray-
plexus of the facial nerve (Fujita, 1934; Davis et al., ment et al., 1987) but it seems that it is also due to the
1956; Bernstein and Nelson, 1984; Katz and Catalano, nature of the complex innervation pattern of the facial
1987) suggest that a polyneuronal innervation type muscles.
could be present in the facial muscles. Perhaps it is the After successful reconstruction of the paralyzed face,
polyneuronal innervation which enables the facial it is necessary for the patient to relearn how to use that
muscles to perform the fine adjustments necessary for part of the face and coordinate the movements with the
emotional expression. However, the employed tech- healthy side (Frisch, 1991). This can only be achieved
nique cannot, at present, identify the innervation type on command, on purpose, and by discipline, but never
(Wokke et al., 1990). by spontaneous emotional reactions (Conley, 1986).
Another reason for multifocally innervated extra- In summary, the data presented concerning the inner-
fusal fibers could be the security of neurotransmission, vation pattern of the facial muscles endeavors to pro-
and quantitative or qualitative aspects of muscle fiber vide a contribution toward a better understanding of
innervation (Zenker et al., 1990; Vrbová et al., 1995) for the mimetic functions. It may lead to the development
the regulation of fine adjustments for facial expression. of new clinical methods for different diseases and
An acceptable physiological explanation for extrafusal disorders of the facial nerve and the facial muscle
muscle fibers with multiple endplates in animals is still system, as well as for the treatment of facial palsy.
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