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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
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. 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.
needed (Zenker et al., 1990), therefore, further research LITERATURE CITED
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