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THE ANATOMICAL RECORD 256:412–424 (1999)
Neuromuscular Organization of the
Canine Tongue
LIANCAI MU AND IRA SANDERS*
Grabscheid Voice Center, Department of Otolaryngology, The Mount Sinai Medical
Center, New York, New York 10029-6574
ABSTRACT
The tongue manipulates food while chewing and swallowing, dilates the
airway during inspiration, and shapes the sounds of speech in humans.
While performing these functions the tongue morphs through many complex
shapes. At present it is not known how the muscles of the tongue perform
these complex shape changes. The difficulty in understanding tongue
biomechanics is partly due to gaps in our knowledge regarding the complex
neuromuscular anatomy of the tongue. In this study the motor and sensory
nerve anatomy of four canine tongues was studied with Sihler’s stain, a
technique that renders most of the tongue tissue translucent while counterstaining nerves. An additional tongue specimen was serially sectioned to
provide a reference for the muscle structure of the tongue.
The hypoglossal nerve (XII) has approximately 50 primary nerve
branches that innervate all intrinsic and extrinsic tongue muscles. Two
extrinsic muscles, the styloglossus and hyoglossus, are innervated by about
three to four branches from the lateral division of the XII. The third extrinsic
muscle, the genioglossus, is composed of oblique and horizontal compartments, which receive about ten nerve branches from the medial division of
the XII. The intrinsic muscles are composed of many neuromuscular compartments. On each side, the superior longitudinal muscle had an average of
40 distinct muscle fascicles that spanned the length of the tongue. Each of
the fascicles is supplied by a nerve branch. The inferior longitudinal muscle
had a similar organization. Each of the transverse and vertical muscles is
composed of over 140 separate muscle sheets, and every sheet is innervated
by a separate terminal nerve. The muscle sheets from the vertical and transverse alternate their orientation 90° throughout the length of the tongue.
It is concluded that the intrinsic canine tongue muscles are actually
composed of groups of neuromuscular compartments that are arranged in
parallel (longitudinal muscles) or in a precise alternating sequence (transverse and vertical muscles). This arrangement suggests that the compartments from the different tongue muscles could cooperate to control the
three-dimensional contractile state of their local area. This hypothesis could
explain how many different tongue shapes are formed, and is supported by
physiologic evidence. Anat Rec 256:412–424, 1999. r 1999 Wiley-Liss, Inc.
Key words: tongue; innervation; tongue muscles; neuromuscular compartment; Sihler’s stain
The tongue is a complex muscular organ constituted of
several intrinsic and extrinsic muscles, innervated by
several cranial nerves (Weddell et al., 1940; Miller et al.,
1964) and involved in several important physiological
tasks such as mastication, swallowing, taste, respiration,
and human speech (Abd-El-Malek, 1955; MacNeilage and
Sholes, 1964; Sauerland and Mitchell, 1970). Although the
tongue is capable of performing complex movements, our
r 1999 WILEY-LISS, INC.
current understanding of the contributions of specific
tongue muscles to precise movement patterns is limited.
*Correspondence to: Ira Sanders, MD, Department of Otolaryngology, Box 1189, The Mount Sinai Medical Center, New York, NY
10029-6574.
Received 22 October 1998; Accepted 23 July 1999
NEUROMUSCULAR ORGANIZATION OF THE TONGUE
Knowing the neuromuscular organization of the tongue is
crucial for understanding how the tongue functions. However, details concerning the nerve supply and muscular
architecture have never been demonstrated in wholemount tongue specimens from any mammal. This is largely
due to the fact that the muscles of the tongue interweave in
complex ways, making it technically impossible to trace
the muscle fascicles and nerve branches by traditional
microscopic dissection.
It is known that four nerves supply innervation to the
tongue. The hypoglossal (XII) nerve supplies motor innervation to all tongue muscles (Miller et al., 1964). The
lingual nerve, a branch of the mandibular division of the
trigeminal nerve, provides both gustatory and general
sensory fibers to the tongue. The gustatory component is
contributed by the chorda tympani branch of the facial
nerve which connects with the lingual nerve. Finally, the
glossopharyngeal (IX) nerve terminates in the mucosa and
the vallate papillae at the posterior third of the tongue to
supply general sensation and taste (Lawn, 1966; Yamamoto, 1975). These classical descriptions on the innervation of the tongue are mainly based on the findings
obtained by gross dissection, nerve degeneration, neural
tracing techniques, and electrophysiological methods (AbdEl-Malek, 1938; Lawn, 1966; Yamamoto, 1975; Lowe,
1980; Hellstrand, 1981; Chibuzo and Cummings, 1982).
Although much information about the innervation of the
tongue has been directly and indirectly provided by the
methods mentioned above, the complete nerve branching
patterns of these nerves within the tongue have never
been demonstrated.
The motor innervation of the tongue is by the XII nerve,
which bifurcates into lateral and medial divisions that
supply the retrusor and protrusor muscle groups, respectively (Abd-El-Malek, 1938; Hellstrand, 1981). However,
the specific muscles supplied by the two divisions of the XII
nerve appear not to be the same in different species. It has
been reported that in the human a smaller lateral division
supplies hyoglossus, styloglossus, and inferior longitudinal muscles while the medial division supplies several
branches to the genioglossus and intrinsic tongue muscles
(Abd-El-Malek, 1938). In contrast, the medial division of
the XII in the cat also supplies branches to the hyoglossal
and styloglossal muscles (Hellstrand, 1981). There is little
information of the terminal branching pattern inside these
muscles.
Recently, an old technique, the Sihler’s stain, has been
modified to study the neuromuscular organization of complex structures such as the larynx (Wu and Sanders, 1992;
Sanders et al., 1993a,b; Mu et al., 1994; Sanders et al.,
1994; Wu et al., 1994; Sanders and Mu, 1998) and the
human pharynx (Mu and Sanders, 1996, 1998a). Sihler’s
stain has the unique capability of rendering a large
postmortem specimen translucent while counterstaining
the entire nerve supply. In the specimens processed by
Sihler’s stain, the peripheral nerve supply and arrangement of individual muscles can be seen in their normal
three-dimensional positions. By careful dissection of the
specimen every motor nerve can be followed to its terminal
branches within each muscle, and every sensory nerve
branch can be traced to the termination in the mucosa. In
addition, small connections between the motor and sensory nerves can be visualized.
In this study the whole-mount Sihler’s stain was used to
investigate: 1) the entire branching and distribution of all
413
motor and sensory nerves to the tongue; and 2) the
arrangement of individual muscles and their intramuscular nerve supply.
MATERIALS AND METHODS
Five tongues were obtained from adult mongrel dogs
which were sacrificed for another, unrelated experiment.
Four tongues were stained with Sihler’s stain to study the
nerve supply and muscular organization and one was
sectioned and stained with hematoxylin and eosin (H&E)
to demonstrate the internal organization of individual
tongue muscles. All procedures for animal care and treatment were approved by the Mount Sinai Medical Center’s
CLAS.
The Sihler’s stained specimens were initially dissected,
and then the gross nerve branches and arrangement of the
tongue muscles were examined. Finally, each tongue muscle
with its supplying nerve was excised off from the tongue
body to study its intramuscular nerve supply pattern.
Procedures for Modified Sihler’s Stain
Solutions needed for Sihler’s stain.
1) 10% formalin.
2) 3% KOH (potassium hydroxide) (3 drops of 3% hydrogen peroxide are added into 100 ml 3% KOH).
3) Sihler’s solution I (1 part glacial acetic acid, 1 part
glycerin and 6 parts 1% aqueous chloral hydrate).
4) Sihler’s solution II (1 part stock Ehrlich’s hematoxylin,
1 part glycerin and 6 parts 1% aqueous chloral hydrate).
5) 0.05% lithium carbonate solution.
6) 50% and 100% glycerin.
Staining steps.
1) Fixation of the tongues studied in 10% formalin for 4–8
weeks.
2) Maceration in 3% KOH solution for 3 weeks with
several changes.
3) Decalcification in Sihler’s solution I for 2 weeks with
several changes.
4) Staining in Sihler’s solution II for 4 weeks.
5) Destaining in Sihler’s solution I for 3–4 hr.
6) Darkening the nerves in 0.05% lithium carbonate solution for 1 hr.
7) Clearing in 50% glycerin for 2–3 days.
8) Preserving the stained specimens in 100% glycerin
with a few thymol crystals.
Microdissection and Photography
The Sihler’s stained tongues were preserved in 100%
glycerin for 1–2 months and then dissected with the aid of
a dissecting microscope (TYP 3555110; Wild, Heerbrugg,
Switzerland) at a magnification of ⫻10–30 by using microsurgical instruments after transillumination by a Xenon
light source (model 610; Karl Storz, Endoscopy-America,
Culver City, California). The relationship between the
individual tongue muscles and orientation of the muscle
fascicles of a given muscle were carefully examined and
recorded. The nerves supplying each of the muscles were
traced from their main trunks to the terminations. The
completed specimens were photographed with an OM-4
414
MU AND SANDERS
Olympus camera (Tokyo, Japan), using a 50, 38, or 20 mm
lens to show the muscle organization and nerve branching
patterns of the tongue. The numbers and branching points
of the major nerve branches derived from the XII, IX and
lingual nerves were recorded.
RESULTS
The neuromuscular organization of the canine tongue
was demonstrated by means of Sihler’s stain (n ⫽ 4) and
H&E staining (n ⫽ 1). Histological examination of the
cross sections stained with H&E allowed us to localize the
individual muscles and make some measures. Sihler’s
stained specimens allowed us to observe the nerve supply
and muscle organization in three-dimensional positions.
Organization of the Tongue Muscles
The canine tongues were about 16 cm in length (n ⫽ 3).
The width of the dorsal surface on each side was measured
to be ⬃19 mm for the anterior, ⬃25 mm for the middle, and
⬃20 mm for the posterior tongue (n ⫽ 3). The thickness of
the tongue close to the midline was ⬃6 mm, 16 mm, and 22
mm for the anterior, middle, and posterior tongue, respectively (n ⫽ 1).
As demonstrated by H&E (Fig. 1A) and Sihler’s stain
(Figs. 1B–E, 2A), the tongue muscles except for genioglossus (a midline muscle) were found to be organized into
three layers: superior, middle, and inferior. The thickness
of the three layers is different. The superior layer accounts
for ⬃18%, the middle layer for ⬃59%, and the inferior
layer for ⬃23% of the whole thickness of the tongue (Fig.
1A).
The superior layer which lies just beneath the dorsum of
the tongue consists of only the superior longitudinal (SL)
muscle (Figs. 1A–C). The thickness of this layer in the
middle portion of a semi-tongue was measured ⬃1 mm, 2
mm, and 2.2 mm for the anterior, middle, and posterior
tongue, respectively (n ⫽ 1). This muscle courses from the
tongue base and hyoid bone to the tip of the tongue. On
each side, the SL was found to be composed of ⬃26, 35, and
58 fascicles on average for the anterior, middle, and
posterior tongue, respectively (n ⫽ 3) (Figs. 1A–C). Cross
section showed that the SL fascicles tend to be oval in
shape and are arranged into a row under the dorsum of the
tongue (Fig. 1A). The sizes of the fascicles are different.
The fascicles in the medial half are larger than those in the
lateral half of the tongue. Two large fascicles close to the
median fibrous septum were recognized (Figs. 1B,C). The
diameter for each of the two largest fascicles was measured to be ⬃1 mm for the anterior, 2 mm for the middle,
and 2.5 mm for the posterior tongue. The most lateral
fascicles are the smallest in size (Fig. 1A). The diameter of
these smaller fascicles was measured to be ⬃0.6 mm.
The middle layer consists of both the transverse and
vertical muscles (Figs. 1A, D). The thickness of this layer
was measured to be ⬃3 mm for the anterior, 7 mm for the
middle, and 13 mm for the posterior tongue (n ⫽ 1).
Sihler’s stain showed that on each side either transverse
or vertical muscle comprises ⬃143 muscular sheets
126⬃157) on average (n ⫽ 3). The muscular sheets of the
two muscles alternate from the tip to the root of the
tongue. The transverse muscular sheets course from the
median fibrous septum to the lateral margin of the tongue,
whereas the vertical muscular sheets travel between the
dorsum and ventral mucosa of the tongue. Therefore, the
muscle fibers of either the transverse or vertical muscles
are relatively shorter than those of other muscles. The
length of the transverse muscle fibers was measured to be
⬃22 mm. The vertical muscle fibers were ⬃4 mm for
the anterior, 14 mm for the middle, and 20 mm for the
posterior tongue (n ⫽ 1).
The inferior layer that is situated just above the mucosa
of the ventral aspect of the tongue consists of the styloglossus, hyoglossus, and inferior longitudinal muscles (Figs.
1A, E). The thickness of this layer was ⬃1.5 mm, 2.8 mm,
and 3.5 mm for the anterior, middle, and posterior tongue,
respectively (n ⫽ 1). The styloglossus which enters the
tongue caudolaterally and mixes up with the hyoglossus
about 2 cm posterior to the hyoid bone (Fig. 1E). The
inferior longitudinal muscle was noted to consist of numerous fascicles that are overlapped. These fascicles are much
more in number and smaller in size than those of the
superior longitudinal fascicles (Fig. 1A).
Branching, Distribution, and Connections of the
Nerves to the Canine Tongue
After processed with Sihler’s stain and trimmed by
microscopic dissection, all the nerves innervating the
tongue were visualized. Figure 1E demonstrates the distribution of the XII, IX, and lingual nerves within a Sihler’s
stained canine tongue. The branching patterns of the
individual nerves to the canine tongue are described as
follows:
The hypoglossal nerve (XII). The details regarding
the branching of the XII are illustrated in Figures 2A and
B. During its course within the tongue, the XII nerve gives
off about 48 (45⬃52) (n ⫽ 3) first-order nerve branches to
supply all the tongue muscles at different levels. On
approaching the lateral aspect of the tongue base, the XII
nerve gives off three to four early branches that correspond
to the classically described lateral division. These branches
leave the main trunk of the XII within a short distance
(about 2 cm) and innervate the styloglossus, hyoglossus,
and inferior longitudinal muscles.
The medial division runs anteriorly to the tip of the
tongue (about 14 cm long). During its course the medial
division gives off several groups of first-order nerve
branches to supply other tongue muscles. First, it gives off
a single branch about 4–5 mm distal to the lateral division
to supply the geniohyoid muscle. It then sends three to
four nerve branches to the superior longitudinal muscle,
three nerve branches to the horizontal part, and seven to
eight nerve branches to the oblique part of the genioglossus muscle. At the level of the genioglossus muscle, the
medial division gives off four to five branches to the
posterior transverse and vertical muscles. In the anterior
tongue, the medial division gives off about 26 (24⬃29) (n ⫽
3) first-order branches to innervate the anterior transverse and vertical muscles.
The glossopharyngeal nerve (IX). The IX nerve
was found to reach the tongue on the lateral margin and
travel beneath the dorsum of the tongue. It usually gives
off three to four first-order branches, which were measured
to be about 5–6 cm in length (n ⫽ 4), to supply the mucosa
and vallate papillae in the posterior one-third of the
tongue (Figs. 1E, 3A,B).
NEUROMUSCULAR ORGANIZATION OF THE TONGUE
415
Fig. 1. Three layers of the canine tongue muscles. A: A cross section
of the right middle tongue stained with hematoxylin and eosin, showing
the three layers of the tongue muscles. Three bars indicate the superior
(S), middle (M), and inferior (I) layers of the tongue muscles, respectively.
L, lateral margin of the tongue; D, dorsal surface of the tongue; V, ventral
surface of the tongue. 7.5⫻. B: A Sihler’s stained canine tongue, showing
the superior layer of the tongue musculature (ventral view). The middle
and inferior layers have been removed. Note that the superior layer (e.g.,
superior longitudinal muscle) is composed of two large fascicles (large
solid arrow) close to the midline (double arrowheads) and numerous small
fascicles (small arrow) lateral to the midline. The open arrow indicates a
vallate papilla. T, tip of the tongue; B, base of the tongue. C: Higher power
view of the superior layer of the anterior tongue in B, showing the
organization pattern of the superior longitudinal muscle fascicles. 3⫻. D:
Higher power view of the middle layer of the Sihler’s stained anterior
tongue. Note that this layer is composed of numerous alternating sheets
of the transverse (T) and vertical (V) muscles. This layer is also seen on
the cross section of the tongue in A. 9⫻. E: The inferior layer of the tongue
musculature demonstrated by Sihler’s stain (ventral view). Note that this
layer consists of the styloglossus (SG), hyoglossus (HG) and inferior
longitudinal (IL) muscles. This layer is also demonstrated by the cross
section of the tongue stained with hematoxylin and eosin stain in A. The
Sihler’s stained canine tongue shows that the hypoglossal (XII) and
lingual (LN) nerves travel on the ventral aspect of the tongue to supply the
muscles and mucosa, respectively. The glossopharyngeal (IX) nerve
supplies the mucosa and vallate papillae in the posterior tongue. In this
specimen the genioglossus and inferior longitudinal muscles have been
removed. a, anterior division of the lingual nerve; p, posterior division of
the lingual nerve.
In the canine posterior tongue, there are two to three
vallate papillae on each side (Figs. 3A,B). It was found that
the first or medial branch of the IX is the major contributor
to the nerve supply of the vallate papillae. In general, the
posterior vallate papilla receives its innervation from the
first branch of the IX, while the anterior vallate papilla
from both the first and second branches of the IX nerve
(Fig. 3A). Each of the vallate papillae is usually supplied
by two to three terminal branches which connect each
other, pass through the center of the papilla, and extend to
the free end of the papilla on the dorsal surface of the
tongue.
The lingual nerve (LN). The LN reaches the tongue
at the middle third and comes into the tongue ventrally
(Fig. 1E). It divides into a posterior (p) and an anterior (a)
division. The posterior division, which has a relatively
shorter length and a smaller innervation area than the
anterior one, sends four to five branches which pass
through the tongue muscles to supply the posterior mucosa of the middle third of the tongue. In addition, the
posterior division of the LN also sends nerve branches to
innervate the vallate papillae (Fig. 3B).
The anterior division of the LN runs forward along with
the medial division of the XII to the tip of the tongue.
During its course, this division gives off about 10 (n ⫽ 3)
first-order branches and numerous twigs (Fig. 4A). These
nerve branches pass through the tongue musculature to
supply the mucosa of the anterior third and anterior part
of the middle third of the tongue. Some terminal twigs of
the LN were found to terminate taste buds in the mucosa
of the anterior tongue (Fig. 4B).
Neural connections between the XII, IX, and
lingual nerves. Numerous neural connections between
the XII, IX, and lingual nerves were found in all specimens
studied (Figs. 5A–D). In Figure 5A, three squares indicate
the sites and patterns of the connections commonly seen in
the canine tongue. In this specimen most muscles have
been removed and the nerve plexus formed by XII and
lingual nerves was placed beside the tongue in order to
show the neural connections. The connections between the
lingual and XII nerves were observed in the plexus and in
the tongue muscles. In addition, the connections between
the IX and lingual nerves were also recognized.
Crossing innervation of the XII and lingual
nerves. In one specimen, the XII was found to send a
branch at the conjunction between the anterior and middle
thirds of the tongue to cross the midline to supply the
muscle on the contralateral side (Fig. 6A). The lingual
nerve also sends nerve branches in the anterior tongue to
cross the median septum of the tongue to supply the
mucosa on the contralateral side (Fig. 6B).
416
MU AND SANDERS
Figure 1
(Continued).
NEUROMUSCULAR ORGANIZATION OF THE TONGUE
417
Fig. 2. Branching and distribution of the XII nerve within the canine
tongue. A: A schematic photograph of a canine tongue (ventral view) that
illustrates the branching pattern of the XII nerve within the three layers of
the tongue muscles on one side. The genioglossus (GG) muscle is
retracted laterally. 1, the inferior layer which is separated and removed to
the lateral side; 2, the anterior part of the middle layer; 3, the posterior part
of the superior layer which is seen after the middle layer is removed. SG,
styloglossus; HG, hyoglossus; IL, inferior longitudinal muscle; T, transverse muscle; V, vertical muscle; SL, superior longitudinal muscle; GG,
genioglossus muscle; O, oblique compartment of the GG muscle; H,
horizontal compartment of the GG muscle; L, lateral division of the XII
nerve; M, medial division of the XII nerve. The asterisks indicate the nerve
branches to the posterior transverse and vertical muscles which have
been removed. The arrow indicates the nerve branch to the geniohyoid
muscle. B: Higher power view of the XII nerve branching pattern in the
posterior tongue, demonstrating the numbers and branching points of the
muscle nerves derived from the XII. M, medial division of the XII nerve; L,
lateral division of the XII nerve; PTV, nerve branches to the posterior
transverse and vertical muscles; SL, nerve branches to the superior
longitudinal muscle; GH, the nerve branch to the geniohyoid muscle; GG,
genioglossus muscle; HG, hyoglossus muscle; SG, styloglossus muscle;
LN, lingual nerve. 3⫻.
The Intramuscular Innervation Patterns of the
Individual Tongue Muscles
Styloglossus, hyoglossus, and inferior longitudinal muscles. The styloglossus, hyoglossus and inferior
Figure 2A shows the three layers of the tongue muscles.
From the ventral to the dorsal aspect of the tongue, the
muscle layers are the inferior (1), middle (2), and superior
(3), respectively. The XII nerve provides motor nerve
supply to all the three layers of the tongue muscles. The
inferior layer of the muscles is supplied by the lateral division,
whereas the middle and superior layers by the medial division
of the XII nerve. The intrinsic musculature studied includes
the transverse, vertical, and superior longitudinal muscles.
The extrinsic musculature studied includes the genioglossus,
hyoglossus, and styloglossus muscles. Each of these muscles
was found to have its own specific intramuscular innervation
pattern as described below.
longitudinal muscles consist of the inferior muscle layer of
the tongue. They receive their nerve supply from the lateral
division of the XII nerve. The lateral division actually consists
of three to four separate nerve branches which are derived
from the XII nerve at different levels within a short distance
(Figs. 1E, 2A,B). The first two branches which are smaller and
shorter than the third one supply the posterior part of the
styloglossus and hyoglossus muscles. The third branch gives
off three to four second-order branches forming a nerve
bundle. These nerve branches run toward the tip of the
tongue and give off many terminal branches along their
courses to supply the inferior longitudinal, styloglossus
and hyoglossus muscles.
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MU AND SANDERS
Fig. 3. Branching and distribution of the IX nerve within the canine
tongue (ventral view). A: After entering the tongue base the IX nerve gives
off three to four nerve branches to supply the vallate papillae (arrows) and
the mucosa of the posterior tongue. The first or medial branch mainly
contributes innervation to the vallate papillae. 3⫻. B: Higher power view
of the nerve supply of the vallate papillae in A. Note that in addition to the
IX the posterior division of the lingual nerve (LN) also gives off small nerve
branches (solid arrows) to innervate the vallate papillae (open arrows). 6⫻.
Fig. 4. Branching and distribution of the lingual nerve (LN) within the
canine tongue. A: Higher power view of Sihler’s stained right anterior
canine tongue. The arrowheads indicate that the dorsal mucosa (D) (left
side) has been separated from the muscles (M) (right side). Note that the
anterior division of the LN (aLN) and the medial division of the XII (mXII)
form a nerve bundle, running forward to the tip of the tongue (top). Nerve
branches derived from the aLN supply the mucosa and taste buds. The
square indicates the area of magnification for B. 3⫻. B: Higher power
view of the area boxed in A. Note that the terminal branches of the aLN
innervate taste buds (arrows). 9⫻.
NEUROMUSCULAR ORGANIZATION OF THE TONGUE
Figure 5.
(Legend, overleaf.)
419
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MU AND SANDERS
Fig. 6. Contralateral innervation of the XII and lingual (LN) nerves
within a canine tongue. A: Higher power view of the median fibrous
septum in the middle tongue. Note that a nerve branch from the XII nerve
(arrow) on left side crosses the median septum (M) to innervate the
superior longitudinal muscle on the contralateral side. 12⫻. B: Higher
power view of the median fibrous septum in the anterior tongue. Note that
the LN on the right side sends nerve branches (arrow) crossing the
median septum (M) to supply the mucosa on the contralateral side. 12⫻.
Transverse and vertical muscles. When the inferior muscle layer (styloglossus, hyoglossus, and inferior
longitudinal muscles) of the tongue was removed, the
middle muscle layer (transverse and vertical muscles) was
identified (Fig. 2A). Of the intrinsic tongue muscles, the
transverse and vertical muscles have relatively shorter
muscle fibers than others. Both muscles receive their
nerve supply from the medial division of the XII nerve
(Figs. 2A, 7A,B). The medial division of the XII nerve on
each side travels along the midline and runs to the tip of
the tongue. It gives off more than 20 first-order branches
and numerous twigs to the transverse and vertical muscu-
lar sheets. Each of the muscular sheets is generally
innervated by a small twig even though numerous connections exist between them (Fig. 7B).
Superior longitudinal muscle. When the inferior
and middle muscle layers of the tongue were removed, the
superior layer (superior longitudinal muscle) was seen
(Figs. 1A–C). The nerve branches to the superior longitudinal muscle is derived from the medial division of the XII
nerve (Fig. 2A). Shortly after the lateral division of the XII
is given off, four to five first-order branches are derived
from the medial division to supply the superior longitudinal muscle. These nerve branches subdivides into many
Fig. 5. Neural connections between different nerves within the canine
tongue. A: A Sihler’s stained canine tongue from which most tongue
muscles have been removed to show the neural connections between the
hypoglossal (XII), lingual (LN), and glossopharyngeal (IX) nerves. The
plexus formed by the XII and LN was dissected and placed beside the
tongue. The square a indicates the connections between the lateral
division of the XII nerve and the anterior (a) division of the LN. The square
b indicates the connections between the medial division of the XII and the
posterior (p) division of the LN. The square c indicates the connections
between the XII and the LN and between the LN and IX nerves. B: Higher
power view of square a in A, showing the neural connections (arrows) in
the plexus formed by the LN and XII nerves. 6⫻. C: Higher power view of
square b in A, demonstrating the neural connections (arrows) between the
LN and XII nerves in the posterior tongue. 6⫻. D: Higher power view of
square c in A, illustrating the neural connections between the LN and XII
nerves (small arrow) and between the LN and IX nerves (large arrow). 6⫻.
NEUROMUSCULAR ORGANIZATION OF THE TONGUE
421
Fig. 7. Innervation of the transverse (T) and vertical (V) muscles in the
canine tongue. A: A Sihler’s stained right semi-tongue, showing that the T
and V muscles receive their nerve supply from the medial division (M) of
the XII. L, lateral division of the XII nerve; LN, lingual nerve. The box
indicates the area of magnification for B. B: Higher power view of the
nerve supply of the anterior transverse (T) and vertical (V) muscles. Note
that almost every sheet of the T and V muscles has a terminal branch that
innervates both. 6⫻.
second-order branches, each of which generally supplying
a fascicle. The nerve branch supplying a muscle fascicle
always gives off finer twigs during its course (Fig. 8).
Genioglossus muscle. The genioglossus is a midline
muscle of the tongue. It originates from the mandible and
inserts into the tongue body and hyoid bone. In the dog,
this muscle was found to comprise at least two distinct
neuromuscular compartments, horizontal and oblique.
The muscle fibers in the horizontal compartment insert
into the tongue base and the hyoid bone, whereas those in
the oblique compartment insert into the tongue body.
Multiple nerve branches that are derived from the medial
division of the XII nerve supply the genioglossus muscle.
The medial division of the XII gives off more than 10 nerve
branches at different levels to supply this muscle. These
nerve branches travel from the insertional end to the
original end of the muscle and supply individual muscular
compartments (Figs. 2A,B, 9A). The intramuscular innervation patterns are different between the two compartments (Fig. 9B). Three to four first-order nerve branches
travel along the muscle fibers and span the whole length of
the horizontal compartment. During their courses they
Fig. 8. Higher power view of the nerve supply of the superior
longitudinal muscle. Note that each of the muscle fascicles is supplied by
a nerve branch which runs along the muscle fascicle, distributing terminal
branches at regular intervals, whereas each of the two larger fascicles is
supplied by several nerve branches. 9⫻.
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MU AND SANDERS
give off several terminal branches. Seven to eight firstorder nerve branches supply the oblique compartment.
The nerve branches in the oblique compartment are arranged in a grid-form (Figs. 2A, 9B).
DISCUSSION
Fig. 9. Innervation pattern of the canine genioglossus (GG) muscles.
A: The medial division (M) of the XII gives off nerve branches to the GG
muscle. GH, geniohyoid muscle; LN, lingual nerve; L, lateral division of
the XII nerve; O, oblique compartment of the GG muscle; H, horizontal
compartment of the GG muscle. B: Higher power view of the right GG
muscle in A. Note that the horizontal (H) and oblique (O) compartments of
the GG muscle have their own specially organized innervation patterns.
The nerve branches to the H compartment travel the whole length of the
muscle, whereas those to the O compartment are arranged in a grid-form.
XII, hypoglossal nerve; LN, lingual nerve; PTV, nerve branches to the
posterior transverse and vertical muscles. 3⫻.
In this study the entire nerve supply of a mammalian
tongue was demonstrated for the first time. The branching
and distribution patterns of the motor (XII) and sensory
(IX and LN) nerves to the canine tongue were studied from
the main nerves to the terminal branches. Largely this
was due to the use of the Sihler’s stain, which has the
unique ability to render a whole specimen such as the
tongue translucent, while still allowing the nerves and
muscles to be studied in their original three-dimensional
relationships. However, to fully demonstrate these relationships each specimen must be meticulously microdissected.
With this combination of techniques several important
observations could be made regarding the canine tongue.
Each of the intrinsic tongue muscles appears to actually be
a group of separate neuromuscular compartments. The
motor nerve supply to these muscles, although highly
complex, has a regular and predictable pattern. Other
observations made were that there were numerous neural
connections between the LN and XII or between the LN
and the IX, and that the innervation of the XII and LN
nerves crosses the midline.
As to the motor innervation of the tongue, Abd-El-Malek
(1938) and Hellstrand (1981) reported that the XII nerve
in man and cats is divided into a lateral and a medial
division and our findings agree with this basic description.
However, we did not find the medial division of the XII
nerve in the dog to supply the hyoglossus and styloglossus
muscles as reported in the cat (Hellstrand, 1981). In the
dog the medial division of the XII sends branches to supply
the superior longitudinal muscle immediately after the
lateral division is given off. This is not in agreement with
the finding obtained from the cat reported by Hellstrand
(1981), who observed that the nerve branches to the
superior longitudinal muscle branch off the medial division more distally. These observations indicate that the
distribution of the XII nerve is different between species.
In this study, the branching order of the XII nerve from
the root to the tip of the tongue was found to be: 1) the
styloglossal branch; 2) the hyoglossal branch; 3) the geniohyoid branch; 4) the inferior longitudinal branch; 5) the
superior longitudinal branch; 6) the branches to the horizontal part of the genioglossus muscle; 7) the posterior
transverse and vertical muscular branches; 8) the branches
to the oblique part of the genioglossus muscle; and 9) the
anterior transverse and vertical muscular branches.
The numbers of the first-order nerve branches to each
muscle are different, ranging from one to two (styloglossus
muscle) to 10 (genioglossus muscle). In addition, the
entrance of the first-order nerve branches to each muscle is
also different. For example, the nerve branches to the
styloglossus, hyoglossus, and superior longitudinal muscles
enter these muscles at their original ends (posterior part of
the tongue), whereas the nerve branches to the genioglossus enter the muscle at its insertional end. Since the
transverse and vertical muscles are arranged in alternating sheets from the base to the tip of the tongue, they
receive their nerve supply from different levels along the
course of the medial division of the XII nerve.
NEUROMUSCULAR ORGANIZATION OF THE TONGUE
The sensory innervation of the canine tongue was also
studied. The results obtained from Sihler’s stain are in
agreement with those reported by previous authors (Miller
et al., 1964; Lawn, 1966; Yamamoto, 1975) who reported
that the lingual nerve provides sensory fibers to the
anterior two-thirds of the tongue mucosa, while the IX
supplies the posterior third mucosa of the tongue and the
vallate papillae. In addition, we found that the lingual
nerve also innervates the vallate papillae.
The relationship among the lingual, XII and IX nerves in
the tongue, which is an important aspect of the neuroanatomy of the organ, was also examined by using Sihler’s
stain. Earlier studies have demonstrated the peripheral
connections between the lingual and XII nerves in the
man, dog, pig, rabbit (Fitzgerald and Law, 1958) and cat
(Fitzgerald and Law, 1958; Blom, 1960; Hellstrand, 1981).
Sihler’s stain revealed numerous neural connections not
only between the lingual and XII, but also between the
lingual and IX nerves. The neural connections between the
lingual and XII were mainly found at the junction of the
posterior and middle third of the tongue, in the plexus
formed by the lingual and XII nerves, and within the
intrinsic tongue muscles. The connections between the
lingual and IX were mainly located at the junction of the
posterior and middle thirds of the tongue. Fitzgerald and
Law (1958) observed two connection patterns, a lateral
and medial lingual-hypoglossal connections. The lateral
lingual-hypoglossal connection is formed by the connection
of one or two branches of the lingual nerve with the lateral
division of the XII nerve. This connection pattern was
found in 90% (36/40) of dissections in man. The medial
lingual-hypoglossal connection is formed by the connection
of one or more branches of the lingual nerve with the
branches of the medial division of the XII nerve. This
connection pattern was revealed in 40% (16/40) of human
dissections. Although the nature and physiological significance of the connecting nerves have never been evaluated
because of technical difficulties, the data concerning the
location and patterns of the neural connections will be
helpful for further studies.
Sihler’s stain also revealed contralateral innervation of
the XII and lingual nerves in one canine tongue specimen.
This finding is not consistent with the traditional concept
that the XII, lingual and IX nerves innervate the ipsilateral musculature and mucosa, respectively (Weddell et al.,
1940; Miller et al., 1964; Lowe, 1980). Although a conclusive statement cannot be made at this point, it is reasonable to assume that with complete unilateral paralysis of
the XII nerve some reinnervation of the paralyzed muscles
by the contralateral side could occur. Further studies will
be worthwhile to study the extent of contralateral tongue
innervation in mammals by means of Sihler’s stain and to
estimate its functional and clinical significance by using
electrophysiological techniques.
In this study, the neuromuscular organization pattern of
the tongue was demonstrated in much greater detail than
previously shown. Recent studies have confirmed that
some muscles traditionally described to be single muscles
are actually composed of smaller neuromuscular compartments that may have different functions (English and
Letbetter, 1982a,b; Windhorst et al., 1989). By using
anatomical, histological, and histochemical criteria such
as orientation of the muscle fascicles, distribution of
muscle fiber types, and intramuscular nerve supply pattern, the compartmentalized neuromuscular organization
423
of many mammalian muscles has been demonstrated in
both the large (English and Letbetter, 1982a,b) and smaller
muscles (Richmond et al., 1985; Richmond and Armstrong,
1988; Zaretsky and Sanders, 1992; Sanders et al., 1994;
Mu and Sanders, 1998b). This concept of neuromuscular
compartments within a single muscle (English and Letbetter, 1982a,b; Windhorst et al., 1989) appears to characterize the tongue muscles. In fact the evidence for separate
neuromuscular compartments in the tongue muscles is so
strong it may be more accurate to refer to them as tongue
muscle groups. Recent studies have indicated that the
regional activation of the tongue muscles appears to shape
and regulate the various motions of the tongue (Napadow
et al., 1999). It is possible that the individual tongue
muscle compartments have some degree of independent
motor function, and this would help explain how a small
number of tongue muscles can cause a large number of
different tongue shapes and movements. Confirming this
functional organization requires much more experimentation. However, the details of the nerve branching will be
helpful for determining functions of individual tongue
muscles or their compartments by electrical stimulation of
specific nerve branches. In addition, it will be useful for
localizing the motor neurons in the hypoglossal nucleus
which innervate a compartment within a given tongue
muscle by injecting horseradish peroxidase (HRP) into the
compartment or muscle layer as revealed by Sihler’s stain.
Clinically, determining the exact branching patterns of the
nerves to the tongue will be helpful for designing neurosurgical procedures to restore sensory or motor function to the
paralyzed or non sensate tongue.
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