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Solitary neurons in human tongue.

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Solitary Neurons in Human Tongue
C . H. U. CHU
Department of Anatomy, School of Medicine, Case Western
Reserve Universitg, Cleveland, Ohio
ABSTRACT
Many solitary neurons, each encapsuled by a number of satellite cells
and surrounded by collagenic fibers and unaccompanied by other nerve cells, are
observed i n specimens of the posterior third of the human tongue. They are ganglion
cells of the parasympathetic nervous system supplying postganglionic fibers that are
adenomotor to von Ebner’s gland and myomotor to the smooth muscle of blood vessels.
The occurence of solitary neurons suggests that a “ganglion” m a y consist of a single
nerve cell. It is emphasized that the lingual branch of the glossopharyngeal nerve
supplying the posterior third of the human tongue is not a sensory but a mixed nerve.
This report describes the solitary neuEach cell has a prominent karyosome
rons found in the human tongue. A soli- or false nucleolus stained deep purple with
tary neuron is a unicellular entity without Harris’ hematoxylin. The nucleus has an
the company of other nerve cells. In the eccentric location, a spheroidal shape and
peripheral nervous system, nerve cells a vesicular appearance. Its scanty chrogenerally aggregate together to form gan- matin granules are either distributed irregglia. A ganglion, be it cranial, spinal, auto- ularly in the karyolymph or accumulated
nomic, collateral or terminal, usually at the inner surface of the nuclear memconsists of many nerve cells. Indeed, it is brane (figs. 3-8). In certain cells, a nuclear
a rare occasion to find solitary neurons in invagination is distinctly recognizable
peripheral nerves. A search of the litera- (figs. 4, 8). A nuclear indentation and a
ture reveals that the vagus is the only peri- cytocentrum cannot be found possibly bepheral nerve in which solitary neurons cause nerve cells ordinarily do not divide.
have been described (Dolgo-Saburoff, ’36; That a nuclear invagination is structurally
Botar et al., ’50; Hoffman and Kuntz, ’57). different from a nuclear indentation has
As far as I am aware, the existence of been emphasized in a previous report
solitary neurons in the human tongue has (Chu, ’60). The cytoplasm appears granular in cells stained with hematoxylin and
not been reported previously.
The solitary neurons reported here were eosin (figs. 3, 4 ) . With the Heidenhain’s
f i s t noticed in a tongue specimen obtained “Azan” method, the Nissl bodies, stained
from a Caucasian male who died of heart- with aniline blue, are clearly discernible
failure at the age of 45 years. The speci- (figs. 7, 8). The axon hillock can be demen was fixed in a Zenker-acetic mixture. lineated in some cells (fig. 4). The amount
Paraffin sections were stained by Harris’ of cytoplasm in these cells appears to be
hematoxylin eosin; Heidenhain’s azocar- less than the amount in dorsal root ganmine aniline blue, or Bodian’s copper pro- glion cells. The outline of the cell body is
often irregular. These cytological features
targol method.
Frequently, near the circumvallate papil- clearly indicate that these cells are neulae at the posterior third of the tongue, rons. Since each of these cells is surseveral cells appearing much larger than rounded by a number of satellite cells, they
the nearby connnective tissue cells are are further identified as ganglion cells
scattered in the stroma between the epi- (figs. 3 - 8 ) . The identification of these cells
thelium and the underlying gland (figs. 1, as neurons is made on purely morphologi2 ) . Closer examination under high magni- cal grounds; a physiological study to test
fication shows these cells to be neurons the conductivity of these cells in the tongue
each possessing the characteristics of a of living human subjects has not yet been
ganglion cell (figs. 3, 4).
attempted .
ANAT. REC., 162: 505-510.
505
506
C. H . U. CHU
The possibility that the particular histological section under observation might
have cut through a single nerve cell situated at the very periphery of a ganglion
of actually many cells would invalidate
the designation of such a neuron as solitary. For this reason, serial sections of the
tongue specimen have been examined carefully to verify its solitude. Assuredly, each
neuron is encapsuled by its satelite cells
and completely isolated by collagenic fibers
of the stroma with no other nerve cell
nearby (figs. 3, 4). Occasionally, a solitary
neuron is found close to a blood vessel.
Between the blood vessel and the satellite
cells, a narrow perivascular space can be
seen (fig. 3).
Thus far, the description of the solitary
neurons is based on the tongue specimen
obtained from a Caucasian male. Obviously, it is essential to see if similar solitary neurons are present in other specimens. Inasmuch as an unfixed human
tongue is not readily obtainable, specimens
of the tongue were collected from six
cadavers used in our gross anatomy laboratory. As expected, the finished slides prepared from cadaverous material left much
to be desired. Nevertheless, the quality of
the slides was sufficient for the purpose
of affirming that solitary neurons are present in the posterior third of the tongue
in all specimens.
Since solitary neurons are found in the
stroma within the tongue, they may therefore be regarded as intramural or terminal
ganglion cells. All terminal ganglia, as
generally agreed among neurophysiologists, are a part of the parasympathetic
division of the autonomic nervous system.
Although the solitary neurons are often
found in the vicinity of circumvallate papillae, they probably do not receive sensory
fibers from the taste buds. Very likely, the
solitary neurons are postganglionic cells
supplying fibers that are adenomotor to
von Ebner’s gland and myomotor to the
smooth muscle of blood vessels. As shown
in figure 7, a nerve fiber appears to emerge
from a ganglion cell; it loops around and
seems to terminate on the wall of a blood
vessel. Unfortunately, a thorough investigation of nerve fibers originating from the
solitary neurons could not be made satisfactorily because the tongue specimen was
fixed in a Zenker-acetic mixture known to
be incompatible with Bodian’s protargol
method (figs. 5, 6).
Many scattered ganglia have been observed between the lobules of von Ebner’s
gland in serial sections of the posterior
third of the human tongue. These ganglia,
like most others, are multicellular; each
consists of two (fig. 6 ) , three (fig. 8), or
more nerve cells. Only in the stroma between the gland of von Ebner and the
epithelium of circumvallate papilla are the
solitary neurons observable.
The posterior third of the tongue is
supplied almost exclusively by the lingual
branch of the glossopharyneal nerve.
The lingual branch enters the tongue
beneath the upper part of the hyoglossus
muscle. Along its course within the tongue,
many scattered ganglia are observable. As
the lingual branch travels in between the
lobules of von Ebner’s gland toward the
epithelium, the number of nerve cells in
each ganglion seems to decrease until, in
the stroma of circumvallate papilla, a
“ganglion” contains but a single nerve cell
as a solitary neuron.
In the literature, several cranial nerves
have been described to contain scattered
ganglia. Langley (1878) was the first to
describe scattered ganglia in the chorda
tympani of the facial nerve. In fact,
the scattered ganglia in the chorda
tympani supplying the submandibular
gland are collectively known as Langley’s
ganglion in honor of its discoverer (Kuntz,
’46). On several occasions, scattered ganglia have been found in the vagus nerve
(Dolgo-Saburoff, ’36; Botar et al., ’50; Hoffman and Kuntz, ’57). In the glossopharyngeal nerve, scattered ganglia are found to
be present in both its tympanic and lingual
branches (Crosby et al., ’62). The fact
that the lingual branch of the glossopharyngeal nerve contains not only scattered ganglia but also solitary neurons
signifies that it is structurally very similar
to the vagus nerve.
Since solitary neurons and scattered
ganglia are not detectable with unaided
eyes, understandably the lingual branch
of the glossopharyngeal nerve is described
in almost all textbooks of gross anatomy as
a purely sensory nerve mediating gustatory
sensation from the taste buds and general
SOLITARY NEURONS
sensation from the posterior third of the
tongue. The nerve cells receptive to these
sensations are located in the petrosal or
inferior ganglion in the region of the jugular foramen. The presence of solitary
neurons and scattered ganglia at the posterior third of the human tongue suggests
that the lingual branch is not purely sensory, but mixed containing motor as well
as sensory fibers. The motor fibers in the
lingual branch are preganglionic originating from cells in the inferior salivatory
nucleus located in the brain stem. The preganglionic fibers make synaptic connections inside the tongue with solitary neurons and scattered ganglia which, in turn,
supply postganglionic fibers to von Ebner’s
gland and the smooth muscle of blood
vessels.
In conclusion, the occurrence of solitary
neurons as described here suggests that
a ganglion is not always made of a group
of nerve cells but may consist of a solitary
neuron. So far, solitary neurons have been
found only in the glossopharyngeal and
vagus nerves. In the peripheral nervous
system, a solitary neuron is a postganglionic cell supplying fibers that are adenomotor to glandular epithelium and myo-
507
motor to smooth muscle. The presence of
solitary neurons and scattered ganglia at
the posterior third of the human tongue
indicates that the lingual branch of the
glossopharyngeal nerve is not a purely
sensory, but a mixed nerve.
LITERATURE CITED
Botar, J., D. Afra, P. Moretz, H. Schiffman and
M. Scholz 1950 Die Nervenzellen und Ganglien des Nervus vagus. Acta Anat., 10: 284314.
Chu, C. H. U. 1960 A study of the subcutaneous connective tissue of the mouse, with
special reference to nuclear type, nuclear division and mitotic rhythm. Anat. Rec., 138:
11-21.
Crosby, E. C., T. Humphrey and E. W. Lauer
1962 Correlative Anatomy of the Nervous
System. MacMillian, New York.
Dolgo-Saburoff, B. 1936 Zur Lehre vom Aufbau
des Vagussystem. I. Vber die Nervenzellen in
den Staemmen des Nervus vagus. Z. Anat.,
u. Entwg., 105: 79-93.
Hoffman, H. H., and A. Kuntz 1957 Vagus
nerve components. Anat. Rec., 127: 551-568.
Kuntz, A. 1946 Components and distribution
of the nerves of the parotid and submandibular
glands. J. Comp. Neur., 85: 21-32.
Langley, J. N. 1878 O n the physiology of the
salivary secretion. Part I. The influence of the
chorda tympani anad sympathetic nerves upon
the secretion of the submaxillary gland of the
cat. J. Physiol. (London), 15: 176-244.
PLATE 1
EXPLANATION OF FIGURES
1
A transverse section of human tongue through a circumvallate papilla
to show the stroma between the epithelium ( E ) and the underlying
gland ( G ) where solitary neurons are usually located as indicated
by an arrow. Note the taste buds a t (T).H. & E. x 7 5 .
2
A solitary neuron i n the stroma between the epithelium ( E ) and von
Ebner‘s gland ( G ) as indicated by an arrow. Note the solitary neuron
is larger than the nearby connective tissue cells. Human tongue.
H. & E. x 750.
Same cell as shown in figure 2. Note the endothelial linings along
the lumen ( L ) of a blood vessel. Also note the perivascular space.
H. & E. X 1,100.
A solitary neuron showing the nuclear invagination indicated by an
arrow. Note the axon hillock next to a satellite cell below the arrow.
H. & E. X 1,100.
A solitary neuron a t one side of a nerve bundle ( N ) . Bodian’s copper
protargol method. x 1,100.
A ganglion of two cells a t one side of a nerve bundle ( N ) . Bodian’s
copper protargol method. x 1,100.
A ganglion cell supplying a n axon ( A ) to a n arteriole containing a
red blood cell ( r ) at one side of a nerve bundle ( N ) Heidenhain’s
“Azan” method. x 1,100.
8
508
A ganglion of three cells, two of which are partly out of the picture
frame. Note the nuclear invagination indicated by an arrow and the
axis cyclinders in a nerve bundle sectioned transversely ( N ) . Heidenhain’s “Azan” method. x 1,100.
SOLITARY NEURONS
U. Chu
PLATE 1
C. H.
509
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