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Occurrence of calcitonin-positive C cells within the distal vagal ganglion and the recurrent laryngeal nerve of the chicken.

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THE ANATOMICAL RECORD 224:43-54 (1989)
Occurrence of Calcitonin-Positive C Cells Within
the Distal Vagal Ganglion and the Recurrent
Laryngeal Nerve of the Chicken
YOKO KAMEDA
Department of Anatomy, Fukuoka University School of Medicine, Fukuoka 814-01, Japan
ABSTRACT
The chicken ultimobranchial glands are richly supplied with
nerve fibers originating from both the main trunk of the vagus nerve and its
branch-the recurrent laryngeal nerve. C cells immunoreactive for calcitonin were
invariably found in the large nerve bundles distributed throughout the ultimobranchial glands. In addition, these cells were often present within the distal vagal
ganglia and the recurrent laryngeal nerves. The frequency of occurrence and the
pattern of distribution of the C cells in the distal vagal ganglia and the recurrent
laryngeal nerves were determined in chickens of various ages by means of an
immunoperoxidase method with anticalcitonin and antineurofilament antisera.
The left and right sides of the ultimobranchial region were asymmetrical. The left
ultimobranchial gland was in close contact with the vagus nerve trunk, especially
with the distal vagal ganglion, but it was separated from the recurrent laryngeal
nerve. The right gland contacted the recurrent laryngeal nerves, its medial edge
being frequently penetrated by the nerve, but the gland was separated from the
distal vagal ganglion. On the left side, C cells were found in 25 out of 39 distal
vagal ganglia but they were not distributed in the recurrent laryngeal nerve. On
the right side, the cells were present in 28 out of 43 recurrent laryngeal nerves but
absent in the distal vagal ganglia. The results indicate that the C cells secreting a
hormone calcitonin can enter into nerves, but their occurrence is restricted to the
nerves in close proximity to the ultimobranchial glands. Electron microscopic studies revealed that C cells in the nerves received numerous axon clusters enveloped
with Schwann cell cytoplasm. Naked axons regarded as axon terminals were found
in direct contact with the surface of C cells. They were mainly composed of efferenttype nerve endings showing the accumulation of numerous small clear vesicles and
a few large dense-cored vesicles. In addition, C cells were partly covered with the
long cytoplasmic processes of Schwann cells and were also in contact with the
Schwann cell perikarya. The C cells in nerves appear to be controlled by neural
stimulation.
In lower vertebrates including birds, C cells are not
distributed in thyroid glands, but form separate organs
called ultimobranchial glands. In contrast to mammalian thyroid C cells which have no relation to neural
elements, ultimobranchial glands of lower vertebrates
receive numerous nerve fibers (Watzka, 1933) and
some C cells of frog and chick ultimobranchial glands
are in close contact with axon clusters (Robertson,
1967; Hodges and Gould, 1969; Stoeckel and Porte,
1969). The innervation of ultimobranchial glands in
the chicken has been studied in detail by the use of an
immunoperoxidase staining with antiserum to chick
neurofilaments (Kameda et al., 1988). The chick ultimobranchial glands are supplied with a large number
of branches derived from both the main trunk of the
vagus nerve, especially the distal vagal ganglion, and
one of its branches-the recurrent laryngeal nerve. In
the course of study of the innervation of chick ultimobranchial glands, I noticed that C cells are distributed
in large nerve bundles projecting to the ultimobran0 1989 ALAN
R. LISS, INC.
chial glands, and furthermore that the cells can migrate into the distal vagal ganglia and the recurrent
laryngeal nerves. The present study was undertaken t o
show the frequency of occurrence, distribution pattern,
and electron microscopic features of the C cells in the
distal vagal ganglia and the recurrent laryngeal nerves.
The results indicate that C cells, functioning its endocrine cells, can be dispersed in the vagus nerve trunk
and its branches and fit into the category of “vagal
paraganglionic cells.”
MATERIALS AND METHODS
Chickens (white leghorn) of both sexes and various
ages, newly hatched to 12 months old, were used.
Received March 1, 1988; accepted November 28, 1988.
44
Y. KAMEDA
C CELLS IN THE VAGUS NERVE OF CHICKENS
45
TABLE 1. The occurrence of C cells in the left distal
vagal ganglia from chickens of various ages
ment antisera. The preparation and characterization of
each antiserum have been described previously (Kameda
and Ikeda, 1979; Kameda et al., 1988). The porNo. of
cine and salmon calcitonin antisera were used at
No. of
animals showing
1:3,000 to 1:5,000 and the neurofilaments antisemm a t
C cells in the
Age
animals
1:1,000 to 1:3,000 dilutions. The rabbit primary anti(days)
examined
distal vagal ganglion
bodies
(IgGs) were localized using goat antirabbit IgG
1
9
6
(Cappel
Labs.) at a dilution of 1:20 for 30 min, rinsed in
5
8
4
phosphate-buffered saline (PBS),pH 7.3, and incubated
10
5
2
with rabbit horseradish peroxidase antiperoxidase com7
6
30
plex (PAP, Miles-Yeda LTD) a t a dilution of 1:lOO for
Adult
10
7
(6-12 months)
30 min. The peroxidase reaction was developed with 5
Total
39
Incidence 25/39 (64.1%) mg diaminobenzidine tetrahydrochloride per 100 ml
0.05 M Tris, pH 7.6, plus 0.01%H202. Control reactions
included replacing the primary antisera with normal
(nonimmune) rabbit serum and absorbing the primary
TABLE 2. The occurrence of C cells in the right antisera with an excess of the respective antigens.
recurrent laryngeal nerves from chickens of various
Electron Microscopy
ages
Fifteen chickens, 1 day, 10 days, and 6 months old,
No. of
were used for electron microscopy. Anesthetized aniNo. of
animals showing
mals were perfused through the heart for 15 min with
Age
animals
C cells in the
2.5%
glutaraldehyde in 0.1 M cacodylate buffer, pH 7.4,
(davs)
examined
recurrent nerve
with 0.02 mM CaClz and 3% sucrose; then the ultimo1
6
2
branchial glands were excised and fixed for an addi6
6
5
tional 2 hr in the same fixative. The tissues were post10
10
4
fixed for 2 hr in 1%osmium tetroxide in the cacodylate
20
4
3
buffer. After dehydration in ethanol and propylene ox11
8
30
ide, the specimens were embedded in Epon epoxy resin
Adult
6
5
(6-12 months)
by the standard method. Thin sections were made with
Total
43
Incidence 28/43 (65.1%) a diamond knife and were then doubly stained with
uranyl acetate and lead citrate.
RESULTS
Histological and lmmunoperoxidase Staining
Ultimobranchial glands, together with adjacent tissues from chickens aged 1day, 5 days, 10 days, 20 days,
1month, 6 months, and 12 months, were removed and
processed. Forty-three right glands and 39 left glands
were examined (see Tables 1,2). Specimens were fixed
in Bouin's solution for 24-48 hr, embedded in paraffin,
and then cut into 5 pm-thick serial sections. Some sections were stained with hematoxylin-eosin or periodic
acid-Schiff (PAS) reaction. For immunoperoxidase
staining, the unlabeled antibody peroxidase-antiperoxidase technique of Sternberger (1979) was used. Prior
to incubation of primary antisera, deparaffinized slides
were placed in methanolic peroxide solution (one part
3%H202 to five parts methanol, v/v) for 30 min at room
temperature to suppress endogenous peroxidase activity. Sections were incubated with the primary antisera
at different dilutions for 18 hr at 4°C. The following
primary antisera were employed: antiporcine calcitonin, antisalmon calcitonin, and antichick neurofila-
Figs. 1-3. Three serial sections of the left ultimobranchial gland
from a 6-month-old chicken, stained by three different methods. The
left distal vagal ganglion (DVG) is located adjacent to the ultimobranchial gland. x 90.
Fig. 1 . Hematoxylin-eosin staining. T w o large branches (arrows)
originating from the distal vagal ganglion enter the ultimobranchial
gland.
Fig. 2. Immunoperoxidase staining with antichick neurofilament
The ultimobranchial glands of chickens consist of C
cells arranged in large and small clusters in the connective tissue stroma. In addition, there were cysts of
various sizes and shapes. They were mostly lined with
a single layer of squamous to cuboidal cells, and partially included a multilayered epithelium. The cyst lumina contained various amounts of colloid-like and
flocculent materials. The C cells distributed in connective tissue stroma and in cyst epithelia were intensely
immunoreactive to anticalcitonin antisera.
Numerous nerve fibers immunoreactive to the antineurofilaments antiserum were observed in chick ultimobranchial glands (Figs. 1, 2). They varied in size.
Some nerves were large and thick with only a few
branches, while others divided into delicate branches
inside the glands and exhibited complex ramifications.
Innervation of chick ultimobranchial glands has been
described in detail in a previous study (Kameda et al.,
1988). The ultimobranchial gland was located between
the main trunk of the vagus nerve, especially the distal
vagal ganglion, and its branch-the recurrent laryn-
antiserum. Numerous nerve fibers immunoreactive for neurofilaments are distributed within the ultimobranchial gland.
Fig. 3. Immunoperoxidase staining with antiporcine calcitonin antiserum. C cells immunoreactive for calcitonin are observed within
the distal vagal ganglion.
Fig. 4. Higher magnification of the distal vagal ganglion in Figure
3. C cells gathered in small clusters are scattered among nerve fibers
and surround the ganglion cells. x 230.
46
Y.KAMEDA
C CELLS IN THE VAGUS NERVE OF CHICKENS
Figs. 9, 10. Consecutive sections of the right ultimobranchial
gland from a 1-month-old chicken, stained by two different methods.
The right recurrent laryngeal nerve (RN) is in close contact with the
ultimobranchial gland. C, cyst. X 140.
47
rent nerve enters the ultimobranchial gland.
Fig. 10. Immunoperoxidase staining with the calcitonin antiserum. Numerous C cells (arrows) immunoreactive for calcitonin are
distributed within the branch.
Fig. 9. Hematoxylin-eosin staining. A large branch of the recur-
geal nerve-at the beginning of the common carotid
artery. The vagus nerve trunk was situated lateral to
the ultimobranchial gland and the recurrent laryngeal
nerve medial to it. The topographical locations of the
right and left ultimobranchial glands were asymmetrical.
On the left side, the ultimobranchial gland was attached to the distal vagal ganglion, but it was separated from the recurrent laryngeal nerve. The left ultimobranchial gland received a large number of branches
originating from the distal vagal ganglion (Figs. 1, 2).
The left carotid body was located cranially in contact
with the ultimobranchial gland (Fig. 5).The prominent
nerve bundles and several ganglion cells derived from
the distal vagal ganglion were observed in the lateral
cranial portion of the ultimobranchial gland, i.e., just
inferior to the carotid body (Fig. 6). At the lateral cranial portion of the gland, numerous C cells were invariably scattered in the large nerve bundles and surrounded the ganglion cells (Figs. 7,8).The large nerve
bundles in the ultimobranchial gland ran toward the
carotid body and contributed to the carotid body innervation. C cells were also distributed in the nerves surrounding the carotid body. Furthermore, the cells were
found within the distal vagal ganglion (Fig. 3). They
were concentrated near the origins of the large
Figs. 5-7. Three serial sections of the left ultimobranchial gland
from a 1-month-old chicken, stained by three different methods. The
left carotid body (CB) is situated cranially in contact with the ultimobranchial gland. C, cyst. x 115.
ultimobranchial gland.
Fig. 5. Hematoxylin-eosin staining. Arrowheads indicate nerve
cells derived from the distal vagal ganglion.
Fig. 6. Immunoperoxidase staining with the neurofilament antiserum.The carotid body is enclosed with numerous nerve fibers. Many
large bundles are observed in the lateral cranial portion of
Fig. 7. Immunoperoxidase staining with the calcitonin antiserum.
C cells intermingle with nerve bundles and ganglion cells in the lateral cranial portion of ultimobranchial gland.
Fig. 8. Higher magnification of the lateral cranial portion of ultimobranchial gland in Figure 7. C cells (arrows) are dispersed within
the large nerve bundles. They (arrowheads) also surround the ganglion cells. x 230.
48
Y. KAMEDA
C CELLS IN THE VAGUS NERVE OF CHICKENS
49
B
A
VN
VN
RN
I
DvIfi
I
RN
DVG
Fig. 15. A,B: Schematic drawings showing the distribution of C
cells within the distal vagal ganglion, the recurrent laryngeal nerve,
and their branches. Each dot represents C cell clusters in the nerve. C
cells always enter the large nerve bundles distributed in the ultimobranchial gland. In addition, the cells follow the reverse course of the
large nerve bundles and migrate into the right recurrent nerve or the
left distal vagal ganglion which is located adjacent to the ultimobranchial gland. UB, ultimobranchial gland; CB, carotid body; VN, vagus
nerve trunk; DVG, distal vagal ganglion; RN, recurrent laryngeal
nerve. A: Ventral view of the right side. The right ultimobranchial
gland contacts the recurrent nerve; the medial edge of the gland is
penetrated by the nerve. Within the recurrent nerve, C cells are concentrated near the origin of the branches projecting to the ultimobranchial gland. B: Ventral view of the left side. The left ultimobranchial gland is located adjacent to the distal vagal ganglion. Within the
distal vagal ganglion, C cells are concentrated near the origin of the
branches projecting to the ultimobranchial gland.
branches projecting into the ultimobranchial gland.
The C cells in the distal vagal ganglia were similar in
appearance and immunohistochemical reaction for calcitonin to the cells in ultimobranchial glands (Fig. 3).
They were intensely immunoreactive to the calcitonin
antisera and usually oval to round in shape. The C cells
were dispersed singly or arranged in small groups
among the nerve fibers, and intermingled with or surrounded the neural cell bodies (Fig. 4). The number of
C cells distributed in the distal vagal ganglia was different from individual to individual. In some ganglia
only 5-6 cells per section were observed, while other
ganglia contained as many as 50-100 cells per section
plane. The occurrence of C cells in the distal vagal
ganglia from chickens at various ages ranging from 1
day to 12 months is shown in Table 1. Twenty-five out
of 39 distal vagal ganglia contained variable numbers
of C cells; the frequency of occurrence was 64.1%.The
incidence of C cells in the ganglia did not differ with
age. At 1 day after hatching, C cells were already apparent in the distal vagal ganglia, although only a few
were present.
The branches originating from the recurrent laryngeal nerve often entered the medial caudal portion of
the left ultimobranchial gland. C cells were also distributed in the branches of the recarrent laryngeal
nerve inside the ultimobranchial glands. However,
they were never detected in the left recurrent laryngeal nerve itself which was separated from the gland.
Thus, in the ultimobranchial gland, C cells were always dispersed in the large nerve bundles which arose
from both the distal vagal ganglia and the recurrent
laryngeal nerves. Figure 15B shows the schematic distribution of C cells in the branches originating from the
distal vagal ganglion and the recurrent laryngeal
nerve, and also within the distal vagal ganglion.
On the right side, the ultimobranchial gland contacted the recurrent laryngeal nerve; the medial edge
of the gland was frequently penetrated by the nerve.
However, it was separated from the distal vagal ganglion. Two prominent branches originating from the
recurrent laryngeal nerve entered the medial cranial
and caudal poles of the right ultimobranchial gland
(Fig. 9). C cells were always detected in these large
branches (Fig. 10). In addition, the cells occurred
within the recurrent laryngeal nerve; they were concentrated near the origins of these large branches
(Figs. 11-13). The C cells were arranged in various
Figs. 11-1 3. Three serial sections of the recurrent laryngeal nerve
Fig. 13. Immunoperoxidase staining with the calcitonin antiserum. C cells immunoreactive for calcitonin are distributed within the
recurrent nerve.
(RN) adjacent to the right ultimobranchial gland from 6-month-old
chicken, stained by three different methods.
X
115.
Fig. 11. Hematoxylin-eosin staining.
Fig. 12. Immunoperoxidase staining with the neurofilament antiserum.
Fig. 14. Higher magnification of the recurrent nerve in Figure 13.
The C cells are dispersed singly or arranged in small clusters within
the recurrent nerve. x 280.
50
Y. KAMEDA
51
C CELLS IN THE VAGUS NERVE OF CHICKENS
sizes of clusters or dispersed singly within the recurrent laryngeal nerve (Fig. 14).The occurrence of C cells
in the recurrent nerves from chickens a t various ages
ranging from 1 day to 12 months is shown in Table 2.
Twenty-eight out of 43 recurrent nerves contained
variable numbers of C cells; the frequency of occurrence was 65.1%. The right carotid body was located
cranially, somewhat apart from the ultimobranchial
gland. The large branches which arose from the recurrent nerve and entered the ultimobranchial gland, ran
toward and terminated in the carotid body. One or two
small branches originating from the distal vagal ganglion penetrated the lateral edge of the ultimobranchial gland. They intermingled with the branches from
the recurrent nerve a t the lateral cranial part of the
gland, and then reached the carotid body. C cells were
observed in and along the nerves surrounding the carotid body. Figure 15A shows the schematic distribution of C cells in the branches originating from the
recurrent laryngeal nerve and the distal vagal ganglion, and also within the recurrent laryngeal nerve. In
contrast to the left side, no C cells were present in the
distal vagal ganglion which was separated from the
ultimobranchial gland.
ked axons were in contact with the C cells. The axons
contained microtubules, neurofilaments, and small
round or spherical mitochondria. In addition, numerous axon terminals forming synaptic contacts with the
surface of C cells were detected (Figs. 17, 18). They
showed the accumulation of synaptic vesicles and a
special differentiation in the membranes, desmosomelike thickening. The synaptic vesicles were commonly
composed of numerous small, clear (30-50 nm in diameter) and occasional large, dense-cored (60-100 nm
in diameter) vesicles (Fig. 18).
Fig. 16. Electron micrograph of a C cell distributed within the
nerve. The C cell contains numerous characteristic secretory granules. The perikaryon of Schwann cell (S) and axons (arrows) are in
close contact with the C cell. N, nucleus of C cell. x 7,100.
axons (arrowheads) showing the accumulation of synaptic vesicles
come into direct contact with the C cell. Large electron-pale granules
intermingle with typical electron-opaque secretory granules in the
cell. N, nucleus of C cell. x 8,500.
Fig. 17. A C cell distributed within the nerve. The cell is partially
enclosed with the long cytoplasmic process of Schwann cell. Besides
the axon clusters ensheathed with the Schwann cell cytoplasm, naked
Fig. 18. An axon terminal (arrowhead) apposed the surface of C
cell within the nerve. It contains numerous small clear vesicles and a
few large dense-cored vesicles. X 15,000.
DISCUSSION
The ultimobranchial glands of chickens are richly
innervated by the branches originating from the vagus
nerve trunk, especially from the distal vagal ganglion,
and the recurrent laryngeal nerve (Kameda et al.,
1988). The present study showed that C cells immunoreactive for calcitonin were invariably distributed in
the large branches from the distal vagal ganglion and
the recurrent laryngeal nerve inside the ultimobranchial glands. Furthermore, the cells were found within
the distal vagal ganglion and the recurrent nerve.
Since the topographical locations of ultimobranchial
glands are asymmetrical, the pattern of distribution of
Electron Microscopy
C cells within the nerves was completely different on
The ultrastructure of C cells in chick ultimobran- the right side and the left side. The left ultimobranchial gland has been described in a previous study (It0 chial gland had intimate contact with the distal vagal
et al., 1986). The C cells distributed in the nerves were ganglion, but it was separated from the recurrent
similar in ultrastructural features to the cells in ulti- nerve, whereas the right ultimobranchial gland conmobranchial glands, except that they were iqtimately tacted the recurrent nerve, the medial edge being often
associated with neural elements. C cells were filled penetrated by the nerve, but it was separated from the
with characteristic secretory granules, ranging from distal vagal ganglion. The invasion of C cells was re100 to 300 nm in diameter (Figs. 16-18). The granules stricted to the left distal vagal ganglion and the right
were electron-opaque and usually round t o oval, al- recurrent nerve adjacent to the ultimobranchial
though they sometimes revealed pleomorphic shapes. glands. There were no C cells in the right distal vagal
In addition, large granules (400 nm in mean diameter) ganglion, and the left recurrent nerve which were sepwith paler content were occasionally observed among arated from the gland. The C cells were concentrated
the typical electron-dense secretory granules (Fig. 17). around the origins of the large branches projecting to
Each granule was surrounded by a limiting membrane. the ultimobranchial glands within the left distal vagal
The C cells were easily discernible by these conspicu- ganglia and the right recurrent nerves. The regions
ous secretory granules from other cellular elements in remote from these branches were devoid of C cells.
the nerves. The C-cell nuclei were round or oval with a Thus, C cells appear to be able to migrate into the
smooth outline. Spheroid and elongated mitochondria distal vagal ganglion and the recurrent nerve along the
were dispersed in the cytoplasm. Golgi complexes were large branches, but their migration distance in the
seen around the nucleus. Free ribosomes arranged in nerves seems to be short.
The number of C cells distributed in the left distal
rosettes and cisternae of the rough endoplasmic reticulum were numerous throughout the cytoplasm. In vagal ganglia and the right recurrent nerves differed
most cases, the C cells were in close contact with the from individual to individual. In the cases showing nuperikarya of Schwann cells (Fig. 16) and were also merous C cells, 50-100 cells per section plane were
partially enveloped by long cytoplasmic processes of detected, while in some cases only a few C cells were
Schwann cells (Fig. 17). Schwann cells were agranular present in the nerves. The frequency of occurrence of C
and had irregular nuclear profiles. They contained nu- cells in the left distal vagal ganglia was 64.1% and that
merous filaments and microtubules and relatively few in the right recurrent nerves was 65.1%; the incidence
cytoplasmic organelles. A large number of axon clus- of C cells in the nerves was almost the same on the left
ters ensheathed with Schwann cell cytoplasm and na- and right sides.
52
Y. KAMEDA
The occurrence of C cells in the nerves did not differ
with age. In chickens at various ages ranging from 1
day to 12 months, C cells were present in the nerve
almost at the same rate. The calcitonin production of
ultimobranchial C cells starts at around 16 days of incubation age; weak immunoreactivity for calcitonin begins to appear in C cells (Kameda, 1984). Thereafter,
calcitonin immunoreactivity of C cells rapidly increases during late embryonic periods. At 1 day after
hatching, almost all C cells in the ultimobranchial
glands exhibit intense immunoreactivity for calcitonin.
At this stage, C cells were already observed in the
nerves and showed the same distribution patterns as
the adults, although the number of C cells in the nerves
was still small in proportion to the volume of ultimobranchial glands. It seems that C cells migrate into
nerves during early embryonic periods.
The ultimobranchial anlage arises from the last pair
of pharyngeal pouches during early embryonic development. By the use of the techniques of heterospecific
grafting (Le Douarin and Le Lievre, 1971) and fluorogenic amine tracer (Pearse and Polak, 1971), it has
been reported that the ultimobranchial bodies of avian
and mammalian embryos are colonized by cells derived
from the neural crest and that the bodies are only the
penultimate origin of the C cells. Although there are
conflicting data concerning the origin of the carotid
body (see Bock, 1982 for reviews), Pearse et al. (1973)
also reported that chief cells (type I cells) of the carotid
body are derived from the neural crest. The expression
of the various phenotypes characterizing neural crest
derivatives has been considered t o depend largely on
environmental cues encountered by crest cells during
their migration and in the site where they settle (see
Le Douarin, 1982 for reviews). Furthermore, exogenous fibronectin and high cell density seem to be necessary for effective directional migration of the crest
cells (Rovasio et al., 1983). In the chickens, the ultimobranchial gland is located in contact with the carotid
body. C cells often surround the carotid body. The carotid body as well as the ultimobranchial gland are
supplied by the branches from the vagus nerve trunk
and the recurrent laryngeal nerve, although the carotid body receives more numerous nerve fibers than
the ultimobranchial gland (Kameda et al., 1988). The
hypothesis of neural crest origin of ultimobranchial C
cells and carotid body chief cells cannot be supported or
refuted by the results of the present study. Even if both
C cells and chief cells are derived from the neural crest,
environmental cues for the expression of each phenotype may be each anlage of the ultimobranchial
gland and the carotid body. Migratory crest cells expressing the same phenotype could not invade different
tissues, i.e., the ultimobranchial anlage and the
nerves. It is more likely that after the ultimobranchial
gland has received the innervation, C cells proliferate
rapidly and migrate into the distal vagal ganglion and
the recurrent nerve.
In mammals, C cells are distributed in thyroid
glands. During early fetal development, mammalian
ultimobranchial bodies are incorporated into and then
dispersed throughout thyroid parenchyma as C cells. In
some animal species, including rabbits, cats, goats, and
dogs, the C cells are also observed in the parathyroid
gland IV and thymus IV, which have an intimate to-
pographical connection with the ultimobranchial anlage during embryonic development (Kameda, 1971,
1981). However, no C cells are dispersed in the parathyroid I11 and thymus 111, which are separated from
the ultimobranchial anlage. Thus, C cells of many animal species seem to have an ability to migrate into
adjacent organs or tissues from their residential places;
in mammals they can enter parathyroid gland and thymus, and in chickens they can enter nervous tissue.
In the chick ultimobranchial gland, C cells distributed around large bundles and complex ramifications
of nerves are in close contact with numerous axon clusters enveloped with Schwann cell cytoplasm (Hodges
and Gould, 1969; Stoeckel and Porte, 1969; Kameda et
al., 1988). In addition, naked axons are observed to
form synaptic contacts with the surface of C cells; they
show an accumulation of synaptic vesicles and a special
differentiation in the membranes, desmosome-like
thickening. Stoeckel and Porte (1969) reported that the
axon terminals in contact with C cells contained small
dense-cored vesicles, which were considered to be sympathetic adrenergic nerve terminals. However, our previous study (Kameda et al., 1988) indicated that the
nerve endings containing small dense-cored vesicles
are only rarely observed and a majority of axon terminals on the C cells show the accumulation of numerous
small clear vesicles and a few large dense-cored vesicles. In addition, very few fluorescent fibers are detected around C-cell groups after treatment with
Falck-Hillarp procedure, in contrast to the presence of
numerous neurofilaments-positive nerve fibers around
C-cell groups. It is considered that C cells of chick ultimobranchial glands are mostly innervated by cholinergic parasympathetic fibers. The C cells distributed in
the distal vagal ganglion and the recurrent laryngeal
nerve also had intimate relation t o neural elements.
Many axon clusters ensheathed with Schwann cell cytoplasm and naked axons regarded as axon terminals
apposed the C cells. The axon terminals showed the
accumulation of numerous small clear vesicles and a
few large dense-cored vesicles; the C cells in nerves
also receive mainly cholinergic efferent type fibers.
Furthermore, they were in close association with
Schwann cell perikarya and partially enveloped by
long cytoplasmic processes of Schwann cells. It appears
that the secretory activity of chicken C cells is controlled by nerve stimulation.
The epithelial cell clusters which are distributed in
and around nerves and show high contents of catecholamines, are often called “paraganglion.”The occurrence of paraganglia in the vagus nerve trunk and
their branches has been described in various mammalian species; the vagal paraganglia are very numerous
and widely distributed (Deane et al., 1975; McDonald
and Blewett, 1981). They are frequently observed in or
near the nodose ganglion, which corresponds to the distal vagal ganglion of the bird (Watzka and Scharf,
1951; Grill0 et al., 1974; Kondo, 1977), and within the
recurrent laryngeal nerves (Dahlqvist et al., 1984). It
has been reported that the vagal paraganglionic cells
are morphologically similar to chief cells of the carotid
body and small intensely fluorescent (SIF) cells of the
superior cervical ganglion; they contain numerous
membrane-bound, electron-opaque granules (60-140
nm in diameter) and are in close contact with numer-
C CELLS IN THE VAGUS NERVE OF CHICKENS
53
ous axon clusters (Grillo et al., 1974; Morgan et al., Dahlqvist, A,, B. Carlsoo, S. Domeij, and S. Hellstrom 1984 Morphometric analysis of glomus cells within the recurrent laryngeal
1976; Kondo, 1977). In addition, the cells show intense
nerve of the rat. J. Neurocytol., 13r407-416.
fluorescence for catecholamines after the treatment of Deane,
B.M., A. Howe, and M. Morgan 1975 Abdominal vagal
Falck-Hillarp procedure (Gorgas and Bock, 1976). Raparaganglia: Distribution and comparison with carotid body, in
the rat. Acta Anat. (Basel), 93:19-28.
dioactive labelling is concentrated over the secretory
granules of the vagal paraganglionic cells after the in- Grillo, M.A., L. Jacobs, and J.H. Comroe, Jr. 1974 A combined fluorescence histochemical and electron microscopic method for
jection of 3H-dopa (Chen and Yates, 1970). The nerve
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terminals apposed the vagal paraganglionic cells are
Neurol., 153:l-14.
Gorgas, K., and P. Bock 1976 Formaldehyde induced catecholamine
mainly provided with numerous small clear vesiclesfluorescence in the mouse inferior laryngeal paraganglion. Cell
efferent-type terminals-although
afferent nerve
Tissue Res., 173r139-142.
endings also make synaptic contacts with the cells Hodges,
R.D., and R.P. Gould 1969 Partial nervous control of the
(Grillo et al., 1974; Morgan et al., 1976; Kondo, 1977).
avian ultimobranchial body. Experientia, 25~1317-1319.
These synapses have been considered to correspond Hodges, R.D., A.S. King, D.Z. King, and E.I. French 1975 The general
ultrastructure of the carotid body of the domestic fowl. Cell Tisfully to those seen in the carotid body. Although the
sue Res., 162:483-497.
functional significance of the vagal paraganglia is not Ito, M.,
Y. Kameda, and T. Tagawa 1986 An ultrastructural study of
known, in view of their close morphological resemthe cysts in chicken ultimobranchial glands, with special reference to C-cells. Cell Tissue Res., 246:39-44.
blance to the carotid body, chemoreceptive properties
Kameda, Y. 1971 The occurrence and distribution of the parafollicuhave been suggested.
lar cells in the thyroid, parathyroid IV and thymus IV in some
In contrast to mammalian species, there is little remammals. Arch. Histol. Jpn., 33:283-299.
search into the vagal paraganglia in lower vertebrates, Kameda, Y. 1981 Distribution of C-cells in parathyroid gland IV and
thymus IV of different mammals studied by immunoperoxidase
including birds. In chickens, however, chief cells of the
method using anti-calcitonin and anti-C-thyroglobulin antisera.
carotid body and granule-containing cells of the aortic
Kawasaki Med. J., 7:97-111.
wall, which belong to “paraganglionic cells,” have been Kameda,
Y. 1984 Ontogeny of chicken ultimobranchial glands studfrequently investigated by electron microscopy (Hodges
ied by a n immunoperoxidase method using calcitonin, somatostatin and 19s-thyroglobulin antisera. Anat. Embryol. (Berl.),
et al., 1975; Taha and King, 1983; Ookawara et al.,
170:139-144.
1974; Kondo, 1974; Abdel-Magied and King, 1984). Kameda,
Y., and A. Ikeda 1979 C cell (parafollicular cellf-immunoBased on the definition of “paraganglion,” chicken C
reactive thyroglobulin: Purification, identification and immunocells distributed within the distal vagal ganglia and
logical characterization, Histochemistry, 60:155-168.
the recurrent laryngeal nerves may be included in the Kameda, Y., K. Okamoto, M. Ito, and T. Tagawa 1988 Innervation of
the C cells of chicken ultimobranchial glands studied by immucategory of “vagal paraganglionic cells.” In fact, C cells
nohistochemistry, fluorescence microscopy and electron microsof chick ultimobranchial glands show intense green
copy. Am. J. Anat. 182:353-368.
fluorescence for dopamine after freeze-drying and fix- Kine. AS.. D.Z. Kine. R.D. Hodees. and J. Henrv 1975 Svnautic morpholob of the cirotid body Gf the domestic 6wl. C e l f T i k e Res.,
ation in paraformaldehyde vapor (Almqvist et al.,
162:459-473.
1971; Kameda et al., 1988). In addition, avian C cells Kondo,
H. 1974 On the granule-containing cells in the aortic wall of
exhibit immunoreactivity for tyrosine hydroxylase, inthe young chick. Anat. Rec., 178t253-266.
dicatingdopamine-containing cells (Takagi et al., 1984). Kondo, H. 1977 Innervation of SIF cells in the superior cervical and
nodose ganglia: An ultrastructural study with serial sections.
However, C cells in the nerves do not resemble the
Biol. Cell, 30:253-264.
paraganglionic cells of the carotid and aortic bodies in Le Douarin,
N. 1982 The Neural Crest. Cambridge Univ. Press, Camtheir ultrastructural features. The major difference is
bridge.
the size of secretory granules; the secretory granules of Le Douarin, N., and C. Le Lievre 1971 Sur l’origine des cellules a
calcitonine du corps ultimobranchial de l’embryon d’oiseau. Bull.
C cells are larger than those of chief cells and granuleAssoc. Anat. (Nancy), 56:558-568.
containing cells. Furthermore, axon clusters or axon McDonald,
D.M., and R.W. Blewett 1981 Location and size of carotid
terminals in close contact with the C cells are less nubody-like organs (paraganglia) revealed in rats by the permeabilmerous than those on chief cells of the carotid body.
ity of blood vessels to Evans blue dye. J. Neurocytol., 10:607-643.
The nerve terminals apposing the C cells are provided Morgan, M., R.J. Pack, and A. Howe 1976 Structure of cells and nerve
endings in abdominal vagal paraganglia of the rat. Cell Tissue
with numerous small clear vesicles-cholinergic efferRes., 169:467-484.
ent-type endings. No afferent-type endings are found in Ookawara, S., K. Suzuki, Y. Yoshida, and G. Ooneda 1974 Monoamine-storing cells in the media of the thoracic aorta of Gallus
relation to the C cells. Afferent and reciprocal synapses
domesticus. Cell Tissue Res., 151~309-316.
are demonstrated in the chief cells of chick carotid bodA.G.E., and J.M. Polak 1971 Cytochemical evidence for the
ies (King et al., 1975; Taha and King, 1983). In con- Pearse,
neural crest origin of mammalian ultimobranchial C cells. Histrast to other paraganglionic cells, C cells synthesize
tochemie, 27:96-102.
and secrete a hormone, calcitonin, with an endocrine Pearse, A.G.E., J.M. Polak, F.W.D. Rost, J. Fontaine, C. Le Lievre,
and N. Le Douarin 1973 Demonstration of the neural crest origin
function, and do not show chemoreceptive properties.
Yl
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