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Neural crest and placodal contributions in the development of the glossopharyngeal-vagal complex in the chick.

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THE ANATOMICAL RECORD 196:71-82 (1980)
Neural Crest and Placodal Contributions in the
DeveI o p ment of the G Iossophary ngeal-Vagal
Complex in the Chick
C. H. NARAYANAN AND Y. NARAYANAN
Department of Anatomy, Louisiana State University School of Medicine,
New Orleans. Louisiana 70119
ABSTRACT
By using the method of quail-to-chick transplantation of neural
crest in one series (VNG)and placodal ectoderm in a second series (VPG) we were
able to determine the relative contribution of cranial neural crest and placodal
ectoderm to the formation of the Glossopharyngeal-vagal complex. In chimeric
embryos, quail cells originating from cranial neural crest grafts of postotic levelsend up in the root ganglia, while quail cells originating from placodal ectoderm of
postotic levels end up in the trunk ganglia. The results clearly indicate that the
caudal levels of the medulla and rostral cervical segments represent the site, and
the neural crest the source, for the neurons of the root ganglia. The neurons form a
homogenous population of the small-cell type. This clearly rules out any contribution to the root ganglia from placodal ectoderm. On the basis of our experiments, it
is also concluded that the neurons of the trunk ganglia are purely placodal in origin
and are composed of a population of cells of the large-cell type. Our experiments
also provide convincing evidence for a neural crest origin for Schwann cell and
ganglionic Satellite cells.
The origin of sensory cranial ganglia from
either neural crest or placodal ectoderm or both
these embryonic components in varying proportions has been a topic of great interest since
the time of His (1868).Based on studies of the
chick embryo, His concluded that the sensory
cranial ganglia were derived from neural crest,
while other investigators have proposed that
these ganglia have a dual origin from both neural crest and placodal components (Landacre,
’lo; Landacre and McLellan, ’12; Coghill, ’16).
Of particular importance, is the work of Hamburger (‘61), who made a careful study of the
relative share of neural crest and placodal material in the formation of the Trigeminal ganglion in the chick embryo. Two distinctly different cell types in the Trigeminal ganglion
have been described, a group of large cells of
placodal origin which stain deeply in ordinary
stains and also show a marked affinity for
silver stains, and a group of smaller cells of
neural crest origin with a relatively poor affinity for silver stains and which stain very lightly
with ordinary stains. A similar cytological duality has been observed in the remaining sensory cranial ganglia. The so-called “root” gan-
glia of the seventh, ninth, and tenth cranial
nerves are composed of the small cells which
are supposedly neural crest in origin (Yntema,
’441,and the so-called “ t r u n k ganglia of the
seventh, ninth, and tenth cranial nerves are
composed of large cells which are supposed to be
of placodal origin (see Hamburger, ’61). The
relative contribution of each of these embryonic
components in the formation of the sensory
cranial ganglia, with the exception of the Trigeminal ganglion, has not been clearly established. In particular, there is some controversy
regarding the contribution of neural crest and
placodal components in the formation of the
Glossopharyngeal-vagal complex. In birds, the
root ganglia of cranial nerves nine and ten are
combined to form the Glossopharyngeal-vagal
complex. The more rostral portion of this complex is the Superior ganglion of the Glossopharyngeal nerve, and the more caudal portion
is the Jugular ganglion of the Vagus nerve.
Each nerve also has a ganglion generally referred to as the trunk ganglion a short distance
from the brain known as the Petrosal ganglion,
Received July 2, 1979 accepted August 29, 1979.
0003-276X/80/19601-0071$02.30 0 1980 Alan R. Liss. Inc.
72
C. H. NARAYANAN AND Y. NARAYANAN
and the Nodose ganglion of the Glossopharyngeal nerve (1x1 and the Vagus nerve (X), respectively.
Marshall ('78) has proposed that the ganglia
of the Vagus nerves are formed from an outgrowth of the neural ridge common to the
Glossopharyngeal and Vagus nerves. Van
Campenhout ('37) described the ganglia of the
Glossopharyngeal and Vagus nerves as being
essentially placodal in origin, with the neural
crest contributing to the sheath cells. The visceral sensory component of the two nerves represented by the neurons of the Petrosal and
Nodose ganglia, according to Levi-Montalcini
('461,are formed exclusively of cells contributed
by the epibranchial placodes, while the root
ganglia take their origin from the neural crest.
An intermingling of both neural crest and
placodal components to form the root ganglia of
the Glossopharyngeal-vagal complex has been
postulated by Johnston and Hazelton ('72). The
existing confusion may be explained by the fact
that experimental work on the contribution of
neural crest and placodal ectoderm in the formation of sensory cranial ganglia is rather limited, due to technical difficulties in demonstrating them unequivocally and characterizing
them successfully. The development of new
methods, particularly, the interspecific transplantation experiments between quail and
chick embryos, has greatly facilitated studies
on the origin and determination of various neuronal centers (Le Douarin, '69, '73; Narayanan
and Narayanan, '78a). In the quail nucleus, the
chromatin, unlike other avian species, appears
as a large central mass that is strongly Feulgen
positive. This unique property of the quail cells
enables one to follow them wherever they migrate and in whatever part or structure they
become eventually located. Thus, quail cells
can be used as natural biological cell markers
and prove to be a valuable tool in studies on the
fate and migration of neural crest cells (Le
Douarin, '73, '74, '75; N a r a y a n a n a n d
Narayanan, '78a, '78b; Noden, '78). The present
study was carried out utilizing the technique of
interspecific transplantation of neural crest
and placodal ectoderm between quail and chick
embyros, with the aim of determining the relative share of neural crest and placodal material
in the formation of the Glossopharyngeal-vagal
complex. Results of this study point unequivocally to a purely neural crest origin for the root
ganglia of cranial nerves IX and X, and a purely
placodal origin for the trunk ganglia of these
two cranial nerves.
MATERIALS AND METHODS
Fertile eggs used in this study were from the
Babcock strain of fowls and the Japanese quail
Coturnix coturnzx japonica. The eggs were incubated in forced draft incubators maintained
at 375°C and relative humidity at 6570%. The
eggs were set for incubation times as follows:
29-33 hours, stage 9, somites 7 for the chick
embryo (Hamburger and Hamilton, '51); 27-30
hours, stage 8 for the quail (Zacchei, '61). The
method of opening the eggs and preparing the
embryo for microsurgery have been fully described in a previous study (Narayanan, '70).
Grafting procedure
Two series of operations were carried o u t
(1)Series VNG-transplantation orthotopically of neural crest from caudal medulla of
donor quail embryos to host chick embryos, and
(2) Series VPG-transplantation
orthotopically of placodal ectoderm from postotic
levels of donor quail embryos to host chick embryos. The procedure described by Narayanan
and Narayanan, ('78b) was followed for the
interspecific transplantation of cranial neural
crest between quail and chick embryos and
is shown in Fig. 1. The excision of the neural
crest fragment from donor quail embryos
usually of the right side was carried out with a
vibrating needle (Wenger, '68). Every effort
was made to cut the neural crest fragment
cleanly without damaging the neuroepithelium and with as little of extraneous material
as possible.
The "placodal" region of the trunk ganglia as
determined by initial trials is postotic, lateral
to the caudal medulla, and extends cadually to
cervical spinal cord segments to about the level
of the third somite (Fig. 1).The operations were
performed a t stage nine, prior to the migration
of cells from the ectoderm. Based on our initial
studies, it was found that the cells begin to
migrate between stages 11and 13, and by the
next several hours appear as a compact group of
cells in their final location. A vibrating needle
was used to cut out a long narrow strip of
placodal ectoderm cleanly without damaging
the mesodermal somites. The operations were
performed with great care and under strict
aseptic conditions.
After the operations, the eggs were sealed
and returned to the incubator for further development. From a total of 70 operations, 28 embryos survived, ranging in age from seven days
to 13 days of incubation. Of the experimental
ORIGIN OF THE GLOSSOPHARYNGEAL-VAGAL COMPLEX
73
n e u r a l crest f r o m
Neural crest
st. 7; 29-30 h.
Position of
auditory pit----/=i
removed f r o m c h i c k
embryo.
Transplantation of
pl accdal mate r i a l
f r o m quail embryo.
1
Fig. 1. Scheme showing the transplantation of neural crest and placodal material between quail and chick
embryo. In this diagram, only host chick embryos and the fragment that is transplanted from donor quail embryos
are shown.
animals, only those in which the wound had
healed very well and were normal i n their external appearance were used in the present
study. The unoperated side of the host embryos
were used as controls. All the operated embryos
were fixed in Zenker's fluid by immersion or
transcardiac perfusion. The brains were proc-
essedfor paraffin embedding, serially sectioned
at 5 or 7 pm in a transverse plane and stained
according to the Feulgen and Rossenbeck's
technique. In addition, a normal series of chick
embryos were impregnated with silver following the method of Cajal de Castro as described
by Levi-Montalcini ('49).
C. H. NARAYANAN AND Y. NARAYANAN
74
RESULTS
Normal root and trunk ganglia of the
Glossopharyngeal-uagalcomplex and
their topographical relationships
The root ganglia of the Glossopharyngealvagal complex and the trunk ganglion of the
Vagus (Nodose) and the Glossopharyngeal
(Petrosal) of a normal embryo of 11days incubation age from serial sections of silver impregnated material are shown in Figs. 2-5.
Fig. 2 is a section through the root ganglia of
the complex showing the relatively poor affinity for silver stains, as compared to a section
through the trunk (Nodose) ganglion of the
Vagus nerve where the cells are intensely
argyrophilic (Fig. 3). Fig. 4 is a section
through the trunk (Petrosal) ganglion of the
glossopharyngeal nerve sharing the same features as the Nodose ganglion of the Vagus
nerve. Of particular significance as landmarks
for the identification of the trunk (Nodose)
ganglion is the close relationship of this ganglion to the superior cervical ganglion, the
Internal Carotid artery and the Jugular vein.
The Nodose ganglion (Fig. 5 ) is composed of
large cells and is found ventral to the Superior
Cervical ganglion. It is flanked by a branch of
the Jugular vein medially and by the Internal
Carotid laterally.
VNG series: transplantation of neural crest
The brains of 18experimental embryos ranging in age from 7 days to 13 days of incubation
were available for detailed study. The graft was
easily identified in all cases on the basis of
characteristic appearance of quail cells when
stained by the Feulgen and Rossenbeck procedure. The chromatin of the quail nucleus appears as a large central mass that is strongly
Feulgen positive, and therefore stands out in
sharp contrast from the surrounding chick
cells. A careful examination of sections through
the operated region showed the unmistakable
presence of quail cells in the root ganglia of the
Glossopharyngeal-vagal complex in all cases.
Fig. 6 is a section through the root ganglia
from a typical case of cranial nerves IX and X.
They are composed of a homogeneous population of neurons of quail origin surrounded by
Satellite cells. No cell of the host chick embryo
is found in the root ganglia in any of the 18
cases included in this report. The root ganglia
had established connections with the medulla
by sensory roots. On the control side, the
Glossopharyngeal-vagal complex showed a
normal root ganglion in its proper location
composed exclusively of host chick cells. The
trunk ganglion (Nodose)of the Vagus nerve of
the experimental (right) side is composed entirely of host chick cells. No neuron of quail
origin is found here. Since the root ganglia of
the operated side in the experimental cases do
not have any cell derived from the host chick
embryo, it is certain that the population of cells
comprising these ganglia is derived entirely
from quail cranial neural crest material. Although the trunk (Nodose) ganglion is composed of host chick cells as described above, the
Schwann cells which accompany the nerve fibers of the Vagus and the Satellite cells surrounding the neurons in the trunk ganglion are
of quail origin (Fig. 7). Evidently, the Schwann
cells and the Satellite cells are derived from
quail neural crest material.
VPG series: transplantation
of placodal material
The following observations are based on ten
cases which showed excellent fusion of the
grafted placodal material from donor quail embryos with the rest of the epidermis of host
chick embryos. All the ten cases used for detailed histological study showed well developed
trunk (Nodose)ganglia, maintaining their typical topographic relations with the Superior
Cervical ganglion, the Internal Carotid, and
the branch of the Jugular vein. The Nodose
ganglion on the operated side was composed
entirely of quail cells, while the root ganglia
were composed entirely of chick cells. The
nerve fibers of the Vagus nerve in these cases
were accompanied by Schwann cells, all of
which, interestingly enough, were composed of
chick cells (Fig. 8). Evidently, the Schwann
cells and the Satellite cells surrounding the
Fig. 2. The root ganglia of the Glossopharyngeal-vagal complex of a normal chick embryo of 11days incubation
age as seen in a section of silver impregnated material. The cells of this ganglion show a poor affinity for silver and
are composed of a population of cells of the small-cell type as seen in this photomicrograph. De Castro silver stain.
Scale: 100 pm.
Fig. 3. Photomicrograph of a section through the trunk ganglion (Nodose)of the Vagus nerve in a normal chick
embryo of 11 days incubation age. Note the ganglion is composed of cells of large-cell type and are markedly
argyrophilic. De Castro silver Stain. Scale: 100 pm.
ORIGIN OF THE GLOSSOPHARYNGEAL-VAGALCOMPLEX
75
76
C. H. NARAYANAN AND Y.NARAYANAN
ORIGIN OF THE GLOSSOPHARYNGEAL-VAGALCOMPLEX
neurons of the trunk ganglion are derived in
this case from neural crest components of the
host chick embryo (Fig. 9).
In summary, analysis of our material with
respect to the composition of the root ganglia of
the Glossopharyngeal-vagal complex and the
trunk (Nodose) ganglion in the experimental
embryos shows: (1)The presence of a homogeneous population of cells in the root ganglia
composed entirely of quail cells in the VNG
series, indicating a neural crest origin for the
ganglia; (2) The presence of uniformly large
cells in the trunk (Nodose)ganglion composed
entirely of quail cells, derived from the graft in
embryos of the VPG series, indicating a
placodal origin for the neurons of this ganglion.
In addition to the two significant features
described above, in the trunk ganglia of the
VNG series, where the neurons are all of chick
origin, the ganglionic Satellite cells surrounding the neurons are all derived from the quail
graft (Fig. 7). In the trunk ganglia of the VPG
series of the experimental side, where the neurons are derived from quail placodal graft, the
Satellite cells surrounding the neurons are of
chick origin (Fig. 9). The results of both these
experiments complement each other and provide strong evidence for a neural crest origin for
the supporting cellular elements associated
with the nerve fibers and neurons of the root
and trunk ganglia of the Glossopharyngealvagal complex.
DISCUSSION
The main objectives of this investigation
were to determine: (1)the relative share of
neural crest and placodal components in the
formation of the root and trunk ganglia of the
Glossopharyngeal-vagal complex; (2) specific
level in the cephalic area of the chick embryo
from which these embryonic components originate; and (3) the origin and distribution of
Schwann cells and ganglionic Satellite cells associated with the Glossopharyngeal-vagal
complex. Our approach using the method of
interspecific transplantation of neural crest
and placodal components between quail and
chick embryos has enabled us to resolve even
77
more clearly some of the problems concerning
the origin and composition of the root and trunk
ganglia of this complex.
Combined root ganglia of the
Glossopharyngeal-uagal comptex
We have compared our own observations
with those of other investigators who have
studied the origin of sensory cranial ganglia in
chick embryos using "-TdR autoradiography
or radical extirpation procedures. Johnston
('66)and Johnston and Hazelton ('72) used '$HTdR autoradiographic techniques in order to
trace the migration and differentiation of neural crest and placodal elements in their studies
on the origin of sensory cranial ganglia. They
concluded that neurons of placodal origin are
present in variable numbers in the root ganglia, particularly of the seventh, ninth, and
tenth cranial nerves. The results of our studies,
however, clearly demonstrate that quail neural
crest material, when grafted orthotopically to
host chick embryos (VNG series), end up in the
root ganglia of the Glossopharyngeal-vagal
complex. Neurons of placodal origin are not
observed in the root ganglia of cranial nerves
IX and X in all the experimental cases. Similarly, when quail placodal ectoderm is grafted
orthotopically to host chick embryos (VPG
series), the quail cells are found in the trunk
ganglia of the host. Taken together, these two
experiments point unequivocally to the conclusion that, in the chick embryo, the combined
root ganglia of the Glossopharyngeal-vagal
complex are indeed purely neural crest in origin.
The discrepancy between our studies and
those of Johnston and Hazelton ('72) is attributable to the techniques used in identifying
the neurons derived from either neural crest
or placodal ectoderm successfully. Autoradiographic methods have proved to be impracticable in this connection for tracing the migration
and differentiation of neural crest and placodal
ectoderm for several reasons. The labelling becomes diluted over a number of cell divisions,
and the label cannot be strictly localized, making both quantitative and qualitative esti-
Fig. 4. Photomicrographof a section through the trunk ganglion (Petrosal) ofthe Glossopharyngeal nerve in a
normal embryo of 11 days incubation age. Note the ganglion is composed of cells of the large-cell type and also
shows a pronounced affinity for silver. DeCastro silver stain. Scale: 100 pm.
Fig. 5. The location of the trunk ganglion (Nodose)is determined on the basis of its topographical relationship
with structures such as the Superior Cervical ganglion (SCG); the Internal Carotid artery (A); and the branch of
the Jugular vein (V) as indicated in this photomicrograph. De Castro silver stain. Scale: 100 pm.
78
C. H. NARAYANAN ANDY. NARAYANAN
ORIGIN OF THE GLOSSOPHARYNGEAL-VAGALCOMPLEX
mates extremely difficult. In addition, since all
actively dividing cells pick up 3H-TdR,there is
always the question whether all of the cells so
labelled are in fact neural crest or placodal in
origin. On the other hand, the natural quail
nuclear marker labelling technique, as stated
by LeDouarin ('731, is not only stable but also
stands out in sharp contrast from those of the
host cells in unparalleled cleanness and constancy with Feulgen staining.
Jones ('42) observed the total elimination of
the root ganglia following removal of both neural crest and tube of the hindbrain. Yntema
('44)and Yntema and Hammond ('54) maintained that removal of neural crest from postotic and cervical levels led not only to the absence of the root ganglia of cranial nerves nine
and ten and of the spinal ganglia a t levels of the
operation, but also resulted in the absence or
reduction of sympathetic ganglia sheath cells
and spinal nerves. Levi-Montalcini ('46), also
employing microsurgical procedures, removed
rhombencephalic neural crest and concluded
that the root ganglia of the Glossopharyngealvagal complex are derived from neural crest.
Although our results are comparable to those of
the authors above, the techniques employed by
these investigators were too drastic, eliminating totally head mesoderm in some cases, as
well as the migrating neural crest material. It
would be difficult in their experiments to determine with certainty the precise source and
site of origin for the neural crest precursors of
the root ganglia of cranial nerves IX and X.
Trunk ganglia of the Glossopharyngeal
and Vagus nerves
Regarding the source and site of origin of the
trunk ganglia of the Glossopharyngeal-vagal
complex, our orthotopic transplantations of
placodal ectoderm (VPG series) clearly indicate
that cells derived from the placodal graft end up
in the trunk ganglia of the Glossopharyngeal-
79
vagal complex. Our results confirm and extend
those of Levi-Montalcini ('46) and Yntema
('44), who observed in their extirpation experiments in chick embryos that the Petrosal and
Nodose ganglia of the Glossopharyngeal and
Vagus nerves are derived exclusively from epibranchial placodes. Johnston ('66) and
Johnston and Hazelton ('72), using 3H-TdRautoradiography, showed that placodal contributions to the sensory cranial ganglia are rather
extensive, particularly to the trunk ganglia of
the seventh, ninth, and tenth cranial nerves.
The presence of quail cells consistently in the
trunk ganglia in our studies further validates
the conclusion that the neurons of the trunk
ganglia of cranial nerves IX and X are in fact
derived from placodal ectoderm of postotic
levels.
Origin of supporting cellular elements
A neural crest origin for Schwann cells was
first established by the pioneering work of Harrison ('06) on amphibian embryos. Later experimental work on the derivation of Schwann
cells from neural crest has been reviewed by
Horstadius ('50). Of particular interest in the
present study is the finding that the supporting
cellular elements (i.e., Schwann cells) accompanying the Glossopharyngeal and Vagus
nerves and the ganglionic Satellite cells of the
root and trunk ganglia are derived exclusively
from neural crest. As can be seen in Figs. 7
and 9, the Schwann cells and Ganglionic Satellite cells show characteristics of the species
from which the neural crest material is derived.
For instance, where the neural crest is of quail
origin, as in our VNG series, the Schwann cells
accompanying the nerves and the ganglionic
Satellite cells of both root and trunk ganglia
show the typical quail cell characteristics.
Conversely, in the VPG series, where the neural crest is derived from the host chick embryo,
the Schwann cells and Satellite cells show the
Fig. 6. Photomicrograph of a section through the root ganglion (VNG 62:13d) in which
quail neural crest was transplanted.The neurons with distinct quail nuclei are clearly seen.
The Schwann cells and the ganglion Satellite cells marked by arrows; (inseta. and b.) are of
quail neural crest origin. Inset a: A higher magnification of Schwann cells which are of
quail neural crest origin. Inset b: A higher magnification of ganglionic Satellite cells
around a neuron, all of which are of quail neural crest origin. Feulgen stain. Scale: 50pm.
Fig. 7. Section through the trunk ganglion (nodose)of experimental case (VNG62: 13d)
inwhich quail neural crest was transplanted. As seen in this photomicrograph,the neurons
of the Nodose ganglion are derived from chick cells, while the ganglionic Satellite cells
(arrows) are derived from grafted quail neural crest. Inset: A higher magnification of
ganglionicSatellite cells of quail neural crest origin in the proximity of a neuron derived
from chick placodal ectoderm. Feulgen stain. Scale: 50 pm.
80
C. H. NARAYANAN AND Y. NARAYANAN
ORIGIN OF THE GLOSSOPHARYNGEAL-VAGALCOMPLEX
characteristics of chick cells. Our observation is
in accord with that of Noden ('781, who concluded from orthotopic transplantation of posterior mesencephalic and metencephalic neural crest from quail t o chick that Schwann cells
and Satellite cells were derived from neural
crest. However, Johnston ('66), in a series of
neural crest transplantation experiments
using "H-TdR autoradiography, was unable to
locate any labelled elements in the trunk ganglia of chick embryos, and concluded that both
neurons and supporting cellular elements of all
trunk ganglia are of placodal origin. We have
no evidence in support of a placodal origin for
the supporting cellular elements of the trunk
ganglia from our experiments.
Cell types of sensory cranial ganglia and
their functional relations
It is clear from the results reported here that
the cells of the root ganglia of the Glossopharyngeal-vagal complex and the trunk ganglia exhibit the cytological duality similar to
those which have been previously described for
the Trigeminal ganglion by Hamburger ('61)
and for the ganglia of seventh, ninth, and tenth
cranial nerves by Yntema ('44). A s can be seen
from Figs. 2, 3, and 4, the distinction between the cell types which comprise the root
ganglia and the trunk ganglia, respectively, in
our silver impregnated material, based on intensity of the stain and size of the cells, is
readily apparent. The root ganglia are composed of a homogeneous population of cells
comparable to the small-cell type of neural
crest origin, and is in agreement with the observation of Hamburger ('61) in that no large
cell of placodal origin is found in the root ganglia in any of our experimental cases. The cells
of the trunk ganglia are uniformly large and
are comparable to the large-cell type of placodal
origin.
The functional significance of the embryonic
components and of the two-cell types (large and
small) have been discussed at length by Ham-
81
burger ('61) and by Johnston and Hazelton
('72). A few points concerning the functional
relations deserve special comments. General
Somatic afferent components are represented
by cells of the root ganglia of the seventh, ninth,
and tenth cranial nerves, as well as in the Trigeminal ganglion. The general visceral and
special visceral afferents (Gustatory) are represented by cells of the trunk ganglia of cranial
nerves seven, nine, and ten. A clear correlation
seems to exist between embryonic origin and
functional components and between cell type
and functional components in each case except
for the Trigeminal ganglion. For example, the
general somatic system of the Vagus is represented by the root ganglion (Jugular), neurons
of which are neural crest in origin and are of the
small-cell type. In contrast, the general visceral component of the Vagus is represented by
the trunk ganglion (Nodose), the neurons of
which are placodal in origin and belong to the
large-cell type. However, the Trigeminal
gangliondoes not fit into this scheme. As stated
by Hamburger ('61), it is a purely general
somatic system, and, unlike the sensory cranial
ganglia of more caudal levels, both neural crest
and placodal ectoderm enter into its formation.
The presence of neurons of placodal origin is
rather puzzling. It has been suggested by
Johnston and Hazelton ('72) that the Trigeminal "placodes" might represent displaced crest
cells. It is conceivable that the Trigeminal
ganglion has acquired new functional capabilities associated with changes in facial
structure in the course of vertebrate evolution
with the placodal elements assuming exteroceptive functions.
ACKNOWLEDGMENTS
We should like to thank Mr. Thomas Lee and
Mr. Russell C. Browne for their excellent technical and photographic assistance in this study,
and Mrs. Susan Orazio for her excellent secretarial help and for the careful typing of the
manuscript. This research was supported in
Fig. 8. Photomicrograph of a section through the root ganglion of the Glossopharyngeal-vagal complex (VPG
10: lld), in which quail placodal ectoderm was transplanted. Observe that the neurons as well as the Schwann
cells and Satellite cells are derived from chick neural crest. Inset: A higher magnification of ganglionic Satellite
cells and a neuron, both derived from chick neural crest. Feulgen stain. Scale: 50 pm.
Fig. 9. This photomicrograph is from a section through the trunk ganglion (Nodose) of an experimental case
( W G : 14:7d), in which quail placodal ectoderm was transplanted. As seen in this figure, the neurons of the trunk
ganglion are of quail origin, but the Schwann cells and the ganglionic Satellite cells (arrows)are of chick origin. A
higher magnification of Schwann cells derived from chick neural crest and two neurons of quail origin is shown in
inset. Feulgen stain. Scale: 5 0 ~ r n .
82
C. H. NARAYANAN AND Y. NARAYANAN
part by the National Institutes of HealthNational Institute of Child Health and Human
Development, Research G r a n t #R01 HD
12064.
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