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Quantitative studies of the greater petrosal nerve of the mouse with the electron microscope.

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Quantitative Studies of the Greater Petrosal Nerve of the
Mouse with the Electron Microscope
ATSUMI SHIMOZAWA
Department of A n a t o ~ n y ,School of Medicine, Chiba University,
Chiba, J a p a n
ABSTRACT
Quantitative counts of the greater petrosal nerve fibers of the
mouse with the electron microscope have shown that, on an average, 70.8% and
28.7% of the total nerve fibers (1,111) were unmyelinated and myelinated fibers
respectively. Unexpected high incidence of unmyelinated fibers in the greater
petrosal nerve may indicate that it contains a fair amount of sympathetic postganglionic fibers. The unmyelinated fibers in the nerve may well represent parasympathetic preganglionic fibers.
The presence of unmyElinated fibers in
the greater petrosal nerve of the cat has
been noted by Foley and DuBois ('43) with
the light micrcscope, a fact which seems to
clarify the nature of the fibers constituting
the greater petrcsal nerve. However, quantitative counts of the unmyelinated fibers
have been difficult with the light microscope. An application of electron microscopy for the fiber count was made in this
study so as to determine the exact number
of unmyelinated fibers within the greater
petrosal nerve.
a n entire area of the greater petrosal nerve
cut transversely.
OBSERVATIONS
I n transverse sections, the entire greater
petrosal nerve showed almost elliptical
form with major and minor diameters of
49-150
and 28--48 respectively (fig. 2,
table 1). The nerve was extremely flattened near the portion of its intermediate
flexion (fig. 1). Out of the eight nerves
examined i n this study, two were composed of two nerve bundles, large and
,
MATERIALS AND METHODS
Four female adult mice weighing 1822 gm were perfused through the heart
with 2.5% glutaraldehyde in Millonig's
phosphate buffer at pH 7.5 (Millonig, '62;
Sabatini et al., '64). The greater petrosal
nerve was then dissected out under the
binocular microscope and a proximal part
of the nerve less than 1.3 m m from the
geniculate ganglion excised and postfixed
in a 1% osmium tetroxide i n Millonig's
phosphate buffer (fig. 1). After dehydration with ethanol, the specimen was embedded in Epon 812. Transverse sections
of the nerve cut on a Porter-Blum microtome were mounted on a 100-mesh grid
coated by collodion, stained with uranyl
acetate and lead citrate (Reynolds, '63)
and viewed in a Hitachi HS-8 electron
microscope. Counts of myelinated and unmyelinated nerve fibers were made on a
montage of electron micrographs covering
ANAT. REC., 170: 303-308.
N. c a n a l i s pterygoidei
. carotis
interna
N. petrosus major
Ggl. geniculi
N. interrnedius
Facial trunk
Fig. 1 A dorsal view of the right greater
petrosal nerve of the mouse. The striped part of
the nerve was used as material in this study.
Received Aug. 31, '70. Accepted Dec. 8, '70.
303
304
ATSUMI SHIMOZAWA
Fig. 2 A montage of electron micrographs covering an entire area of the greater petrosal
nerve of the mouse (no. 4, L ) cut transversely.
QUANTITATIVE STUDIES OF N. PETROSUS MAJOR
305
Fig. 3 A higher magnification of tlte region outlined in figure 2. M, Myelinated nerve
fibers; U, unmyelinated nerve fibers.
small (no. l L , no. 3L). Within the nerve
bundle enclosed by the perineural sheath,
a blood capillary was found in two of the
eight nerves (no. 2L, no. 4R), and some-
times a few scattered ganglion cells were
encountered at the locus near the geniculate ganglion. No communicating branches
to or from the greater petrosal nerve were
306
ATSUMI SHIMOZAWA
TABLE 1
A fiber atzalysis of the greater petrosat nerve of the mouse, as shown by electron microscopy
Diameter of
the nerve
Animal
no.
Side
Distance from
ggl. genic.
Minor
Major
Myelinated
Unmyelinated
Undetermined
Total
mm
Right
Left
0.4-1.0
0.5-1.0
35
38
105
110
243
239
720
784
3
2
966
1025
R
L
0.5-1.0
0.0
40
35
49
82
215
247
725
680
5
6
945
933
R
0.0-0.2
0.2-0.4
55
39
95
99
335
293
1049
1037
5
6
1389
1336
1.1-1.3
0.0
28
48
150
107
497
487
621
677
8
7
1126
1171
319
(28.7)
787
(70.8)
L
R
L
5
(0.5)
1111
TABLE 2
Minor and major diameters of myelinated fibers i n the greater petrosal nerve of the mouse
-
Animal
no.
1
2
3
4
Side
1-2p
2-3p
3-4p
10
185
37
162
20
47
134
69
103
1
59
6
85
Minor
Major
Minor
Major
67
6
21
1
148
173
217
59
36
9
141
45
1
Minor
Major
Minor
Major
3
227
30
209
12
101
164
79
149
4
114
1
113
27
423
148
392
139
45
269
87
277
79
4
67
Minor
Major
Minor
Major
Minor
Average
(%)
4-5p
0-1p
Minor
Major
Minor
Major
Major
2
4
29
4
245
55
17
(5.3 (76.8’1
.
, (17.3
.
1
77
159
(0.3) (24.1) (49.9)
noticed under the binocular microscope at
the time of dissection.
Intermingled within the greater petrosal
nerve were the myelinated and unmyelinated fibers that measured in minor
diameters 0.6-3.4 EL and 0.1-1.0 EL respectively. These fibers generally were round,
oval or elliptical in form, but some myelinated fibers showed an irregular contour at the sectional level normal to their
fiber axis (fig. 3 ) . Although the thickness
__
5-6p
Total
243
13
29
6-7p
1
239
215
2
(0.6)
70
19
1
4
247
335
293
497
487
319
12
of individual myelin sheaths varied to a
considerable extent, it was rare to find
such a myelinated fiber surrounded by less
than three myelin lamellae.
Quantitative fiber counts of the eight
greater petrosal nerves from four mice
(table 1) showed that, on an average, each
nerve contained a total of 1,111 fibers, of
which only 319 (28.7% ) were myelinated
whereas 787 (70.8% ) had no investment
of the myelin sheath at all. In addition,
QUANTITATIVE STUDIES OF N. PETROSUS MAJOR
there were on the average five profiles undetermined as to whether myelinated or
not. Most of them showed a collar of processes of Schwann cells around the axiscylinder indicating that they may possibly
represent a transverse sectional level
through the node of Ranvier.
The myelinated fibers in the greater
petrosal nerve ranged from 0.6-3.4
in
minor diameters with the majority (76.8% )
being 1-2 p, while their major diameters
varied from 0.8-6.3
with those measuring 2-3 p being most frequent (table 2).
DISCUSSION
It is widely accepted that the greater
petrosal nerve contains not only secretory
fibers to the lacrimal gland, but also parasympathetic and sensory fibers innervating
the mucous membrane of the nasal cavity
and palate, as well as some taste fibers
(Beninghoff-Goerttler, '57; Gray, '58;
Mitchell, '53; Morris, '53). With regard to
the relation between form and nature of
the nerve fiber, it has been believed that,
at most, the autonomic preganglionic fibers
are thinly myelinated and the postganglionic fibers are unmyelinated, whereas
the sensory fibers are myelinated with quite
a variable diameter (Bloom and Fawcett,
'68). Therefore, it seems that the myelinated fibers, making up about 30% of
the total fibers in the greater petrosal nerve
of the mouse, represent the parasympathetic preganglionic fibers to the lacrimal gland, the sensory and parasympathetic preganglionic fibers innervating
the nasal and palatine mucosa, and some
taste fibers as well.
In a previous study of the myelinated
fibers in the greater petrosal nerve of the
crab-eating monkey (Shimozawa, '68)
with a fan-wise split preparation method
(Fukuyama, '54), it was shown that the
nerve contained thick and thin myelinated
fibers in almost equal quantities. Because
of the difference of the methods used, i t
is difficult to compare the results in the
present study for the mouse with those in
the previous study. However, it seems that
the proportion of thin myelinated fibers in
the greater petrosal nerve of the mouse
may be more than that in the crab-eating
monkey.
307
On the nature of the unmyelinated fibers, representing about 70% of the total
number of fibers in the greater petrosal
nerve, the following three probabilities are
considered; ( 1 ) the sympathetic postganglionic fibers, ( 2 ) the parasympathetic preganglionic fibers, ( 3 ) the parasympathetic
post ganglionic fibers.
Although sympathetic fibers in the
greater petrosal nerve have not been reported, their presence in the facial trunk
distal to the geniculate ganglion has been
shown in the cat by Foley ('48). The
greater petrosal nerve unites with the deep
petrosal nerve which contains a large number of the sympathetic postganglionic fibers, so it is probable that some fibers corresponding with those of the deep petrosal
nerve may come into the facial nerve
somewhere and pass through the greater
petrosal nerve.
Foley and DuBois ('37) have shown the
presence of unmyelinated parasympathetic
preganglionic fibers in the vagus nerve of
the cat. Subsequently, after a section of
the root of the facial nerve of the cat, they
demonstrated that about 62% of the fibers
of the greater petrosal nerve are visceral
motor fibers, 80-90% of which are myelinated. So it seems also probable that the
unmyelinated fibers in the greater petrosal
nerve of the mouse may in part represent
the parasympathetic preganglionic fibers.
Okinaka et al. ('50) have shown that in
the dog vagus nerve the unmyelinated fibers increased distal to the superior and
inferior ganglia; the authors regarded
many of the unmyelinated fibers in the
vagus nerve as postganglionic in nature.
However, the presence of parasympathetic
postganglionic fibers in the greater petrosal
nerve may be eliminated based on the
findings that the geniculate ganglion i s
composed of unipolar cells (Rhinehart,
'18). Multipolar cells have not been yet
iound in the ganglion.
Thus, i t is postulated that the greater
petrosal nerve of mice contains a considerable amount of the sympathetic postganglionic fibers and that some of the parasympathetic preganglionic fibers in the
greater petrosal nerve may well be unmyelinated. Further experiments must be
done to test the above postulations.
308
ATSUMI SHIMOZAWA
ACKNOWLEDGMENTS
The author wishes to thank Dr. U. Fukuyama, Dr. T. Nagano and Dr. A. Yamauchi
for their help and advice.
LITERATURE CITED
Benninghoff, A., and K. Goerttler 1957 Lehrbuch der Anatomie des Menschen. 5 Aufl.,
Urban & Schwarzenberg. Muunchen-BerlinWien, 111: 302-303.
Bloom, W.,and D. W. Fawcett 1968 A Textbook of Histology, 9th ed. W. B. Saunders Co.
Philadelphia-London-Toronto. pp. 327-333.
Foley, J. O., and F. S. DuBois 1937 Quantitative studies of the vagus nerve in the cat. J.
Comp. Neur., 67: 49-68.
1943 A n experimental study of the
facial nerve. J. Comp. Neur., 79: 79-105.
Foley, J. 0. 1948 The special visceral efferent
zone of the seventh cranial nerve i n the canalis
facialis. J. Conip. Neur., 88: 4 3 9 4 5 1 .
Fukuyama, U. 1954 O n the constituents of the
hypogastric nerve. Fukushima J. Med. Sci., I:
117-139.
Johnston, T. B., D. V. Davis and F. Davis 1958
Gray’s Anatomy, 32nd ed. Longmans, Green &
Co., London, New York, Toronto. p. 1,118.
Millonig, G. 1962 Further observations on a
phosphate buffer for osmium solutions in fixation. Proc. 5th Intern. Cong. Electron Microscopy, Philadelphia, Vol. 11, Academic Press,
New York. p. 8.
Mitchell, G. A. G. 1953 Anatomy of the Autonomic Nervous System. 1st ed. E & S Livingstone Ltd. Edinburgh and London, pp. 162-164.
Okinaka, S. 1950 O n the morphology of the
autonomic nerve fibers. Nippon Rinsho, 8:
12-21.
Reynolds, E. 1963 The use of lead citrate at
high pH as a n electron-opaque stain in electron
microscopy. J. Cell Biol., 17: 208-212.
Rhinehart, D. A. 1918 The nervus facialis of
the Albino mouse. J. Comp. Neur., 30: 81-125.
Sabatini, D. D.,F. Miller and R. J. Barrnett 1964
Aldehyde fixation for morphological and enzyme histochemical studies with the electron
microscope. J. Histochem. and Cytochem., 12:
57-71.
Schaeffer, J. P. 1953 Morris’ Human Anatomy.
11th ed. McGraw-Hill Co., New York.
1102-1 104.
Shimozawa, A. 1968 Myelinated nerve fibers
i n the facial nerve of the crab-eating monkey.
Acta Anat. Nipponica, 43: 73-88.
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