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Proprioceptive afferents in facial nerves of some insectivores.

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F'roprioceptive Afferents in Facial Nerves of
Some Insectivores '
KINZIRO KUBOTA AND TOSHIAKI MASEGI
Section of Anatomy, Institute of Stomatognathic Science, Tokyo
Medical and Dental University, Yushima I-chome, Tokyo, japan
ABSTRACT
Fiber-caliber analysis of the facial nerve was made in the Japanese lesser shrew-mole and the Japanese shrew-mole possessing muscle spindles
in the snout muscles and in the shinto shrew with no spindles. Using an enlarged
photographic scale ( x 250) prepared from the object-micrometer (1/100mm),
the measurement of the fiber-caliber was made on the enlarged photograph
( X 1250) of the cross paraffin section treated with a modified myelin-sheath
staining procedure by Pettersen et al. ('70). The facial nerves of the shrew-moles
contained fibres of 1 to 10 p in diameter, while the facial nerve of the shrew consisted of fibers of 1 to 6 p . The spectra of the former have a slight bimodality
with the highest peak at 2 P and smaller one at 6 P. The spectrum of the latter
has a unimodality with a greater peak at 2 r . Each peak revealed a log-normal
distribution curve. Statistically, it can be said that there is a significant difference
in the caliber-spectra between the facial nerves supplying the snout muscles with
muscle spindles and without spindles.
For testing whether the skew of the spectrum can be the result of a truly bimodal distribution, the left facial nerve of the Japanese shrew-moles was cut at
the site beneath the auditory capsule. Complete degeneration of spindle innervation in the snout muscles was observed histologically in animals seven days
after operation.
The question whether mammalian facial tains no muscle spindles (Kubota and
nerve contains proprioceptive fibers has Masegi, '71), and ( 2 ) by determining the
been posed by the following investigators degeneration of fibers after cutting the
in the past (Wakeley and Edgeworth, '33; facial nerve at its peripheral portion.
Carmichael and Wollard, '33; van Buskirk,
MATERIALS AND METHODS
'45; Elliot, '54; Hamilton, Boyd and Moss(1) Arithmetric approach
man, '59; Huber, '61; Davies and Davies,
The material for this study was the
'64). However, this question still remains
Japanese lesser shrew-mole (Dymecodon
unsolved. Recently, the present authors pilirostris) and the shinto shrew (Sorex
reported the conspicuous distribution of shinto shinto), because both animals are
muscle spindles in the snout musculature much the same in body size. For making
of the Japanese shrew-mole (Kubota and a comparison with these species, the JapIdasegi, '72). Since the facial nerve in anese shrew-mole (Urotrichus talpoides),
this species has no peripheral anastomosis much bigger than the former two, was
with other cranial nerves, the propriocep- used. The facial nerves were removed at
tive fibers from the spindles might make the site beneath the auditory capsule under
their way to the facial nerve. The present a stereoscope and fixed in 10% formalin.
histological and experimental investiga- Paraffin cross sections were prepared at
tions were designed to clear the popula- 5
in thickness. Sections were stained
tion difference of fibers in the facial nerve with a modification of Weigert's myelin( 1 ) by comparing fiber diameters from sheath staining procedure (by Pettersen
'Talpidae in which muscle spindles exist
Received Nov. 15, '71. Accepted Mar. 17, '72.
jn the snout muscle, with those from
1Read at the 76th Annual Meeting of Japanese
!Soricidae in which the snout muscle con- Association
of Anatomists, Tokyo, April 3 4 , 1971.
ANAT. REC., 173: 353-364.
353
354
KINZIRO KUBOTA AND TOSHIAKI MASEGI
RESULTS AND DISCUSSION
and Sadjadpour, '70). On the other hand,
the motor root of the mandibular division
of the trigeminal nerve to the masticatory
muscles with muscle spindles and some
peripheral muscle nerves to the forelimb
were examined in serial celloidin sections
from the Japanese shrew-mole and the
shinto shrew.
As shown in figures 4, 5 and 6, the enlarged photomicrographs ( X 1250) were
taken from the section. Measurement of
the caliber of nerve fibers was made on
them using an enlarged photographic
scale ( X 250) prepared from an object
micrometer (1/100 mm). The value of
the measurement obtained was statistically
scrutinized by Dr. Hiroshi Maeda, Professor of Public Health Department, Tokyo
Medical and Dental University School of
Medicine.
Arithmetric results
Representative aspects in cross sections
of facial nerves from three species of Insectivores are shown in figures 4, 5 and 6.
One may find many myelinated fibers with
a greater caliber in the nerves of the
Japanese lesser shre w-mole and Japanese
shrew-mole than in that of the shinto
shrew. As shown in table 1, the fibers were
divided into groups of 1 p unit, for example, 1 p group ranging from 0.3 to 1.4 p,
2 p group from 1.5 to 2.4 p , etc. The caliber-spectra are presented in the percentage
histogram of the facial nerves of these
three species (fig. 1). This histogram represent& the mean of the findings in several
sections from each of the facial nerves examined.
The mean number of the fibers counted
on the facial nerve was 1674 in the Jap(2) Experimental approach
anese lesser shrew-mole, 2077 in the
The degeneration method was employed Japanese shrew-mole and 1182 in the
to gain convincing evidence of propriocep- shinto shrew. The Japanese lesser shrewtive fibers in the f acid nerve. The material mole contains fibers with a caliber from
used for this experiment was six Japanese 1 to 10 p, and the Japanese shrew-mole
shrew-moles captured with the Sharman has fibers with a size range from 1 to 8
live-trap (small type) in the area of
Mt. Fuji. After feeding them in the laboratory with mealworm, earthworm and
5 60mouse intrinsic organs for one or two
. ...
..""!
8
55weeks, the animals were operated under
i i
50ether anesthesia. The facial nerve on the
4 45 left side was exposed beneath the auditory
40capsule under a stereoscope and cut with
35an electric knife. The surgical operation
2 30was successful in three animals, but the
other three died during or soon after oper- 2 2 5 ation. In the successful cases, one died 30
hours after operation, and the other two
were fed for seven days until they were
killed for histological examination. After
I 2 3 4 5 6 7 8 9 10 microns
the brains were carefully removed from
the facial crainium, they were immersed
in 10% formalin solution on a rotator.
Diameter of nerve f i b c r
The facial crania were embedded in celFig. 1 Percentage histogram of the number of
loidin for serial section after decalcifica- nerve
fibers according to a diameter of fiber in
tion. Serial transverse or sagittal sections the facial nerve supplying the snout musculature
were prepared from them at 30 in thick- in the insectivores. The thick line indicates the
ness. Sections were stained in every other Japanese lesser shrew-mole, the thin line the
shrew-mole and the dashed line the
section with hematoxylin-eosin and a Japanese
shinto shrew. Ordinate: number of nerve fibers,
silver impregnation method (Kubota et al., Abscissa: fiber-diameter (including myelin'56).
sheath).
5
g
Pi
-
Y
355
FACIAL NERVES OF SHREW AND SHREW-MOLES
TABLE 1
Comparison of diameter distribution of facial nerve fibers in the insectivores
Japanese lesser shrew-mole
Diameter
of fiber
Number
of fibers
%
Y
8
9
10
142.7
647.3
344.3
195.7
143.3
143.3
36.0
18.3
2.0
1.o
Total
1673.9
1
2
3
4
5
6
7
Frequency
Japanese shrew-mole
Number
of fibers
8.5
38.7
20.6
11.7
8.6
8.6
2.2
1.1
0.1
0.1
Frequency
Shinto shrew
Number
of fibers
%
218.5
1037.5
289.5
218.0
161.0
116.0
33.5
2.5
0
0
2078.5
in diameter. The shinto shrew, however,
contains fibers with a caliber from 1 to 6 p,
while only three out of 1182 fibers are
above 5 in diameter.
As shown in table 1, the ratio of the
large diameter axons over 5 to the total
fibers of the facial nerve is 15 to 20% in
ithe shrew-moles and only 3% in the shrew.
Contrary to this, the ratio of the small
diameter axons below 4 to the total fibers
is 80 to 85% in the former two and 97%
in the latter. Thus, spectra of facial nerves
Erom the shrew-moles show a slight bimodality with the highest peak at 2
and a small one at 6 and that from the
shinto shrew only a conspicuous unimodality with the peak at 2 p. All peaks reveal
a log-normal distribution curve (fig. 3).
Measurement of the fiber-diameter of
various peripheral muscle nerves in mammals has been made by investigators in
the past. Rexed and Therman ('48)
examined the nerves to the cat anterior
tibialis and gastrocnemius muscles, Hunt
('54) the nerves to the cat soleus and
median gastrocnemius muscles, Boyd ('62)
the nerves to the cat soleus, tenuissinus
and interosseous muscles, Donovan ('67)
the cat optic nerve and Karlsen ('69) the
nerves to the cat masticatory muscles.
Thilander ('64) reported the caliber-spectrum of fibers in the human lateral pterygoid nerve. Murphy and Cameron ('67)
studied the nerves to the horse masticatory muscles. Korneliussen ('64) made a
measurement of fiber-diameter in spinal
nerve roots of the whale and Jacobs and
10.5
50.0
13.9
10.5
7.8
5.6
1.6
0.1
Frequency
%
173.0
682.3
165.0
126.5
32.3
2.8
0
0
0
0
14.6
57.7
14.0
10.7
2.8
0.2
1181.9
Jensen ('64) in cranial nerves of the great
whale. Their assay reports showed that
the fibers range from 1 to 20 in the cat,
1 to 17 in the human, 1 to 2 3 /*. in the
horse and 1 to 15 ,? in the whale.
Comparing the size range from 1 to 10
of the facial nerve fibers in the insectivores
examined with that in the other mammals
cited above, it seems that the former shows
a much narrower range of fiber size than
the latter. As a practical question, it is
possible that if other peripheral muscle
nerves are studied in these three species
of insectivores a greater range of fiber
sizes would show up with a new population with a mean size greater than 10 ?.
Survey of the motor roots of the mandibular division of the trigeminal nerve
supplying the masticatory muscles, with
abundant muscle spindles, of the shrewmoles and the shrew showed a size range
of fiber sizes from 1 to 10 p . Several peripheral muscle nerves to the forelimb
studied also had no fibers over 8 in diameter. These findings indicate that a population of large axons over 10 p in diameter
does not exist in nerves of these species.
In view of the findings from three
species listed in table I , it is notable that
the fibers with a size range from 1 to 6
exist in the facial nerve of the shinto
shrew but the fibers (with a size range
from 1 to 10 p ) over 6 in diameter are
present in the shrew-moles. Hence, in
order to study the distribution of the fibercaliber, the cumulative frequency shown
in table 2, which is calculated from the
356
KINZIRO KUBOTA AND TOSHIAKI MASEGI
TABLE 2
Percentage o f cumulative frequency and corrected
cumulative frequency of fiber-caliber in facial
nerve o f the shinto shrew
Diameter
of fiber
J
!
1
2
3
4
5
6
Cumulative
frequency
Corrected
cumulative frequency
%
%
14.6
72.3
86.2
96.9
99.8
100.0
14.0
68.0
91.0
96.8
99.8
100.0
observed values of the fiber-caliber in
table 1, is plotted on probability paper
(fig. 2). When the diameter of the fibers
is taken on the abscissa in log scale, it is
almost a straight line in the shinto shrew.
From this it is thought that the distribution type in the shrew is of a log-normal
distribution. However, since the straight
line bends around the middle in the shrewmoles, one can not postulate that the distribution type in them has linearity adaptation. This bending of the straight line
indicates that this line consists of two different elements. As a sufficient reason, i t
might be adduced that (1) a linearity is
not kept in the shrew-moles possessing
fibers over 6 EL and ( 2 ) no fibers over 6
in diameter exist in the facial nerve of the
shinto shrew.
What if the distribution pattern of the
shrew-moles is superimposed on that of
the shinto shrew? Such a comparison
seems to be the only remaining alternative
to be examined and that requires use of
“trial and error” methodology. Hence, the
cumulative frequency is calculated from
the observed values of the shinto shrew,
and then the corrected values are calculated when the line is straight (table 2).
As shown in table 2, it does not matter
Diameter o f nerve f i b e r ( m i c r o n ) , log
Fig. 2 Adaptation to the probability paper of the fiber-diameter in facial nerves of
shinto shrew
Japanese lesser shrew-mole ( X ) and Japanese shrew-mole ( m ) . Ordinate:
probability scale, Obscissa: diameter of fiber (&) in log scale.
(a),
357
FACIAL NERVES OF SHREW AND SHREW-MOLES
mated that it is 43 in the 5 group. Up
to 5 it becomes 1373 in total. Hence,
the cumulative frequency of the fibers
over 5 in diameter shows the following
distribution: 100 (143 minus 43 equals
100) in the 5
group, 143 in the 6
group, 36 in the 7 group, 18 in the 8
group, 2 in the 9 group, and 1 in the
10 group. This distribution also can be
considered as a log-normal distribution.
In coordination of the above-mentioned
results, it is thought that the two patterns
of distribution type overlap each other at
the value of 5 (fig. 3).
which corrected values are taken. But, in
consequence of the trial and error method
the percentage of the cumulative frequency from 1 to 4 p is determined to
be 96.8.
In the Japanese lesser shrew-mole the
cumulative frequency of the fibers with a
size range from 1 to 4 p becomes 1330,
being 96.8%, and therefore 100% becomes 1373. In consequence, the cumulative frequency of the fibers from 1 to 4 p
is as follows: 143 in the 1 group, 647
in the 2
group, 344 in the 3 group,
196 in the 4 group, and i t can be esti-
Frequency
Japaner e
I100
s hre w-mole
I000
900
800
700
Shinto
shrew
lesser
shrew - m o l e
Japanese
600
50 0
40 0
30 0
200
too
0
1
2 3 4 9 6
1
1
1
1
1
I 2 3 4 5 6
Ib
I
I
I
I
I
1 2 3 4 5 6 7 8
Diameter o f nerve f i b e r i n f a c i a l nerve (micron)
Fig. 3 Frequency curve of fiber-caliber of the facial nerves in shinto shrew (left),
Japanese lesser shrew-mole (middle) and Japanese shrew-mole (right).
358
KINZIRO KUBOTA AND TOSHIAKI MASEGI
The same thing can be said for the
Japanese shrew-mole. Since the cumulative frequency of the fibers with a size
range from 1 to 4 becomes 1765, being
96.8% , 100% becomes 1823. Therefore,
the cumulative frequency of the fibers
from 1 to 4
is as follows: 219 in the
1 group, 1038 in the 2 group, 290 in
the 3 group, and 218 in the 4 group,
and it can be estimated that it is 58 in
the 5
group. Against this, that of the
fibers over 5 in diameter becomes 103
(161 minus 58 equals 103) in the 5
group, 116 in the 6 group, 34 in the 7
group and 3 in the 8 group. From this
observation it is though that the distribution pattern is composed of two types of
distribution, both of which are of a lognormal distribution.
Thus, the facial nerve is unimodal in
the shinto shrew and bimodal in the
Japanese lesser shrew-mole and Japanese
shrew-mole (fig. 3). The conclusion drawn
from the present statistical data is that
there is a significant difference in the caliber-spectra between the facial nerves supplying the snout muscles possessing muscle spindles and those with no spindles.
In other words, two populations of great
and small diameter axons occur in the
shrew-moles in which muscle spindles
exist in the snout muscle and only one
population of small diameter axons are
present in the shinto shrew in which the
snout muscle contains no muscle spindles.
This highly suggests that the presence or
absence of muscle spindles in the snout
muscle influences the population difference in the caliber-spectrum of fibers in
the facial nerve of the insectivores
examined.
Experimental results
No evidence presently exists that the
spectrum of fiber diameters of the facial
nerve of the shrew-moles is bimodal. If
the large diameter fibers represent the
spindle afferents in the facial nerve, cutting this nerve should result in the degeneration of fibers in the most peripheral
portion, especially in the spindle region
of snout muscles. In cranial nerve territory, however, it seems to be very difficult
to test experimentally whether the skew
of the fiber-caliber spectrum shown in
figures 1 and 3 can be the result of a
truly bimodal distribution, because one can
not cut the anterior- or posterior element
separately, in contrast to the spinal cord
in which the anterior and posterior roots
can be selectively lesioned. For this anatomical reason, the present experimental
design was employed to test our proposed
hypothesis.
After operation, the vigorous movement
was lost completely and the long snout
bent toward the healthy (right) side. The
animal showed a marked fall in food
gathering activities, that is, he was unable
to catch the earthworm to eat, and his
interest in mealworm and mouse intrinsic
organs was reduced.
Histological examination showed the
degeneration of the facial nerve in the
snout muscle area. Complete degeneration
of the nerve fibers was seen in the spindle
innervation of the snout muscles as well
as in extramuscular and intramuscular
areas on the surgically paralyzed side
(left side) (figs. 7, 8). This is more conspicuous by comparing the intact innervation of the muscles on the opposite side.
Blood vessel innervation remains intact
in the muscles on the denervated side.
From the arithmetric and experimental
results demonstrated here, it can be said
that the large diameter fibers in the peripheral portion of the facial nerve of the
shrew-moles, having muscle spindles, are
proprioceptive afferents.
ACKNOWLEDGMENTS
The authors wish to express their deepest thanks to Professor Dr. Hiroshi Maeda
of Public Health Department, Tokyo
Medical and Dental University School of
Medicine, for statistically scrutinizing the
data obtained in this study and to Mr.
Yoshiharu Imaizumi, Research Fellow of
Institute of Stomatognathic Science, for
collecting the specimens used for this experimental study. We also thank Dr.
Takara Yonaga, Associate Professor of
Pharmacology Department , Tokyo Medica1
and Dental University School of Medicine,
for his excellent technical assistance in
surgical operation.
LITERATURE CITED
Boyd, I. A. 1962 The structure and innervation of the nuclear bag muscle fibre system
FACIAL NERVES OF SHREW AND SHREW-MOLES
and the nuclear chain muscle fibre system in
mammalian muscle spindles. Philos. Trans.
Royal SOC. Lond., 245: 81-136.
Carmichael, E. A,, and H. H. Wollard 1933
Some observations on the fifth and seventh
cranial nerves. Brain, 56: 109-125.
Davis, D. V., and F. Davies 1964 Gray’s
Anatomy: Descriptive and Applied. Thirty-third
Ed. Longmans, Green and Co., Ltd., Lond.
Donovan, A. 1967 The nerve fiber composition of the cat optic nerve. J. Anat., 101: 1-11.
Elliot, H. C. 1954 Textbook of the Nervous
System. A foundation for clinical neurology.
Second Ed. J. B. Lippincott Co.; Cranial nerves,
p. 157, Philadelphia, Lond. and Montreal.
Hamilton, W. J., J. D. Boyd and H. W. Mossman
1959 Human Embryology (Prenatal Development of Form and Function). Third Ed.
W. Heffer and Sons Ltd., Cambridge.
Huber, E. 1930 Evolution of facial muculature and cutaneous field of trigeminus, Part 111.
Quart. Rev. Biol., 5: 389-437.
Hunt, C. C. 1954 Relation of function to diameter in afferent fibers of muscle nerves. J. Gen.
Physiol., 38: 117-131.
,Jacobs, M. S., and A. V. Jensen 1964 Gross
aspects of the brain and a fiber analysis of
cranial nerves i n the great whale. J. Comp.
Neur., 123: 55-72.
Karlsen, K. 1969 Fibre calibre spectra of
nerves to the masticatory muscles i n the cat.
Acta odont. scand., 27: 263-270.
Korneliussen, H. K. 1964 Fiber spectra of
spinal roots i n Cetacea (Balaenoptera physalus). J. Comp. Neur., 123: 325-334.
359
Kubota, K., and T. Masegi 1971 O n the spindle
distribution i n the snout musculature and fiber
composition of the facial nerve i n some insectivores (Mammalia). Acta Anat. Nippon. (Kaibo
Z . ) , 46: 31-32. (Japanese abstract).
1972 Muscle spindle distribution in
snout musculature of Japanese shrew-mole.
Anat. Rec., 172: 703-710.
Kubota, K., Y. Sato and J. Kubota 1956 A silver
impregnation method of peripheral nerves with
frozen sections. J. Jap. Stomatol. (Kokubyo
Zassi), 23: 167-274. (Japanese with English
abstract).
Murphy, T. R., and H. U. Cameron 1967 The
number and size of nerve fibers to the masticatory muscles of the horse. Archs. oral Biol.,
12: 1159-1165.
Pettersen, E., and K. Sadjadpour 1970 A
method for combined staining of myelin
sheaths and cell elements in the central
nervous system, from Anat. Inst. (Prof. J.
Jansen), Univ of Oslo, Norway. (Personal
communication).
Rexed, B., and P. 0. Therman 1948 Calibre
spectra of motor and sensory nerve fibers to
flexor and extensor muscles. J. Neurophysiol.,
11: 133-139.
Thilander, B. 1964 Fibre analysis of the lateral
pterygoid nerve. Acta odont. scand., 22:
157-163.
van Buskirk, C. 1945 The seventh nerve complex. J. Comp. Neur., 82: 303-333.
Wakeley, C. P. G., and F. H. Edgeworth 1933
A note on the afferent nerve supply of the
facial muscles. J. Anat., 67: 420-421.
PLATE 1
EXPLANATION OF FIGURES
Scale i n each figure is represented at 6 p.
360
4
Cross section of the facial nerve to the snout musculature of the
Japanese lesser shrew-mole. Myelin-sheath stain. x 1250.
5
Cross section of the facial nerve to the snout musculature of the
Japanese shrew-mole. Myelin-sheath stain. x 1250.
6
Cross section of the facial nerve to the snout musculature of the
shinto shrew. Myelin-sheath stain. X 1250.
FACIAL NERVES OF SHREW AND SHREW-MOLES
Kinziro Kubota and Toshiaki Masegi
PLATE 1
361
Abbreviations
A, m. zygomaticus major
B, m. levator labii superioris
C, m. levator alae nasi superioris
D. m. levator alae nasi inferioris
E, m. zygomaticus minor
fd, degenerated nerve fibers in muscle spindle
region
if, intrafusal muscle fibers
Mp, profundus portion of masseter muscle
Ms, superficial portion of masseter muscle
Nd, degenerated nerve to snout muscles on
operated (1eft)side
Ni, intact nerve to sonut muscles on nonoperated (right) side
ns, nerve fiber to intrafusal muscle fibers
nt, main intramuscular nerve trunk (intact)
Z, zygomatic arch
PLATE 2
EXPLANATION O F FIGURES
362
7a
Cross section of the snout muscles i n the Japanese shrew-mole on
the non-operating (right) side, showing intact innervation to the
muscles. Silver-impregnation method. x 60.
7b
Enlarged photomicrograph of a part marked in figure 7a to show
intact spindle innervation. x 300.
8a
Cross section of the muscles on the opposite, operating (left) side
i n the same section as that in figure 7a, showing complete degeneration of the nerve to the muscles. Two arrows also indicate muscle
spindles. Silver-impregnation method. x 300.
8b
Enlarged photomicrograph of a part marked in figure 8a to show the
details of the complete degeneration in muscle spindle innervation.
X 500.
FACIAL NERVES OF SHREW AND SHREW-MOLES
Kinziro Kubota and Toshiaki Masegi
PLATE 2
363
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