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THE ANATOMICAL RECORD 248:129–136 (1997)
Ultrastructural Changes in the Nerve Fiber Population of
Anastomosed Vagal and Spinal Accessory Nerves in the Sheep
1Laboratoire de Neurobiologie Fonctionnelle, UST Lille, Villeneuve d’Ascq Cedex, France
2Laboratoire de Physiologie de la Reproduction, C.N.R.S./I.N.R.A.,
Université Pierre et Marie Curie, Paris Cedex, France
3Department of Veterinary Physiology and Biochemistry, University College of Dublin,
Dublin, Ireland
Background: The ultrastructure of the vagal and spinal
accessory nerves was studied 1) in normal sheep and 2) in sheep in which
an experimental crossed-nerve anastomosis had been made by sectioning
the supranodose vagal and spinal accessory nerves, then suturing the
distal end of the vagal nerve to the distal end of the spinal accessory nerve,
and allowing time for regeneration to occur. This study was carried out in
order to analyze the modifications liable to occur when this technique is
used and to specify the origin and the nature of the fibers that colonize the
spinal accessory nerve.
Methods: The study was performed in 4- to 5-month-old sheep. After the
surgical procedure, the animals were housed indoors during 1 year until
their sacrifice by fixative perfusion. Then, nerve samples were dissected
out, processed for electron microscopy, examined, and systematically
photographed. After printing, the diameters of the nerve fibers were
Results: In sheep, the ratios of nonmyelinated to myelinated fibers
(NF/MF) in the infranodose and supranodose vagal nerve and accessory
spinal nerve were 1.21, 1.67, and 3.21, respectively. In both parts of the
vagal nerve, the myelinated fibers had a unimodal diameter distribution
around a peak of 4 mm; whereas, in the spinal accessory nerve, they were
distributed bimodally, and 53% had values of 15–18 mm. After making the
above anastomosis, the centrifugal vagal fibers degenerated, and the
NF/MF ratios increased in the centripetal infranodose vagal nerve, in the
reinnervating supranodose vagal nerve, and in the reinnervated spinal
accessory nerve (approximately 1.87, 1.72, and 6.04, respectively). In all of
these nerves, the myelinated fibers had a unimodal distribution with a
peak at 4 mm, as in the vagal nerve of normal sheep.
Conclusions: These results reveal the large part taken by the nonmyelinated fibers in the nerve fiber population of the vagal nerve and support the
vagal origin of the fibers reinnervating the spinal accessory nerve. Anat.
Rec. 248:129–136, 1997. r 1997 Wiley-Liss, Inc.
Key words: heterogeneous nerve anastomosis; vagal nerve; spinal accessory nerve; ultrastructure; nerve fiber populations
To study vagal receptor activity in conscious sheep,
Rousseau (1970, 1973) conceived and successfully developed a method of heterogeneous nerve anastomosis
between the peripheral stump of a cut supranodose
vagal nerve (SVN) and the peripheral stump of the
ipsilateral spinal accessory nerve (SAN). Allowing time
for nerve regeneration and muscle reinnervation enables centripetal vagal receptor activation to be reflected in activation of motor units of a superficial
skeletal muscle in the neck. With this technique (Fig.
1A,B), the peripheral stump of the SVN end, sectioned
as cranially as possible, is sutured to the peripheral
stump of the SAN, the SAN being the motor nerve of the
mastoidohumeral muscle in sheep. After an interval of
several months, there is partial reinnervation of this
denervated muscle by certain centripetal vagal axons.
Received January 9, 1995; accepted October 28, 1996.
*Correspondence to: Professor Pierre Delorme, Laboratoire de Neurobiologie Fonctionnelle, UST Lille, F.59655 Villeneuve d’Ascq Cedex,
Contract grant sponsor: M.E.N., and CNRS; Contract grant no: V.A. 308.
Fig. 1. Vagal and spinal accessory nerves located in the neck of the
sheep. Schematic illustrations of the normal anatomical structure (A),
the heterogeneous anastomosed nerve after 1 year (B), and the section
of the supranodose vagal nerve without anastomosis shown after 40
days (C). The numbers show the nerve samples taken. Their analyses
are reported in this order in Table 1. IVN, infranodose vagal nerve;
NG, nodose ganglion; SVN, supranodose vagal nerve; SAN, spinal
The term ‘‘centripetal vagal axons’’ is used to include
afferent axons that constitute the majority of centripetal axons as well as a small number of recurrent
contralateral vagal motor axons whose existence was
demonstrated by Dalal et al. (1988).
Electrophysiological studies have confirmed the functional reality of reinnervation (Coget and Rousseau,
1983; Falempin and Rousseau, 1983). Of the 26,000–
36,000 neurons located in the nodose ganglion, only one
afferent vagal axon out of every 600 is able to reestablish neuromuscular junctions (Rousseau and Falempin,
Before determining the ultrastructure of the vagal
fibers that reinnervate the SAN, fiber populations of
the SVN and the infranodose vagal nerve (IVN) were
analyzed. Previously, the vagal nerve of sheep has been
the object of light microscopic studies that were unable
to reveal the contribution of the nonmyelinated fraction. For this reason, we have analyzed first the normal
nerves (IVN, SVN, SAN; Fig. 1A) and, then, the anastomosed nerves [reinnervating centripetal IVN (RCIVN),
reinnervated SAN (RSAN); Fig. 1B] and the vagus
nerve after the degeneration of the efferent fibers
[centripetal IVN (CIVN); Fig. 1C].
accessory nerve; MHM, mastoidohumeral muscle; RCIVN, reinnervating centripetal infranodose vagal nerve; RSAN, reinnervated spinal
accessory nerve; CIVN, centripetal infranodose vagal nerve. Long
dashed line, vagal centripetal (motor) fibers; Dashed-and-dotted lines,
spinal accessory motor fibers; solid lines, vagal centrifugal (sensory)
fibers; short dashed line, degenerated fibers.
Nerve anastomoses (Fig. 1B) were performed on the
left side in 4- to 5-month-old sheep of the ‘‘Préalpes du
Sud’’ breed following the procedure described by Falempin and Rousseau (1983). After the surgical procedure,
the sheep were housed indoors, allowed free access to
water, and fed a diet of meadow hay ad libitum plus 300
g/day of pellets. One year after the anastomosis, the
reinnervation of the mastoidohumeral muscle was demonstrated in each sheep by recording the electrical
activity of reinnervated motor units, which was evoked
by stimulating the anastomosed vagal nerve in its
cervical. The three animals were killed immediately
afterward. The vagus nerve in its infranodose part up to
the suture site and to the peripheral SAN stump were
dissected. We checked that the suture site was entirely
disconnected from the surrounding tissues, namely,
from the proximal ends of both nerves, which could still
be easily located by the presence of clips.
To determine the population of the centripetal vagal
contingent, the left vagal nerve was sectioned above the
nodose ganglion (Fig. 1C) in a fourth sheep. This sheep
was 15 months old at the time of the vagal section and
Fig. 2. A demonstration of the extent to which the nervous tissue sections may be masked by the wires of
a support grid. A: Semithin section from a spinal nerve observed under light microscopy. B: The same
section as it appears when it is displayed on a grid.
was born in the same breeding and during the same
period as the three other sheep. It was killed 40 days
after the operation.
All experiments were carried out in compliance with
the principles of laboratory animal care and the French
laws on the protection of animals. In particular, operative techniques were performed under general anesthesia. An intravenous injection (200 mg of sodium pentobarbitone and 500 mg of sodium thiopentone dissolved
in 25 ml of physiological saline) induced a brief anesthesia, which allowed the insertion of an endotracheal
tube. Then, anesthesia was maintained by inhalation of
0.5–2.0% halothane in air.
The tissues of the neck and the head were fixed by
perfusion through the left common carotid artery of 4
liters of a glutaraldehyde (2.5%) paraformaldehyde
(0.5%) solution in 0.2 M sodium cacodylate buffer, pH
7.4. The nerves were dissected out, fixed for another 2
hours by immersion in the same fixative, and then cut
up to a size compatible with processing for electron
The fragments were washed with cacodylate buffer,
postfixed for 1 hour in 1% buffered osmium tetroxide,
then dehydrated in graded alcohols and propylene
oxide, and finally embedded in Epon 812. Semithin or
ultrathin sections were cut on a Reichert OM U3
Ultrotome. Semithin sections were stained with toluidine blue to allow location of the fiber bundles (Fig.
2A). Ultrathin sections collected on 75 mesh grids
coated with Formvar film were contrasted with uranyl
acetate and lead citrate and examined with a Siemens
Elmiskop 1A electron microscope.
The unavoidable presence of the grid wires (Fig. 2B)
masking areas of greater or lesser importance did not
allow the complete study of the nerves: Only the
bundles showing a sufficiently free area were analyzed.
The analysis was completed by observations of the
adjacent sections. Therefore, the choice of the analyzed
bundles was purely arbitrary. The visible parts of the
bundles were first carefully drawn and were then
systematically photographed at an initial magnification of 32,000, the photographs partly overlapping in
order to facilitate the reconstruction of the nerve section. After printing, the bundles were reconstructed,
and the diameters of the nonmyelinated fibers (NFs)
and the myelinated fibers (MFs) were determined,
taking into account the final magnification of 34,000.
Because the section of a fiber was rarely round, we
decided to determine its diameter by taking the average
of a long and short axis, including the myelin sheath, to
make our results more comparable with those obtained
from light microscopic observations (Tiao and Blakemore, 1976).
Nerve samples of the three sheep with nerve anastomosis were observed in the electron microscope, but, in
consideration of the vast amount of work, morphometric studies were only performed from IVN, SVN, SAN,
RCIVN, and RSAN samples of one of the sheep; the
samples from the other two sheep were used only for
qualitative observations. Morphometric studies were
also carried out from the CIVN sample of the fourth
sheep, including the supranodose section of the vagus
nerve, to compare its composition and distribution of
the centripetal fibers with those of the RCIVN sample
in the infranodose level.
Qualitative Aspects
The distribution of the nerve fibers in the normal IVN
or SVN (Fig. 3A) is not homogeneous. This heterogeneity is due not only to the differences between the fiber
diameters but also to the repartition of these various
fibers among the different nerve bundles and inside
each bundle. The relatively small diameter of most
fibers that compose this nerve results in a high-density
fiber population. On the contrary, in the normal SAN
(Figs. 2A, 3B), the distribution appears much more
homogeneous. Density of fibers is relatively low, as the
fibers of larger diameter are the most numerous. This
explains why, for nearly equivalent nerve areas analyzed, the fiber count was very different between samples of normal vagus nerve and normal SAN (Table 1).
Observation of the sectioned then anastomosed SAN
(Fig. 1B) reveals a very collagenous endoneurium divided into small fascicles by the long, thin processes of
endoneurial cells (Fig. 3D). Inside these thin-walled
muffs, small- and middle-diameter vagal fibers, both
MFs and NFs, alone or in groups of two or three,
colonize the peripheral stump of the SAN, which is now
emptied of its own axons. Similitude of observations in
the samples of the three sheep, including reinnervation
of vagal fibers into the SAN, led us to carry out the
morphometric studies on the same animal.
Quantitative Aspects
Normal vagal nerve
The normal vagal nerve was sampled central to the
nodose ganglion (i.e., SVN) and peripheral to the ganglion (i.e., infranodose ganglion; IVN). Analysis of the
IVN indicated that, of the 7,589 fibers measured, 3,443
were myelinated (i.e., 45% of the total; Table 1). The MF
diameter distribution was unimodal (Fig. 4A). This
fiber population was particularly concentrated between
2 µm and 7 µm. The NF distribution was also unimodal:
The diameters of the NF fibers ranged from 0.25 to 2
µm, with a peak close to 1.5 µm (Fig. 4A).
In the SVN (Fig. 4A), the proportion of MFs was
slightly lower than in the IVN, because these fibers
represented only 37% of the total population (3,720 of
9,935; Table 1). The diameter ranges over which both
fiber types were distributed were nearly the same as in
the infranodose part, although the MF peak was again
located at 4 µm, whereas the NF peak had shifted to
0.75 µm.
Sectioned SVN
The vagal nerves were sectioned central to the nodose
ganglion with and without creating an anastomosis. In
both cases, the centrifugal efferent fibers degenerated,
so that the peripheral stump sampled distal to the
nodose ganglion would contain only centripetal fibers.
In the CIVN (Fig. 4C), the MFs represented 35% of
the fiber population. It was slightly lower than the 37%
of the IVN population. Their distribution was always
unimodal, but the peak shifted to 3 µm. On the other
hand, the NF population displayed a greater range
(0.25–4.0 µm), and its peak was shifted toward slightly
greater diameters (1.5–1.75 µm).
In the RCIVN (Fig. 4B), the MF diameter distribution was like that in the IVN, but the most important
component of the MF population, although it was still
centered at 4 µm, fell from 32% to 24% of the total.
Moreover, the NF/MF proportion was increased from
1.2 to 1.72 (2,020 of 5,514 RCIVN fibers analyzed; Table
1). The NF distribution ranged from 0.25 to 2.5 µm, but
it did not have a well-defined peak.
Normal SAN
Analysis of the SAN demonstrated that the MF
component was smaller than the NF component (Fig.
5A): Indeed, it represented only one-fourth (24%) of the
fibers measured (Table 1). The total fiber population of
the SAN can be estimated as about 9,600, because
Falempin (1981) estimated the total number of MFs to
be about 2,300. The MF diameter spectrum was bimodal, with a lower peak (16% of the MFs) of 6–8 µm and a
higher peak (53% of the MFs) of 15–18 µm. The NFs
were distributed between 0.25 and 1.25 µm, with a peak
of 0.75 µm.
After anastomosing the distal stump of the sectioned
vagal nerve to the distal stump of the sectioned SAN,
the regenerating axons of the vagal centripetal neurons
invaded the empty endoneurial fascicles of the degenerated spinal accessory motor nerve fibers (RSAN; Fig.
5B). In the RSAN, the NF spectrum was a little
modified; its peak of 0.5 µm had slightly shifted compared with the NF peak in the normal SAN.
The MF spectrum had changed substantially. The
bimodal MF distribution in the normal SAN became
unimodal in the RSAN, with a peak at 4 µm. This peak
had the same location as that of the SVN, IVN, and
CIVN. Comparison of the MF sizes in the different
photomicrographs of Figure 3 illustrates this fact. The
modal MF percentage in the normal SAN (24%) is even
lower in the RSAN and corresponds to only 14% of the
total fiber population (Table 1).
The aim of this study was to analyze and to compare
the populations of MFs and NFs in the normal vagal
nerve and SAN with nerves in which a peripheral
vagoaccessory nerve anastomosis had been made (Fig.
1B) as a means of recording afferent vagal activity in
conscious sheep (Rousseau, 1973). The relatively heterogeneous distribution of the various nerve fibers in the
Fig. 3. Ultrastructural aspect of the myelinated (MFs) and nonmyelinated (NFs) nerve fibers in bundles from the normal vagal nerve
(A), the normal spinal accessory nerve (B), the reinnervating centripetal infranodose vagal nerve (C), and the reinnervated spinal accessory nerve (D). Sometimes, Schwann cells (S) are observed near nerve
fibers that are surrounded by abundant collagen (Co). The arrow in D
indicates the thin processes of the endoneurial cells that form the
small endoneurial fascicles. The MF diameters of the RSAN (D) are
like those of the SVN and RCIVN myelinated fibers (A,C). Scale bars 5
2 µm.
Fig. 3.
TABLE 1. Populations of nerve fibers in the various nerves studied
No. of
sample in
Figure 1
Analyzed nerves
Normal infranodose vagus nerve (IVN)
Normal supranodose vagus nerve (SVN)
Normal spinal accessory nerve (SAN)
Reinnervating centripetal IVN (RCIVN)
Reinnervated SAN (RSAN)
Centripetal infranodose vagus nerve (CIVN)
No. of
fibers (NF)
fibers (MF)
analyzed Total no. (TN) of
bundles measured fibers Number % of TN Number % of TN NF/MF
Fig. 4. Comparisons of the distributions (expressed as percentages of
the total fibers) of the myelinated (MFs) or nonmyelinated (NFs) nerve
fibers between the normal infranodose (IVN) and supranodose (SVN)
vagal nerves (A), between the IVN and the reinnervating centripetal
infranodose vagal nerve (RCIVN; B), between the IVN and the
centripetal infranodose vagus nerve (CIVN; C), and between the
RCIVN and the CIVN (D). Each pie chart indicates the number and
the percentage of the analyzed MFs and NFs for each nerve. The
numbers above the pie charts summarize the total number of fibers
analyzed in each nerve studied.
vagal nerves induced us to analyze more bundles in this
nerve than in the SAN, the fiber distribution of which
seemed more homogeneous. To obtain a reasonably true
fiber representation, all the workable bundles that
were not masked by the grid wires were photographed
and were then reconstituted before analysis.
bution of vagal MFs is not exceptional, because it is also
found in other species, such as the cat (Burgh-Daly et
al., 1953; Mei et al., 1980) and the ferret (Asala and Brower,
1966), whereas Bronson et al. (1978) have described an
MF bimodal distribution in the rat vagal nerve.
The originality of this study lies mostly in the fact
that the NF component in normal vagal nerves of sheep
was estimated. The NFs represent 55% of the fibers in
the infranodose part and represent 63% in the supranodose part (Table 1). These proportions are considerably
greater than the 10–30% of the NFs estimated in
thoracic vagal nerve by Habel (1956). The only previous
studies (Iggo, 1956; Dussardier, 1960) on vagal nerves
in sheep used light microscopy and led to an underestimation of the NF component of these nerves. However, this component in sheep is less important than
Composition of the Normal Vagus Nerve
Estimation of the total numbers
The MF distributions in the SVN and the IVN were
near enough to those that were described by Iggo (1956)
or Dussardier (1960) from light microscopy observations. These authors found that the great majority of
the MFs (about 80%) had diameters between 2 and 4
µm, and, in our study, a similar percentage pertained to
the fibers, with a peak of 4 µm. Such a unimodal distri-
Supranodose vs. infranodose
Fig. 5. Comparisons of the distributions of the myelinated (MFs) and
nonmyelinated (NFs) nerve fibers between the normal spinal accessory nerve (SAN) and the reinnervated spinal accessory nerve (RSAN;
A) and between the RSAN and the reinnervating centripetal infranodose vagal nerve (RCIVN; B). For details, see the legend to Figure 4.
that observed by electron microscopy in the cat vagal
nerves, where it represents 68–85% of the infranodose
fibers and 86–90% of the supranodose fibers (Mei et al.,
1980). The relative wealth of MFs in the vagal nerves of
sheep could be accounted for by the large innervation of
the complex stomach of ruminants, the sequential
motility of which is triggered once every 45 seconds by
the medullary gastric centers through the vagal nerves.
From our observations, the total number of fibers in
the cervical vagal nerve could be determined only
approximately. The number of bundles that we have
analyzed corresponded to about one-sixth of the whole
area of the IVN section. Therefore, we can estimate the
total nerve fiber population of the IVN to be about
45,000 fibers. Dussardier (1960) estimated that there
were 10,000–12,000 MFs present in each dorsal thoracic vagal nerve and 8,000–10,000 in the common
ventral thoracic vagal trunk. Taking into account the
45% of MFs that we found in the IVN and the observation that the IVN contains the fibers from one of the
dorsal thoracic vagal nerves and one-half of those from
the ventral thoracic common vagal trunk, we can
calculate from Dussardier’s results the total population
of the IVN to be 31,000–38,000 fibers. Consequently,
the results of Dussardier (1960) represent an underestimation, probably because of the difficulty in counting the NFs by light microscopy.
The different composition of the SVN and the IVN
must be emphasized. The SVN contains more NFs than
the IVN, the NF/MF ratio being 1.67 against 1.2 (Table
1). The difference between these two levels is plainly
less marked than in the cat, in which the NF/MF ratios
are 7 to 9 and 4 to 6 for the supranodose and infranodose parts of the vagal nerves, respectively (Mei et al.,
1980). This comparison confirms the more important
myelinization of cervical vagal nerve fibers in sheep.
Similar to cat vagal nerves, the unimodal distribution
of the NFs presents different maxima when we consider
the whole SVN (0.75 µm) on the one hand and the whole
IVN or its centripetal contingent (1.25–1.5 µm) on the
other hand.
In the infranodose region, the CIVN remaining after
supranodose nerve section and the degeneration of the
centrifugal (motor) fibers contains relatively fewer MFs
than the normal IVN (35% vs. 45%). The presence of the
centripetal fibers in the normal IVN, therefore, is
responsible for the higher percentage of MFs, suggesting that efferent vagal fibers are proportionally more
myelinated than afferent vagal fibers. If the 16,613
centripetal fibers (Table 1) that we counted in the CIVN
represented about two-thirds of the area of this nerve,
then we can estimate the infranodose afferent component to be 25,000 fibers, i.e., about 55% of the estimated
total IVN population of 45,000 fibers. Taking into
account the whole population, if 45% of all fibers are
MFs and 35% of all centripetal fibers are myelinated,
then the calculation shows 60% of the infranodose
efferent component to be NFs, i.e., 27% of the total
population in which there are 45% efferent fibers.
These estimations are in line with those given by
Prechtl and Powley (1990) for the rat. Those authors
consider that the efferent fiber component of the vagal
nerves is more important than it has been proposed
previously, namely, 10% (Agostini et al., 1957; Evans
and Murray, 1954; Kemp, 1973). Compared with the
afferent MF spectrum of the CIVN, the IVN MF spectrum is shifted to the right (Fig. 4C), suggesting that
the myelinated centrifugal fibers generally have a
greater diameter that the centripetal fibers.
Reinnervation of the SAN
The new population, which consists principally of
small-diameter MFs, differs markedly from the population of the normal SAN (compare Fig. 3D with Fig. 3B)
and rather resembles the population observed in the
normal vagus nerve (Fig. 3A) or in the reinnervating
IVN (Fig. 3C). The relative similarity of the fiber
distribution (Fig. 4D) and of the MF percentages, 35%
and 37%, respectively (Table 1), in the CIVN and in
the RCIVN, is not surprising, because, in both cases,
the nerves are deprived of their efferent component.
The MF component changes from being bimodal in the
intact SAN to becoming unimodal in the RSAN. Distributed around a peak at 4 µm, the spectrum of their
diameters is identical to that observed in the RCIVN.
On the other hand, the NF diameter is smaller in the
RSAN than in the RCIVN (Fig. 5B). In other respects,
they are plainly more numerous, because, in the RSAN,
the NF/MF ratio is 3.5 times greater than in the
RCIVN. This situation could be due to the fact that, in
the RSAN, many axons from vagal sensory neurons,
which colonize the endoneurial fascicles of the recipient
nerve, are in the process of maturation and have not yet
reached their final size.
It is possible to compare the diameter spectrum of the
RCIVN fibers with the distribution of the conduction
velocities measured between two points of stimulation
on this nerve (Falempin and Rousseau, 1983). In sheep,
the maximum of the evoked responses (44%) is obtained
by the stimulation of fibers with conduction velocities of
6–12 meters/second corresponding to fiber diameters of
about 1–2 µm. Eighteen percent of the responses are
evoked by stimulation of fibers of diameters less than 1
µm, and 25% are evoked by stimulation of fibers of 2-4
µm in diameter. In other words, the diameter spectrum,
which is deduced from the distribution of conduction
velocities, is shifted to the left compared with those
established by direct histological observation. This
means that, among the vagal centripetal fibers running
below the nodose ganglion, about 62% of those that had
reinnervated the neck muscle are either slightly myelinated or nonmyelinated, with diameters equal or less
than 2 µm. They would correspond to the peripheral
processes of sensory neurons, because retrograde labeling of nerve cells was evidenced in the ipsilateral
nodose ganglion following successful reinnervations
(Falempin and Rousseau, 1983). They could also be
centrally directed recurrent collateral branches of preganglionic efferent gastric fibers from the contralateral
vagus nerve, as suggested by subsequent results (Dalal
et al., 1988).
The authors thank Yolande Dodey and Sophie Duclos
for their secretarial help and Claudine Guichard for her
photographic assistance. This research was supported
by grants from M.E.N. and from C.N.R.S. (U.A. 308).
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