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Prolonged individuality of the accessory contribution to the vagusA peculiarity of the pig.

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Prolonged Individuality of the Accessory Contribution
to the Vagus: A peculiarity of the pig
A. H. SAFANIE
Department o f Biological Structure, College of Veterinary Medicine,
University of Illinois, Urbana, Illinois
The bulbar and spinal components of the accessory nerve of the pig
are thoroughly integrated i n a common trunk at the jugular foramen. The fibers of
bulbar origin separate from this trunk to form the internal ramus. The latter is
especially demonstrable in the pig, since it is independent over a considerable distance
i n the upper part of the neck before joining the vagus. As f a r distally as the origin
of the recurrent laryngeal nerve, the efferent fibers contributed to the vagus by the
accessory nerve remain histologically separate from the afferent fibers belonging
properly to the vagus. Parasympathetic, branchiomotor and afferent fibers can be
distinguished in the vagal trunk without the necessity of inducing selective degeneration by supranodose vagotomy.
ABSTRACT
The accessory nerve, as customarily de- ('14), "No such thing as the internal
scribed in mammals, originates by the branch of the accessory exists in the dog."
union of bulbar and spinal roots and di- Similar observations have been made in
vides almost immediately into internal and other mammals (Kiss, '32; DuBois and
external rami. The internal ramus is con- Foley, '36; Holzmann and Dogiel, 'lo), intributed to the vagus, and constitutes a cluding man (van Gehuchten and Molhant,
major portion, if not the entire, efferent '12).
In the pig, the distance between the
component of that nerve, distal to the origin of its pharyngeal branch (House and brain stem and the nodose ganglion is
Pansky, '60). This terminology has often disproportionately long. The internal rabeen criticized on the grounds that the in- mus of the accessory nerve (actually the
ternal and external rami actually represent motor root of the vagus) is atypically long
unaltered continuations of the bulbar and and distinct, being anatomically separate
spinal roots, respectively (Holl, 1878; from the vagus as far distad as the caudal
Lesbrb: and Maignon, '07; Chase and Ran- pole of the ganglion (Lesbrt5 and Maignon,
son, '14; Kiss, '32; DuBois and Foley, '36; '07; Kiss, '32; Holzmann and Dogiel, '10;
Both et al., '37). Thus, there are two sep- Dogiel and Archangelsky, '06). The present
arate fiber populations, originating from study was undertaken to determine
the medulla and the spinal cord, whose whether this segregation of afferent and
only basis for being Considered together is efferent components might be histologia transitory union at the jugular foramen. cally discernible at lower levels of the
According to Holl (1878), Willis' original vagal trunk. With a view to subsequent
description of the accessory nerve included quantitative studies, right and left vagi of
only that portion which originates by the more than 50 randomly selected pigs were
coalescence of spinal rootlets and termin- examined for evidence of component segates as the external ramus. The bulbar regation in closely spaced transverse secrootlets and internal ramus, originally de- tions. Some were prepared by the Wolters
scribed as part of the vagus, were mis- method (Quilliam, '56) and others by routakenly identified with the accessory nerve tine histological procedures.
through misinterpretation of Willis' paper
OBSERVATIONS
by Scarpa and others of his day.
Throughout
its course in the neck and
The internal ramus usually loses its
identity almost immediately through inte- upper thorax, the vagal trunk was regugration of its fibers with those of the vagus. larly subdivided into two contrasting zones
Thus, as emphasized by Chase and Ranson (fig. l a ) whose architecture conformed
ANAT. Rec., 159: 1 4 .
1
2
A . 11. SAFANIE
closely with descriptions of segregated afferent and efferent fiber populations observed intracranially in other species
(Chase and Ranson, '14; Botiir et al., '37;
Heinbecker and O'Leary, ' 3 3 ) . The afferent bundles were traced proximally into
the nodose ganglion, the efferents to the
accessory nerve. The latter did not enter
the ganglion but were loosely adherent to
its lateral surface. Rostra1 to the ganglion,
the two groups of fasciculi were grossly
separate.
As shown in figure l b , the bundles contributed by the accessory nerve consisted
of closely packed myelinated fibers of two
distinct sizes. The larger ones (8-12 11)
peeled off en masse in the recurrent laryngeal nerve and were traced to the laryngeal
muscles. The more numerous, small fibers
(2-4 11) were accordingly identified as
parasympathetic. The afferent bundles
(fig. l c ) contained iiiyclinated fibers in a
continuous range of thicknesses, some as
large as 10 11; but the smallest ones predominated. Between them, in myelinstained sections, were relatively wide intervals of unstained tissue, in which could
be seen the indistinct outlines of numerous
unmyelinated fibers.
A t the jugular foramen, the bulbar and
spinal components of the accessory nerve
Fig. 1 Vagus of pig as seen histologically at
cervical and upper thoracic levels, Wolters myelin
stain. a: efferent (left) and afferent (right)
sectors are apposed along an oblique line ( X 29).
b: efferent, and c, afferent fiber populations
( x 333).
were thoroughly integrated in a common
trunk, which contradicts the view that the
two groups of fibers are related merely by
loose intrathecal approximation (Holl,
1878; Chase and Itanson, '14; DuBois and
Foley, '36). In figure 2, just proximal to the
parting of the internal and external rami,
the original segregation of bulbar and
spinal fibers has been almost reestablished,
but a degree of interchange between the
two regrouping populations is still visible.
The fibers of spinal origin, now constituting the external ramus, are uniformly
large. In the internal ramus can be seen
large and small fibers of bulbar origin,
representing branchiornotor and parasympathetic components, destined for distribution in branches of the vagal trunk. As
the intracranial trunk of the accessory
nerve is independent of the vagus, it is
probable that the only efferent fibers actually contained in the vagus at this level
are those of its pharyngeal ramus.
I~ISCUSSIOIK
Segregation o l afferent and efferent vagal components in other mammals is apparently limited to the sorting of large,
branchiomotor fibers into a peripheral zone
of the lower cervical vagus, preparatory to
their detachment in the recurrent laryngeal nerve (Chase and Ranson, '14; Botjr
et al., '37; IIeinbecker and O'Leary, '33;
Foley and DuBois, '37; Evans and Murray,
'34; Agostoni et al., ' 5 7 ) . Insofar as I
have been able to determine, no species
has been described previously in which the
Fig. 2 Accessory nerve dividing to form external (left) and internal (right) rami. Fibers of
spinal (left) and bulbar (right) origin are intermixed at center. Hulbar component, now constituting the internal ramus, continues as the
efferent component of the vagus. Wolters myelin
stain ( x 92).
ACCESSORY CONTRIBUTION T O VAGUS O F PIG
accessory contribution of branchiomotor
and parasympathetic fibers remains histologically distinct throughout the extent
of the cervical and upper thoracic vagus.
Previous quantitative studies of vagal components in other mammals have largely
depended upon subtracting the number of
fibers which survive supranodose vagotomy
from the number normally present in the
vagus (DuBois and Foley, ’36; Foley and
DuBois, ’37; Evans and Murray, ’54; Agostoni et al., ’57). Because thc afferent and
efferent components of the vagus of the pig
arc histologically separate, their individual
fiber populations can be analyzed and
compared quantitatively in the same nerve
trunk, without the necessity of inducing
selective degeneration by vagotomy.
LITERATURE CITED
Agostoni, E., J. E. Chinnock, M. DeB. Daly and
J. G. Murray 1957 Functional and histological studies of the vagus nerve and its branches
to the heart, lungs and abdominal viscera in
the cat. J. Physiol., 135: 182-205.
BotPr, J., G. Popjak and A. Bense 1937 Die
Fasern des Ncrvus vaguacessorius beim Menschen und bei Saugetieren. Cluj Transylv., Acta
Mcd. Szeged., 8 (fasc. 2 ) : 93-229.
Chase, M. R., and S. W. Ranson 1914 The
structure of the roots, trunk and branches of
the vagus nerve. J. Comp. Neur., 24: 31-60.
Dogiel, J., and K. Archangclsky
1906 Der
Bewegungshemmcnde und der motorische
3
Nevenappatat des Herzens. Arch. ges. Physiol.,
113: 1-96.
DuBois, F. S., and J. 0. Foley 1936 Expcrimental studies on the vagus and spinal accessory
nerves in the oat. Anat. Rcc., 64: 285-307.
Evans, D. H. L., and J. G. Murray 1954 Histological arid functional studies on the fiber
composition of the vagus nerve of the rabbit.
J. Anat., 88: 32G337.
Foley, J. O., and F. S . DuBois 1937 Quantitative studies of the vagus nerve in the cat. I.
The ratio of sensory to motor fibres. J. Comp.
Neur., 67: 49-64.
van Gehuchten, A., and M. Molhant 1912 Contribution a l’ctude anatomique de nerf pneumcgastrique chcz l’homme. Le Nevraxe, 13: 55-97.
Heinbecker, P., and J. OLeary 1933 The mammalian vagus nerve. A functional and histological study. Am. J. Physiol., 106: 623-646.
Holl, &‘I
1878
.
Uebcr den Nervus Accessorius
Willisii. Arch. f . Anat. u. Physiol, Anat. Abt.,
pp. 491-517.
Holzmann, K., and J. Dogicl 1910 Uber die
Lage und den Bau des Ganglion nodosum n.
vagi hi einigen Saugetieren. Arch. f. Anat. u.
Physiol., Anat. Abt., pp. 33-43.
House, E. L., and B. Pansky 1960 A functional
approach to neuronanatomy. Elakiston, New
York.
Kiss, F. 1932 Das Verhaltnis zwischen Vagus
und Sympatheticus. Cluj Transylv., Acta Med.
Szcged., 6: 129-150.
Lesbre, F. X., and F. M’aignon 1907 Sur la
part qui revient la branche anastomotique du
spinal dans les proprietes physiologiques du
pneumogastrique ou pneumospinal. J. de M6d.
Vet. et de Zootech., pp, 212-227.
Quilliam, T. A. 1956 Some characteristics of
myelinated fibre populations. J. Anat., 90: 172187.
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