Download autonomic accessory ganglia in nerves reaching organs of the

Bull Vet Inst Pulawy 50, 183-188, 2006
AUTONOMIC ACCESSORY GANGLIA IN NERVES REACHING
ORGANS OF THE UROGENITAL SYSTEM IN THE EWE
ZBIGNIEW BORATYŃSKI, AGNIESZKA PEDRYCZ1
AND IZABELA KRAKOWSKA
Department of Animal Anatomy and Histology,
Agricultural University, 20-934 Lublin, Poland
e-mail:[email protected]
1
Department of Histology and Embryology with Laboratory of Experimental Cytology,
Medical University of Lublin, 20-080 Lublin, Poland
Received for publication February 02, 2006.
Abstract
In sheep, nerve cell concentrations were found in
nerves reaching organs of the urogenital system, which were
called autonomic accessory ganglia (AAG) due to the region
they occurred. Location of AAG in the studied nerves and their
branches is changeable and their shape and size depend on the
amount of ganglion cells from which AAG are made. The
structure of AAG was described, as well as the appearance of
nerve cells being part of it. Moreover, it was found that most
of AAG in the studied nerves or their branches could only be
confirmed by microscopic examination. The results were
compared with those obtained in earlier studies of other
authors and probable functions and role of AAG in the
autonomic peripheral nervous system were discussed.
Key words: ewe, autonomic
autonomic nerves, urogenital organs.
ganglia,
A conclusion can be drawn from earlier
experimental studies that the system of peripheral
autonomic ganglia is not only the area of passing or
switching (synapting) from the preganglionic nerve
fibres coming from the central nervous system, but also
the main outlet of nerve fibres supplying the internal
organs (9, 10-13, 30). It was also found that nerve fibres
came from different outlets supplying the internal organs
or their parts, which is an example of complex
connections between the autonomic peripheral nervous
system and these organs. Moreover, autonomic
peripheral ganglia play a certain role in the pathogenesis
of some nosologic units, such as achalasia (19) or
megacolon (29).
On the basis of literature review it is implicit
that in the complex of the autonomic peripheral ganglia
innervating the internal organs, apart from the main
ganglia of the abdominal and pelvic cavities well known
and described (14, 15, 21, 24, 26, 31, 32, 34), also these
ganglia should be included which were by chance found
to exist in the course of visceral branches joining the
sympathetic trunk with the main ganglion and plexuses
of the abdominal and pelvic cavities, and the ganglia
found in the nerves joining the main autonomic
peripheral ganglia with the walls of individual internal
organs (1, 9-11, 13, 32). These ganglia are of interest
because of their probable functions and significance in
the peripheral autonomic nervous system. The
mentioned ganglia were termed by some authors the
accessory ganglia and by others the intermediate
ganglia. Up to the present, no paper has been
encountered which would deal with the problem of
autonomic accessory ganglia (AAG) in an overall way.
There is a lack of exact data about their location and
functions both in the humans and domestic animals. The
purpose of these studies is to determine the location and
morphology of the AAG in the nerves reaching the
urogenital organs in the sheep.
Material and Methods
Six sexually mature ewes at the age of 3-5
years were used in the studies. After slaughter the
following material was taken for the examination of
individual trunks and nerve branches:
1. Nerves running from the coeliac ganglion and
plexus to the hilus of the kidney;
2. Nerves running from the intermesenteric plexus
to the hilus of the kidney;
3. Nerves branching out of the sympathetic trunk
to the hilus of the kidney;
4. Nerve branches from the sympathetic trunk to
the caudal mesenteric ganglion and hypogastric
plexus;
5. Nerve branches from the caudal mesenteric
ganglion to the ovarian plexus;
6. Hypogastric nerves and their main branches in
the hypogastric plexus;
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7.
Pelvic nerves and their main branches in the
pelvic plexus.
The material was fixed in the 4% solution of
neutral formalin, dehydrated in ethyl alcohol, and
embedded in paraffin. Paraffin blocks were cut into
15µm sections and stained with methylene blue
according to the Nissl, Klüver-Barrera and AlzheimerMann methods.
Results
It was found that in the course of nerves and
their branches running to the urogenital organs of sheep
there were concentrations of nerve cells forming ganglia
which, due to the area of their occurrence and to
differentiate them from the main autonomic ganglia of
the abdominal and pelvic cavities, were termed the
AAG.
There were concentrations of ganglion cells in
the course of nerve branches reaching the hilus of the
kidneys from the coeliac ganglion and plexus. In the
longitudinal sections the nerve cells were situated one
after another, as usual, parallel to the course of nerve
fibres. The ganglion cells, arranged in such a way,
occurred either in the marginal part of the nerve fibre
bundle or inside it. The number of nerve cells forming
AAG in these branches was various, from several to
several hundred. Also the number of ganglion cells
occurring in the studied ganglia affected their shape.
When the cells were few, they were usually situated one
after another and the distance between them was small.
When the cells were numerous they were close one to
another and whole ganglion had a shape of elongated
spindle. Nerves running from the intermesenteric plexus
to the hilus of the kidney did not always occur. They
were found in 5 sheep. In these nerves ganglion cells
were also found to exist. The way the ganglia were
arranged in individual nerves was fairly characteristic.
In each of them one to three small ganglia were
observed and in their transverse sections from several to
several dozen nerve cells were visible (Fig.1).
Nerve branches running from the sympathetic
trunk to the hilus of the kidneys most often came from
the ganglia located on the level of the first and second
lumbar vertebrae (L1 and L2). The picture of AAG in
these nerve branches was basically the same as the
picture of the ganglia described in previous nerves. The
location of AAG in the mentioned branches was
changeable. Part of them occurred not far from the
sympathetic trunk, others were found in the medial part
of nerve branches, and in the remaining cases they were
localized close to the kidneys.
The nerves connecting the sympathetic trunk
with the caudal mesenteric ganglion came from the
ganglia of the sympathetic trunk on the level of
neuromers L3, L4 and L5, but in three cases (in two sheep
on the left side and in one sheep on the right side) the
nerve from ganglion L5 of the sympathetic trunk was
connected with the hypogastric plexus. In all the
examined animals the best shaped were the nerves
connecting the caudal mesenteric ganglion with the
ganglia of the sympathetic trunk situated at the level of
the 4th lumbar neuromer. In two sheep the nerve coming
from ganglion L3 was connected with the nerve coming
from ganglion L4 of the sympathetic trunk before
reaching the caudal mesenteric ganglion. In one sheep
the nerve coming from ganglion L3 of the sympathetic
trunk ran directly to the area of the ovarian artery and
further on to the ovarian plexus. AAG occurred often in
the mentioned nerves (Fig. 2).
A great many nerve cells grouped in ganglia of
different sizes were particularly observed in the nerves
coming from ganglion L4 of the sympathetic trunk. In
the nerve branch coming directly from ganglion L3 of the
sympathetic trunk to the ovarian plexus, a ganglion was
found which was 1.5 mm long and was situated only in
one of the nerve fibre bundles forming the mentioned
branch. In the area of the ovarian plexus, sometimes
little small ganglia were observed which had from 10 to
30 nerve cells and were situated at the external area of
small blood vessels. Hypogastric nerves, coming from
the caudal mesenteric ganglion did not occur as
individual nerve trunks but as 3 - 5 nerve branches
which after a short course passed into the hypogastric
plexus. Sometimes, one or two of these branches ran
through the hypogastric plexus and were divided into
thin branches in the area of the final part of the ureters
or in a short distance from the urinary bladder. In all the
animals small ganglia were found in the hypogastric
nerves. The shape of AAG in the longitudinal sections
was usually spindle-like, but in the transverse sections
the cells forming the ganglia were scattered all over the
sections area of one bundle of nerve fibres. Moreover,
almost all along the hypogastric nerves individual
ganglion cells were encountered. They were situated
most often in central part of the bundle of nerve fibres
(Figs 3, 4, 5).
Pelvic nerves occurred as individual fairly thin
nerve trunks coming from the ventral roots of the sacral
nerves at the level of S2 to S4. After a short course as
separate nerves, they reached the pelvic plexus and just
there were divided into a number of nerve branches. In
the course of pelvic nerves, the beginning from to the
area of their division, no ganglion cells were observed,
but their presence was found in the course of the main
nerve branches being part of the hypogastric and pelvic
plexuses. In the nerve branches of both plexuses the
AAG occurred as concentrations of several to several
hundred ganglion cells, or these cells occurred
individually in the course of nerve fibres (Figs 6, 7). The
size and shape of AAG depended on the number of the
ganglionic neurons being part of them. Small ganglia
containing from several to several dozen cells arranged
one after another along the course of nerve fibres were
separated from the fibres with a thin layer of glial cells
which were knitted closely together. Larger AAG were
usually of elongated spindle shape and sometimes they
were oval. These ganglia, occurring both in individual
nerves and nerve plexuses were surrounded with a thin,
connective tissue capsule. Lack of the ganglion capsule
was found only in the areas of the inlet and outlet of the
nerve fibres. It was also found that not all the nerve
fibres being part of the ganglia spread in them and ended
their course there.
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Fig. 1. Autonomic accessory ganglion (AAG) in the nerve branch connecting the coeliac ganglion with the hilus of the
left kidney. Stained with methylene blue (according to Nissl’s method). About 70x.
Fig. 2. Autonomic accessory ganglion in the nerve connecting the sympathetic trunk with the caudal mesenteric
ganglion. Stained with methylene blue (according to Nissl’s method). About 70x.
Fig. 3. Transverse section of the nerve branch connecting sympathetic trunk with ovarian plexus. AAG is visible in one
of the nerve bundles. Stained according to Klüver-Barrera’s method. About 80x.
Fig. 4. Small AAG (white arrow) situated in the area of the ovarian plexus in the direct vicinity of the blood vessel
(black arrows). Stained according to Klüver-Barrera’s method. About 80x.
Fig. 5. Ganglion cells in the hypogastric nerve. Stained with methylene blue (according to Nissl’s method). About 70x.
Figs 6, 7. Individual ganglionic neuron (6) and small AAG (7) in the nerve branches of the pelvic plexus. Stained
according to Klüver-Barrera’s method. About 70x.
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Fig. 8. Longitudinal section of AAG. Arrows show a bundle of nerve fibres running through the ganglion inside its
capsule. Stained according to Alzheimer-Mann method. About 60x.
Fig. 9. Transverse section of AAG. The shape (outline) of the nerve fibres bundle of different diameter running inside
the ganglion was marked with white dashed line. Stained according to Alzheimer-Mann method. About 260x.
Figs 10, 11. Nerve cells forming AAG. One, two (10) or three (11) nucleoli are visible in the cell nucleus. Stained with
methylene blue (according to Nissl’s method). About 420x.
Part of the fibres, after entering the ganglion, came
towards the internal area of the ganglion capsule, and
then they left the ganglion running further in the
peripheral direction (Fig.8). Bundles of nerve fibres
inside the ganglia were also observed in the transverse
sections and nerve fibres of different diameter were
found to be part of them (Fig.9).
Nerve cells forming AAG were most often of
oval shape, round cells were fewer, but individual
neurons localized in the course of nerve fibres had
usually the shape of elongated oval. The size of ganglion
cells ranged from 20 to 50µm. In the ganglion cells there
was a round cell nucleus visible with nucleolus in the
central position, and in neuroplasma granular tigroid
was found (Fig.10). Fairly often the cells were observed
whose nucleus had two nucleoli (Fig.10). There were
three nucleoli in the area of pelvic plexus in the cell
nucleus of some ganglionic neurons (Fig.11). Such
nerve cells were noticed very rarely, however.
Observations made in all the sheep allowed, to
state that there are no basic differences in the
distribution and size of AAG in the nerves reaching the
urogenital organs within the whole group studied.
Discussion
The results presented above make it possible to
state, that in the course of nerve fibres running to the
urogenital organs in the ewe, besides the main
autonomic ganglions of the abdominal and pelvic
cavities, also numerous AAG are engaged, which are
localized in the nerves and their branches reaching the
mentioned organs.
Presence of the AAG was found in the course
of nerves running both from the sympathetic trunk and
from the coeliac ganglion and plexus, and from
intermesenteric plexus to the hilus of the kidneys. The
results are in agreement with the earlier studies carried
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out in the man, ape, cat, and dog (20, 27, 28, 31), which
confirm the presence of small autonomic ganglia in the
mentioned nerves. The present studies also confirm
other investigations (20, 27, 28) which say that AAG are
possible to be detected only with the help of microscopic
examinations. The contradictory observations were
made by Grottel (16) who while describing innervation
of the adrenal gland in the cat, dog, and rabbit, often
encountered ganglia macroscopically visible, located in
the course of nerve branches running from ganglia L1
and L2 of the sympathetic trunk and reaching the renal
plexus. In the examined sheep, in the remaining visceral
nerves running from the posterior part of the lumbar
sympathetic trunk mainly to the caudal mesenteric
ganglion, also the presence of AAG of different sizes
was found. Similar ganglia were found in the nerve
branches in sheep (9, 10, 11) and in the cow (12, 13).
Similar results were obtained in the man, ape, sheep, cat,
and dog (24, 31, 34). According to these studies, it is
possible that the nerve cells of AAG localized in the
mentioned nerve branches are the source of
postganglionic fibres for the autonomic nerve structures
(ganglia and plexuses), with which the branches are
connected. Presence of ganglionic neurons was found in
the hypogastric nerves. The ganglia and individual nerve
cells in these nerves were also observed by other authors
(4, 26). AAG present in the hypogastric nerves should
be included in all the nerve cells occurring in the
hypogastric plexus.
Recently, more attention is paid to the
integration of sympathetic and parasympathetic
innervation at the level of the peripheral ganglia in
relation to some internal organs (8). Elbadawi and
Schenk (5, 6) brought anatomical evidence proving the
existence of such an integration. These authors showed
that in the vinicity of some organs or their walls the so–
called mixed ganglia occurred, in which adrenergic and
cholinergic neurons occurred one beside another, and
also, they observed the occurrence of individual nervous
cells of both kinds outside the ganglia – in the bundles
of nerve fibres. Moreover, they found the presence of
adrenergic structures around the cholinergic neurons. In
the small autonomic ganglia belonging to the
hypogastric plexus situated near the urinary bladder –
sympathetic postganglionic synapses occur modulating
the activity of “short adrenergic neurons” which act on
the cells of smooth muscles of the urinary bladder (7).
Also the ureters are innervated by the hypogastric
plexus. Ogata et al. (23) found numerous little
autonomic ganglia in the vinicity of the 2/3 anterior part
of the ureters, which probably are responsible for the
“peristalsis” of the ureters. Despite numerous studies,
the integration of the autonomic innervation at the level
of peripheral AAG is poorly known.
Some authors (19, 29) point to a direct
connection of AAG and ganglia in the intramural
plexuses with the organs innervated by them. They
found degenerative lesions in the ganglion cells of the
intramurial plexuses in the case of achalasia of the
cardia (19) and in the AAG neurons localized in the
nerve branches from the lumbar part of the sympathetic
trunk to the caudal mesenteric ganglion in the case of
megacolon (29).
The structure of AAG does not differ basically
from the descriptions presented by other authors (25). In
all the sheep the occurrence of ganglionic neurons of
two nucleoli was noticed fairly often. Similar ganglionic
neurons were observed by others (3, 24). Intermediate
ganglia, described by many authors should also be
mentioned (2, 17, 27, 33). They occur in the white and
gray communicating branches. Gruss (17) thought that
these ganglia could be the remnants of the secondary
sympathetic trunk, Alexander et al. (2) and Wrete (33)
presented opinion, that these ganglia originated from the
neuroblasts which, in the embryonal growth, did not
manage to reach the basic ganglion of the sympathetic
trunk. Both authors seem to believe that intermediate
ganglia passing the postganglionic sympathetic fibres to
the spinal nerve omitting the sympathetic trunk cause
lack of efficiency of sympathectomy used
experimentally and sometimes in clinical conditions as
well.
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