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Trophic effect of the sympathetic nervous system on the early development of the rat parotid glandA quantitative ultrastructural study.

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THE ANATOMICAL RECORD 201545-654 (1981)
Trophic Effect of the Sympathetic Nervous System on the
Early Development of the Rat Parotid Gland: A Quantitative
Ultrastructural St udy
Departments o f Anatomy, Histology, Medicine and Otolaryngology,
Uniuersity of Umea, and the National Defence Research Institute, Dept. 4,
Umea, Sweàen
Rats were sympathetically denervated on one side by avulsion of
the superior cervical ganglion either immediately after birth (within 4 hr) or when
the salivary glands were fully developed. Nine weeks after ganglionectomy the
parotid glands were subjected to microscopical studies. As shown by the lack of
specific fluorescence, sympathetic denervation caused an almost total depletion of
catecholamines in the acini. This was further substantiated at the electron microscopic level using KMn04 as fixative. No alterations in either gland weight or in
acinar cell size were noticeable after adult sympathectomy. On the other hand,
neonatal denervation caused a decrease in gland weight as well as acinar cell hypotrophy. The mem volume of individuai acinar cells was reduced by roughiy 25%
and the granule volume density by about 50%. Also the mean volume of individual
granules was decreased. These findings indicate an important role for the sympathetic nerve system in the maturation of the rat parotid gland.
Salivary glands are supplied with both parasympathetic and sympathetic nerves and
gland function depends on the integrity of the
two nerve systems. The parasympathetic division seems to be of importance for certain
gland functions such as secretion of electrolytes and enzymes, and for maintaining gland
structure under physiologic conditions (e.g.,
Schneyer and Hail, 1967, 1976; Emmelin,
1967). In the rat parotid gland adrenergic
nerves are intimately associated with the acinar cells (Norberg and Olson, 1965; Bloom et
al., 1977). Activation of the adrenergic
P,-adrenoceptor gives rise to a pronounced
amylase secretion in vitro (Butcher et al., 1975;
Carlsöö et al., 1978, 1981) whereas &adrenoceptors or cholinergic receptors appear to play
a minor role in this respect (e.g., Bdolah et al.,
1964; Bloom et al., 1979).
Long-term superstimulation of rodent salivary glands with the 0-adrenoceptor agonist
isoprenaline or prolonged electrical stimulation of the superior cervical ganglion induces a
tremendous enlargement of the glands (BrownGrant, 1961; Selye et al., 1961; Barka, 1965;
Muir et al., 1975; Bloom et al., 1979). This
effect may be blocked by a B-adrenoceptor
antagonist such as propranolol, suggesting a
direct action of the drug via the P-adrenoceptor
(Schneyer, 1969). Repeated administration of
isoprenaline to newborn animals, causes not
only an enlargement of the acinar cells, but
als0 an acceleration of their development
(Schneyer and Schackleford, 1963).
The cell bodies of sympathetic nerves to the
salivary glands are located in the superior cervical ganglion. Extirpation of this structure in
adult animals results in an almost complete
depletion of noradrenaline and a loss of catecholamine fluorescence in the rat parotid and
submandibular glands (e.g., Perec et al., 1975;
Alm and Ekström, 1977). Long-term
deprivation of adrenergic stimuli caused by
surgical or pharmacological denervation
induces a slight decrease of acinar cell size as
well as of total gland weight (Schneyer and
Hall, 1967; Perec et al., 1975).
In the present investigation, ganglionectomy
was performed in adult as weìl as in newbom
Received March 25. 1981; accept4 Mav 27. 1981.
Send reprint requests to Dr. R. Henriksson, Department of Histology
and Cel1 Biology. University of UmeB. S90187 UmeB. Sweden.
rats. After a period of 9 weeks, quantitative
stereological methods at the ultrastructural
level were employed to study characteristics of
the acinar cells.
Animals and tissue preparation
Pregnant rats of the Sprague-Dawley strain
and adult rats were purchased from Anticimex, Stockholm, Sweden. Food and water
were available ad libitum.
Within 4 hr after delivery, the newborn rats
were anesthetized by hypothermia (Fairfield,
1948)and through a midline incision the left carotid bifurcation was exposed. The left superior cervical ganglion was cut free from pre- and
postganglionic fibers and removed. After suturation the newborn rats were resuscitated
over a warm plate (37°C)to adapt to normal
body temperature. After recovery the animals
were returned to their litter and kept there for
another 4 weeks. Only female rats were used
for this study. In another series of experiments
6-week-oldfemde rats were anesthetized by iv
injection of Brietal (a short acting barbiturate)
and the left superior cervical ganglion was r e
moved as described above.
The extirpated tissue was squashed between
glass slides, stained witb 1%toluidine blue and
examined in a light microscope to verify the
success in ganglionectomy. Nine weeks after
surgery the animals were starved for 18 hr
with free access to water. They were then anesthetized and the sympathectomized as well as
the contralateral nondenervated parotid
glands were removed, weighed, and prepared
for light and electron microscopy.
To verify the degree of denervation of the
salivary gland, the tissues were studied by a
glyoxylic acid method for visualization of
monoamines (De la Torre and Surgeon, 1976).
In brief, the method was as follows: The freshly dissected glands were freeze sectioned at
-25--30°C. The 15- to 20-pm sections were
placed on a glass slide, dipped in a glyoxylic
acid solution, and then air dried. When dry, the
sections were heated in an oven at 80°C to
complete the formation of the fluorophor. They
were mounted and studied in a fluorescence
The distribution of autonomic nerves in normal and denervated glands was studied at the
electron microscopic level with the aid of the
potassium permanganate technique of
Richardson (1966)and Hökfelt (1968).
For the ultrastructural sterological studies
the parotid glands were fixed by vascular per-
fusion through the aorta ascendens. As fixative 2.5% glutaraldehyde in 0.1 M Na-cacodylate buffer (pH 7.4) was used. After 10 min of
perfusion (120 cm H20;20 mlímin) the parotid
glands were removed, cut int0 smal1 pieces,
and fixed for another 20 min by immersion in
the fixative. After a buffer rinse the tissue was
postfixed in 1% Os04in the same buffer for 1.5
hr at 4°C. Following dehydration in graded
ethanol solutions and propylene oxide the
specimens were embeded in Epon 812.
Thick (i-pm)as well as thin (70-nm)sections
were cut on an LKB Ultrotome. The thin sections were collected on naked copper grids.
They were poststained with uranyl acetate
andlor lead citrate. The microscope employed
was a Philips EM 300 electron microscope.
Stereological methods
The electron microscopic stereological measurements were carried out on randomly taken
micrographs of acinar cells which display their
nucleus. Since the acinar celis are polarized,
the morphometric measurements were limited
to micrographs where both apical and basal
cell surfaces were seen (Helander, 1978).From
each animal 10 micrographs were chosen als0
at random and paper prints of the cells were enlarged to a total magnification of 6500. The
random sampling procedure was used since the
parotid gland is homogeneous with the individual components, i.e., acinar cells, not specifically oriented with respect to the plane of section.
In such cases no special precautions are required either for sampling tissue blocks or for
obtaining sections of micrographs (Weibeland
Bolender, 1973; Weibel, 1979).
The point counting method was used employing a multipurpose grid (Weibel, 1979).
The volume density of the secretory granules
was determined in relation to the cytoplasmic
volume (not including the nucleus). The nuclear volume density was determined in relation to the total cell volume. All measurements
were carried out by the same person and they
were repeated some weeks later in order to calculate the personal error in measuring
(Eränkö, 1955). This error, expressed as a
percentage of the mem values, was 5% for the
cell profile area, 5% for nuclear volume density, and 4% for the zymogen granule volume
The diameters of a l l secretory granules in the
electron micrographs were measured in a Zeiss
TGZ-3 particle size analyzer. I t can be expected that only a minority of the granules were
sectioned through their centers and the others
were sectioned at various distances from the
center. The resulting granule profile diameters
were thus smaller than the “true” diameter of
the granules. The true granule diameter can be
calculated from the size distributions of the
slices by several methods. In the present study
we used the method described by Bach, since it
als0 takes the section thickness int0 consideration (Bach, 1967).Assuming that the nuclei are
als0 spherical, their radii were estimated and
the true nuclear radius calculated as suggested
by Giger and Riedwyl (1970) (Weibel, 1979).
This value was then used for calculating the
mean nuclear volume, and by dividing with the
corrected nuclear volume density (see below),
mean cell volume was obtained (Helander,
There are several systemic errors to consider
when the above-described methods are used.
Since we used the nuclear biased sample, i.e.,
only cells were measured that displayed their
nuclei, we overestimate the nuclear volume
density (Konwinski and Koslowski, 1972; Weibel, 1979).Methods for correcting this are only
approximations since they assume that the
component and its containing volumes are
both spheres. Therefore the method by Konwinski and Koslowski (1972) was used as a
rough means of correction. However, Helander
(1978) has shown that the error in using the
correction of Konwinski and Koslowski is negligible when presuming that zymogen cells are
spherical, although they have the shape of
truncated pyramids, as do rat parotid acinar
I t has to be noted that the absolute values
obtained by stereological methods and calculations are restricted with different errors due to
the preparative procedures such as fixation,
dehydration, embedding, and sectioning which
cause changes in the tissue. This means that
major interest should be focused on comparisons between the different groups of glands,
i.e., ganglionectomized glands versus contralateral controls, rather than on the absolute
Upon recovery from anesthesia the adult
rats exhibited ptosis on the operated side but
not on the contralateral control side. The findings were identical in rats sympathectomized
a t birth but they were first observed at 10
days, viz., at the time when the animals generally opened their eyes.
The light microscopical technique used in
the present study to identify monoaminergic
nerves clearly demonstrated lack of such nerve
terminals in glands from the ganglionectomized side. The only exceptions to this rule
were occasional fluorescent nerve fibers in
close association with blood vessels. In nondenervated glands, however, the parenchyma
was crisscrossed by fibers with varicosities exhibiting the characteristic fluorescenceof catecholamines (Figs. l a and lb).
Employing the KMn04technique for electron
microscopic demonstration of adrenergic and
cholinergic nerve terminals the findings coincided with the light microscopic observations.
Neonatally ganglionectomized glands
Sympathetic denervation caused a small but
significant reduction in gland weight compared to contralateral glands (0.19 * 0.01 gm
vs 0.23 * 0.02 gm; p < 0.05; N = 6). Table 1
summarizes the results of the stereological
measurements and it is obvious that the
parotid acinar cells in neonatally denervated
glands were reduced in volume. The size of the
nuclei was, however, unchanged. Consequently the nuclear volume density was increased.
The volume of individual zymogen granules
was significantly diminished as was the number of granule profiles per cell profile. The size
distribution of the secretory granules showed a
unimodal distribution in both groups. I t was
als0 observed that cellular granule content
varied to a greater extent in cells from sympathectomized animals. Furthermore, granule accumulation was frequently noted in the apical
portion of the acinar cells whereas the granules
were uniformly dispersed throughout the cytoplasm of the normal control cells.
A schematic illustration (Fig. 2) depicts in
condensed form a comparison between quantitative differences in parotid acinar cells from
neonatally sympathectomized glands and nondenervated controls. Figures 3 and 4 show the
ultrastructural and light microscopic appearance of sympathectomized and nondenervated
Adult ganglionectomized glands
Sympathetic denervation of adult parotid
glands was not accompanied by any apparent
morphological changes in acinar cells when
compared to nondenervated glands (Fig. 5).
Stereological analysis confirmed these observations (Table 2). A small but not significant
weight decrease was noted in denervated
The secretory acini and blood vessels of the
rat parotid gland are well supplied with adren-
Fig. 1. Histofluorescence of the monoaminergic nerves
in parotid gland of neonatauy ganglionectomized rats. (A)
Neonatally ganglionectomized parotid gland. Note the
paucity of fluorescent nerves in the parenchyma. Occasional
fluorescent nerve terminals are observed in the close vicini-
t y of b l d vessels. x 250. (B) Nondenervated, control parotid gland. The parenchyma of the gland exhibits numerous
fibers and varicosities which are characterized by a yellowgreen fluorescence indicative of catecholamines. "he blood
vessels are nchiy innervated. x 250.
TABLE I . Stereological data for rat parotid acinar cells of control and neonatal sympathetic denervated glands
Cel1 profile area
Calculated volume of
acinar cells
Nuclear profile area
Nuclear volume density
Nuclear volume density
corrected according t o
(Konwinski and Kozlowski, 1972)
Caiculated nuclear volume
Granule volume density
Number of granule profiles
per cel1 profile
Granule profile diameter
Calculated true
granule diameter
Volume of one granule
(n= 6)
I 1.1
I 0.7*
f 0.8*
18.1 f 2.1;'
w 3
102.8 f 6.6
i 62
37.8 f 4.5
0.81 f 0.02
f 3.8'
i 25**
22.7 f 2.2**
0.67 f 0.02**
0.81 f 0.03**
0.29 f 0.03'*
Fig. 2. Schematic illustration of quantitative morphologica1 data from parotid glands of control and neonatally
ganglionectomized rats. Mem volume of acinar cells (repre
sented by circles) in controls = 859 pm’; in denervated rats
= 649 pm’. Sectors represent volume densities of granules
(V ), nuclei (Vm) and residual cytoplasm (Vvc).
TABLE 2. Stereological data for rat parotid acinar cells of control and adult sympathetic deneruated glands
Cel1 profile area
Calculated volume of
acinar cells
Nuclear profile area
Nuclear volume density
Nuclear volume density
corrected according t o
(Konwinski and Kozlowski. 1972)
Calculated nuclear volume
Granule volume density
Number of granule profiles
per cel1 profile
Granule profile diameter
Calculated true
granule diameter
Volume of one granule
(n= 6)
f 5.7
I 55.4
I 0.6
I 1.3
(n= 6)
731.6 h105.8
19.3 i 1.6
20.5 I 2.1
f 4.4
35.5 i 3.2
0.84 I 0.02
34.6 i
0.87 I
1.01 I 0.03
0.54 I 0.04
1.03 i
0.58 i
Values are means
+ SEM.
ergic nerves (Norberg and Olson, 1965; Bloom
et al., 1977). Removal of the superior cervical
ganglion led to a pronounced reduction in catecholamine fluorescense in the parenchyma of
the glands. However, some sympathetic nerve
fibers were still observed in the close vicinity
of the blood vessels. These observations are in
agreement with previous studies and verify
that not al1 synapses between pre- and postgangiionic parotid sympathetic neurons are 10cated in the superior cervical ganglion ( A h
and Ekström, 1977).Utilizing an isotope technique (Pimoule et al., 1980) and quantitative
analyses of noradrenaline contents (Perec et
al., 1975) unilateral ganglionectomy has been
proved to effectively diminish the stores of
this catecholamine in submandibular glands of
the rat.
According to de Camplain et al. (1970) and
Owman et al. (1971)sympathetic nerve fibers
are detectable in rat salivary glands at 1day of
age. The activity of choline acetyltransferase
and the content of noradrenaline reaches adult
levels at Days 15-18 (Ludford and Talamo,
1980) and fi-adrenoceptor density does not
reach adult levels before 25 days (Ludford and
Fig. 3. (A) Parotid gland from neonatally ganglionectomized rat. There is variation in grande content of individual
ules. Light micrography x 400. (B)Light micrographof contralateral nondenervated gland. x 400.
ceìls as weii as pronounced apical localization of the gran-
Talamo, 1980). Furthermore, Mangos (1978)
and Grand et al., (1975)report that the secretory activity is not mature even at this time
and structural development of the parotid
gland is reported to continue up to 6 weeks
(Redman and Sreebny, 1971; Taga and Sesso,
1979). Thus, in our study the neonatal ganglionectomy was performed in animals with immature parotid glands, and adult denervation
was carried out when gland development was
The weight of the parotid gland was clearly
reduced 9 weeks after neonatal extirpation of
the superior cervical ganglion. Morphometric
analyses showed a significantly decreased
acinar cell size, whereas nuclear size was unchanged. In contrast, Schneyer and Hall (1967)
observed no alteration in gland weight or cell
size 2 weeks after ganglionectomy performed 8
days after birth. This would seem to indicate
either that the induction of hypotrophic
changes takes place at a very early stage of
gland development, or that the period of 2
weeks is too short to bring about the changes
observed in this study. The former hypothesis
is further supported by the fact that we did not
notice any significant effect on either gland
weight or cell size after adult sympathectomy.
However, Schneyer and Hall (1966) observed
slight and variable decrease in weight and cell
size between 2 and 6 weeks after sympathectomy. The dissimilar results could als0 be due
to differences in quantitative techniques employed. The contralateral control glands did
not display compensatory hypertrophy when
compared to age-matched nonoperated rats.
Fig. 4. Electron micrographs of control and neonatally
denervated parotid acinar cells. (A)Denervated gland. Granule profile numbers are decreased as compared to controls.
Grandes are preferentially located in the apical cytoplasm.
65 1
x 5,300. (B) Contralateral nondenervated control gland.
The acinar cells are densely packed with secretos. grandes.
x 5,300.
Fig. 5. Electron micrographs of adult denervated and control parotid acinar cells. (A)Adult denervated gland. x 5.300.
(B)Contralateral control gland. x 5,300. There are no major changes in cel1 or grande morphology.
Stereological measurements in neonatally
ganglionectomized glands showed a significant reduction in number of grandes as wel1 as
in grande diameters. Adult denervation r e
vealed no changes whatever in the grande population. This would seem to indicate the importante of a sympathetic influence for the early
development and maturation of the secretory
Wilborn and Schneyer (1972) reported a
marked heterogeneity of the acinar cell population 2 weeks after adult ganglionectomy. The
morphological features described were considered indicative of either low or high secretory
activity. They suggested that the sympathetic
nervous system plays an important role in regulating secretory synchrony of acinar cells. In
the present study we could not observe the
“light” and “ d a r k cells of the above authors
although we did notice variations in grande
contents between different acinar cells.
In conclusion, sympathetic denervation
when performed at birth gives rise to hypotrophy of the parotid gland, whereas the same operation performed in adult rats is essentially
without effect. The interpretation of this could
be that the sympathetic nerve system plays a
fundamental role in the development of the
parotid gland, which is reinforced by the
studies of Srinivasan and Chang (1977)on the
submandibular gland. In the adult gland the
acinar cells are already fully differentiated and
the cells therefore only undergo minor morphological changes after sympathetic denervation.
This investigation was supported by grants
from the Swedish Medical Research Council
(19X-04992), the Medical Faculty of Umea,
and from Svenska Medicinska Säilskapet.
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