THE ANATOMICAL RECORD 258:252–261 (2000)
Colloid in the Pituitary Pars Distalis
of Viscacha (Lagostomus maximus
maximus): Ultrastructure and
Occurrence in Relation to
Season, Sex, and Growth
FABIAN MOHAMED,1* TERESA FOGAL,2 SUSANA DOMINGUEZ,1
LUIS SCARDAPANE,1 JORGE GUZMÁN,1 AND RAMÓN S. PIEZZI2
1
Cátedra de Histología y Embriología, Universidad Nacional de San Luis,
5700 San Luis, Argentina
2
Instituto de Histología y Embriología, Universidad Nacional de Cuyo, Consejo Nacional
de Investigaciones Científicas y Técnicas (CONICET), 5500 Mendoza, Argentina
ABSTRACT
Randomly distributed extracellular colloidal accumulations were observed in the pars distalis of viscacha (Lagostomus maximus maximus).
They were preferentially located in the peripheral zone of the gland and
showed variability in shape and size. Two different types of colloidal accumulations were found by electron microscopy: 1) those surrounded by nongranulated follicular cells that correspond to characteristic follicles, and 2)
those surrounded by granulated cells. In the follicles lined by nongranulated follicular cells, long, prominent microvilli and cytoplasmic processes
protruded into the lumen. The frequency of these accumulations varies
during the year in adult male animals, showing an increase in number
during summer and a decrease during winter. The lowest value was registered in August (winter). The mean follicular diameter did not vary seasonally. The number of colloidal accumulations did not vary seasonally in adult
female viscachas, but a significant difference in the mean follicular diameter between pregnant and non-pregnant females was observed. Pituitaries
of immature animals contain fewer colloidal accumulations than those of
adults. In fetuses, these accumulations were absent. The administration of
melatonin provoked a decrease in the number of these structures. The
numeric changes of the colloidal accumulations observed in this study are
associated with: 1) the seasonal reproductive activity in adult males, and 2)
the reproductive condition, body weight and sexual maturity in males and
females. The fact that melatonin administration decreases the population of
colloidal accumulations in males suggests participation of the pineal gland
in these changes. Anat Rec 258:252–261, 2000. © 2000 Wiley-Liss, Inc.
Key words: Lagostomus maximus maximus; pituitary; colloid;
season; sex; growth
Extracellular accumulations of colloid have often been
described as normal components of the vertebrate pituitary gland. Colloidal accumulations vary greatly in size
and frequency. They have been reported within the pars
distalis and pars intermedia in mammals, birds, reptiles,
amphibians and fishes (Benjamin, 1981), and pars tuberalis (Kameda, 1990). Colloid has been described within
the residual lumen of Rathke’s pouch in many species that
©
2000 WILEY-LISS, INC.
Grant sponsor: CONICET; Grant number: PIP 4936; Grant sponsor: P. 7303 CyT (UNSL).
*Correspondence to: Dr. Fabian Mohamed, Cátedra de Histología y Embriología, Facultad de Química, Bioquímica y Farmacia, Universidad Nacional de San Luis, Av. Ejército de los Andes
950 – 2° Piso, 5700 San Luis, Argentina.
E-mail: mcamp@unsl.edu.ar
Received 22 April 1999; Accepted 12 October 1999
COLLOID IN PARS DISTALIS OF VISCACHA
retain this space as a hypophysial cleft throughout adulthood (Seyle, 1943; Bassett, 1951; Vanha-Perttula and Arstila, 1970, Correr and Motta, 1981).
Very little is known about the origin, composition or
function of pituitary colloid. In this regard, numerous
reports made by different authors suggest changes in colloidal accumulations following experimental treatments
such as osmotic stress (Selye, 1943; Selye and Hall, 1943),
gonadectomy (Ellison and Wolfe, 1934; Kirkman, 1937;
Ferrer, 1956; Curé et al., 1971; Dingemans and Feltkamp,
1972; Vila-Porcile, 1972), adrenalectomy (Farquhar, 1957;
Dingemans and Feltkamp, 1972; Vila-Porcile, 1972), thyroid inhibition (Curé et al., 1971; Dingemans and Feltkamp, 1972) and dehydration (Ciocca and González,
1978). In the pars distalis of bats, dogs, and man, the
follicular cells have an ability to form colloid-containing
follicles (Kagayama, 1965; Fukuda, 1973; Nunez and Gershon, 1982; Anthony and Gustafson, 1984). The colloidcontaining follicles of bats show seasonal changes (Nunez
and Gershon, 1982), and the colloid content increases
gradually from birth through sexual maturity (Anthony
and Gustafson, 1984). In the human pars distalis, the
follicles are frequently observed in fetal life but are rare in
adults (Fukuda, 1973). It is also known that the follicles
greatly increase in number and size with age in pars
distalis of guinea pig (Kameda, 1991). Ogawa et al. (1996,
1997) reported that the glycoproteins that occur in senescent porcine pituitary colloids are of two types, namely,
albumin fragments and clusterin.
However, the precise proximate stimuli promoting colloid formation remain unclear. Nevertheless, since colloidal accumulations exhibit considerable variability with
endocrine conditions it has been suggested that these elements may be related to the secretory activities of the
adenohypophysis (Harrison et al., 1982a,b; Nunez and
Gershon, 1982). Therefore, it would be reasonable to suspect that changes in colloid content might accompany the
extensive modifications in endocrine function that characterize the annual cycle of seasonal breeders.
The adult male viscacha is a photoperiodic mammal
that exhibits an annual reproductive cycle under natural
conditions (Fuentes et al., 1991; Muñoz et al., 1997, 1998),
as occurs with other species such as the Syrian hamster
(Gaston and Menaker, 1967). For this reason, the viscacha
appears to provide an interesting case study of the influence of environmental regulation on pituitary secretion
and its probable connection with the colloidal accumulations. In this study, the pituitary pars distalis colloid
content of immature and adult male and female viscachas,
which were collected throughout the year, was quantified.
Seasonal, sex-related and growth-related variations were
independently assessed using standard statistical analyses. Furthermore, their light and electron microscopic features were investigated. This study is the first carried out
in viscacha, and establishes this rodent as an excellent
model for a variety of future studies of the histophysiologic
role of pituitary colloid.
MATERIALS AND METHODS
Adult and immature viscachas were captured in their
habitat near San Luis, Argentina (33° 20' south latitude,
760 m altitude) during 1996 and 1997.
In summer there is up to 14 hr light daily in San Luis
with an average temperature of 25°C. In winter, the light
phase decreases to 10 hr and the average temperature to
253
10°C. The rainfall is 206 mm in summer and 18 mm in
winter.
The reproductive condition of the viscachas was carefully assessed on the basis of observations by light microscopy of testes and ovaries and, additionally, on the basis of
body weight (Llanos and Crespo, 1954; Branch et al.,
1993).
The animals were anesthetized with Nembutal (pentobarbital) and killed by decapitation. The brain was rapidly
exposed and the pituitary gland was excised, sagittally
sectioned and processed for light microscopy, fixed in
Bouin’s fluid, embedded in paraffin, serially sectioned in
the horizontal plane at 5 ␮m and stained with hematoxylin-eosin and periodic acid-Schiff (PAS).
Structural stereological studies were performed using
the optical slides of pituitaries of viscachas captured in
different months of the year. Cross sections stained by
PAS were examined in a Orthoplan Leitz microscope.
For morphometric studies the tissue sections were examined using a 40⫻ objective and 10⫻ eyepiece. Ten paraffin horizontal sections (5 ␮m thickness) regularly spaced
throughout the pituitary of each viscacha gland were chosen for the numeric analysis of colloid content. For each
section 10 fields (0.4 mm2) were chosen and counted including both median and lateral areas of pars distalis. The
total number of colloid structures was determined for each
pituitary. The diameters of the colloidal accumulations
counted in male and female adult viscachas were measured using an ocular micrometer.
Statistical analyses were performed using a two-tailed
Student’s t-test (differences between two groups) or oneway analysis of variance followed by Tukey’s multiple
comparison test (differences between all means). P ⬍ 0.05
was considered significant. Values of solar irradiation expressed as heliophany were provided by the “Servicio Meteorológico Nacional San Luis.”
For electron microscopy the tissues were fixed “in situ”
with formaldehyde-glutaraldehyde in phosphate buffer
(Karnovsky, 1965) for 10 min, removed and placed in the
same fixative for an additional 6 hr at room temperature,
post fixed in cold 2% OsO4 for 12 hr, dehydrated in acetone, and embedded in Spurr’s resin. One-micrometerthick sections were obtained with a Porter Blum ultramicrotome and dyed with toluidine blue for light microscopy.
Ultrathin sections were stained with uranyl acetate and
lead citrate (Milloning, 1961) and were observed under a
Siemens Elmiskop I electron microscope.
Administration of melatonin: eight adult male viscachas
(4,000 to 5,000 g body weight) captured during the month
of February (summer) were used. The rodents were kept
in isolated boxes with free access to water and food at 20
⫾ 2°C. One group (experimental) received two daily sub-
Figures 1– 4 (overleaf): Paraffin sections of the parenchymal pars distalis of adult viscacha showing extracellular PAS ⫽ positive colloidal
accumulations.
Fig. 1. Adult male captured in February (summer). Arrow, colloidal
accumulation.
Fig. 2. Adult male captured in August (winter), the number of colloidal accumulations is decreased.
Fig. 3. Pregnant female captured in August.
Fig. 4. Non-pregnant female captured in February. The number of
colloid accumulations is similar to that in Figure 3, but the follicular
diameter is smaller. Magnification ⫻200.
254
MOHAMED ET AL.
Figures 1– 4.
COLLOID IN PARS DISTALIS OF VISCACHA
Figures 5–7. (Legend, overleaf.)
255
256
MOHAMED ET AL.
cutaneous injections of melatonin (Sigma, 100 mg/Kg body
weight in oil solution) at 09:00 hr and 17:00 hr, 9 weeks.
Controls received only the diluent.
RESULTS
Morphology and Ultrastructure of Colloidal
Accumulations
The viscacha pituitary gland exhibits a well defined
pars distalis. It is formed by granulated and nongranulated cells, dispersed both in cords and clusters in contact
with a well-developed vascular irrigation. A prominent
pituitary cleft separates the pars distalis from the pars
intermedia, and is lined with epithelial cells.
Colloidal accumulations were observed to be randomly
distributed in the medial zone, preferentially in the peripheral region of the pars distalis and were the strongest
PAS-positive components of the adenohypophysis. In viscachas of both sexes collected during different seasons of
the year the colloidal structures were round, ovoid or
irregularly elongated in shape (Figs. 1– 4).
The colloid-containing follicles were mostly formed by
nongranulated follicular cells (Fig. 5). Their ultrastructural features resembled those of the follicular cells in the
pars distalis of other rodents. The follicular cells surrounding the colloid lacked secretory granules. The nucleus of this cell was oval, elongated, or irregular, and
relatively euchromatic. The cytoplasm contained moderate numbers of mitochondria and scanty amounts of rough
endoplasmic reticulum. The lateral membranes of the apical region were joined by prominent junctional complexes
and desmosomes. From the apical poles of the cells, a large
number of long microvilli and cytoplasm processes protruded into the follicular lumen (Fig. 6). Follicular lumen
were filled with an electron-dense, homogeneous material.
The ultrastructural features varied from small follicles
with scarce colloid to large follicles with abundant electrodense colloid, long microvilli and secretory granules in the
follicular lumen (Figs. 7, 8).
Other types of colloidal deposits were observed frequently in the adult male viscachas captured in summer.
These structures showed an homogenous and electron
dense colloid. Cellular debris comprising vacuoles, altered
membranes and mitochondria could also be distinguished
in the lumen. The lumen was in direct contact with the
membranes of the adjacent parenchymal cells. These cells
contained secretory granules of different size, shapes and
electron density. The remaining structural characteristics
of the cytoplasm showed notable differences, probably representing diverse granulated cell types (Figs. 9, 10).
Some cells exhibited granular fusion, forming elongated
irregularly shaped lacunar structures containing an ho-
Fig. 5. Electron micrograph of a typical follicle (F) from adult male
viscacha surrounded by nongranulated follicular cells. The cells protrude
long prominent microvilli (M) into the lumen. Well-developed complex
junctions (arrows) are observed at apical lateral surface. N, nucleus of
nongranulated follicular cell. G, granulated cell. Magnification ⫻4,000.
Fig. 6. Higher magnification of a portion of the follicle of Figure 5. A
complex junction (arrow) is present along with a desmosome (arrowhead). Magnification ⫻10,000.
Fig. 7. A small follicle (F) from the pituitary gland of an immature
viscacha. Three follicular cells are surrounding a follicular lumen with
scarce electro-dense colloid. Magnification ⫻2,500.
mogeneous and dense colloid-like material. These structures were in contact with the lumen of the colloidal accumulation (Fig. 10). Dense lysosomes-like bodies were
also abundant in the cytoplasm of the cells bordering the
colloid deposits.
Stellate or irregular cells in different stages of involution could be found. They showed an irregular and picnotic
nucleus and an homogeneous cytoplasm containing vacuoles or the remains of disintegrated cytoplasmic elements.
These cells were frequently observed in the glands of male
adult viscachas obtained in June and August (winter)
(Fig. 11).
Relationships Between the Number of Colloidal
Accumulations, Season, Sex, and Body Weight.
Administration of Melatonin
The number of colloidal accumulations showed significant differences in the glands of male adult viscachas
during the course of the year (Table 1; Figs. 1, 2). The
highest values were registered in December and February
(summer). These values were followed by a significant
decrease in June and August (winter) (P ⬍ 0.001). The
number of colloidal accumulations increased again in October (early spring) and rose progressively, reaching a
peak in December and February. The lowest value was
registered in August. The heliophany showed parallel values in relation to the seasonal variations of the colloid
deposits (Table 1). The mean follicular diameter did not
vary seasonally in adult male viscachas (Table 2).
No seasonal differences in the number of the colloidal
accumulations were observed between pregnant and nonpregnant adult females (P ⬎ 0.05) (Table 1; Figs. 3, 4). All
females collected in winter were pregnant. The mean follicular diameters increased only in the pregnant female
(Table 2).
In both immature males and females, the number of
colloidal accumulations were significantly smaller with
respect to adult animals (P ⬍ 0.05), (Table 3). Colloidal
accumulations were not observed in fetuses.
The colloidal accumulations of the glands of adult male
viscachas treated with melatonin showed a substantial
decrease (P ⬍ 0.001) (Table 4).
DISCUSSION
This work describes the presence of colloidal accumulations in the pituitary pars distalis of the viscacha. They
are periodic acid-Schiff-positive with a morphology similar
to that described in other species of rodents (Benjamin,
1981). The cells bordering on the follicular lumen were
nongranulated follicular cells. Concerning the functional
role of follicular cells, various hypotheses have been proposed: 1) the cells are supporting or sustentacular elements of the adenohypophysis, 2) the cells are phagocytes,
as they engulf extracellular debris and degenerating cells,
and 3) the cells are precursors that can transform into
granulated secretory cells with the ability to secrete the
adenohypophysial hormones (Nunez and Gershon, 1982).
The present study supports the hypothesis that the follicular cells in pars distalis of viscacha are sustentacular
elements and phagocytes and, moreover, that they have a
function in the secretion and absorption of colloid. The
identification of the nature of colloid stored in the follicles
will help to clarify their function.
COLLOID IN PARS DISTALIS OF VISCACHA
Figures 8 and 9. (Legend, overleaf.)
257
258
MOHAMED ET AL.
Fig. 10. Electron micrograph of an irregular extracellular accumulation of colloid (A). The parenchymal cells are in contact with them and
delimit the lumen. These cells show different types of secretory granules.
Colloid is homogeneous and dense. Magnification ⫻2,500. Left inset:
Lacunar structures with dense colloid-like material inside are present in
the cytoplasm of the cell bordering the colloidal accumulation. Some of
these are apparently continuous with the lumen (arrow). Magnification
⫻10,000.
Fig. 11. Electron micrograph from of viscacha captured in winter, an
irregular cell (C) shows an advanced grade of involution (picnotic nucleus, remains of membranes and numerous vacuoles). Magnification
⫻6,000.
Fig. 8. Follicle composed of nongranulated follicular cells from
a pregnant female viscacha. Abundant electro-dense and secretory
granule-like material (S) is observed in the follicular lumen. N, nucleus
of nongranulated follicular cell. G, granulated cell. Magnification
⫻2,500.
Fig. 9. Electron micrograph of an extracellular colloidal accumulation
(A) from adult male viscacha captured in summer surrounded by parenchymal granulated cells. They show different morphological types. Remains of membranes, altered mitochondria and secretory granules can
be distinguished in the lumen. Magnification ⫻4,000.
259
COLLOID IN PARS DISTALIS OF VISCACHA
TABLE 1. Seasonal variations in number of colloidal
accumulations per microscopic field in the pars
distalis of adult male and female viscachas
Male
(Mean ⫾ SE)
Female
(Mean ⫾ SE)
Heliophany
(H)
19.15 ⫾ 0.07 a
17.90 ⫾ 0.07 b
14.30 ⫾ 0.06 c
11.36 ⫾ 0.26 c
10.56
7.78
5.63
6.60
7.04
7.39
7.98
11.07
Months
February
April
June
July
August
September
October
December
12.05 ⫾ 0.30 c
12.87 ⫾ 0.09 *c
13.02 ⫾ 0.12 *c
12.11 ⫾ 0.50 c
10.92 ⫾ 0.12 cd
9.24 ⫾ 0.10 d
9.91 ⫾ 0.07 d
13.90 ⫾ 0.05 c
17.48 ⫾ 0.07 b
18.05 ⫾ 0.05 ab
TABLE 2. Mean diameter (in ␮m ⴞ SE) of colloidal
accumulations in the pars distalis
February
August
December
Sex (n)
Mean diameter
Male (4)
Non-pregnant female (4)
Male (4)
Pregnant female (4)
Male (5)
Non-pregnant female (4)
12.67 ⫾ 0.38
12.13 ⫾ 0.30
11.58 ⫾ 0.39
20.62 ⫾ 0.76***
11.50 ⫾ 0.39
11.42 ⫾ 0.35
The mean follicular diameter only increased significantly during the pregnancy.
***P ⬍ 0.001.
TABLE 3. Number of colloidal accumulations per
microscopic field in the pars distalis of Lagostomus
maximus maximus grouped according to body
weights and reproductive condition
Male
Body weight (g)
300–600
800–2,000
3,000–4,500
6,000–8,000
Female
Mean
SE
n
Mean
SE
n
2.47
4.36
0.10
0.23
3
2
1.69
3.79
13.02 (P)
9.24 (NP)
0.45
0.04
0.12
0.10
2
2
4
4
0.07
0.07
4
4
19.15 (F)
9.91 (A)
Group
Control
Experimental
Mean
SE
n
23.85
11.65***
0.27
0.18
4
4
***P ⬍ 0.001 vs. control, determined by Student’s t-test.
Four viscachas were observed in each month.
*All females were pregnant.
(H) Quantity of solar irradiation expressed as heliophany.
Monthly average.
Seasonal difference in the number of colloidal accumulations
was determined for each sex separately by one-way of analysis of variance followed by Tukey’s test. Means with the same
letter are not significantly different at the 0.05 level.
Month
TABLE 4. Number of colloidal accumulations in
pituitary pars distalis of adult male viscachas
administered with melatonin
The number of colloidal accumulations increased with body
weight.
F, February; A, August; P, pregnant; NP, non-pregnant.
Growth difference in the number of colloid accumulations was
determined for each sex separately by one-way of analysis of
variance followed by Tukey’s test.
On the other hand, cells in involution are found in the
pituitary of male adult viscachas captured in winter.
These cells may represent old elements in the processes of
degradation and lysis. The rest of the cytoplasmic components of these cells are found in the lumen of colloidal
formation. This may be associated with the changes in the
number of colloidal accumulations throughout the year
and may explain the existence of a transitory mode of
colloidal accumulation. During winter these cells may represent an early stage in the process of colloid formations.
They might suffer a dynamic process of structural changes
in relation to season. The observation of cells showing
cytoplasmic vacuoles and inclusions of colloid-like material in continuity with the lumen of colloidal structures
suggests that such cells might gradually contribute to the
formation of new colloidal accumulations. Similar observations were made by other authors in the adenohypophysis of rabbits (Shionati, 1980), avians (Harrison et al.,
1982a,b) and bats (Nunez and Gershon, 1982) suggesting
that this process may be related to secretory activity.
Wolfe (1943) and Ciocca and González (1978) suggested
that the colloid is a bioproduct of cellular degeneration.
Futhermore, the results of this study demonstrate that
in male viscachas the population of colloidal accumulations changes in relation to the variations in the natural
photoperiod, expressed as heliophany. These changes are
also related to the annual reproductive activity described
by Fuentes et al. (1991) and Muñoz et al. (1997, 1998) for
this species. In effect, in summer and autumn there is an
increase in the population of colloid contents associated
with great reproductive activity. On the other hand, colloid deposits decrease in winter while a gradual decrease
of testicular activity was observed. In August both events,
colloid deposits and gonadal activity, reached their lowest
values. These results suggest that the colloidal content of
the pars distalis is coincident to the gonadal seasonal
changes previously described in adult male viscachas (Fuentes et al., 1991; Muñoz et al., 1997, 1998).
The evidence for a significant decrease in the colloid
population after melatonin administration supports the
hypothesis that these changes could be mediated by the
pineal gland through its hormone. Thus, we can propose
that administration of melatonin reduces the colloid population inducing the characteristics of a winter pars distalis gland when the heliophany is at its lowest values of
the year. Scardapane et al. (1983) showed the same effect
of melatonin on the pars intermedia of the viscacha. A
possible relationship between pineal activity and gonadal
regression in males was also suggested by Dominguez et
al. (1987), Fuentes et al. (1991) and Muñoz et al. (1997,
1998). These previous data and our present results suggest that hormones such as the gonadotrophins and MSH,
probably stored in colloid structures, decrease during the
winter period. This reduction may be associated with a
low endocrine activity of the pineal-pituitary-gonadal axis
during the winter season.
Conversely, in the adult female the number of colloidal
accumulations does not change in relation to the season,
but the mean follicular diameters are higher in pregnant
with respect to non-pregnant females. Variations in pituitary colloid associated with female reproductive activity
have been reported in a few mammalian species. Colloid
260
MOHAMED ET AL.
content increases during pregnancy in the bat Macrotus
californicus (Richardson, 1980) and in the guinea pig
(Kirkman, 1937). A rise in colloid content has been reported during lactation in rats (Vila-Porcile, 1972) and
cats (Curé et al., 1971). On the other hand, Curé et al.
(1971) reported no changes in pituitary colloid in pregnant
hamsters, cats and hedgehogs. These results indicate that
the effect of female reproductive activity on pituitary colloid may vary considerably from species to species.
Some authors have also reported sex-related differences
in the amount of pituitary colloid in guinea pigs (Wolfe
and Eaton, 1940), and in hamsters and hedgehogs (Curé et
al., 1971). In the present study, statistical comparisons
between males and females of similar body weights
showed that the seasonal changes of pituitary colloid in
viscacha demonstrate a sexual dimorphism.
In fetuses the colloid was absent. However, the number
of colloidal accumulations in the pars distalis of the viscacha increases from the immature stage to the mature
sexual stage. Similar changes in pituitary colloid content
have been reported previously in numerous mammals. In
rats (Wolfe, 1943), cattle (Bassett, 1951) and bat (Anthony
and Gustafson, 1984), colloid is a conspicuous component
of adult pituitary glands. Colloidal accumulations are rare
and reduced in size in immature hamsters, guinea pigs,
hedgehogs, and porcine, but these structures are larger
and more numerous in older animals (Wolfe and Eaton,
1940; Shanklin, 1948; Hanke and Charipper, 1948; Spagnoli and Charipper, 1955; Curé et al., 1971; Kameda,
1990, 1991; Ogawa et al, 1996, 1997). The results obtained
in pars distalis of viscacha suggest that the follicle formation was closely related to the body weight. According to
the results published by Llanos and Crespo (1954) and
Branch et al. (1993) the body weights in this rodent are in
relation to the age. Then, the viscachas used in our study
are in different stages of the growing up. From this point
of view, the body weights showed in the Table 3 correspond to immature animals (300 – 600 g); juvenile adult
animals (800 –2,000 g); adult female animals (3,000 –
4,500 g); and adult male animals (6,000 – 8,000 g).
From these observations we conclude that the number
of colloidal accumulations in the pituitary pars distalis of
Lagostomus maximus maximus varies with the endocrine
activity of the gland, and is an excellent model for future
studies of their histophysiologic role.
ACKNOWLEDGMENTS
The authors are grateful to Juan Arroyuelo, Noe Perez,
and Alejandro Sabez for their technical collaboration and
Dr. Sean Patterson (Department of Neurobiology, Medical
Center, Duke University, Durham, North Carolina) for his
careful revision of the English language.
Grants provided by CONICET (PIP 4936) and P. 7303
CyT (UNSL). R.S. Piezzi is a Research Career Member of
CONICET.
LITERATURE CITED
Anthony EPL, Gustafson AW. 1984. A quantitative study of pituitary
colloid in the bat Myotis lucifugus lucifugus in relation to age, sex,
and season. Am J Anat 169:89 –100.
Bassett EG. 1951. The anterior lobe of the cattle pituitary II. Distribution of colloid. J Endocrinol 7:215–220.
Benjamin M. 1981. Cysts (large follicles) and colloid in pituitary
glands. Gen Comp Endocrinol 45:425– 445.
Branch LC, Villarreal D, Fowler GS. 1993. Recruitment, dispersal,
and group fusion in a declining population of the plains vizcacha
(Lagostomus maximus; Chinchillidae). J Mammal 74:9 –20.
Ciocca DR, González CB. 1978. The pituitary cleft of the rat: an
electron microscopic study. Tissue Cell 10:725–733.
Correr S, Motta PM. 1981. The rat pituitary cleft: a correlated study
by scanning and transmission electron microscopy. Cell Tissue Res
215:515–529.
Curé M, Gerry H, Girod C. 1971. Observations sur les structures
pseudo-folliculaires du lobe antérieur de l’hypophyse chez plusieurs
espêces de Mammifêres et chez l’Homme. C S Soc Biol (Paris)
165:1616 –1669.
Dingemans KP, Feltkamp CA. 1972. Nongranulated cells in the
mouse Adenohypophysis. Z Zellforsch Mikrosk Anat 124:387– 405.
Dominguez S, Piezzi RS, Scardapane L, Guzmán JA. 1987. A light and
electron study of the pineal gland of the viscacha (Lagostomus
maximus maximus). J Pineal Res 4:211–219.
Ellison ET, Wolfe JM. 1934. The effect of castration on the anterior
hypophysis of the female rat. Endocrinology 18:555–575.
Farquhar MG. 1957. “Corticotrophs” of the rat adenohypophysis as
revealed by electron microscopy. Anat Rec 127:291.
Ferrer J. 1956. Histophysiology of the pituitary cleft and colloid cysts
in the adenohypophysis of the rat: changes after gonadectomy and
adrenalectomy. J Endocrinol 13:349 –353.
Fuentes LB, Caravaca N, Pelzer LE, Scardapane L, Piezzi RS,
Guzmán JA. 1991. Seasonal variations in the testis and epididymis
of viscacha (Lagostomus maximus maximus). Biol Reprod 45:925–
928.
Fukuda T. 1973. Agranulate stellate cells (so-called follicular cells) in
human fetal and adult adenohypophysis and in pituitary adenoma.
Virchows Arch Pathol Anat 359:19 –30.
Gaston S, Menaker M. 1967. Photoperiodic control of hamster testis.
Science 158:925–928.
Hanke HH, Charipper A. 1948. The anatomy and cytology of the
pituitary gland of the golden hamster (Cricetus autarus). Anat Rec
102:123–139.
Harrison F, Van Hoof J, Vakaet L. 1982a. The relationship between
the folliculo-stellate network and the thyrotropic cells of the avian
adenohypophysis. Cell Tissue Res 226:97–111.
Harrison F, Van Hoof J, Vakaet L. 1982b. Processing of cell debris
suggestive of phagocytosis in the follicular cavities of the avian
adenohypophysis. Cell Biol Int Rep 6:153–161.
Kagayama M. 1965. The follicular cell in the pars distalis of the dog
pituitary gland: an electron microscope study. Endocrinology 77:
1053–1060.
Kameda Y. 1990. Occurrence of colloid-containing follicles and ciliated
cysts in the hypophysial pars tuberalis from guinea pigs of various
ages. Am J Anat 188:185–198.
Kameda Y. 1991. Occurrence of colloid-containing follicles in the pars
distalis of pituitary glands from aging guinea pigs. Cell Tissue Res.
263:155–124.
Karnovsky MJ. 1965. A formaldehyde-glutaraldehyde fixate of high
osmolarity for use in electron microscopy. J Cell Biol 27:49A.
Kirkman H. 1937. A cytological study of the anterior hypophysis of the
guinea pig and statistical analysis of its cell types. Am J Anat
61:233–287.
Llanos AC y Crespo JA. 1954. Ecología de la vizcacha (Lagostomus
maximus maximus Blainv.) en el Nordeste de la Provincia de Entre
Ríos. Revista de Investigaciones Agrícolas. Extra Nueva Serie no.
10:5–95.
Milloning G. 1961. A modified producer for lead staining of thin
sections. J Biophys Biochem Cytol 11:736 –739.
Muñoz E, Fogal T, Dominguez S, Scardapane L, Guzmán JA, Piezzi
RS. 1997. Seasonal changes of the Leydig cells of viscacha (Lagostomus maximus maximus): a light and electron microscopy study.
Tissue Cell 29:119 –128.
Muñoz E, Fogal T, Dominguez S, Scardapane L, Guzmán J, Piezzi RS.
1998. Stages of the cycle of the seminiferous epithelium of the
viscacha (Lagostomus maximus maximus). Anat Rec 252:8 –16.
Nunez EA, Gershon MD. 1982. Phasic secretion by follicular cells of
the bat adenohypophysis during the prearousal period of their
annual cycle. Am J Anat 165:111–120.
COLLOID IN PARS DISTALIS OF VISCACHA
Ogawa S, Couch EF, Kubo M, Sakai T, Inoue K. 1996. Histochemical
study of follicles in the senescent porcine pituitary gland. Arch
Histol Cytol 59:467– 478.
Ogawa S, Ishibashi Y, Sakamoto Y, Kitamura K, Kubo M, Sakai T,
Inoue K. 1997. The glycoproteins that occur in the colloids of
semescent porcine pituitary glands are clusterin and glycosylated albumin fragments. Biochem Biophys Res Commun 234:
712–718.
Richardson BA. 1980. The pars distalis of the female California leafnosed bat, Macrotus californicus, and its possible role in delayed
development. Doctoral thesis, University of Arizona.
Scardapane L, Lucero JB, Dominguez S, Piezzi RS, Guzmán JA.
1983. Effect of chronic administration of melatonin on viscacha
pars intermedia (Lagostomus maximus maximus). Com Biol
2:183–188.
Seyle H. 1943. Experiments concerning the mechanism of pituitary
colloid secretion. Anat Rec 86:109 –119.
Selye H, Hall CE. 1943. Further studies concerning the action of
sodium chloride on the pituitary. Anat Rec 86:579 –583.
261
Shanklin WM. 1948. On the presence of calcific bodies, cartilage, bone,
follicular concretions and the so-called hyaline bodies in the human
pituitary. Anat Rec 102:469 – 491.
Shionati Y. 1980. An electron microscopic study on stellate cells in the
rabbit adenohypophysis under various endocrine conditions. Cell
Tissue Res 213:237–246.
Spagnoli HH, Charipper HA. 1955. The effects of aging on the histology and cytology of the pituitary gland of the golden hamster
(Cricetus auratus), with brief reference to simultaneous changes in
the thyroid and testis. Anat Rec 121:117–139.
Vanha-Pertulla T, Arstila AU. 1970. On the epithelium of the rat
pituitary residual lumen. Z Zellforsch Mikrosk Anat 108:487–500.
Vila-Porcile E. 1972. Le réseau des cellules folliculo-stellaires et les
follicules de l’adénohypophyse du rat (pars distalis). Z Zellforsch
Mikrosk Anat 129:328 –369.
Wolfe JM. 1943. The effects of advancing age on the structure of the
anterior hypophyses and ovaries of female rats. Am J Anat 72:361–
383.
Wolfe JM, Eaton ON. 1940. Quantitative histologic studies on the anterior pituitaries of various of guinea pigs. Am J Anat 67:347–360.